In the previous post in this series I looked at the some of the easily available raw data on neural spine bifurcation in Morrison sauropods. In this post I’ll explain how serial variation–that is, variation along the vertebral column in one individual–is relevant to the inferences made in the new paper by Woodruff and Fowler (2012). But first, a digression, the relevance of which will quickly become clear.

How do you recognize an adult sauropod?

There are only a handful of criteria that have been used to infer adulthood in sauropods. In rough order from least to most accurate–so far as I can tell!–they are:

1. sheer size
2. fusion of the neural arches to the centra
3. fusion of the sacral vertebrae to each other, and fusion of the sacral ribs to form the sacricostal yoke
4. fusion of the cervical ribs to the centra and neural arches
5. fusion of the scapula to the coracoid
6. presence of an external fundamental system in the cortices of the long bones

I’ll discuss each one in turn. (Please let me know in the comments if I’ve missed any.)

These vertebrae are rather dissimilar in size and form. Click through to find out why.

1. Size alone is pretty useless. The mounted Giraffatitan is a pretty damn big animal by anyone’s standards, but it’s demonstrably smaller than another individual from Tendaguru, and the scap-coracoid joint is unfused. On the other hand, there are things like dicraeosaurids that apparently matured at relatively small sizes (for sauropods). There is definitely some individual or low-level taxonomic variation. Marsh’s “Brontosaurus” excelsus holotype YPM 1980 is an adult but about the same size as the subadult Apatosaurus ajax holotype YPM 1860 that it ended up being generically synonymised with (see the sacra of the two taxa compared below). The giant Oklahoma Apatosaurus is about 1.4 times the size of A. louisae CM 3018 in most linear measures, but some of the neural arches and cervical ribs are unfused (the vertebra in the linked post is only a quarter bigger than the corresponding element in CM 3018, but there are other elements of the Oklahoma Apatosaurus that are proportionally even larger). On the flip side, I have seen some comparatively tiny Diplodocus material at BYU in which all of the neural arches are fused to the centra, despite the vertebrae being about half the size of those in the mounted D. carnegii CM 84/94. So I am very leery of size as a reliable indicator of age in sauropods. It is a bad criterion in general, and especially bad for cervical vertebrae, which can change so much along the column. C15 of D. carnegii CM 84/94 has a cotyle diameter almost four times that of C3 in the same animal.

Sacra of Apatosaurus excelsus YPM 1980 and A. ajax YPM 1860 at the same scale, from Ostrom and McIntosh (1966:plates 27 and 29)

2. People often cite closure of the neurocentral synostoses* as an indicator of adulthood, but again I am skeptical. There’s no doubt that the neurocentral synostoses do eventually close; my skepticism runs the other way, in that there are sauropods with closed neurocentral synostoses that do not appear to have reached full size. The HM SI** individual of Giraffatitan is one example–it’s about 75% of the size of the mounted (SII) individual, and only 66% the size of the giant HM XV2 (by cross-scaling through HM SII; SI and XV2 share no overlapping elements), and yet the neurocentral synostoses are all closed. Same deal with Apatosaurus CM 555, which has open joints as far back as C8 but is between one-half and two-thirds the size of A. louisae CM 3018. If you found a posterior cervical or anterior dorsal of CM 555 by itself, without the open joints on the more anterior vertebrae to guide you, you’d think it was full grown based on arch fusion. So it seems safest to say that neurocentral synostosis closure is a necessary but not sufficient condition for inferring adulthood.

* Hat tip to Jerry Harris, who alerted me that the term ‘sutures’ is reserved for skulls only, and that the joints between neural arches and centra are properly called synostoses. Thanks also to physical anthropologist Vicki Wedel, who confirmed this.

** Yes, I’m using the old Humboldt Museum numbers here, out of convenience, and because HM SII probably means more to more readers than the correct M.B. R. number that only six people have memorized.

3. Coalescence of the sacrum and formation of the sacricostal yoke have intuitive appeal. The sacricostal yokes are banana-shaped bars of bone formed by the union of the sacral ribs that articulate with the ilia–you can see them on either side of the apatosaur sacra in the image above, and in this post on the sacrum of Camarasaurus lewisi. Since the sacricostal yokes are the bony interfaces between the axial skeleton and the hindlimb girdles, we might expect them to be biomechanically important and for their formation to be closely related to the attainment of adult size. But I’m putting them fairly low on the list for reasons both practical and theoretical. On the practical side, fusion of the sacral vertebrae and ribs is hard to assess unless the sacrum has fallen apart. An intact sacrum might be intact because the bones were actually fused together, or because the unfused bits just happened to hang together through the process of fossilization (if that sounds unlikely, just remember that it’s true of almost every articulated fossil skull you’ve ever seen). On the theoretical side, the timing of sacral fusion seems to be variable. A. ajax YPM 1860 has fused neural arches and cervical ribs but a very incompletely fused sacrum, whereas D. carnegii CM 84/94 has the five sacral centra coossified and a sacricostal yoke uniting the ribs of S2-S5*, but some of the cervical ribs are unfused. Yes, I realize that discounting this criterion because it conflicts with other mutually conflicting criteria is a bit wonky, but (1) that’s the essential challenge of doing non-histological skeletochronology on sauropods–none of the signs seem to tell us what we want–and (2) I’m happy to fall back on the practical reason if you find the theoretical one unconvincing. Last item: I have seen both ‘sacricostal’ and ‘sacrocostal’ used in the literature–can anyone make a case for one being more correct than the other? ‘Sacrum’ is from the Latin sacer, ‘sacred’, apparently because the sacra of animals used to be sacrificed to the gods (not sacroficed–maybe there’s my answer?).

*Hatcher (1901) described an 11th dorsal and four sacral vertebrae, but he noted that the 11th dorsal “functions as a sacral” and “is coossified by the centrum with the true sacrals”. The D. carnegii holotype was one of the first nearly complete sauropod skeletons to be monographically described, and it was not yet clear that the typical number of sacrals for the North American diplodocids–and indeed for most other sauropods–is five (some primitve taxa have four, many titanosaurs have six).

4. Cervical rib fusion might be better. Giraffatitan HM SI and Diplodocus CM 84/94 both have their cervical neurocentral synostoses closed, but both have unfused cervical ribs as far back as C5. This suggests that cervical rib fusion proceeded from back to front (in at least those taxa) and that it followed neurocentral fusion. The sole exception that I have seen is a subadult Apatosaurus cervical from Cactus Park in the BYU collections, which has fused ribs but open neurocentral joints.

5. It’s hard to tell if fusion of the scapula to the coracoid is better or worse than cervical rib fusion, because the timing varies among taxa (hence the caveat that these criteria are in rough order). Giraffatitan HM SII has fused neural arches and fused cervical ribs but open scap-coracoid synostoses (yes, again, synostoses rather than sutures) ; Diplodocus CM 84/94 has a fused scap-coracoid but some unfused cervical ribs. This is probably another necessary but not sufficient condition.

6. The gold standard for determining cessation of growth is the formation of an external fundamental system (EFS) in the outer cortex of a bone. Unfortunately that requires destructive sampling (even if only drilling), is time-consuming, and has been done for few individual sauropods.

The upshot of all of the above is that the readily available ways of determining adulthood in sauropods are all inexact and frequently conflict with each other. Neural arch fusion does not indicate full growth–some sauropods appear to have fused their neurocentral joints when they were only two-thirds grown (in linear terms; 30% grown in terms of mass).

For the purposes of this post and the next, I am going to refer to the big mounted skeletons–Apatosaurus louisae CM 3018, Diplodocus carnegii CM 84/94, etc.–and individuals of like size as ‘adults’ to indicate that they had attained adult morphology, without implying that they were done growing or had EFSs, and also not implying that smaller individuals were necessarily subadult. ‘Adult’ here is used a term of convenience, not a biological fact.

Implications of serial changes in bifurcation for isolated elements

From here, this post picks up right where the last one in this series left off, so feel free to refer back to the previous post for any points that are unclear.

In the diplodocids, adults are expected to have unsplit spines as far back as C5, C6 may be only incompletely bifid (e.g., D. carnegii CM 84/94), and the spines in the posterior dorsals are expected to be either very shallowly notched at the tip or completely unsplit. Therefore it is impossible to say that an isolated vertebra belongs to a juvenile individual on the basis of neural spine bifurcation alone. Depending on how one defines “anterior cervical”, one half to one third of anterior cervicals are expected to have unsplit spines even in adults.

Serially comparable dorsal vertebrae in different Camarasaurus species or ontogenetic stages. Left: dorsal vertebra 7 (top) and dorso-sacral (= D11) (bottom) of Camarasaurus supremus AMNH 5760 and 5761 “Dorsal Series II”, both in posterior view, with unsplit neural spines. Modified from Osborn and Mook (1921: plate LXXI). Right: dorsal vertebrae 7-11 of Camarasaurus lewisi holotype BYU 9047 in posterodorsal view, with split spines. From McIntosh, Miller, et al. (1996: plate 5). Scaled so that height of D11 roughly matches that of C. supremus.

In Camarasaurus the picture is less clear. The immense C. supremus AMNH 5761 has unsplit spines in C3-C4 and in the last three or four dorsals, but some of those very posterior dorsals have extremely shallow depressions in the tips of the spines, with little consistency among the four individuals that somewhat confusingly make up that specimen. In the geriatric C. lewisi all of the post-axial presacral neural spines are at least incompletely bifid. Even in the very posterior dorsals there is still a distinct notch in the neural spine, not just a very slightly bilobed tip as in the posterior dorsals of C. supremus. Either this is an interspecific difference or some amount of ontogenetic bifurcation happened well into adulthood; current evidence is insufficient to falsify either hypothesis.  (That’s the trouble with n=1.)

A final thing to note: as I briefly mentioned in the earlier post, it is easier to detect deep bifurcations than shallow ones if the material is broken or incomplete. The neural spine tips are usually narrow, fragile, and easily broken or lost. If a vertebra is missing the top half of its spine but the bottom half is not split, it is usually impossible to say whether it would have been bifid or not. But if the spine is deeply bifurcated, even a small piece of bone from the base of the trough or one of the metapophyses is enough to confirm that it was bifid.

“Primitive” morphology can be an effect of serial position

Even in ‘adult’ sauropods like the big mounted Apatosaurus and Diplodocus skeletons, the anterior cervicals are less complex than the posterior ones. Compared to posterior cervicals, anterior cervicals tend to have simpler pneumatic fossae and foramina, fewer laminae, and unsplit rather than bifid spines. In all of these things the anterior cervicals are similar to those of juveniles of the same taxa, and to those of adults of more basal taxa. This is also true in prosauropods–in Plateosaurus, the full complement of vertebral laminae is not present until about halfway down the neck (see this subsequent post for details).

An important implication of this is that an isolated cervical might look primitive (1) because it comes from a basal taxon, or (2) because it is from a juvenile, or (3) because it is from near the front of the neck.

Woodruff and Fowler (2012:Fig. 2)

In their Figure 2, Woodruff and Fowler (2012) compare an adult Mamenchisaurus cervical, an isolated cervical of a putative juvenile Diplodocus (MOR 790 8-10-96-204), and a cervical of D. carnegii CM 84/94. The point of the figure is to show that the isolated ‘juvenile’ vertebra is more similar in gross form  to the Mamenchisaurus cervical than to the adult D. carnegii cervical.

Unfortunately the figure confuses ontogenetic and serial variation. Based on the proportions of the centrum and the shape of the neural spine, the isolated MOR cervical is probably from a very anterior position in the series. No measurements are given in the paper or supplementary information (grrr), but using the scale bar in the figure I calculate a centrum length of about 28 cm, a cotyle height of 7 cm, and an elongation index (EI, centrum length divided by cotyle diameter) of 4. That EI, combined with the overall shape of the neural spine and the very long overhang of the prezygapophyses, make the vertebra most similar to C4 and C5 of D. carnegii CM 84/94. But the D. carnegii cervical included in the figure is C12. It differs from the isolated cervical in having a forward-leaning, bifurcated neural spine, a much more complicated system of laminae with many accessory laminae, and more complex pneumatic sculpturing. All of these differences are more likely to be caused by serial variation than by ontogeny–the same characters separate C12 from C4 and C5 in the same individual.

Diplodocus carnegii CM 84/94 cervicals 2-15 in right lateral view, from Hatcher (1901:pl. 3)

So here’s how that figure would have looked, had the comparable C5 of CM 84/94 been used instead of C12:

Woodruff and Fowler (2012:Fig. 2), with Diplodocus carnegii CM 84/94 C12 replaced by C5.

It’s now immediately apparent B more closely resembles C than A, in the possession of overhanging prezygapophyses, non-overhanging postzygapophyses, elongation index, anterodorsal inclination of the cotyle margin, lack of anterior deflection of diapophysis, etc. The biggest differences between B and C are the shape of the neural spine and, for want of a better word, the ‘sinuosity’ of the ventral centrum margin in lateral view. Both characters are highly variably serially within an individual, among individuals in a species, and among species in Apatosaurus and Diplodocus, so it is hard to attach much weight to them.

What is MOR 790 8-10-96-204?

It gets more complicated. The isolated MOR vertebra is presented as an example of juvenile morphology. But does it actually belong to a juvenile?

Here’s what we know for certain about the vertebra:

• it has an EI of 4 (this is a proportion, so it’s still accurate even if the scale bar is off)
• the cervical ribs are fused to the neural arch and centrum

In addition, the figure appears to show that:

• it has a centrum length of 28 cm, although this could be off if the scale bar is incorrectly sized (which is why I prefer measurements to scale bars)
• the neural arch appears to be fused to the centrum. Admittedly, the image in the figure is small and I haven’t seen the specimen in person. But we know this much: the centrum and neural arch stayed together through the process of preservation and preparation, which does not usually happen unless they have at least started coossifying; the photo does not show an obvious line of fusion between the centrum and neural arch; and the cervical ribs are fused, which in almost all sauropod vertebrae happens after closure of the neurocentral synostoses.

Now, as we’ve just seen above, the morphology of MOR 790 8-10-96-204 is indistinguishable from the morphology of an anterior cervical vertebra in an adult, and it compares especially well to C4 and C5 of D. carnegii CM 84/94. The apparent centrum length (measured from the scale bar in the figure) of MOR 790 8-10-96-204 is 28 cm, compared to 29 cm and 37 cm for C4 and C5 of D. carnegii CM 84/94, respectively. So MOR 790 8-10-96-204 is roughly the same size as the adult C4 and about 80% of the size of the adult C5. Furthermore, its neural arch appears to be fused and its cervical ribs are fused to the neural arch and centrum, whereas the cervical ribs of the ‘adult’ D. carnegii CM 84/94 are not yet fused in C2-C5.

In sum, the isolated MOR vertebra shown in Woodruff and Fowler (2012:Fig. 2) is most likely a C4 or C5 of an adult Diplodocus similar in size to D. carnegii CM 84/94, and based on cervical rib fusion it may be from an individual that is actually more mature than CM 84/94. All of the differences between that vertebra and the D. carnegii C12 shown in the same figure are more easily explained as consequences of serial, rather than ontogenetic, variation.

MOR 790 8-10-96-204 and the Mother’s Day Quarry

MOR 790 8-10-96-204 is from the Mother’s Day Quarry (Woodruff and Fowler 2012:Table 1), which is supposed to only contain juvenile and subadult sauropods (Myers and Storrs 2007, Myers and Fiorillo 2009). Myers and Fiorillo (2009:99) wrote:

The quarry has a strikingly low taxonomic diversity, with one sauropod taxon and one theropod taxon present. However, the relative abundance of elements from these taxa is so uneven – diplodocoid sauropod material comprises 99% of the recovered bones – that the quarry is effectively monospecific (Myers and Storrs, 2007). The theropod material consists of isolated teeth only and is probably related to scavenging of the sauropod carcasses. All identifiable sauropod elements belong to either juvenile or subadult individuals (Fig. 2); none is attributable to a fully-adult individual (Myers and Storrs, 2007).

The Figure 2 cited in that excerpt shows two sauropod centra, a dorsal and a caudal, both with unfused neural arches. And yet here is MOR 790 8-10-96-204, similar in size and morphology to D. carnegii CM 84/94, and with at least partially closed neurocentral synostoses and fused cervical ribs. By all appearances, it belongs to an adult or nearly adult animal. It is hard to avoid the conclusion that the Mother’s Day Quarry includes at least one adult or near-adult Diplodocus. The only alternative is that MOR 790 8-10-96-204 is a juvenile in which the neural arch and cervical ribs fused very early.* But if that were the case, what basis would we have for thinking that it belonged to a juvenile, other than that it came from a quarry that only produced juveniles up until now? I trust that the circularity of that logic is clear. It is much more parsimonious to infer that MOR 790 8-10-96-204 is just what it appears to be–an anterior cervical of an adult or near-adult Diplodocus–and that the Mother’s Day Quarry is not exclusively filled with juvenile sauropods.

* Another wrench in the gears: if MOR 790 8-10-96-204 is a juvenile that had freakishly early fusion of its various bits, then clearly its ontogeny has departed from that of Diplodocus, all bets are off about developmental timing, and we shouldn’t be using it to make inferences about the normal ontogeny of diplodocids anyway. It’s damned if you do (it’s an adult), damned if you don’t (it’s a freak).

I’m not criticizing the work of Myers and Storrs (2007) on the taphonomy of the Mother’s Day Quarry or Myers and Fiorillo (2009) on age segregation in sauropod herds, by the way. It’s possible that they never saw MOR 790 8-10-96-204, or that if they did see the specimen they mistook it for a juvenile vertebra based on its size. All it takes is one bone to show that an animal is present in a quarry, and no number of other bones can prove that said animal is absent; if they only saw juveniles, the inference that the quarry only contained juveniles was sound (the operative word is was). If MOR 790 8-10-96-204 is a C5, it’s still only 80% the size of the same vertebra in D. carnegii CM 84/94, so maybe it was the oldest one in the group, or maybe it was an adult slumming with the juveniles, or maybe groups of juvenile sauropods often had one or more adults present to keep an eye on things. Or maybe it happened along earlier or later and just got buried in the same hole. There are a host of possibilities, most of which do not contradict the general conclusions of Myers and Storrs (2007) and Myers and Fiorillo (2009).

Conclusions

Size matters. Size alone is a horrible, horrible criterion for inferring age, especially in a clade (Diplodocoidea) in which adult size is known to vary, and especially with vertebrae. We should expect cervical vertebrae in a single individual to differ in diameter by a factor of 4.

Serial position matters. Not all vertebrae turn out the same. Even in adults, anterior cervicals look very different from posterior cervicals, and have different character states. Anterior cervicals and cervicals of juvenile individuals often look similar. The best way to tell them apart is to rely on articulated series–which is why I went to the trouble of writing the first post in this series.

Skeletochronology matters. The fact that MOR 790 8-10-96-204 has an apparently fused arch and fused cervical ribs should have been huge red flag that maybe it wasn’t actually a juvenile.

I went through that example at length because it shows how serial changes in size and morphology can mimic or suggest ontogenetic changes. In the next post I will examine the rest of the data Woodruff and Fowler (2012) used to support the hypothesis of ontogenetic control of neural spine bifurcation.

The rest of the series

Links to all of the posts in this series:

• Part 1: what we knew a month ago
• Part 2: why serial position matters
• Part 3: the evidence from ontogenetic series
• Part 4: is Suuwassea a juvenile of a known diplodocid?
• Part 5: is Haplocanthosaurus a juvenile of a known diplodocid?
• Part 6: more reasons why Haplocanthosaurus is not a juvenile of a known diplodocid

and the post that started it all:

• Changes through growth in sauropods and ornithopods

 References

• Hatcher, J.B. 1901. Diplodocus (Marsh): its osteology, taxonomy, and probable habits, with a restoration of the skeleton. Memoirs of the Carnegie Museum 1:1-63.
• Myers, T.S., and Fiorillo, A.R. 2009. Evidence for gregarious behavior and age segregation in sauropod dinosaurs. Palaeogeography, Palaeoclimatology, Palaeoecology 274:96-204.
• Myers, T.S., and Storrs, G.W. 2007. Taphonomy of the Mother’s Day Quarry, Upper Jurassic Morrison Formation, south-central Montana, U.S.A. PALAIOS 22:651–666.
• McIntosh, J.S., Miller, W.E., Stadtman, K.L., and Gillette, D.D. 1996. The osteology of Camarasaurus lewisi (Jensen, 1988). BYU Geology Studies 41:73-115.
• Osborn, H.F. and Mook, C.C. 1921. Camarasaurus, Amphicoelias, and other sauropods of Cope. Memoirs of the American Museum of Natural History 3:247-287.
• Ostrom, John H., and John S. McIntosh.  1966.  Marsh’s Dinosaurs.  Yale University Press, New Haven and London.  388 pages including 65 absurdly beautiful plates.
• Woodruff, D.C, and Fowler, D.W. 2012. Ontogenetic influence on neural spine bifurcation in Diplodocoidea (Dinosauria: Sauropoda): a critical phylogenetic character. Journal of Morphology, online ahead of print.