In the previous article I provided brief reviews of all currently recognised pygopodid 'genera'*. Except one. I've left this one until last, largely because it's the most spectacular (up to 75 cm in total length) and (arguably) most fascinating pygopodid. We've seen throughout this series of articles that pygopodids are convergent with certain snake groups, and may in fact have been so successful at filling up ecological niches occupied elsewhere by colubroid snakes that they effectively prevented such snakes from evolving: you can imagine this as the 'pygopodids got there first' hypothesis.
As we'll see here, the Lialis species - the two snake-lizards - are strongly convergent with lizard-eating snakes in many respects [two individuals of the highly variable Burton's snake-lizard L. burtonis shown here; photos by Stewart Macdonald, used with permission. Notice what the animals are able to do with their pupils]. I don't know about you, but I find it absolutely remarkable that, of all squamates, gekkotans would be the ones that have come to mimic predatory snakes so closely in anatomy and behaviour.
* As you might have noticed if you followed the comments on the previous article, Wells (2007) proposed the new generic name Abilenia for the Aprasia species with longer, more pointed snouts, and also argued that Aprasia, Abilenia and Ophidiocephalus should be separated from Pypogodidae as the 'family' Aprasiaidae. I don't see anything wrong with using this name for the Ophidiocephalus + Aprasia clade, but recognising it as a 'distinct family' would mean that the remaining Pygopodidae is paraphyletic.
So, Lialis has to be one of the most remarkable of all gekkotans. Its skull is just incredible: look at the digimorph image below and remember that you're looking at a gekkotan lizard. The snout is extremely long and slender and the numerous teeth are fine, thin and hard to see without magnification. The post-orbital region of the skull is also elongate compared to that of other pygopodids: essentially, the whole of the skull has been 'stretched' considerably compared to the normal pygopodid (and gekkotan) condition. In the live animal, the head looks something like that of a miniature Chinese dragon [adjacent head drawings of the two species from Kluge (1974)].
The long jaws are presumably an adaptation for rapid (rather than powerful) biting and have allowed the evolution of an increased number of teeth and hence an improved ability to engage with smooth-scaled lizard prey. These especially slender jaws might also allow these predators to use their jaws as forceps and hence to pluck prey from small crevices (J. Weigel, cited in Patchell & Shine (1986a)). And while the teeth of pygopodids like Pygopus and Delma are sometimes described as 'peg-like' and suited for crushing, those of Lialis are pointed, recurved and hinged at their bases. This recalls the hinged teeth seen in specialised, skink-eating snakes: their teeth "fold down when pushed from the front, but [lock] into an erect position when pushed from behind (Patchell & Shine 1986a, p. 62).
While most pygopodids are predators of spiders and insects, the Lialis species are highly effective predators ('highly effective' because more than 80% of attacks are successful) of other lizards, especially skinks (agamids and elapid snakes are also eaten on occasion, and both cannibalism and predation on Delma have been observed in captivity) (Patchell & Shine 1986b). They wait for prey to come within reach before lunging, grabbing it at or anterior to the pectoral girdle, and they subdue it in their flexible jaws. Some of the lizards they swallow are proportionally big - often being bigger than those swallowed by similar-sized snakes.
Cranial kineticism and caudal luring
The frontoparietal joint is highly mobile so the whole snout can be flexed around the captured lizard [adjacent drawing by B. Jantulik, from Shea (1989)]. The muscular tongue then holds the prey against the upper jaw while the lower jaw is opened and used to manipulate the prey such that it's oriented to be pointing head-first toward the pygopodid's throat. By disengaging, lifting and re-engaging the upper jaw, the pygopodid is then able to drag the prey right into the mouth, eventually swallowing it whole and undamaged (Patchell & Shine 1986a).
This sounds superficially like what snakes do, and in a way it's reminiscent of the 'pterygoid walking' practised by alethinophidian snakes (where the teeth of the maxillae, pterygoids and mandibular rami are hooked into the prey and used to pull it back toward the throat prior to disengaging and moving forward for another cycle). However, 'pterygoid walking' occurs asymmetrically - the snake uses the maxilla, pterygoid and mandibular ramus on the left, then the maxilla, pterygoid and mandibular ramus on the right, and so on (for previous discussion see the scolecophidian article and stiletto snake article]. Lialis doesn't do this, and indeed it can't, as the two halves of its lower jaw aren't independently moveable. The Lialis technique also differs from the snake one in that the pygopodid's tongue is muscular and important in oral prey transport, whereas this definitely isn't the case in snakes. [Image of L. burtonis below by dad1, from wikipedia. Note that the tail tip is a different colour from the rest of the animal.]
Murray et al. (1991) described how unsuccessful attacks in L. burtonis would lead this pygopodid to switch tactics and draw the intended victim closer by way of 'caudal luring'. This behaviour - best known for pitvipers - involves rapid movement of the raised tail tip: intended lizard prey are then tricked into approaching the predator and hence come within striking range. It's assumed that the twitching tail tip mimics an insect larva or other small prey object. While many lizards twitch or wiggle their tails while preparing to grab prey, this seems to be the only case where the tail is apparently used as a lure. It's an interesting convergence with snakes. Indeed, as noted by Murray et al. (1991), Lialis is superficially snake-like in quite a few features: its skull and tooth shape, its cranial kinesis, sit-and-wait hunting style, preference for lizard prey, and its use of caudal luring.
You became a skink-eating specialist.... when, exactly?
I've made several inferences here about the acquisition of the morphological features seen in Lialis: I implied, for example, that its long, slender jaws and numerous teeth are modifications relative to the pygopodid 'ground-plan'. We don't have any fossil proto-types to go on, so these inferences are necessarily speculative. But they seem absolutely reasonable based on what we know about pygopodid (and whole-gekkotan) phylogeny: all the out-groups to Lialis (including all the pygopodids that surround it in the phylogeny [see simplified phylogeny below], and basal diplodactylines, carphodactylines and gekkonids) have relatively short, blunt, rounded snouts and lower tooth counts.
It appears reasonable to speculate that the various cranial and dental specialisations and the relatively large size of Lialis all evolved under selection to improve its performance as a lizard predator.
In the pypogodid phylogeny proposed by Jennings et al. (2003), the Lialis lineage diverged early on from other pygopodids (perhaps as early as the Late Eocene) while the lineages leading to the two extant Lialis species (L. burtonis of Australia and New Guinea, and L. jicari of New Guinea and New Britain) diverged during the Late Miocene. This raises the question of whether the evolution of Lialis occurred in step with that of its main prey, skinks.
Fossils demonstrate that the Australian skink radiation was well underway prior to the Late Oligocene (Martin et al. 2004) but there's no convincing evidence that the lineages involved were diversifying as early as the Late Eocene. However, while the Lialis lineage might have diverged in the Eocene, it doesn't necessarily follow that the specialised morphology of the crown clade evolved that early. We can't go any further for now: here's where we need fossils, as we have no idea at the moment when species along the Lialis stem took on the distinctive appearance of the crown clade. It's a fair bet that modification occurred prior to the Late Miocene, since the common ancestor of L. burtonis and L. jicari must have lived at or prior to this time, and it was surely 'modern' in appearance too. So - be sure to drop me a memo when you have a fossil snake-lizard...
Here ends our (if I say so myself) fairly comprehensive look at pygopodid gekkotans. I hope you enjoyed it - these lizards are fascinating and their diversity and biology needs to be better known, especially given that many are increasingly threatened by habitat fragmentation and loss. As I've been saying all along, my use here of the term pygopodid for the reduced-limbed snake-like clade is not universal and many herpetologists now use Pygopodidae for a more inclusive gekkotan clade. I'll be discussing this issue in the last article in the gekkotan series - I'm aiming to publish it soon... but, then, I often say stuff like this.
For previous articles in the gekkotan series, see...
- The Tet Zoo guide to Gekkota, part I
- Gekkota part II: loud voices, hard eggshells and giant calcium-filled neck pouches
- Squirting sticky fluid, having a sensitive knob, etc. (gekkotans part III)
- Lamellae, scansor pads, setae and adhesion... and the secondary loss of all of these things (gekkotans part IV)
- The incredible leaf-tailed geckos (gekkotans part V)
- 300 years of gecko literature, and the 'Salamandre aquatique' (gekkotans part VI)
- Whence Uroplatus and... there are how many leaf-tailed gecko species now?? (gekkotans part VII)
- Ptychozoon: the geckos that glide with flaps and fringes (gekkotans part VIII)
- Meet the pygopodids (gekkotans part IX)
- The pygopodid radiation: diverse diets and the 'pygopodids got there first' hypothesis (gekkotans part X)
- Blindsnake mimics, scaly-foots and javelin lizards (gekkotans part XI)
And for previous Tet Zoo articles on other kinds of squamates, please see...
- Pompey and Steepo, the world-record-holding champion slow-worms
- Arboreal alligator lizards - yes, really
- Amazing social life of the Green iguana
- Hell yes: Komodo dragons!!!
- Ermentrude the liolaemine
- Evolutionary intermediates among the girdled lizards
- The Great Goswell Copse Zootoca
- Of giant plated lizards and rough-necked monitors
- 'Cryptic intermediates' and the evolution of chameleons
- Tell me something new about basilisks, puh-lease
- Tongues, venom glands, and the changing face of Goronyosaurus
- Mosasaurs might have used the same microscopic streamlining tricks as sharks and dolphins
- Dinosaurs come out to play (so do turtles, and crocodilians, and Komodo dragons)
- Isopachys: worm-like skinks from Thailand and Myanmar
- Mystery emo skinks of Tonga!
- Cambodia: now with dibamids!
Refs - -
Jennings, W. B., Pianka, E. R. & Donnellan, S. 2003. Systematics of the lizard family Pygopodidae with implications for the diversification of Australian temperate biotas. Systematic Biology 52, 757-780.
Kluge, A. G. 1974. A taxonomic revision of the lizard family Pygopodidae. Miscellaneous Publications, Museum of Zoology, University of Michigan 147, 1-221.
Martin, J. E., Hutchinson, M. N., Meredith, R., Case, J. A. & Pledge, N. S. 2004. The oldest genus of scincid lizard (Squamata) from the Tertiary Etadunna Formation of South Australia. Journal of Herpetology 38, 180-187.
Murray, B., Bradshaw, S., & Edward, D. (1991). Feeding Behavior and the Occurrence of Caudal Luring in Burton's Pygopodid Lialis burtonis (Sauria: Pygopodidae) Copeia, 1991 (2) DOI: 10.2307/1446599
Patchell, F. C. & Shine, R. 1986a. Feeding mechanisms in pygopodid lizards: how can Liasis swallow such large prey? Journal of Herpetology 20, 59-64.
- . & Shine, R. 1986b. Food habits and reproductive biology of the Australian legless lizards (Pygopodidae). Copeia 1986, 30-39.
Shea, G. M. 1989. Family Pygopodidae. In Glasby, C. G., Ross, G. J. B. & Beesley, P. L. (eds). Fauna of Australia. Australian Capital Territory, Canberra. [published online.]
Wells, R.W. 2007. Some taxonomic and nomenclatural considerations on the class Reptilia. A review of species in the genus Aprasia GRAY 1839 (Aprasiaidae) including the description of a new genus. Australian Biodiversity Record 6, 1-17.
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I'd like to see a face-off between a lialis and a swallowtail caterpillar!
Oh, off topic, a proposed origin of feathers, insect wings, nipples and prolegs at my site.
Epic series; thanks very much.
One of my profs in grad school came back from Oz once with some live Lialis and we kept them for a while by tossing them Uta. So, so cool. That first pic captures the 45-deg angle at which that pointed snout is always held. I always suspected this pose matched some common feature of the local vegetation, like maybe eucalyptus leaf litter?
Watching at feeding time, I always got the distinct impression that they could wrap or bend their jaws around struggling prey. That xtra-cool skull pic suggests this might have been an illusion--those curves are built in.
Tet Zool rox
No illusion, Sven - major mesokinesis, as shown in the Jantulik drawing (and various published phtos). Mosasaurs seem to have an analogous bite mechanism, with similar overall head shape but the main kinesis at the middle of the mandible instead of the cranium. The extant hinge-toothed snake groups (Xenopeltis and various 'colubrids', see a couple of papers by Alan Savitzky) also have lots of intramandibular mobility but different mechanics, with shorter, rounded snouts.
And Lialis really is the acme of snake mimicry, in the sense that when night-driving it's impossible to distinguish one on the road from an elapid by the way they move (unless the tail is severely truncated). Not at all true of Delma or Pygopus.
And if you interchange stripes and bands (rotate all pattern elements 90 degrees!), I reckon that every colour and pattern morph in Lialis can be found in either Acanthophis (especially New Guinea forms) or Demansia. Also caudal lurers (or flushers in the whips' case).
Darren, have considered making this series (or some others) into published papers? I say we always need more general summaries of specialized groups in the literature. It makes it much easier to catch-up.
But this has been an amazing series. Them some mean-lookin' predatory snake-geckos.
Great series! Its funny to think that L. burtonis is a 'trash' lizard here in Oz. They're probably just below Boiga irregularis in being the most common reptile encountered at night, at least where I am. Nevertheless, I should really start photographing them more often.
Great series Darren, and really good to see the Aussie pygopids getting the attention they deserve. I'm getting quite fond of them: I've got flourishing colony of Delma tincta in my backyard around my compost bin and I see a 'Burton's' on a monthly basis when I'm out bush in summer- they are a spectacular beast, that unmistakable snout!
I'm going to forward this to my herp-nerd pals here in Alice Springs.
Is it clear what extant geckos might be closely related to pygopods? The head of that delma reminds me a bit of one of the new zealand geckos like naultinus or something.
It should be kept in mind, however, that pygopodids aren't alone in filling the 'typical colubrid [sic] niche' (if it can be called that) in Australasia. Some Australian elapid snakes (which are, of course, colubroids too) are also rather similar in morphology and/or ecology to certain 'colubrids' in other continents - just like the so-called death adders are similar to true vipers.
Also, as I've said in previous pygopodid comments threads, all available evidence suggests that 'colubrids' are (geologically speaking) very recent arrivals in Australasia. An Oligo-Miocene pygopodid radiation obviously can't have prevented 'colubrids' from evolving in Australia if the latter only arrived there in the Plio-Pleistocene.
Many thanks for comments. It's been a joy reading and writing about these animals. They definitely need a better online presence (wikipedia's coverage of them is really poor).
Zach: would love to get it all published in paper literature, but not sure what venue would want it.
Ethan: more on this topic in the next article, if you can wait that long.
Dartian: note that I said 'colubroids', not colubrids. But you're right - some elapids do what some colubrids (s. l.) do elsewhere.
Sorry, Dartian, I should have read your comment more carefully.
Sure they can - by filling up niches and hence removing ecological opportunities (both for 'colubrid'-like elapids, and for colubrids (s.s.) and homalopsids). This is why I called it the 'pygopodids got their first' hypothesis. I didn't say that pygopodids 'prevented' elapids/colubrids/homalopsids from evolving in Australia; rather, that they beat them to it in terms of filling up certain sections of ecospace.
The snout does look gekkotan to me, just lengthened, but not at all snake-like, with that large pitted maxilla and the tiny teeth.
Behind the eyes, the skull looks like that of a badly ossified aÃ¯stopod. :-) Except of course for the squamate-style quadrate.
How does Lialis breathe while swallowing? Does it have a snake-like protruding larynx?
Regarding a venue for publication (OK, not paper, but still useful): ToLWeb. It's really easy to get added as a scientific contributor. Try it.
Wonderful series as usual ... I've been following from the beginning. Any chance of a series on mosasaurs?
If it really is easy, then yes!!!
Hey, a thing I have wondered about before on this topic:
Why have only a few lineages of terrestrial vertebrates become limbless predators in this way? Seems like it would have been a fine thing for some mustelid to do. Or viverrids, better yet. OK, snakes may have evolved first and occupied the ecospace, but then why not a proto-mammal of some kind? Why are there no limbless terrestrial mammals?
@Shelton - How many limbless tetrapods (that just doesn't sound right) existed in the Permian and early Triassic? I suspect that this was a bauplan that evolution had not yet stumbled upon (save for caecilians, but that is more fossorial). The other thing to keep in mind is that while many squamates evolved limblessness, it seemed that it wasn't until the advent of limblessness and extreme streptostyly that the snake-like bauplan really took off. There seems to be something about being limbless and yet still able to tackle large prey, that opens up vast new opportunities. At least that's the current thinking.
FWIW, among the "lepospondyls", there are limbless tetrapods from the Carboniferous and Permian, such as Ophiderpeton, Oestocephalus and Phlegethontia.
And there is the specialised Miocene fossorial hedgehog Proterix, which is said to be possibly limbless, although it's just as likely that limb elements just haven't been found yet.
@18: Not that anyone is expressing interest, but I chased down the Proterix reference, and it's freely available at http://deepblue.lib.umich.edu/bitstream/2027.42/48612/2/ID475.pdf, p. 91, with reduced limb speculation at p. 97.
Thanks to the anonymous commenter at Lord Geekington (and Darren)for the lead.
We had that discussion just a few posts ago...
Probably it's because it would be impossible for a snake-shaped animal to keep a constant body temperature. Already, weasels have a metabolism that is twice as high as in other mammals of that mass, because otherwise they just can't keep up with the heating.
The mammalian tradition of dorsoventral as opposed to lateral undulation may also play a role.
These are aÃ¯stopods. They were probably terrestrial, but lacked skull kinesis.
The Early Carboniferous adelogyrinids and Acherontiscus are possibly limbless possible lepospondyls. :-) They were, however, aquatic and more comparable to eels than to snakes.
At least as eel-like were the Late Carboniferous and Early Permian lysorophians, which had very short limbs and very long trunks (the extreme is the Permian Brachydectes elongatus with 97 presacral vertebrae). They (or at any rate B. elongatus) aestivated in burrows, like lungfish.
@Zach miller I agree with you.This is one of the best written piece that i have read in long time.This series can be put together in a form of ebook and i am sure that it will sale like hot cake.This series has increased my interest in reptiles.