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You have your giant fossil rabbit neck all wrong

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Among the most intriguing of recently described fossil mammals has to be the Minorcan giant rabbit Nuralagus rex, published recently in Journal of Vertebrate Paleontology (Quintana et al. 2011). It’s a very neat discovery, whether you’re interested in lagomorph diversity or not. As usual, the one thing that everyone has been interested in is the size of this animal: how big was Nuralagus? With an estimated mass of about 12 kg, it was about ten times bigger than an average modern bunny (the examplar is of course the [ancestrally] Euro-African Oryctolagus cuniculus) and about twice as big as both the largest domestic rabbit (the Flemish) and the largest modern lagomorph of them all (the European hare Lepus europaeus). [Image below - by Sa monea, from wikipedia - shows a Nuralagus femur compared to that of Oryctolagus.]

Nuralagus is also morphologically peculiar compared to many other rabbits and hares. Relatively small eyes and small auditory bullae suggest that its senses weren’t as acute as those of continental lagomorphs, and its spreading digits, the nature of its limb bone articulations, and the low degree of flexibility in its spine all indicate that it was a relatively slow-moving walker, not a jumper or sprinter (Quintana et al. 2011).

However, you may well have heard all of this before, and it’s not why I’m here. I see two other things relevant to Nuralagus that are worth commenting on.

Firstly, fossil lagomorph diversity is reviewed all too infrequently in my opinion, so here are a few comments. According to Quintana et al. (2011), the closest relative of Nuralagus seems to be Alilepus, a widespread fossil rabbit, the different species of which are known from the Miocene, Pliocene and Pleistocene of Europe, Asia and North America. Both taxa share various detailed tooth characters, and it seems that Nuralagus is more similar in some respects to Eurasian Alilepus species than to North American ones (does this mean that Alilepus might be paraphyletic with respect to Nuralagus?).

For the record, note that all rabbits and hares are united within the group Leporidae. Leporids are the sister-group to Ochotonidae, the pikas (pikas had their heyday in the Miocene, it seems, when they far outnumbered leporids in number of species). A small number of fossil taxa from the Paleocene and Eocene (eurymylids, Gomphos and the mimotonids) appear to be stem-lagomorphs, and all of these taxa just mentioned have been united in the clade Duplicidentata (Wyss & Meng 1996, Asher et al. 2005).

So – we know that Nuralagus is close to Alilepus…. but what sort of leporid is Alilepus? Quintana et al. (2011) don’t include a phylogenetic analysis in their article, but a few preceding studies allow us to get a rough handle on leporid phylogeny.

In pursuit of a cladogram for fossil rabbits

McKenna (1982) published a hand-cranked phylogeny for lagomorphs [shown below: click to enlarge]. Pentalagus (the very special Ryukyu rabbit), Oryctolagus and Lepus formed a crown-group while Hypolagus (a widespread, long-lived taxon with species from the Miocene, Pliocene and Pleistocene of North America and Eurasia) and Archaeolagus (from the Oligocene and Miocene of North America) were arranged in successively more distant locations along the leporid stem. Chadrolagus, Palaeolagus and Litolagus were placed in a polytomy with this Hypolagus + crown-leporid clade (note that Palaeolagus was recovered as a stem-lagomorph by Asher et al. (2005) and hence removed from Leporidae entirely: P. haydeni – the type species (from the Lower Oligocene of Nebraska) – is shown in the adjacent image).

Dawson (2008) also provided a hand-cranked phylogeny; this time with more taxa included, and with names used for various of the clades and (dare I say it) grades. Dawson certainly wasn’t the first to use these names: in a rabbit classification published in 1929, Lee R. Dice proposed a subdivision of Leporidae into three ‘subfamilies’, and other authors introduced more such subdivisions later on. Anyway, the ‘base’ of Dawson’s tree was occupied by Procaprolagus, the various species of which are from both the Eocene and Oligocene of Asia and North America. A diversity of Eocene, Oligocene and Miocene taxa were then grouped into the paraphyletic ‘Palaeolaginae’, while the two clades Archaeolaginae and Leporinae were shown as sharing an ancestor with a ‘palaeolagine’ clade that included Mytonolagus and Palaeolagus (Dawson 2008). Tooth characters show that Alilepus is a leporine but, beyond that, Dawson didn’t elucidate: Pronotolagus from the Miocene of North America was identified as the most basal leporine, but the affinities within Leporinae weren’t the focus of her interest.

Again, let’s note that both the McKenna and Dawson trees are what we call hand-cranked: this means (it’s a very much informal term) that these workers constructed their trees ‘by hand’, following their assessment of a relatively small number of characters. History has shown us that hand-cranked trees are (generally) approximately right, but because (normal) humans aren’t able to assess the hundreds or even thousands of data points that need to be compared simultaneously whenever organisms are examined in detail, you need computers that run parsimony algorithms to best assess the data you collect. You know all this already: it’s phylogenetics 101.

But one thing that becomes quickly obvious when you try to look at fossil rabbit phylogeny is that hardly any work has been done, which is a bit surprising given the number of specimens that are known and the quality of their preservation. Wible (2007) published a parsimony-based cladogram of leporids [it's shown here]: Pronolagus and Romerolagus were shown as being outside the crown-clade, but few other fossil leporid taxa were included. A few other phylogenetic studies have incorporated data from fossil leporids (Meng & Wyss 2001, Asher et al. 2005, Kraatz et al. 2010), but they also don’t include enough taxa to flesh out the tree at all. So, as yet, there’s no real idea as to how such taxa as Alilepus and Nuralagus relate to other rabbits. For now, the adventure ends here. As I said above, the lack of work on lagomorph phylogeny is surprising given the quality of much of the fossil material and the number of specimens involved, and also given that lagomorphs are just so freakin’ weird compared to other placental mammals. Seriously, they’re insane. If any newbies want elaboration on that, I’ll be happy to oblige.

Incidentally, most of the phylogenetic hypotheses that have been published for leporids rely heavily on data that comes from tooth cusp anatomy. Rabbit teeth are very weird and experts have argued for years over how their tooth cusps should be homologised with those of other mammals – I’d love to discuss this matter in more detail but now is not the time. As it happens, Kraatz et al. (2010) have recently published an open-access paper on this very issue, so you can check it out for yourselves [adjacent image, showing postulated transformation in lagomorph tooth cusp anatomy, from Kraatz's website].

And thanks much to Brian Kraatz for his help and sage advice on leporid phylogeny, by the way. He has big plans for fossil rabbits – hopefully they’ll pan out.

The neck, the neck, oh, the neck

The second thing I wanted to say about Nuralagus is a little more arcane than its phylogenetic position, and there might not be that many people who have the required overlapping fields of interest to even think it worthy of note, but here I go.

Quintana et al. (2011) include a very nice reconstruction of Nuralagus in their paper on the animal: you might already have seen it online. It’s really very good: it shows the animal to scale with a European rabbit, and portrays it in nice, realistic fashion. But… they almost certainly have the neck horribly wrong.

They show the neck skeleton of Nuralagus held just about straight, in a strange, sub-horizontal pose, and with no curve in it whatsoever. I presume they did this because they imagine that’s how extant rabbits hold their necks. In fact – as you’ll know if you followed the neck posture stuff I published with Mike P. Taylor and Mathew Wedel (Taylor et al. 2009) [link to pdf below] – it definitely ain’t so. Like rodents and other ‘short necked’ mammals, rabbits actually have a strongly curved neck skeleton that descends sharply close to the cervico-thoracic transition before ascending to meet the occiput. None of this is at all obvious in the living animal and is only revealed in x-ray (or when other imaging techniques are applied). It’s crazy, but it’s really there: rabbits have a virtually S-shaped neck skeleton: check out the x-rays of a live rabbit below, from Vidal et al. (1986).

Regardless of whatever preconceptions you might have, we really should assume by default that the neck of this weird, giant, island-endemic rabbit was also S-shaped, with a strong curvature just like seen in extant rabbit species. And it’s no use saying that the fossil bones won’t allow this sort of posture, since one of the things that’s obvious from x-rays of living animals is that the postures their necks maintain during life aren’t readily reproducible from dry bones either. The soft tissues present in the living animal make the neck skeleton more flexible that is the case in the dry skeleton, not less.

So, there we have it. My initial plan here was just to make a quick observation on Nuralagus and tie it into work I and colleagues have done on neck posture, but it seems there’s an awful lot to say about fossil lagomorphs. As usual, I’ve barely touched on the many neat things you could say about these animals: I think we’ll definitely be coming back to them in time.

Refs – -

Asher, R. J., Meng, J., Wible, R. R., McKenna, M. C., Rougier, G. W., Dashzeveg, D. & Novacek, M. J. 2005. Stem Lagomorpha and the antiquity of Glires. Science 307, 1091-1094.

Dawson, M. R. 2008. Lagomorpha. In Janis, C. M., Gunnell, G. F. & Uhen, M. D. (eds) Evolution of Tertiary Mammals of North America. Volume 2: Small Mammals, Xenarthrans, and Marine Mammals. Cambridge University Press, 293-310.

Kraatz, B. P., Meng, J., Weksler, M. & Li, C. 2010. Evolutionary patterns in the dentition of Duplicidentata (Mammalia) and a novel trend in the molarization of premolars. PLoS ONE 5(9): e12838. doi:10.1371/journal.pone.0012838

McKenna, M. C. 1982. Lagomorph interrelationships. Geobios, mémoire spécial 6, 213-223.

Quintana, J., Köhler, M. & Moyà-Solà, S. 2011. Nuralagus rex, gen. et sp. nov., an endemic insular giant rabbit from the Neogene of Minorca (Balearic Islands, Spain). Journal of Vertebrate Paleontology 31, 231-240.

Taylor, M. P., Wedel, M. J. & Naish, D. 2009. Head and neck posture in sauropod dinosaurs inferred from extant animals. Acta Palaeontologica Polonica 54, 213-220.

Vidal, P. P., Graf, W. & Berthoz, A. 1986. The orientation of the cervical vertebral column in unrestrained awake animals. Experimental Brain Research 61, 549-559.

Wible, J. R. 2007. On the cranial osteology of the Lagomorpha. Bulletin of Carnegie Museum of Natural History 39, 213-234.

Wyss, A. R. & Meng, J. 1996. Application of phylogenetic taxonomy to poorly resolved crown clades: a stem-modified node-based definition of Rodentia. Systematic Biology 45, 559-568.

Darren Naish About the Author: Darren Naish is a science writer, technical editor and palaeozoologist (affiliated with the University of Southampton, UK). He mostly works on Cretaceous dinosaurs and pterosaurs but has an avid interest in all things tetrapod. His publications can be downloaded at darrennaish.wordpress.com. He has been blogging at Tetrapod Zoology since 2006. Check out the Tet Zoo podcast at tetzoo.com! Follow on Twitter @TetZoo.

The views expressed are those of the author and are not necessarily those of Scientific American.





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  1. 1. BilBy 8:57 am 07/11/2011

    Darren – talking of neck postures; the reconstructions of pterosaurs, particularly the fantastic pictures of azhdarchids by Mark Witton, always show a very straight neck and always look slightly top heavy to me. Long-necked birds like herons, cranes and storks have very flexible necks that can ‘fold up’ – even things like ground hornbills, which you compare with azhdarchids, can fold up the neck. Is there a good reason why you and Mark favour a straight neck in the azhdarchids with a neck profile that closely follows the bones beneath, or was it simply the most parsimonous reconstruction?

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  2. 2. naishd 9:04 am 07/11/2011

    Heya. In the birds you’re thinking of, the neck skeleton is made up of numerous vertebrae (c. 17), the joint surfaces of which allow for substantial flexibility. The necks of azhdarchid pterosaurs are unusual – the number of vertebrae is comparatively low (c. 9 vertebrae), and the vertebrae themselves are very long, cylindrical, and with only a small amount of flexibility being possible at each joint. It seems that azhdarchid necks were relatively stiff and straight, but with substantial movement being possible at the head-neck and cervico-dorsal transitions. This was not, of course, true for all pterosaurs – I’m only talking about azhdarchids.

    Darren

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  3. 3. DMA12 11:15 am 07/11/2011

    A nice way to start up Tetrapod Zoology. Speaking of necks, would sauropods hold their necks up all the time (except for eating and drinking), or would they have walked sometimes walking with dinosaurs style.

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  4. 4. Symbiartic.km 11:39 am 07/11/2011

    Sigh! Another scientific paper that neglects to mention the illustrator in its acknowledgments (I’m referring to Quintana et. al, 2011). What’s your experience, Darren – does that usually mean the authors did them? Even so, it’d be nice to know which author was responsible. Hmmm…

    Love the post, though. Fascinating about the neck position…

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  5. 5. naishd 12:21 pm 07/11/2011

    Thanks for comments. Sauropod necks: assumed ‘habitual posture’ should indeed be raised; there’s no reason to assume that they really walked around with their heads and necks held low as a matter of course. See the Tet Zoo ver 2 article from 2009.

    Nuralagus artwork: if an artist isn’t credited, yes, I think you should assume that one of the authors was responsible. Indeed, some online sources credit the illustrations to Meike Köhler (second author on the paper), so I reckon she’s responsible.

    Darren

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  6. 6. Heteromeles 2:16 pm 07/11/2011

    Can I point out that if a rabbit is sniffing, its neck is going to be held out more in the posture seen in the color collage at the top (see, for example: http://www.istockphoto.com/stock-photo-13043159-sniffing-rabbit.php).

    I’m not a rabbit expert, but I’ve seen enough of them with necks extended (when standing, sniffing, etc), that I wasn’t bothered by the posture on Nuralagus. I don’t think that’s its rest posture by a long shot.

    I’m honestly more puzzled by the short ears. Minorca’s not the Sahara, but it’s not chilly either. I’d gotten the impression somewhere that jack rabbits lost heat through their ears. Presumably a giant rabbit would need larger ears, rather than smaller ones, just for thermoregulation. Is there evidence for it being short-eared that I’m missing?

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  7. 7. naishd 4:12 pm 07/11/2011

    Heteromeles: yes, rabbits can straighten the neck, and they can flex the neck in order to bring the mouth/nose down to the ground, of course. But I’m talking specifically about the pose adopted by the cervical skeleton. Fact is, even when the neck is in a ‘straightened’ or ‘bending down’ posture, the neck skeleton remains curved – with a strong descent at the cervico-dorsal junction, and obvious ascent from there to the occiput (I’ll have to publish the x-rays). You cannot get the neck skeleton straightened out like that, and people only assume that this might happen because they expect the neck skeleton to mirror the surrounding soft tissue outline. As we said on SV-POW!, necks lie.

    As for those ears, Nuralagus has particularly small auditory bullae (as mentioned above). Quintana et al. (2011) note that similarly small bullae are also seen in the extant Pentalagus – and it has proportionally short pinnae. This is why Pentalagus has been restored with such short ears.

    Darren

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  8. 8. Therizinosaurus 5:30 pm 07/11/2011

    “History has shown us that hand-cranked trees are (generally) approximately right,…”

    Is that so? Certainly doesn’t seem that way considering the manual trees in my area of study-
    Paul, 1984 on segnosaur position, very wrong.
    Bakker et al., 1988 on Nanotyrannus, very wrong.
    Paul, 1988 in PDW, had many good ideas for the time but not very parsimonious.
    Elzanowski, 1999 on oviraptorids being close to birds, wrong.
    Anything by the BANDits/ABSRDists/MACIACs, very wrong.

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  9. 9. Neil K. 5:41 pm 07/11/2011

    Not that it adds that much, but I tracked down some interesting radiographs of running pika, from Witte et al. 2002.

    While Ochotona does not appear to be quite as extreme as the rabbit x-ray in the post, the cervical curvature is clearly there, even when the neck is extended during running.

    Witte et al. 2002 Torque patterns of the limbs of small therian mammals during locomotion on flat ground J Exp Biol 205, 1339-1353.

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  10. 10. Nick Gardner 6:29 pm 07/11/2011

    I would very much like to see those Xrays published. Do you intend to get that out any time soon?

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  11. 11. Heteromeles 11:57 pm 07/11/2011

    Thanks for the clarification Darren.

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  12. 12. naishd 4:32 am 07/12/2011

    Mickey/Therizinosaurus (comment 8): I should clarify that I was talking about the vague shape of trees, not the specific relationships between ‘genus’-level taxa or that sort of thing. So, even in the hand-cranked theropod phylogenies you draw attention to, the people concerned identified ceratosaurids as being outside of a clade that included allosauroids, tyrannosaurids and maniraptorans (Bakker et al. 1988, Paul 1988), and Bakker et al. (1988) regarded tyrannosaurids as part of a clade that included ornithomimosaurs and maniraptorans and not Allosaurus. Elzanowski’s tree is standard (viz, it agrees with most other phylogenies) in overall shape. So, these trees are indeed “approximately right”.

    I think it’s kinda misleading, by the way, to say that the BANDits are worthy of inclusion in this discussion – we know that they have a predetermined agenda and aren’t really interested in evaluating the affinities between taxa.

    Darren

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  13. 13. Therizinosaurus 8:53 am 07/12/2011

    True they weren’t completely wrong, but to be approximately right instead of approximately wrong, they’d have to have more correct nodes than incorrect ones and I don’t know if that’s true. Bakker et al.’s tree has ten internal nodes and would take five rearrangements to agree with the current consensus, so it seems only half right for instance. It would be an interesting study to see if you’re right, and you may be, I just don’t think anyone’s looked at the problem yet.

    As for your second point, I don’t think BANDits are all that different than McKenna or many early cladists (e.g. Gauthier, Chiappe, Cracraft) in having a predetermined agenda. I notice McKenna has only 3 out of 51 characters exhibit homoplasy, which suggests either rabbits are incredibly immune to convergence and reversal, or he picked the characters which supported the phylogeny he noticed/wanted. So like most of Sereno’s cladograms, McKenna is really more demonstrating his hypothesis than he is testing it. This is what the BANDits do too, they just have a ton of other problems which make them more contemptable. The BANDits are even more honest in a way since at least they openly discount parsimony, whereas many cladists go through the motions of making a matrix and running it through PAUP, as if their tree wasn’t designed into the matrix in the first place.

    Ugh, I just defended BANDits. Must mean it’s time to sleep ;)

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  14. 14. naishd 6:04 pm 07/13/2011

    Mickey: good call, I can see where you’re coming from. But my basic point is that the shapes of the hand-cranked trees are, often, more or less “about right”: ‘basal’ taxa get placed ‘near the base’, the youngest taxa get placed ‘near the top’, and the ‘intermediate’ ones get placed in ‘intermediate’ positions. So, a hand-cranked theropod tree (like Paul’s, or Bakker’s) has coelophysids and ceratosaurids outside an allosaur-coelurosaur clade, and allosaurs are outside a coelurosaur clade. The hand-cranked trees are not totally ‘wrong’ compared to the parsimony-generated ones: they’re typically approximately right in general form.

    Darren

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  15. 15. naishd 6:05 pm 07/13/2011

    … and we really should be talking about fossil rabbits, anyway.

    Darren

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  16. 16. Heteromeles 7:50 pm 07/13/2011

    Okay, fossils it is. Are uintatheres and anagalids still considered lagomorph outgroups, or has that been conclusively disproven?

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  17. 17. naishd 10:16 am 07/14/2011

    Asher et al. (2005) found some anagalids to group with sengis (Macroscelidea) and a Hyopsodus + Phenacodus clade… they are thus well removed from Euarchontoglires in their tree (which contradicts the notion of Anagalida as favoured by McKenna & Bell (1997)). And the ‘giant horned bunnies’ hypothesis hasn’t stood up at all well – I’d be very interested to know what’s in Shawn Zack’s Phd thesis (‘The phylogeny of eutherian mammals: a new analysis emphasizing dental and postcranial morphology of Paleogene taxa’).

    Darren

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  18. 18. Valerio Peverelli 5:19 am 07/16/2011

    I’m sure that you are intresting on this news:

    “Garzeno (Mountain near Como Lake, N 46°o8’2.4″, E 9°,15′) 23 horses killed by a bolt”

    Probably the newspaper isn’t correct, and we have more than a single bolt.

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  19. 19. John Harshman 10:14 am 07/16/2011

    Darren, may I make my usual pro forma complaint about “basal” and “youngest”? And “bottom” and “top”, for that matter.

    As for bias among other than BANDits, of course it exists. But let’s not put Gauthier in there. I seem to recall he set out initially with the objective of disproving that silly “birds are dinosaurs” idea. Still, there are a lot of cladograms out there with suspiciously low amounts of homoplasy.

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  20. 20. naishd 10:33 pm 07/16/2011

    Point taken, John (about ‘basal’, ‘youngest’, ‘top’ etc). Thanks. While I hate to seem sloppy, I just couldn’t think of quicker, easier ways to describe what I meant. And I do typically employ quote marks when using these terms – an attempt to show that they’re being used for convenience only.

    Darren

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  21. 21. David Marjanović 5:02 pm 08/8/2011

    I’d be very interested to know what’s in Shawn Zack’s Phd thesis (‘The phylogeny of eutherian mammals: a new analysis emphasizing dental and postcranial morphology of Paleogene taxa’).
    Zack presented his results at the SVP meeting of 2008, and they’re awesome, but lots of work remained to be done at that time, and I don’t know why no publication has been forthcoming… or if the thesis is even finished; given the sheer size of the problem, it may not be…

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  22. 22. naishd 9:42 pm 08/9/2011

    The thesis is finished – I now have a copy :)

    Darren

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