Tetrapod Zoology

i-c8f11b845c73b99e16b3f162e3fd5018-Lee & Werning allosaur fig.jpg

It seems that this story is already all over the internet – I would have posted on it sooner this morning but was busy with amphibians! Anyway… back in 2005 Mary Schweitzer and colleagues dropped a bombshell into the world of dinosaur palaeontology: they reported the discovery of medullary bone within a Tyrannosaurus rex specimen (Schweitzer et al. 2005). Medullary bone is a specialized, densely mineralized, highly vascularized tissue laid down on the endosteal surface of long bones: its formation is triggered by hormones that are produced during ovulation, and it functions as a calcium store used in eggshell production. It was always thought unique to birds (though, incidentally, some palaeontologists had speculated that we should at least look for it in nesting dinosaur fossils (Martill et al. 1996)). However – as with quite a few traits of behaviour and anatomy conventionally thought unique to birds – its discovery in T. rex (a non-avian coelurosaurian theropod) has changed that. A new study, published today, takes this research to the next level…

[the image used above shows a cross-section through an Allosaurus tibia and reveals growth rings and the position of medullary bone. This individual died at 10 years old. Silhouettes indicate the relative sizes of a juvenile and a fully-grown Allosaurus. From the UC Berkeley newscenter site.]

I went to a talk given by Mary on the subject of medullary bone a few years ago. Firstly, having seen giant on-screen projections of the T. rex medullary bone compared with the medullary bone of extant birds, I can’t see how the T. rex tissue can be anything other than medullary bone. Secondly, the audience at the talk included comparative endocrinologists and histologists, and not just palaeontologists. While the latter are mostly unfamiliar with medullary bone, the others aren’t, and I note that they were in strong agreement with the identification. If medullary bone is present in tyrannosaurs, then by inference it presumably must also occur in many other coelurosaurs, given that most of them are closer to birds than tyrannosaurs are. Has it been found in other theropods, or in other non-avian archosaurs? A careful and thorough search failed to find it in crocodyliforms (Schweitzer et al. 2006).

i-6049168fb09ad8d43556009c7efc3efc-medullary bone in tyrannosaur.jpg

But in a new study published today, Andrew Lee and Sarah Werning at the University of California report medullary bone in a non-coelurosaurian theropod (Allosaurus) and, more excitingly, in an ornithischian (Tenontosaurus). This indicates that the production of medullary bone goes back to the Triassic common ancestor of Ornithischia and Saurischia at least [adjacent image shows - at top - medullary bone in a chicken (it's the red spongy-looking stuff) with the medullary bone of a tyrannosaur below].

But the paper does a lot more than simply report new occurrences of medullary bone. Recent work on dinosaur growth rates (primarily based on counts of growth lines seen in bone sections) have shown that dinosaurs grew surprisingly quickly, with sauropods and hadrosaurs for example growing at rates comparable to placental mammals and precocial birds (Erickson et al. 2001, 2007, Sander et al. 2004). The presence of medullary bone in three non-avian dinosaurs now allows us to demonstrate sexual maturity in these taxa, and by counting growth lines we can go better and say exactly how old they were when they reached this age: Lee & Werning (2008) show that Tenontosaurus, Allosaurus and Tyrannosaurus were respectively 8, 10 and 18 years old when they were at sexual maturity (note that the presence of medullary bone doesn’t necessarily mark the onset of sexual maturity, as the animals might have been producing it when they were even younger).

i-28cca3f0b2d7adea6ae8361dc900beb7-Lee & Werning tenontosaur fig.jpg

Particularly interesting is that the inferred presence of sexual maturity in these dinosaurs does not correlate with asymptotic growth – at the ages given above, the animals were about half of full adult size, so they still had a way to go before growth stopped (asymptotic growth can be determined from bone histology by the presence of an external fundamental system or by tightly spaced growth lines at the bone’s outer edges). In other words, these dinosaurs were, potentially, teenage parents [adjacent image shows cross-sections through Tenontosaurus tibia, again showing growth rings and medullary bone. This individual was 8 years old when it died. Also from the UC Berkeley newscenter site].

The study goes one stage further. By using this sexual maturity data, Lee & Werning compared the estimated growth rates of these dinosaurs to those seen in extant non-avian reptiles. We know from their bone histology that dinosaurs grew quickly: however, if non-avian dinosaurs grew like scaled-up conventional reptiles, sexual maturity would have occurred decades later than what’s indicated by the presence of medullary bone. In fact, Lee & Werning estimate that Tenontosaurus, Allosaurus and Tyrannosaurus would have reached sexual maturity at 82, 87 and 218 years respectively if they grew like conventional reptiles (I’m not going into all the details here, you’ll need to see the paper if you want that). Indeed, if big dinosaurs grew like conventional reptiles (i.e., if we scaled conventional reptiles to tenontosaur, allosaur or tyrannosaur sizes), they’d have to reach sexual maturity at something like one-tenth of full size, and would have to keep growing for five to ten decades. These predictions are exactly the opposite of what the evidence indicates.

i-11cbd724617fece3e339ff4e52278c08-dinosaur growth curves from erickson et al.jpg

The new data showing that tenontosaurs, allosaurs and tyrannosaurs were all able to reproduce before reaching full adult size agrees with other lines of evidence. Animals that breed before reaching asymptotic size tend to suffer from high mortality as adults – there is therefore a rush to reproduce. And indeed what we know indicates that even adult mortality was high in dinosaurs: as Tom Holtz says, life was cheap in the Mesozoic. The onset of sexual maturity when young also means that particularly big dinosaurs – like giant sauropods – could have started reproducing before they grew to full ridiculous size. Modern birds have since evolved to do things differently, as they effectively obtain asymptotic growth by the time they leave the nest (though, incidentally, data indicates that this wasn’t the case for basal birds like archaeopterygids) [adjacent image shows dinosaur growth curves: note exponential growth early in development followed by achievement of asymptotic size. These graphs are from Erickson et al. (2001) and were borrowed from here on the Nature site].

There’s a lot more in Lee & Werning (2008) than I’ve hastily summarized here, but it’s an excellent study that adds a lot to our growing view (no pun) of dinosaur biology. Of course, all this stuff about rapid growth leads on to all those awkward questions about metabolic rates and endothermy. After all, all good scientists are inherently sceptical of the silly notion that dinosaurs might have been endothermic aren’t they……. to be continued….

Thanks to Sarah for help with this, and congrats!

Refs – -

Erickson, G. M., Curry Rogers, K., Varricchio, D. J., Norell, M. A. & Xu, X. 2007. Growth patterns in brooding dinosaurs reveals the timing of sexual maturity in non-avian dinosaurs and genesis of the avian condition. Biology Letter 3, 558-561.

- ., Curry Rogers, K. & Yerby, S. A. 2001. Dinosaurian growth patterns and rapid avian growth rates. Nature 412, 429-433.

Lee, A. H. & Werning, S. 2008. Sexual maturity in growing dinosaurs does not fit reptilian growth models. Proceedings of the National Academy of Sciences 105, 582-587.

Martill, D. M., Barker, M. J. & Dacke, C. G. 1996. Dinosaur nesting or preying? Nature 379, 778.

Sander, P. M., Klein, N., Buffetaut, E., Cuny, G., Suteethorn, V. & Le Loeuff, J. 2004. Adaptive radiation in sauropod dinosaurs: bone histology indicates rapid evolution of giant body size through acceleration. Organisms, Diversity & Evolution 4, 165-173.

Schweitzer, M. H., Dacke, C., Horner, J. & Lamm, E. 2006. Do egg-laying crocodilian (Alligator mississippiensis) archosaurs form medullary bone? Bone 40, 1152-1158.

- ., Wittmeyer, J. L. & Horner, J. R. 2005. Gender-specific reproductive tissue in ratites and Tyrannosaurus rex. Science 308, 1456-1460.


  1. #1 Jerzy
    January 15, 2008

    I wonder if rapid growth means that sauropods somehow fed their offspring. Pretty difficult to sustain growth speed like blue whale otherwise…

    I intuitively thought that medullary bone is somehow associated with that birds produce egg clutch approaching own weight within one – two weeks. Dinosaur egg clutches appear much smaller in relation to body size. So why the bone? How many eggs dinos really laid? Or maybe this bone in dinos had different purpose?

  2. #2 John Conway
    January 15, 2008

    Medullary bone in pterosaurs, that’s what we want to see.

  3. #3 Thylacine
    January 15, 2008

    Awesome post! This is what obsessively check the blog for three times a day! Thanks for the Fix!

  4. #4 David Marjanovi?
    January 15, 2008

    I wonder if rapid growth means that sauropods somehow fed their offspring. Pretty difficult to sustain growth speed like blue whale otherwise…

    The following book chapter says these growth rates are overestimates:

    Thomas M. Lehman: Growth and Population Age Structure in the Horned Dinosaur Chasmosaurus, 259 — 317 in Kenneth Carpenter (ed.): Horns and Beaks. Ceratopsian and Ornithopod Dinosaurs, Indiana University 2007

    It also says a lot of other interesting stuff…

    Medullary bone in pterosaurs, that’s what we want to see.

    In the absence of hard eggshells?

  5. #5 Darren Naish
    January 15, 2008

    The following book chapter says these growth rates are overestimates:

    I know, did you read my review of this volume (here, pp. 121-125). In the discussion of taxa named after Crichton and Jurassic Park, I forgot about Crichtonsaurus. D’oh!

    On pterosaurs and medullary bone.. Lorna Steel looked for it in as many specimens as she could and never found it. I know, negative evidence.

  6. #6 Michael P. Taylor
    January 15, 2008

    The idea that sauropods may have fed their offspring in order to achieve their astonishing growth rates has come up once or twice before. In light of the “crop milk” of pigeons and some other birds, and the “exo-milk” of some caecilians (which I only learned about a few days ago on TZ) plus of course the True Milk of mammals, it doesn’t seem wholly impossible that something analogous could have evolved in non-avian dinosaurs, too. (Darren and I once had a long-running email thread on this topic, under the subject The Nourishing Vomit of Eucamerotus … which I always thought would make a good name for a magic widget in a poorly written Epic Fantasy series.)

    The problem with this idea (well, a problem) is, do we have any evidence at all for any kind of parental care in sauropods? In ornithopods you have Horner’s partially trampled and, to be fair, also partially rebutted nests; and of course there are all those great family-group Chinese dinosaur nests, including both theropods and ceratopsians. But I can’t offhand think of anything similar in sauropod-world. Nor in thyreophorans, for that matter.

  7. #7 Martin R
    January 15, 2008

    How cool! Thanks!

  8. #8 Zach Miller
    January 15, 2008

    I love it! Perhaps teenage pregancies led to the downfall of the Dinosauria. Unwed teenage mother tyrannosaurs trying to survive without a…man…I can’t keep this up.

    Awesome paper, though, and certainly adds to what we already know! Darren, could I get the paper from you? PLoS wants a subscription, which I’m unwilling to give.

  9. #9 David Marjanovi?
    January 15, 2008

    did you read my review of this volume

    No, I’m not a member and didn’t know the newsletter even existed. Thanks a lot for the link, it contains several interesting articles!

    What I alluded to were the metabolic conclusions that Lehman draws. Why didn’t you mention them in your review? Anyway, I’ll try to write a lengthy DML post about them later this week.

  10. #10 David Marjanovi?
    January 15, 2008

    PLoS wants a subscription


  11. #11 Sven DiMIlo
    January 15, 2008

    the metabolic conclusions that Lehman draws. Why didn’t you mention them in your review?

    Why didn’t you mention them in your comment? What is DML?

  12. #12 Sven DiMIlo
    January 15, 2008

    all good scientists are inherently sceptical of the silly notion that dinosaurs might have been endothermic aren’t they

    Well, I know that I am–for sauropods at least. Looking forward to the alluded-to post on metabolic rates…

  13. #13 Nathan Myers
    January 15, 2008

    Hasn’t it already been established on physical grounds that critters as big as sauropods would find it difficult not to be more or less endothermic, in the sense that shedding heat would be harder for them than retaining it? (Could the neck have functioned as a heat-radiating surface?) Also, given their diet, mightn’t coprophagy suffice to feed the wee ones?

  14. #14 Michael P. Taylor
    January 15, 2008

    Zach, it’s in PNAS (Proceedings of the National Academy of Sciences), not PLoS (Public Library of Science).

    David, you (and everyone) ought to be a member of PalAss. It’s not expensive, and it includes a subscription to Palaeontology, the world’s leading journal of new sauropod taxa established on single partial vertebrae. (Source: Thomson Scientific.)

    Sven, DML = Dinosaur Mailing List, an Internet mailing list for the discussion of (mostly Mesozoic) dinosaurs. See http://dinosaurmailinglist.org/

    Sven again: if you contend that sauropods were not bradymetabolic, you have a lot of explaining to do about their growth rates. Even allowing for the reputiation of some studies that recovered very fast rates, there is still plenty of evidence that they grew as fast as the fastest-growing placental mammals. How?

    Nathan, your suckling-substitute hypothesis is pretty foul … but neat :-) You would probably find Greg Paul’s 1998 paper “Terramegathermy and Cope’s Rule in the land of titans” (Modern Geology 23:179-217) interesting. Paul argues that endothermy is a prerequisite of large size on land, and to be fair all our empirical evidence seems to support this: the largest known terrestrial unambiguous ectotherms weighed in at a weedy 1 tonne.

  15. #15 Nathan Myers
    January 15, 2008

    The idea of juvenile ruminant coprophagy can’t possibly be original to me, can it? Considering what human teenagers are seen to eat, coprophagy can’t be much of a stretch for any chordate to adopt.

    I find in “Coprophagy as an avenue for foals of the domestic horse to learn food preferences from their dams” [here].

    “Coprophagy of the foal on maternal faeces does, however, correspond chronologically with the foal learning to graze selectively. This correspondence suggests that, as well as other uses, in domestic horses coprophagy may function to imprint on the foal the food-selective values of its dam.”

    Apparently it’s also a normal part of rabbit, rat, beaver, and dog weaning, besides being part of their day-to-day life. I don’t recommend being reincarnated as one of these creatures.

  16. #16 Christopher Taylor
    January 16, 2008

    Apparently it’s also a normal part of rabbit, rat, beaver, and dog weaning

    Also koalas, who apparently eat nothing else for a period. I believe the reason is that the second-hand exposure to eucalyptus allows them to build up immunity to the toxins therein before moving on to the hard stuff.

  17. #17 Tengu
    January 16, 2008

    Well, that would make sense

    but Im not so sure in sauropods; they would have had such high food needs that I expect their systems were super efficient, with dung (albeit in large quantities) only suitable for roses.

    I favour regurgitation. easier to control

  18. #18 Jerzy
    January 16, 2008

    The problem with this idea (well, a problem) is, do we have any evidence at all for any kind of parental care in sauropods?

    Well, mammary glands don’t fossilise. It’s pretty difficult to find what would be good evidence of parental feeding and could fossilize.

    (thinking, thinking)

    Did anybody compare tooth wear of juvenile and adult sauropods? This would be interesting.

    Corpophagy – well, digestible nutrients were already removed from faeces. Unless sauropods developed diarrhoea as parental care ;-)

    BTW, interestingly, growth rings also show that Allosaurus lived in seasonal environment. Curious.

  19. #19 Raymond
    January 16, 2008

    “Corpophagy – well, digestible nutrients were already removed from faeces. Unless sauropods developed diarrhoea as parental care ;-)”

    -Pray that the OZGawd never comes across this sentence.-

  20. #20 David Marjanovi?
    January 16, 2008

    Why didn’t you mention them in your comment?

    Due to chronic lack of time.

    Sven again: if you contend that sauropods were not bradymetabolic

    Tachymetabolic (fast metabolism), you mean.

    I have free online access to Palaeontology here in the lab…

    BTW, interestingly, growth rings also show that Allosaurus lived in seasonal environment.

    No, in crocodiles the growth rings are endogenous: they appear even under laboratory conditions. However, the Morrison Fm environment was seasonally dry.

  21. #21 DDeden
    January 16, 2008

    Coprophagy is also in gorillas, I thought beneficial to transfer symbiotic bacteria.

    Marine reptiles (Plesiosaur, mososaur, ichthyosaur) lacked medullary bone growth, then, since they had no hard shell eggs? While sea turtles would have it?

    Carnivorous dinosaurs that relied on stomach acids rather than chewing to process food would be more likely to regurgitate food to young (penguin milk) I’d think.

  22. #22 Matt Wedel
    January 16, 2008

    Marine reptiles (Plesiosaur, mososaur, ichthyosaur) lacked medullary bone growth, then, since they had no hard shell eggs? While sea turtles would have it?

    No, not everything that lays hard shelled eggs has medullary bone. Crocs resorb existing bone tissue to get calcium for laying eggs, and presumably turtles do the same. Medullary bone appears to be a way to avoid raiding your skeleton for calcium, by stocking some up in advance. As Darren explained above, medullary bone is so far only known in dinosaurs. It might prove to be more widely distributed, but all of those marine reptiles are pretty far out, phylogenetically (they’re pretty far out physically, too ;-). A lot more distant than crocs, which lack medullary bone.

  23. #23 Noni Mausa
    January 16, 2008

    … do we have any evidence at all for any kind of parental care in sauropods?

    Perhaps the nestful of newly-hatched carnivores made deceptively helpless baby-bird or baby-kitten noises — then leapt out en masse and ate the smaller carnivores who came looking for them! Yeah!


  24. #24 Nathan Myers
    January 16, 2008

    I suspect some here haven’t grasped the point of coprophagy, or indeed of rumination. The point, as I understand it, is that the nutrients aren’t actually available in the plant material consumed, but are made accessible or actually produced by fermentation in the gut. I.e. ruminants are not really consuming and digesting plants; rather, they may be said to be feeding and then consuming colonies of bacteria. (Humans are not entirely exempt from this description.) Therefore, manure may be more directly nutritious than raw plants, particularly to a creature with a short, immature gut.

    Regurgitation is practical for creatures whose food needs little digestion.

    I find related terms: caecotropy (the reingestion of soft feces or caecotrophs) and allocoprophagy (eating the feces of others).

  25. #25 Matt Wedel
    January 16, 2008

    Corpophagy – well, digestible nutrients were already removed from faeces.

    Along the lines of what Nathan Myers just said, there is a lot of recognizable plant material in the feces of big herbivores. I’ve seen some elephant poop that was basically brown grass. And putative sauropod coprolites contain identifiable plant material, too.

    There certainly would have been a lot of sauropod poop around. It would be curious if lots of things weren’t taking advantage of it.

    Do I smell a paper in here?

  26. #26 Nathan Myers
    January 16, 2008

    Is that what papers are made of?

  27. #27 Matt Wedel
    January 16, 2008

    I like your style.

  28. #28 Nathan Myers
    January 17, 2008

    Presuming they are ambulatory upon hatching, we can imagine the wee sauropods just hanging around in the herd, waiting for road apples to drop. Given the size difference, there ought to be plenty for everyone.

    This makes a more faithful “The Land before Time” production a bit more amusing to contemplate. On that note… http://cantrip.org/pancho.html .

  29. #29 Alan Kellogg
    January 17, 2008

    So for immature sauropods getting dumped on was a good thing.

  30. #30 John Scanlon, FCD
    January 17, 2008

    I really like this coprophagy idea, someone please write the book on it. There are all kinds of weird digestion arrangements in herbivores, including kangaroos that keep a load of roundworms in the stomach and digest worm-flesh further back (fide Tim Flannery, I haven’t seen a primary reference).
    As an analogue of medullary bone, consider the gekkonine gekkonids which, in contrast to diplodactylines and most if not all other oviparous squamates, have hard calcareous-shelled eggs. Gekkonines have calcium storage organs (endolymphatic sacs) in the throat, present in both sexes but larger in females just about to oviposit (usually easily visible through the skin from below). It’ll be interesting when these turn up in the fossil record.

  31. #31 Darren Naish
    January 17, 2008

    The Flannery kangaroo reference John has in mind is probably Flannery et al.’s tree kangaroo book. If not, well, it’s discussed in there anyway…

    Flannery, T. F., Martin, R. & Szalay. A. 1996. Tree Kangaroos: A Curious Natural History. Reed Books, Melbourne.

    And I must blog about tree kangaroos one day…

  32. #32 Nathan Myers
    January 17, 2008

    Littlefoot, hurry! Your breakfast is getting cold!”

  33. #33 Darren Naish
    January 17, 2008

    To put a sorry end to this entertaining series of exchanges… baby sauropods (and other herbivorous dinosaurs) quite probably did ingest the faeces of adults because – as herbivores that require symbiotic microbes for digestion – they have to get them somehow and aren’t born with them. In fact it’s been argued that dedicated herbivory (which requires symbiotic microbes in the gut) can only evolve in species where the hatchlings/newborns are in close association with adults, and hence have access to their parent’s droppings (for the record, this theory is flawed in that even precocial babies are quite capable of seeking out and eating faeces on their own thank you very much – and what about the lissamphibians which we now know have symbiotic gut microbes? When they hatched they weren’t in close proximity to their parents).

    But coprophagy isn’t the answer we’re looking for here in that the partially digested remains of adult meals aren’t really going to be providing the sort of nutrition required to fuel super-rapid growth. It’s not the answer – which is why we come back to that nutritious vomit..

    I always think of squid when discussing this area. They grow to full adult size in a really short span of time and die young (e.g., Jackson & O’Dor 2001): a giant squid, for example, might grow to full size in a year. But then… squid grow by constantly adding new muscle fibres, something that tetrapods aren’t too good at…

    Ref – -

    Jackson, G. D. & O’Dor, R. K. 2001. Time, space and ecophysiology of squid growth, life in the fast lane. Vie Milieu 51, 205-215.

  34. #34 Jerzy
    January 17, 2008

    Hot topic ;)

    To make sure – there is difference between eating small bits of sh*t to obtain symbiotic microbes and eating lots of sh*t to obtain nutrients.

    Squids – nice, but squids are carnivores. Their food is more energy-dense.

  35. #35 David Marjanovi?
    January 17, 2008

    kangaroos that keep a load of roundworms in the stomach and digest worm-flesh further back

    :-o :-O :-o :-O :-o :-O :-o

  36. #36 Nathan Myers
    January 17, 2008

    How nutritious could (undigested) sauropod vomitus be? It’s just minimally chopped up leaves, right? Mightn’t the adult ruminant’s manure be allowed to retain much of its original, potential nutritional value, but have been processed to make it available to (e.g.) the offspring? Cf. lagomorphs’ caecotrophs: “The reingested soft feces can then be digested in the stomach and small intestine yielding up to five times as many vitamins as in the original food.”

  37. #37 Graham King
    January 26, 2008

    Re Jerzy’s first commment: could medullary bone in adults have served as a calcium store, not solely for the (low relative mass) eggshells, but also for the bones of rapidly-growing young? If so, what is needed of course is a mechanism of transfer. Regurgitation/excretion of (parental-calcium-enriched) predigested food, or, a de novo calcium-rich ‘milk’ analogue secreted?
    Re Darren’s comment above… given that eggs are laid through the cloaca common to droppings, and that hatchlings may eat their own eggshells on emergence, is there any mileage in the idea that gut bacteria could be transferred adult-to-young by that route? (Of course the bacteria might have to be in spore form to survive their out-of-body experience.)