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Posts Tagged ‘dem bones’

To me, there is no question that the Galerie de Paléontologie et d’Anatomie comparée of Paris’s Muséum national d’Histoire naturelle (MNHN) is the mecca of organismal anatomy, as their homepage describes. Georges Cuvier got the morphological ball rolling there and numerous luminaries were in various ways associated with it too; Buffon and Lamarck and St Hiliaire to name but a few early ones. It is easy to think of other contenders such as the NHMUK in London (i.e., Owen), Jena in Germany, the MCZ at Harvard (e.g. Romer) and so forth. But they don’t quite cut the dijon.

As today is John’s Freezer’s 7th blogoversary, and I was just at the MNHN in Paris snapping photos of their mecca, it’s time for an overdue homage to the magnificent mustard of that maison du morphologie. The exhibits have little signage and are an eclectic mix of specimens, but this adds to its appeal and eccentricity for me. I’ve chosen some of my favourite things I saw on exhibit on this visit, with a focus on things that get less attention (NO MESOZOIC DINOSAURS! sorry), are just odd, or otherwise caught my fancy. It’s a photo blog post, so I shall shut up now, much as I could gush about this place. I could live here.

Need plus-grand images? Clic!

Stomach-Churning Rating: 7/10 for some potentially disturbing anatomical images such as viscera, preserved bits, models of naughty bits etc.

Greetings. Note the stomach-churning rating above, please.

Right. We’ll get the amazing first view as one steps into the gallery done first. Mucho mecca. Anatomy fans simply must go here at least once in their life to experience it, and one cannot ever truly absorb all the history and profound, abundant details of morphology on exhibit.

Less-often-seen views from the balcony; one more below.

Indian Rhinoceros from Versailles’s royal menagerie; came to the MNHN in 1792.

Brown bear hindlimb bones.

Brown bear forelimb bones and pelvis.

Two baby polar bears; part of the extensive display of ontogeny (too often missing in other museums’ exhibits).

Asian elephant from Sri Lanka.

Lamb birth defect. Like ontogeny, pathology was a major research interest in the original MNHN days.

Wild boar birth defect.

Fabulous large Indian gharial skull + skeleton.

“Exploded” Nile crocodile skull to show major bones.

Let’s play name-all-the-fish-skull-bones, shall we?

Rare sight of a well-prepared Mola mola ocean sunfish skeleton.

Diversity of large bird eggs.

Asian musk deer (male), with tooth roots exposed.

Freaky gorilla is here to say that now the really odd specimens begin, including the squishy bits.

Freaky tamandua, to keep freaky gorilla company. Displaying salivary glands associated with the tongue/pharynx. These are examples of anatomical preparations using older analogues of plastination, such as papier-mâché modelling. I’m not completely sure how the preservation was done here.

Tamandua preserved head, showing palate/tongue/pharynx mechanism.

Chimp ears. Because.

Why not add another chimp ear?

Many-chambered ruminant stomach of a sheep.

Simpler stomach of a wolf. Not much room for Little Red Riding Hood, I’m afraid.

Expansive surface area of a hippo’s stomach; but not a multi-chambered ruminant gut.

Cervical air sacs of a Turquoise-fronted Amazon parrot.

Heart and rather complex pulmonary system of a varanid lizard.

It’s pharynx time: Keratinous spines of a sea turtle’s throat. All the better to grip squids or jellies!

Pharynx convergent evolution in a giraffe: keratinous spines to help grip food and protect the pharynx from spiny acacia thorns while it passes down the long throat.

Tongue/hyoid region of the pharynx of a varanid, showing the forked tongue mechanism.

Palaeontological awesomeness on the upper floor (the 2nd part of the gallery’s name). Here, the only Siberian woolly mammoth, I’m told, to have left Russia for permanent display like this. Frozen left side of face, here, and 2 more parts below.

Mammuthus primigenius freeze-dried lower ?left forelimb.

Skeleton that goes with the above 2 parts. It’s big.

But “big” is only relative- my large hand for scale here vs. a simply ginormous Mammuthus meridionalis; full skeleton below.

Four-tusked, moderate-sized Amebelodon elephantiform.

Naked woolly rhinoceros Coelodonta.

Extinct rhino Diaceratherium, with a pathological ankle (degenerative joint disease). I love spotting pathologies in specimens- it makes them stand out more as individuals that lived a unique life.

Glyptodont butt and thagomizer, to begin our tour of this business-end weaponry.

Eutatus leg bones, from a large fossil armadillo; Argentina. Really odd morphology; Xenarthrans are so cool.

Giant ground sloth (Megatherium) foot; ridiculously weird.

Giant ground sloth hand is full of WTF.

Metriorhynchus sea-crocodile from the Cretaceous: hind end.

Odobenocetops one-tusked whale that I still cannot get my head around, how it converged so closely on the morphology of a walrus.

Thalassocnus, the large marine sloth… few fossils are so strange to me as this one. But modern sloths swim well enough so why not, evolution says!

Rear end of the sea-sloth.

Megaladapis, the giant friggin’ lemur! Not cuddly.

A basilosaurid whale Cynthiacetus, one of the stars of the show, as the denouement of this post. Plan your visit now!

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Today is the 210th anniversary of Charles R. Darwin’s birthday so I put together a quick post. I’d been meaning to blog about some of our latest scientific papers, so I chose those that had an explicit evolutionary theme, which I hope Chuck would like. Here they are, each with a purty picture and a short explainer blurb! Also please check out Anatomy To You’s post by Katrina van Grouw on Darwin’s fancy pigeons.

Stomach-Churning Rating: 1/10 science!

First, Brandon Kilbourne at the Naturkunde Museum in Berlin kindly invited me to assist in a paper from his German fellowship studying mustelid mammals (otters, weasels, wolverines, badgers, etc.; stinky smaller carnivorous mammals). Here we (very much driven by Brandon; I was along for the ride) didn’t just look at how forelimb bone shape changes with body size in this ecologically diverse group. We already knew bigger mustelids would have more robust bones, although it was cool to see how swimming-adapted and digging-adapted mustelids evolved similarly robust bones; whereas climbing ones had the skinniest bones.

The really exciting and novel (yes I am using that much-abused word!) aspect of the paper is that Brandon conjured some sorcery with the latest methods for analysing evolutionary trends, to test how forelimb bone shapes evolved. Was their pattern of evolution mostly a leisurely “random walk” or were there early bursts of shape innovation in the mustelid tree of life, or did shape evolve toward one or more optimal shapes (e.g. suited to ecology/habitat)? We found that the most likely pattern involved multiple rates of evolution and/or optima, rather than a single regime. And it was fascinating to see that the patterns of internal shape change deviated from external shape change such as bone lengths: so perhaps selection sometimes works independently at many levels of bone morphology?

Various evolutionary models applied to the phylogeny of mustelids.

Then there, coincidentally, was another paper originating in part from the same museum group in Berlin. This one I’d been involved in as a co-investigator (author) on a Volkswagen (yes! They like science) grant back about 8 years ago and since. There is an amazing ~290 million year old fossil near-amniote (more terrestrial tetrapod) called Orobates pabsti, preserved with good skeletal material but also sets of footprints that match bones very well, allowing a rare match of the two down to this species level. John Nyakatura’s team had 3D modelled this animal before, so we set out to use digital techniques to test how it did, or did not, move—similar to what I’d tried before with Tyrannosaurus, Ichthyostega and so forth. The main question was whether Orobates moved in a more “ancestral” salamander-like way, a more “derived” lizard-like way (i.e. amniote-ish), or something else.

The approach was like a science sledgehammer: we combined experimental studies of 4 living tetrapods (to approximate “rules” of various sprawling gaits), a digital marionette of Orobates (to assess how well its skeleton stayed articulated in various motions), and two robotics analysis (led by robotics guru Auke Ijspeert and his amazing team): a physical robot version “OroBOT” (as a real-world test of our methods), and a biomechanical simulation of OroBOT (to estimate hard-to-measure things in the other analyses, and matches of motions to footprints). And, best of all, we made it all transparent: you can go play with our interactive website, which I still find very fun to explore, and test what motion patterns do or do not work best for Orobates. We concluded that a more amniote-like set of motions was most plausible, which means such motions might have first evolved outside of amniotes.

OroBOT in tha house!

You may remember Crassigyrinus, the early tetrapod, from a prior post on Anatomy To You. My PhD student Eva Herbst finished her anatomical study of the best fossils we could fit into a microCT-scanner and found some neat new details about the “tadpole from hell”. Buried in the rocky matrix were previously unrecognized bones: vertebrae (pleurocentra; the smaller nubbins of what may be “rhachitomous” bipartite classic tetrapod/omorph structure), ribs (from broad thoracic ones to thin rear ones), pelvic (pubis; lower front), and numerous limb bones. One interesting trait we noticed was that the metatarsals (“sole bones” of the foot) were not symmetrical from left-to-right across each bone, as shown below. Such asymmetry was previously used to infer that some early tetrapods were terrestrial, yet Crassigyrinus was uncontroversially aquatic, so what’s up with that? Maybe this asymmetry is a “hangover” from more terrestrial ancestry, or maybe these bones get asymmetrical for non-terrestrial reasons.

The oddly asymmetrical metatarsals of Crassigyrinus.

Finally, Dr. Peter Bishop finished his PhD at Griffith University in Australia and came to join us as a DAWNDINOS postdoc. He blasted out three of his thesis chapters (starting here) with me and many others as coauthors, all three papers building on a major theme: how does the inner bone structure (spongy or cancellous bone) relate to hindlimb function in theropod dinosaurs (including birds) and how did that evolve? Might it tell us something about how leg posture or even gait evolved? There are big theories in “mechanobiology” variously named Wolff’s Law or the Trajectorial Theory that explain why, at certain levels, bony struts tend to align themselves to help resist certain stresses, and thus their alignment can be “read” to indicate stresses. Sometimes. It’s complicated!

Undaunted, Peter measured a bunch of theropod limb bones’ inner geometry and found consistent differences in how the “tracts” of bony struts, mainly around joints, were oriented. He then built a biomechanical model of a chicken to test if the loads that muscles placed on the joints incurred stresses that matched the tracts’ orientations. Hmm, they did! Then, with renewed confidence that we can use this in the fossil record to infer approximate limb postures, Peter scanned and modelled a less birdlike Daspletosaurus (smaller tyrannosaur) and more birdlike “Troodon” (now Stenonychosaurus; long story). Nicely fitting many other studies’ conclusions, Peter found that the tyrannosaur had a more straightened hindlimb whereas the troodontid had a more crouched hindlimb; intermediate between the tyrannosaur and chicken. Voila! More evidence for a gradual evolution of leg posture across Mesozoic-theropods-into-modern-birds. That’s nice.

Three theropods, three best-supported postures based on cancellous bone architecture.

If you are still thirsty for more papers even if they are less evolutionary, here’s the quick scoop on ones I’ve neglected until now:

(1) Former PhD student Chris Basu published his thesis work w/us on measuring giraffe walking dynamics with force plates, finding that they move mostly like other quadrupeds and their wobbly necks might cost them a little.

(2) Oh, and Chris’s second paper just came out as I was writing this! We measured faster giraffe gaits in the wilds of South Africa, as zoo giraffes couldn’t safely do them. And we found they don’t normally go airborne, just using a rotary gallop (not trot, pace or canter); unlike some other mammals. Stay tuned: next we get evolutionary with this project!

(2) How do you safely anaesthetize a Nile crocodile? There’s now a rigorous protocol (from our DAWNDINOS work).

(3) Kickstarting my broad interest in how animals do “extreme” non-locomotor motions, we simulated how greyhounds stand up, finding that even without stretchy tendons they should, barely, be able to do it, which is neat. Expect much more about this from us in due time.

(4) Let’s simulate some more biomechanics! Ashley Heers, an NSF research fellow w/me for a year, simulated how growing chukar birds use their wing muscles to flap their way up steeper inclines (“WAIR” for devotees), and the results were very encouraging for simulating this behaviour in more detail (e.g. tendons seem to matter a lot) and even in fossil species; and finally…

(5) Hey did you ever think about how bone shape differs between hopping marsupials (macropods) and galloping artiodactyl (even-toed) mammals? We did, in long-the-making work from an old BBSRC grant with Michael Doube et al., and one cool thing is that they mostly don’t change shape with body size that differently, even though one is more bipedal at faster speeds—so maybe it is lower-intensity, slower behaviours that (sometimes?) influence bone shape more?

So there you have the skinny on what we’ve been up to lately, messing around with evolution, biomechanics and morphology.

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One of my favourite museums in the world, and certainly one of the best natural history museums in the UK, is Cambridge’s Museum of Zoology, AKA “University Museum of Zoology at Cambridge” (UMZC). It is now nearing a lengthy completion of renovations; the old museum exhibits and collections were excellent but needed some big changes along with the re-fabbed “David Attenborough Building” that houses them. As a longtime fan of the exhibits and user of the collection (and microCT scanner), I hurried to see the new museum once it officially opened.

And that makes a great excuse to present a photo-shoot from my visit. This focuses on the “mammal floor” below the entrance- the upper floor(s?) are still being completed and will have the birds, non-avian tetrapods, fish, etc. But the UMZC is strong in mammals and so it is natural for them to feature them in this chock-full-o-specimens display. Less talk, more images. Here we go!

All images can be clicked to mu-zoom in on them.

Stomach-Churning Rating: 3/10; bones and taxidermy and innocuous jars.

The building. The whale skeleton that hung outside for years is now cleaned up and housed right inside; you walk under it as you enter.

Entrance.

First view past the entryway: lots of cool specimens.

View from the walkway down into the ground/basement level from the entry. As specimens-per-unit-volume goes, the UMZC still scores highly and that is GOOD!

Explanation of frog dissection image below.

Gorgeous old frog dissection illustration; such care taken here.

Leeuwenhoek’s flea woodcut; I think from Arcana Naturae Detecta (1695). There is an impressive display of classic natural history books near the entryway.

Dürer/other rhino art image and info.

Darwin was famed for collecting beetles when he should have been studying theology at Cambridge as a youth, and here is some of his collection. Dang.

Darwin’s finches!

Darwin kicked off some of his meticulous work with volumes on barnacles; specimens included here; which helped fuel insights into evolution (e.g. they are “retrograde” crustaceans, not mollusks).

Darwin’s voyage: fish & other preserved specimens.

I think this is a solitaire weka (flightless island bird; see Comment below). I’ve never seen them displayed w/skeleton + taxidermy; it’s effective here.

Eryops cast. More early tetrapods will surely be featured on the upper floor; this one was on the timeline-of-life-on-Earth display.

I LOVE dioramas and this seabird nesting ground display is very evocative, especially now that I’ve visited quite a few such islands.

Mammal introduction; phylogenetic context.

Monotreme glory.

UMZC is well endowed with thylacines and this one is lovely.

“TAZ FEEL NAKED!”

Narwhal above!

Rhinocerotoidea past, present, and fading glory. 😦

Ceratotherium white rhino. The horn is not real; sadly museums (and even zoos) across the world have to worry about theft of such things, given that some people think these horns are magic.

Ceratotherium staring match. You lose.

Ceratotherium stance.

Foot of a Sumatran rhino juxtaposed with a horse’s for Perissodactyla didaction.

A tapir. As a kid, I used to wander around the house pretending to be a tapir but I did not know what noise they’d make so I’d say “tape tape tape!”.

Big Southern Elephant Seal.

Squat little fur seal.

Hippopotamus for the lot of us. (baby included)

Hippo facedown.

Skull of a dwarf Madagascar hippo.

Cave bear and sabretooth cat make an impressive Ice Age demo.

It’s a wombat.

Ain’t no don like a Diprotodon! (also note its modern miniature cousin the wombat, below)

Diprotodon facial.

Diprotodon shoulder: big clavicles bracing that joint region.

Diprotodon knee: even in big marsupials, the “parafibula”/lateral sesamoid of the knee is still generally present. And why it is there/what it does deserves much more study.

Diprotodon hip. I just find this animal’s anatomy fascinating head-to-tail.

Diprotodon front foot. Absolutely freakish.

Diprotodon hind foot. Even weirder.

Your view after having been trampled in a supine position by a Diprotodon. Not a good way to go.

Diprotodon got back.

Elephant seal’s butt continues my series of photos of big animals’ bottoms.

Asian elephant’s butt view.

African elephant butt.

Sectioned elephant skull to show pneumatic resonating chambers.

Paenungulates: hyraxes, Sirenia, elephants & kin (evolutionary demo).

AND MY HYRAX!
Sorry. Had to.

Megatherium side view.

Megatherium. Yeah!

Megatherium hindlegs fascinate me. Well-heeled.

Tamandua duo.

Silky anteater; wonderful.

Armadillos.

Anteaters round out a fab display on Xenarthra.

The UMZC has everything from aardvarks to zebus. Here, conceptualized with other Afrotheria.

Golden moles: the more I read about them, the more they fascinate me.

We can all use some more solenodons in our lives!

Example of the phylogenetic context used throughout exhibits.

If you’ve got a good Okapi taxidermy, you’d better use it.

It’s a giraffe. Did you guess right?

Gerenuk showing off its bipedal capacity.

Warthogs have an inner beauty.

Pangolin. Glad to see it back on exhibit.

Nice little brown bear.

Double-barrelled shot of hyenas.

Colugo!

Nice to see some Scandentia featured.

My brain says this is a springhare (Pedetes) so I am going with what my brain says and anyway I really like this display.

When I saw this I thought, “That’s a nice… rodent thingy.” And so “rodent thing” it shall be labelled here. Enjoy the rodent thingy. Some serious taxidermy-fu in action.

Moonrats– now there’s something you seldom see a full display of. Well done!

That’s part I of this sneak peek at the evolving exhibits- I will put up a part II once the upper floor exhibits open. I highly encourage a visit!

For Mike: gimlet

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Back in November 2016 I got an exciting email from colleague Dr. Richard Thomas, who was building a team of experts for a proposed documentary on Jumbo the elephant; the famed proboscidean of the Victorian era (and arguably most famous elephant of all time, first international celebrity animal, etc.). I knew him from social media and from our mutual interests in chicken anatomy and evolution. And that exciting email, for once, worked out! Over coming months I chatted with the film producers and they could see a place for me in the programme, contributing my expertise in elephant (postcranial) anatomy, locomotion, health/welfare etc. Lo and behold, in May 2017 I met Sir David Attenborough at Heathrow and we flew out to New York City to film with the skeleton at the American Museum of Natural History. And to cap it off, I got to meet another childhood science communication hero: Professor David Suzuki of CBC’s “The Nature of Things“– my adrenaline levels were sky high!

Brooklyn neighborhood by our hotel. Lots to do!

The show has aired in the UK and is coming very soon to Canada and the world (details below). Here’s my part of the story.

Stomach-Churning Rating: 3/10– bad bones but no blood.

We filmed from 15-19 May 2017 at the AMNH’s warehouse of mammalian skeletal remains, which is housed deep in the Brooklyn Army Terminal; a picturesque site in and of itself. And it is a site with a lot of history— WWI and II, Elvis and more.

It was a hectic week of the usual documentary stuff: repeat the same lines and motions again and again from different angles and with different paces and intonations (I cannot help in these cases but think about the Simpsons “Fallout Boy” episode), from ~9am-5pm, with plenty of downtime watching setup or other bits being filmed. I’m used to all that. But having the time to peer around the collection and chat to Richard and colleague Dr. Holly Miller (handling the tissue isotopes side of the story) about Jumbo’s skeleton was a lot of fun during downtime and filming itself. Not to mention the utter joy of studying one of the most famous museum specimens ever, and an animal widely held to be one of the largest of its kind, with much mystery surrounding its history despite its fame. (Wikipedia does a fair job of summarizing some of this)

Here are some photos to tell the story:

Photo of the team, courtesy of Infield Fly Productions (CBC production, “Jumbo: The Life of An Elephant Superstar”.

The Brooklyn Army Terminal, with a view of the harbour beyond.

Inside the terminal: old army staging area and an evocative wooden Liberty/tank artwork.

Army terminal cat. Shipping still comes through the terminal so I guess there are plenty of rats and handouts from cat-lovers to keep it going. I miss our cats when I travel so this moment was appreciated.

Whale skulls and other specimens inside the AMNH warehouse.

First view of Jumbo’s remains.

Photo opp with Sir David.

Photo opp with Prof Suzuki.

That’s the setup. I’ve done ~15 other documentary episodes/shows but this was like nothing else– simply an awesome experience.

Now the delivery: we set to studying those bones. We’d seen photos before, and Henry Fairfield Osborn had illustrated the specimen as his type of “Elephas africanus rothschildi” (Sudanese elephant; no longer valid but those were different times– it’s now just a nicely preserved Loxodonta africana africana), so we knew some of what to expect.

Looking at Osborn’s classic monograph. Oddly he didn’t address the GLARING MASSIVE PROBLEMS WITH THE TEETH!

Skull with terrible tooth pathologies– and let’s play spot Mumbo, my daughter’s toy elephant! He might even appear in some TV footage!

We had noted some serious issues with some bones (pathologies). I won’t spoil the message here but will show some images. I know some experts have voiced issues with how the tooth pathologies/growth were explained in some footage but I can’t address that here; it’s not my expertise. The important point to me is that the teeth are incredibly messed up and that can easily be linked to bad diet and other management/health issues, as the documentary explains.

Jumbo’s torso in left side view. Glorious preservation.

Right forelimb, showing that the “growth plates” (epiphyses”) were not all fused, consistent with Jumbo still growing– as expected for an African male elephant in his 20’s.

Right elbow with some pathologies consistent with degenerative joint disease.

Surprisingly, Jumbo’s feet were not in nasty condition in terms of pathologies. I’d expected to see that. They’d been painted and drilled for mounting, but were not riddled with arthritic changes that I could see.

Strange bony plaque on the left pelvis (hip) region; something I’d never seen before in any elephant (and I’ve seen many). Why? The programme offers a reasonable explanation.

Jumbo’s right hip, with bad erosion of the bone and thus presumably the overlying cartilage. Ouch!

Strange extra prong on one right rib in Jumbo- we didn’t figure that out. It could conceivably be natural variation.

So, poor Jumbo suffered some jumbo-sized problems, and in complex ways. That’s just scratching the surface of what his skeleton tells us, and there’s plenty more in the show plus plenty more we can say later– there’s real science that came out of this programme! I was surprised to find how little had been stated anywhere in the scientific literature about Jumbo’s pathologies.

Sad as Jumbo’s skeletal story is, the broader story of his life and death is sadder still. For purposes of time I don’t think any of the three versions of the show will get to delve into how Jumbo’s mother may have been slashed to death by a broadsword, as the story below describes was the ancient practice:

I’d hate to be “so pestered by a popinjay”, too.

Adding insult to injury, we can reflect on how Jumbo was taken from the Sudan to the east (across the Suez), then on boat to Italy and then overground to Paris, where he lived for a little while until the zoological garden sold him to London. Luckily Jumbo avoided becoming a meal to starving Parisians during the Prussian siege of 1870-1. So he did not become elephant consommé like some of his co-captives did. The more one learns about Jumbo’s life and the life of elephants in captivity in the 1800s, the more harrowing the tale becomes.

Jumbo is THE celebrity elephant. His name has come to mean ‘big’ and ‘bombastic’, from applications to jumbo jets to hot dogs and other (darkly ironic) forms of consumption and extravagance. He has had a jumbo effect on Western culture, but also symbolizes the complex human-elephant relationship, such as the inspiration for “Dumbo’s” own sad story. We love elephants but our fascination with them can also be their undoing, such as poaching for the ivory trade or mistreatment in captivity. Jumbo’s story writ large is also the story of elephants, and our story to learn from. If anything comes out of my participation in the Jumbo documentary for the public’s benefit, I hope it is increased empathy for how we interact with elephants. They are like us in many ways (maybe over-emphasized with anthropomorphism in many accounts), but also unlike us (maybe even unfathomable) in not only their size and anatomy but also in aspects of their prodigious intellect, emotions and social structure. Elephants aren’t just jumbo spectacles. They are jumbo responsibilities for humans now that we dominate the planet so much.

Want to catch a version of the Jumbo show? I’ll try to keep this list up to date:

BBC iplayer now: https://www.bbc.co.uk/iplayer/episode/b09jcxrj/attenborough-and-the-giant-elephant

BBC One: 5:05pm on January 31st

CBC: 8pm on January 7th– trailer is here:

http://www.cbc.ca/player/play/1115035715562

And the international version is coming soon, plus the above versions surely will circulate globally in some ways.

Have a jumbo time (in a good way) in the rest of 2017 and onwards into 2018!

-John

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An epiphysean Sispyhean task today: solve this mystery that has been bothering me for >15 years. It’s about bird knees. Read on.

Stomach-Churning Rating: 1/10- bones and brief words. Nothing to worry about.

Here is an ostrich. I was interviewing undergrads the other day and looked up to see it, then thought something like: “Oh yeah, that little bit of bone really bothers me. I cannot figure it out.” What little bit of bone?

Right leg, side view, ostrich…

This little bit of bone. Zooming in on that ostrich’s knee:

Who am I? (femur above; tibiotarsus below; “PTE” is the crest of bone with the white arrow on it)

The little bit of bone is not talked about much in the scientific literature on bird knees. But we know it’s there and it is part of the composite bone called the tibiotarsus (ancestral tibia, this bit of bone, and the proximal tarsal [ankle] bones on the other end; the astragalus and calcaneum of earlier dinosaurs).

What is it? We call it something like the proximal tibial epiphysis (PTE for short, here). An epiphysis is an end of a bone that fuses up with the shaft during growth, around the time of skeletal maturity; ultimately ending longitudinal (length-wise) growth of that bone. Mammals almost ubiquitously have them. So do lizards and tuataras. And some fossil relatives. Not much else– except birds, in this particular region (the two ends of the tibiotarsus; also in the foot region; the tarsometatarsus; which also has its share of mysteries such as the hypotarsus; I won’t go there today). You can see the PTE in mostly cartilaginous form if you take apart a chicken drumstick.

This PTE, like other well-behaving epiphyses, fuses with the tibiotarsus in mature birds, forming one bone. But the young ostrich’s knee above shows the PTE nicely; and other living birds show more or less the same thing.

It begs for explanations. I’ve talked about it in a few of my papers. But I’ve always punted on what it really means– does it have anything to do with the patella (they appear at similar times in evolution; we know that much, roughly)? Where does it come from, developmentally? (we sort of know that but more work is needed in different species and in high resolution) When did it evolve? What does it tell us? Why is it there in living birds and almost no other extinct birds/other dinosaurs? Does it have anything to do with why birds, during their evolution, seem to gradually increase the fusion of skeletal elements or ossify new ones (tendons, kneecaps, etc)? Why here and not in the femur or several other long bones of birds? How much do these PTEs vary between (or within) bird species?

This is the challenge in the post’s title. I present to you: solve this puzzle. Developmentally, biomechanically, evolutionarily, genetically, whatever– why does this PTE happen? There are hints– e.g. this paper proposes why growth rates of long bones favour the formation of “secondary centres of ossification” like this. But I’m unable to satisfy myself with any solutions I can find. Maybe you can complete The Bird Knee Challenge?

Have a go at it in the Comments below! There are plenty of papers or even a grant or something involved in sorting out this single mystery; one of the many basic mysteries about animal anatomy.

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Uh oh, a “why?” question in biology! There are many potential, and not mutually exclusive, answers to such questions. Ultimately there is a historical, evolutionary answer that underpins it all (“ostriches evolved two kneecaps because…”). But we like ostrich knees and their funky double-kneecaps (patellae; singular = patella) so we wanted to know why they get so funky. One level of addressing that question is more like a “how?” they have them. So we started there, with what on the surface is a simple analysis. And we published that paper this week, with all of the supporting data (CT, MRI, FEA).

Stomach-Churning Rating: 6/10 because there is a gooey image of a real dissection later in the post, not just tidy 3D graphics.

First author Kyle Chadwick was my research technician for 2 years on our sesamoid evolution grant, and we reported earlier on the detailed 3D anatomy of ostrich knees (this was all part of his MRes degree with me, done in parallel with his technician post). Here, in the new paper with Sandra Shefelbine and Andy Pitsillides, we took that 3D anatomy and subjected it to some biomechanical analysis in two main steps.

Ostrich (right) knee bones. The patellae are the two knobbly bits in the knee.

First, we used our previous biomechanical simulation data from an adult ostrich (from our paper by Rankin et al.) to estimate the in vivo forces that the knee muscles exert onto the patellar region during moderately large loading in running (not maximal speed running, but “jogging”). That was “just” (Kyle may laugh at the “just”– it wasn’t trivial) taking some vectors out of an existing simulation and adding them into a detailed 3D model. We’ve done similar things before with a horse foot’s bones (and plenty more to come!), but here we had essentially all of the soft tissues, too.

Ostrich knee with muscles as 3D objects.

Second, the 3D model that the muscular forces were applied to was a finite element model: i.e., the original 3D anatomical model broken up into a mesh, whose voxels each had specific properties, such as resistance to shape change under loading in different directions. The response of that model to the loads (a finite element analysis; FEA) gave us details on the stresses (force/area) and strains (deformations from original shape) in each voxel and overall in anatomical regions.

Finite element model setup for our study. If you do FEA, you care about these things. If not, it’s a pretty, sciencey picture.

The great thing about a computer/theoretical model is that you can ask “what if?” and that can help you understand “how?” or even “why?” questions that experiments alone cannot address. Ostriches aren’t born with fully formed bony kneecaps; indeed those patellae seem to mature fairly late in development, perhaps well after hatching. We need to know more about how the patellae form but they clearly end up inside the patellar (knee extensor) tendon that crosses the knee. So we modelled our adult ostrich without bony patellae; just with a homogeneous patellar tendon (using the real anatomy of that tendon with the bony bits replaced by tendon); and subjected it to the loading environment for “jogging”.

The right knee of an ostrich hatchling. The patellae have yet to form; indeed there is little bone around the knee region at all, yet.

We then inspected our FEA’s results in light of modern theory about how tissues respond to loading regimes. That “mechanobiology” theory, specifically “tissue differentiation”, postulates that tendon will tend to turn into fibrocartilage if it is subjected to high compression (squishing) and shear (pushing). Then, the fibrocartilage might eventually be reworked into bone as it drops the compression and shear levels. So, according to that theory (and all else being equal; also ignoring the complex intermediate states that would happen in reality), the real ostrich’s kneecaps should be located in the same positions where the FEA, under the moderately large loads we applied, predicts the homogeneous tendon to have high compression and shear. But did the real anatomy match the mechanical environment and tissue differentiation theory’s predictions?

Tissue differentiation diagram displaying the theoretical pathways for transformation of tissues. If tendon (red) experiences high shear (going up the y-axis) and high compression (going toward the left), it should turn into fibrocartilage (purple). Transformation into bone (diagonally to the bottom right) would reduce the shear and compression.

Well, sort of. The image below takes some unpacking but you should be able to pick out the red areas on the bottom row where the patellae actually are, and the yellow shaded regions around some of those patellar regions are where the compression and shear regimes are indeed high and overlapping the actual patellar regions. The upper two rows show the levels of compression (or tension; pulling) and shear, but the bottom row gets the point across. It’s not a bad match overall for the first (“real”; common to all living birds) patella, located on top of the upper knee (femur). It’s not a good match overall for the second (unique to ostriches) patella, located below the first one (and attached to the tibia bone).

FEA results! (click to embiggen)

Kyle says, “Being a part of this project was exciting because of the application of engineering concepts to interesting biological (including evolutionary) questions. Also, it never gets old seeing people’s reactions when I tell them I study ostrich knees.

The study had a lot of nuances and assumptions. We only looked at one instant in slow running and only at one adult ostrich, not at the full development of ostrich anatomy and loading. That’s harder. We started simple. The tissue differentiation theory is used more for fracture healing than for sesamoid bone formation but there’s some reason to suspect that similar mechanisms are at play in both. And there’s much more; if you want the gory details see the paper.

So did we solve why, or how, ostriches have two kneecaps? We felt that the mechanical environment of our FEA was a good theoretical explanation of where the first patella forms. We originally expected the second patella, which evolved more recently and might be more mechanically sensitive as a result, to be a better match than the first one, but it was the opposite. C’est la science!

Enough models, let’s have some reality! I warned you this post would get messy, and here it is. Left leg (skinned) of an ostrich showing the muscles around the knee. The patellar region would be in the gloved hand of the lucky individual shown.

This study, for me, was a fun experience in moving toward more fusion of “evo-devo” and biomechanical analyses, a research goal of mine lately– but there’s still a ways to go with the “how?” and “why?” questions even about ostrich kneecaps.

We felt that the best conclusion supported by our analyses was that, rather than have homogeneous stresses and strains throughout their knee tissues (e.g. the patellar tendon), ostriches have a lot of regional diversity in how those tissues are loaded (in the condition we modelled, which is adequately representative of some athletic exertion). Look at the complex FEA coloured results above again, the top two rows: there are a lot of different shades of compression/tension and shear; not homogeneous strains. That diversity of regional loading sets those tissues up for potential transformation throughout growth and development. And thus ONE of the reasons why ostriches might have two kneecaps is that the heterogeneous loading of their knee tendon favours formation of heterogeneous tissue types.

Another, compatible, explanation is that these different tissues might have consequences for how the muscles, tendon and joint operate in movement behaviours. In due time there will be more about that. In the meantime, enjoy the paper if this post makes you want to know more about the amaaaaaazing knees of ostriches!

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A Confuciusornis fossil; not the one from our study but prettier (more complete).

Today almost three years of collaboration come together in a publication that is a fun departure from my normal research, but also makes sense in light of it. Professor Baoyu Jiang from Nanjing University in China has been being working on the taphonomy of the Early Cretaceous Jehol biota from northeastern China (Manchuria) for a while, and he found a lovely Confuciusornis (early bird) fossil; one of thousands of them; from the volcanic pyroclastic flow-based lake deposits there.

Although at first glance the skeletal remains of that fossil are not fabulous compared with some other Confuciusornis, what makes this one lovely is that, on peering at it with multiple microscopic and other imaging techniques, he (and me, and a China-UK collaboration that grew over the years) found striking evidence of very well-preserved fossil soft tissues. Our paper reporting on these findings has gone live in Nature Communications so I can blog about it now.

Reference: Jiang, B., Zhao, T., Regnault, S., Edwards, N.P., Kohn, S.C., Li, Z., Wogelius, R.A., Benton, M., Hutchinson, J.R. 2017. Cellular preservation of musculoskeletal specializations in the Cretaceous bird Confuciusornis. Nature Communications 8:14779. doi: 10.1038/NCOMMS14779

Stomach-Churning Rating: 3/10; gooey, but fossil gooey, except for some colourful, gastrically-tolerable histology of bird tissue.

Front view of the ankle/foot of our specimen.

Back view of the ankle/foot of our specimen.

What has been fun about this collaboration is that, for one, it fits in perfectly with my prior work. Ever since my PhD thesis I’d been wondering about odd bones in the legs of birds, including a very puzzling and very, very neglected bit of bone called the tarsal sesamoid, on the outside of the upper end of the ankle joint. Furthermore, a tunnel of tissue called the tibial cartilage sits next to that sesamoid bone, and then across the ankle joint there is a bony prominence with grooves and tunnels that vary highly among bird species; that is called the hypotarsus. These structures are all known in living birds and, to a degree, in extinct fossil cousins. Our specimen seems to reveal an earlier stage in how these little features of bird ankles originated, which we concluded to be a step along the transition to the more crouched legs that modern birds have.

This study has also challenged me to broaden my horizons as a scientist. Although this was a big collaboration and thus we had several specialists to apply supercharged technological techniques to our fossil, I had to learn something about what all that meant. My kind colleagues helped me learn more about tissue histology, scanning electron microscopy, synchrotron mapping, FTIR and mass spectrometry and more. I won’t go through all of these techniques but there are some pretty pictures sprinkled here and in the paper, and a lot more detail in the paper for those who want the gory techno-detail. Basically we threw the kitchen sink of science at the fossil to crack open some of its secrets, and what we found inside was nifty.

Scanning electron micrograph image of probable tendon or ligament fibres (arrow) in cross-section, from near the ankle joint.

We found preserved cells and other parts of connective tissues including tendons and/or ligaments, fibrocartilage (the tougher kind) and articular cartilage (the softer joint-padding kind). That’s great, although not unique, but the kitchen sink also flushed out even more reductionist data: those tissues included some organic residues, including what appear to be bits of proteins (amino acids); particularly the collagen that makes up tendons.

Fibrocartilage (“fc”) from the ankle joint region.

Hopefully we’re right, and we included as much of the data as we could manage so that others can look at our findings. The specimen is crushed into nearly two dimensions, like all Jehol biota organisms, so its anatomy was hard to interpret but we think we got it right. All of the other kitchen-sinky tools have their own nuances and pitfalls but we did our best with a superb team of experts. We’ve had to wait 125 million years to uncover this specimen and a few more years to find out if we’ve looked at the right way is no greater test of patience.

I thank my coauthors, especially Baoyu Jiang for the kind invitation to participate and the very fun experience of collaborating. I think I’ll remember this study for a long time because, for me, it takes a step beyond just describing Another Case of Jaw-Dropping Fossilization (can you hear the hipsters recounting the excitement and cynicism of the 1990s when this all was dawning? I was there and maybe now I’m one of them). By combining all of those methods we learned new things about the palaeobiology of birds and the evolution of traits within birds. Confuciusornis, not shockingly, had ankles that should have functioned in ways intermediate between those of bog-standard non-avian theropods and modern birds.

Same anatomical regions in an extant bird as in the main fossil specimen. Left distal tibiotarsus (TT; below) and proximal tarsometatarsus (TMT; above) from an adult helmeted guineafowl (Numida meleagris) after formalin fixation. (from our paper’s Supp Info)

I’m hopeful that more synthesis of molecular/cellular, imaging, biomechanical and other tools (not to mention good old palaeontology and anatomy!) can wash away some more of this mystery. And it was fun to be a part of a study that adds to overwhelming evidence that was heretical ~25 years ago: some hardy biomolecules such as collagen and keratin can survive hundreds of millions of years, not just thousands. Pioneers such as Prof. Mary Schweitzer led the original charge that made reporting on discoveries like ours much easier today.

I know how the birds fly, how the fishes swim, how animals run. But there is the Dragon. I cannot tell how it mounts on the winds through the clouds and flies through heaven. Today I have seen the Dragon.“– Confucius, ca. 500 BCE.

Let’s finish with some images of a living bird’s ankle region, by co-author and PhD student Sophie Regnault. We considered these for inclusion in the paper but they didn’t fit quite right. I love them anyway so here they are:

Patchwork of histology slide images, from a guineafowl’s ankle (as per photo above). The numbered squares correspond to zoomed-in images below. The tibiotarsus is on the proximal end (bottom left); the tarsometatarsus is on the distal end (right side); and the enigmatic tarsal sesamoid is at the top. Magnification: 20x overall.

Region 1. nice (fibro)cartilage-bone inferface at ligament insertion.

Region 2: longitudinal slice through ligaments connecting the tibiotarsus to the tarsometatarsus across the ankle joint.

Region 3: front (bottom) of the tibiotarsus/upper ankle.

Region 4: tendon fibres in longitudinal section; on the back of the tibiotarsus. Some show mineralization into ossified tendons (“metaplasia”); another curious feature of modern birds.

Region 5: muscle attachment to the back of the upper tarsometatarsus bone. Small sesamoid fragment visible.

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