Yes, it was a kiwi


Better late than never... what was the identity of that unusual string of vertebrae I featured here however-many-days-ago? Most of you realised - correctly - that it was the neck of a bird, and several of you guessed moa. This wasn't a bad guess, but it wasn't the right one. The correct answer was given three guesses in by Adam Yates of Dracovenator. Yes, it's the neck of a kiwi (Apteryx). Well done Adam, your Tet Zoo-ing skills serve you well (I'll not mention the fact that Adam's skills also extend to fishes and molluscs, gack). Why post a picture of a kiwi neck? Because it's so frikkin' weird, that's why. The neck vertebrae of kiwi look very broad and robust for a bird, and I was hoping that these characteristics might have fooled you into thinking that you were looking at a baby apatosaur neck or something...

Mivart (1877) provided a very good description of ratite vertebral anatomy and described how Apteryx 'differs from all [other ratites] in the greater relative stoutness of the neck and production of its processes' (p. 34). Like all 'ordinary' tetrapod vertebrae, the cervical vertebrae of Apteryx have prezygapophyses, postzygapophyses and neural spines on the neural arch, and parapophyses and diapophyses on the centrum [for help with the terminology see Tutorial 2 at SV-POW!]. Adjacent to the posterior part of the neural spine and sitting atop the postzygapophyses are additional structures, the hyperapophyses (singular: hyperapophysis. Not to be confused with hypapophysis [plural: hypapophyses]. Hypapophyses are keel-like structures that project from the ventral surface of the centrum: in the kiwi neck, they're small on the atlas, absent on the axis, and then present from the 12th cervical to the third dorsal). I'm not entirely sure what hyperapophyses are (homology-wise): it's tempting to think that they might be homologous with the epipophyses of non-avian theropods and basal birds, but epipophyses are typically placed more posteriorly on the postzygapophyses. I could say a lot more about kiwi cervical vertebrae, but I think I should move on.


Indeed, it's worth briefly discussing the other weirdness present in the kiwi skeleton. I'll try and keep comments on the skull as brief as possible as we all know how easy it is to find loads to say about skulls. In marked contrast to most other maniraptorans, the orbits of kiwi are small and, in contrast to other crown-group birds, the nostrils are located right down at the tip of the bill. Clustered around the tips of both the upper and lower jaws are numerous small pits that house specialised cells called mechanoreceptors (specifically, the sort of mechanoreceptors present in bird bills are called Herbst corpuscles and Grandry corpuscles). These provide kiwis with tactile jaw tips (Martin et al. 2007), so they don't rely on their well-developed olfaction entirely as used to be thought. We previously looked at avian bill mechanoreceptors back when Mark Witton and I paid some attention to them in our work on azhdarchids. The kiwi bill is long, but what's surprising is how variable its length is within the group, both between sexes and between species (Sales 2005). Having mentioned species, I should note that kiwi taxonomy has recently been revised (or, at least, is in the process of being revised): genetics indicates that there are several cryptic species within what used to be known as Apteryx australis [adjacent image, showing kiwi bill tips, from Martin et al. (2007). Image of kiwi skull below from Digimorph].


Moving to the thoracic skeleton, the neural spines on the dorsal vertebrae are tall and - in some kiwi taxa - so long anteroposteriorly that they butt up against one another to form a continuous neural lamina. They aren't fused together, however, as they are in some other neornithines (when the neural spines fuse together, they create a laterally compressed structure termed a notarium). The ribs are also weird in being strikingly broad.

What the hell is going on with those weird uncinate processes?

The large, flattened uncinate processes are also broad: in most birds (and other maniraptorans) they're slender and spur-like. Uncinate process have been shown to play a role in anchoring muscles that facilitate flaring of the ribcage when movement of the sternum is prevented during sitting (Codd et al. 2005). Kiwi sit down when, for example, brooding their gigantic eggs. At such times they are, like other birds, unable to use the sternum to ventilate the posterior thoracic and abdominal air sacs (which, like those of other ratites, are small and reduced compared to those of other neornithines). However, kiwi have a particularly short sternum [more on the sternum below] that does not extend further posteriorly than the fourth thoracic rib (in most other neornithines it extends at least as far posteriorly as the sixth rib).

Might it be, therefore, that the big uncinate processes are needed in order to compensate for the small sternum? This idea requires testing and I'm not aware of data that might have a bearing on it. However, it doesn't look like it's the case, because other maniraptorans with similarly small sterna (including oviraptorosaurs, dromaeosaurs, elephant birds and emus) don't have the weird, broad uncinate processes so characteristic of kiwi. Could the uncinate processes help stabilise the rib cage somehow? Maybe, but I can't think why kiwi would need special lateral stabilisation like this. For now, the evolution of those broad ribs and uncinate processes is mysterious.


Weird arms, hands, legs and feet

The kiwi scapulocoracoid is small with subparallel margins that make the whole structure look strap-like. The wing is strange: all the bones are tiny and gracile, the humerus is strongly curved and very slender, and the hand is monodactyl with a small claw (though this is not always present). The number of phalanges seems to vary between two and four. The kiwi taxa differ in how stiff their wing quills are.

The sternum is anteroposteriorly short and very broad with a convex ventral surface that usually lacks a keel (a vestigial keel is occasional present). It's also thin at its lateral margins. The very short coracoidal sulci are widely separated on anterolateral processes by a large U-shaped border that lacks any kind of anterior process. Unlike that of other ratites, the kiwi sternum has two lateral trabeculae, both of which have incisions on their medial sides. Some sterna are perforated by one or two foramina. There are five prominent articular facets for sternal ribs: the ribs themselves increase in length posteriorly.

The kiwi pelvis is interesting because, if you know non-avian dinosaurs, it has a more familiar look to it and lacks some of the weirdness of the neornithine pelvis that often confuses people [kiwi pelves below from McGowan (1982)]. Ordinarily in neornithines, the dorsal surface of the elongate ischium is fused for much of its length to the ventral surface of the post-acetabular part of the ilium, leaving a large foramen (the ilioischiadic foramen) ventral to the anterior part of the post-acetabular part of the ilium. At the same time, the strongly reduced, rod-like pubis usually extends posteroventrally in close contact with the ischium. In contrast, the pubis and ischium of kiwi are clearly distinct and project posteroventrally beneath the ilium, being separate both from each other and from the ilium (thought the pubis and ischium may occasionally unite distally). The pelves of moa and elephant birds are similar in these respects. In case you haven't noticed, the pelves of dromaeosaurs, basal birds, palaeognaths and neognaths form a neat and obvious 'sequence'. But then, you could say the same about any other part of theropod anatomy when looked at within a phylogenetic context.


The pelvis in kiwi is remarkable for its breadth, which exceeds that of any other ratite. In dorsal view the flaring blades of the ilia produce a heart-like shape. The tail is long and a pygostyle is generally stated to be absent (and, in the kiwi material I've looked at, it doesn't look like any caudal vertebrae are fused together to form a pygostyle). However, Mivart (1877) thought that a pygostyle is indeed present and that it consisted of 'three or four successively smaller and smaller vertebrae ankylosed together' (p. 39). Pygostyles seem to be generally absent in ratites, but ostriches have a short one (De Beer 1956). Mivart's comments make me think that further work is needed in order to determine the distribution of pygostyles within the ratites.

Finally, there is also some interesting stuff in the hindlimb. The middle trochlea on the tarsometatarsus projects markedly distally and there are two short hypotarsal ridges on the posterior surface of the tarsometatarsus, as there are in moa. Cracraft (1974) used this character (among a few others) to support the monophyly of a kiwi + moa clade, but since then some studies have rejected the existence of such a clade. The most unusual thing about the kiwi hindlimb is that the hallux is not reversed as it is in other neornithines (that is, metatarsal I does not project posteriorly from the tarsometatarsus): instead, it projects anteromedially (forwards and inwards). In this respect it is similar in orientation to that of non-avian theropods (McGowan 1979*, Paul 2002). This is unlikely to be a retained primitive character, and is almost certainly a reversal.

* Note that some of the observations made in this paper were corrected by Vanden Berge (1982).


That all went on for much longer than I'd planned. It's obvious that kiwi are highly specialised for a nocturnal lifestyle in which flight and good eyesight have been replaced with cursoriality and a reliance on olfaction and tactile abilities. These features, combined with the hair-like feathers, whiskers, and cryptic habits of kiwi have led many biologists to regard these bizarre birds as 'honorary mammals'. What makes them doubly interesting is that, in several aspects of their morphology, they are reminiscent of Mesozoic maniraptorans and might have been similar to them in physiology and soft-tissue anatomy [adjacent image from wikipedia].

There's tons more that could be said about kiwi. While doing research for some of the text above, I discovered some old material on the group that I'll recycle here at some stage.

Refs - -

Codd, J. R., Boggs, D. F., Perry, S. F. & Carrier, D. R. 2005. Activity of three muscles associated with the uncinate processes of the giant Canada goose Branta canadensis maximus. The Journal of Experimental Biology 208, 849-857.

Cracraft, J. 1974. Phylogeny and evolution of the ratite birds. Ibis 116, 494-521

De Beer, G. 1956. The evolution of ratites. Bulletin of the British Museum of Natural History (Zoology) 4, 59-70.

Martin, G. R., Wilson, K.-J., Wild, J. M., Parsons, S., Kubke, M. F. & Corfield, J. 2007. Kiwi forego vision in the guidance of their nocturnal activities. PLoS
2 (2): e198. doi:10.1371/journal.pone.0000198

McGowan, C. 1979. The hind limb musculature of the brown kiwi Apteryx australis mantelli. Journal of Morphology 160, 33-74.

- . 1982. The wing musculature of the the brown kiwi Apteryx australis mantelli and its bearing on ratite affinities. Journal of Zoology 197, 173-219.

Mivart, S. G. 1877. On the axial skeleton of the Struthionidae. Transactions of the Zoological Society 10 (1), 1-52.

Paul, G. S. 2002. Dinosaurs of the Air: the Evolution and Loss of Flight in Dinosaurs and Birds. Johns Hopkins University Press (Baltimore).

Sales, J. 2005. The endagered kiwi: a review. Folia Zoologica 54, 1-20.

Vanden Berge, J. C. 1982. Notes on the myology of the pelvic limb in kiwi (Apteryx) and in other birds. The Auk 99, 309-315.

More like this

Back in 2006 my good friend Matt Wedel - who you may know better as one of the three SV-POWsketeers or as plain old Dr Vector - produced a short article on an emu dissection he participated in at the University of California at Santa Cruz [adjacent image: an Emu Dromaius novaehollandiae... though…
While checking a few details on kiwi skeletal anatomy the other day, I discovered some old material I'd written on these strange birds. I've updated it, and here's the first lot of it. Kiwi have been known to science since 1813. In that year George Shaw (then the Keeper of Zoology at the British…
Next time you're cutting up a fresh bird, try looking for the lungs. They're about where you'd expect them to be, but they're nestled up dorsally against the ribs and vertebrae, and they're surprisingly small. If you think about it, the the thorax of a bird is a fairly rigid box, with that large…
A little while ago, news of a new paper by Devon Quick and John Ruben, both of Oregon State University, appeared on the newswires. It got its fair share of publicity. Entitled 'Cardio-pulmonary anatomy in theropod dinosaurs: implications from extant archosaurs', the paper (Quick & Ruben 2009…

Are the cervical ribs of Apatosaurus that short? My logic went as follows: lots of cervicals (way more than 7) + very short cervical ribs = bird. So I picked the swans, at least some of which are said to have 25 cervical vertebrae...

By David MarjanoviÄ (not verified) on 14 Feb 2009 #permalink

I am reminded of the Gould essay that talks about egg size and allometry with respect to kiwis; it had an xray picture of a kiwi more or less full of egg.

I wonder both if the uncinate processes and broad ribs predate the shrinking process and if they're somehow necessary for the poor thing to breathe during the late stages of producing an egg.

I think lithornids were also probers as well (flying ones though). Paleognaths do seem capable of being more than ratite or galliforme like

Well, I guess this post blows the stuff I saw them talking about over at the speculative evolution forum out of the water, specifically that terrestrial, nocturnal bird are impossible to evolve. We've already got one.

And Darren, I think the fact that the vertebrae looked recent and unfossilized is what made no one guess sauropod. Not to mention the neck arcs far to much for a diplodocid sauropod.

By Metalraptor (not verified) on 14 Feb 2009 #permalink

Kiwis are adorable and interesting, what collection is the piece from?

Also I think i need to brush up my Avian Osteology, are there any helpful websites? (googling just got me the book 'Avian Osteology')

@Metalraptor: You must be joking, because there's no such post on our forum. If there is, then it wasn't made by me thats sure

In regard to hyperapophyses, many maniraptoriforms (including most oviraptorosaurs and alvarezsaurids) have more anteriorly placed epipophyses. So the morphology isn't unheard of. From what I can tell from the kiwi neck photo, I'd be fine calling those epipophyses if they were on a Mesozoic theropod vertebra.

No, I was not joking. However, you are right, the post was not made by you. If I remember correctly, it was a rather early post on the forum, someone said that since birds had not developed terrestrial, nocturnal forms today or in the past (as well as some other niches), that they could not develop in the future.

Just because an animal has not developed into a certain niche now or in the past, doesn't mean it won't do so in the future. For example, in the Permian diapsids were a fringe group, mostly muscled out by anapsids and synapsids. But after the P-T extinction, they diversified into a huge number of forms, including modern birds and crocs. Who would have guessed that little Protorosaurus could have done that? But I do think that if a group had gone into niches in the past, it does make it seem more likely that they could do so in the future.

Probably the best example of a possible future mainland nocturnal, terrestrial bird might be one of the galliforms. Perhaps one with huge eyes to keep a watch for predators, looking like a weird cross between a troodont and a quail. Or perhaps on an island a species of flightless nightjar, perhaps taking the place of amphibians, who always tend to be lacking on islands.

Anyway, back to the matter at hand, kiwis. Darren, to me it appears that the most likely reason for the kiwis developing such odd, broad pelvises and strong ribcages is to facilitate the carrying of the egg. Don't kiwis have one of the largest egg-to-body ratios in all of birdkind? In that case, one would expect the kiwi body to be built for carrying such large bulk. Of course, this is just a hypothesis.

Making the kiwi seem even weirder, I have heard that some genetic tests suggest that the kiwi is not closely related at all to the other new zealand ratites, the moas, and is instead related to the cassowaries and emus, while the moa is related to the ostrich. This would be odd, because it makes one wonder what happened to the emu-like ratites of New Zealand? Did they die out from competition with proto-moas? Or did they just never evolve?

By Metalraptor (not verified) on 15 Feb 2009 #permalink

This would be odd, because it makes one wonder what happened to the emu-like ratites of New Zealand? Did they die out from competition with proto-moas? Or did they just never evolve?

Unfortunately, there's just no way of knowing at present (though my money would perhaps be on them never existing in the first place). Even compared to the poor fossil record of birds in general, the known fossil record for ratites prior to the Quaternary is just pitiful.

@Metalraptor: True, other nocturnal birds might evolve in the future. It would just not be a very common phenomena, since most birds (aside from the kiwi) rely on the eye sight to guide themselves, and they don't like to wander blindly in the dark. My money goes on the swifts, which seem capable of limited echolocation.

Oh, on the New Zealand ratite matter, I doubt there were ever emu or cassowary (whatever you spell it) like forms in New Zealand, because moas seem to be a very old group (indeed they completly lost the wings, suggesting a long time of flightlessness), and there doesn't seem to be much room for two very similar groups in an island like that.

One must note ratites lost flight multiple times (according to a recent genetic testing), and they evolved from galliforme like paleognaths like tinamous. Of course, the last common ancestor between emus, cassowaries (wahtever you spell that) and kiwis was one of those ancestral flying forms, and it flew to New Zealand 14 million years ago or something like that (it likely also used island hoping, unless it was a much better flier than modern tinamous). In the presence of moas and the absence of mammals, it then took a very unusual niche.

So it was a kiwi, eh? I certainly would not have thought of that. Although you must admit, Darren, that it was a bit naughty of you to rotate that picture ninety degrees... That led me to believe that the vertebrae belonged to some long-legged bird. The pose looked a bit unnatural* to me, but I tried to think like a taxidermist. Hence my flamingo guess; I thought someone had been inspired by this (in)famous flamingo picture, and had tried to produce something like it...

* Alas, it is very common to see animals/skeletons mounted in grossly incorrect anatomical positions, even at respectable natural history museums.


birds had not developed terrestrial, nocturnal forms today or in the past

But there are terrestrial, nocturnal birds, and not only on isolated islands either. The woodcocks Scolopax, of which there are seven species around the world, are mainly active at dark, and rest on the ground during the day. Their cryptic plumage seems to offer them quite sufficient protection. (Woodcocks are admittedly not flightless, but they're very slow fliers; the American species S. minor is supposedly the slowest flier of all birds.)

Hmm. Come to think of it, perhaps rather than quasi-mammals, kiwi could be regarded as flightless, giant quasi-woodcocks?

I wonder...if the uncinate processes ...[are] somehow necessary for the poor thing to breathe during the late stages of producing an egg. appears that the most likely reason for the kiwis developing such ... strong ribcages is to facilitate the carrying of the egg.

If so, then one would expect some rather obvious sexual dimorphism in this character. Anyone have both male and female kiwis in their available collections? And I would suspect that Darren would have mentioned this if there were such dimorphism.

This suggests that both sexes have some use for stronger "huffing" abilities than one would 'expect' for a non-flying bird. Well, as Darren has described, these critters are highly specialized in their feeding anatomy, and presumably in their feeding behaviour as well. Perhaps spending a high percentage of time with one's nostrils below ground is more easily accomplished with robust ribs with uncinate processes. And even more speculatively, particular patterns of breathing through the nostrils [such as short, forceful breaths] may produce reactive movements of some prey items making their detection easier for those mechanoreceptors in the bill tip.

And BTW, do the uncinate processes facilitate inhalation only, or might they also help exhalation as well?

"birds had not developed terrestrial, nocturnal forms today or in the past"

That's what I said, someone had argued that since there hadn't been any in the past or present, there would not be any in the future. But like I said, they were wrong, because we have those sort of birds today! Perhaps the woodcock would make a likely ancestor for my hypothetical large-eyed quail-like bird.

Carlos, I have not heard anything about echolocation in swift, but if they do, it would make them likely for such a niche. Perhaps the South American oilbird would be more likely for such a niche. It has also been demonstrated to have some form of echolocatory abilities, and to top it off they are already nocturnal. However, even though birds usually depend on sight in their environment, some birds have developed excellent senses of smell (turkey vultures), and hearing (owls). New groups of nocturnal birds could also secondarily develop advanced non-visual senses. Who knows, perhaps a kiwi-like turkey vulture.

As for the kiwi, with its "mammal-like" and bird features, I am surprised that the creationist movement has not tried to use it as an "mosaic form" or whatever their latest excuse for transitional forms are. Kiwis have mammal-like feathers (especially to one who does not understand the evolution of birds), they have an excellent sense of smelle, a sense usually not developed in birds, and such. I realize that this is a very poorly inferred observation, but hey, the creationist movement has done worse.

On the subject of the large ribs, perhaps the large uncinate processes, if they support the lungs, allowed the kiwis to lay massive eggs, and natural selection was favorable to large egg kiwis, for whatever reason.

By Metalraptor (not verified) on 16 Feb 2009 #permalink

@Metalraptor: I've seen it in a documentary, in which swifts that nest in caves appearently use echolocation to guide themselves

I see, but oilbirds seem more likely, since they are already nocturnal to some degree (being members of the Caprimulgiformes), the same order that includes the nighjars and kin. However, I do like the swift idea. I looked up the swifts, they do echolocate. The group that specifically do are the swiftlets.

By Metalraptor (not verified) on 16 Feb 2009 #permalink

Have they settled the controversy on the guacharo/oilbird's ancestry? Because I remember there were some suggestions it wasn't a caprimulgiforme.

Swifts and hummingbirds, on the other hand, are indeed derived from caprimulgiformes

From what I've heard, the oilbird is either a nightjar, or it is in its own distinct order, related to the nightjars. As for swifts and hummingbirds, they do not appear to be derived from nightjars, but are instead related to a group of birds (owlet-nightjars) from which they shared a common ancestor; one group becoming more adapted for daytime flight, and the other becoming more nocturnal. This group of hummingbirds, swifts, and owlet-nightjars then form a clade with the true nightjars and their kin.

I realized there are two other dilemmas one must solve if there is to be a terrestrial, nocturnal swift. Firstly, cave swiftlets are primarily diurnal, and only return to the safety of their caves at night. That one is probably easily solved. But the other one is that the members of the Apodiformes, hence the name, do not use their legs for much else than perching. A nocturnal, echolocating swift would be much more likely to stay on the wing and catch insects than become terrestrial.

By Metalraptor (not verified) on 17 Feb 2009 #permalink

Still, it does appear that nightjars, owlet-nightjars, and the other nightjar-esque species would radiate out to dominate the niches of nocturnal birds. They are already nocturnal, some of them have some form of echolocation (in the swifts only the cave swifts have echolocation), and they have better developed legs and wings, swifts cannot even land on flat surfaces.

By Metalraptor (not verified) on 17 Feb 2009 #permalink

If I could choose one bird as a pet, it would undoubtedly be the kiwi. Adorable little bird. If one has the funds, one can buy a kiwi skeleton (reproduction) from Skulls Unlimited. I think it costs something like $900.

As for terrestrial nocturnal birds there are several in addition to kiwis, thought they aren't flightless. Thick-knees (Burhinidae) for example, and some Coursers (Cursorius) and the Plains-Wanderer (Pedionomus)

By Tommy Tyrberg (not verified) on 21 Feb 2009 #permalink

I'm not in the sciences, just a curious NZ reader. Just thought I'd say: I was under the impression that kakapo are both nocturnal and terrestrial. Is that not the case?

By Matty Smith (not verified) on 01 Jul 2010 #permalink

Why is the kiwi egg so ridiculously oversized? Is the chick uber-precocial?

Not like a megapode, AFAIK -- but it's big. K-strategy.

By David MarjanoviÄ (not verified) on 02 Jul 2010 #permalink