One of my shortish-term goals at Tet Zoo has been to complete the series on gekkotan lizards I started in April 2010 (see below for links to previous parts). We continue with that series here, and this time round we’re going to look at what should definitely be regarded as the weirdest of gekkotans: the near-limbless pygopodids, pygopods or flap-footed lizards, all of which inhabit Australia and New Guinea (and at least some of the surrounding islands). Because there’s a lot to say about them, the article you’re reading is the first of three. [Excellent paintings below by Alan Male, from Philip Whitfield's 1983 Reptiles & Amphibians. These were the first images of pygopodids I ever saw.]
For the record, I’m using Pygopodidae in the restrictive, ‘traditional’ sense here. As we’ll see in a later article, most authors now use Pygopodidae for a more inclusive clade that also includes certain limbed gekkotan lineages (if you can’t wait until then, there’s preliminary discussion of the issue at hand here).
Anyway, Pygopodidae of tradition consists of about 40 species arranged in eight genera (Aclys, Aprasia, Delma, Lialis, Ophidiocephalus, Paradelma, Pletholax and Pygopus), though not all of these names are used by all authors. As is typical for Australasian herps, new species are described fairly regularly. The newest at the time of writing is Roberts’ scaly-foot Py. robertsi Oliver et al., 2010 from Queensland.
The literature on pygopodids is fairly scattered across the herpetological journals. Harold Cogger’s Reptiles & Amphibians of Australia includes species-by-species accounts with excellent photos (Cogger 2000), and an enormous amount of information on all taxa known up to the time of publication is included in Arnold Kluge’s monograph on the group (Kluge 1974) (oh, how I’d love an original copy).
Right across Australia, and hello New Guinea
Pygopodids occur right across continental Australia, but don’t occur on Tasmania (though… there are some Tasmanian records; to be discussed in a later article). They’re extremely abundant in some areas: Kluge wrote of areas where Aprasia individuals could be discovered beneath virtually every single slab or chip or rock, and it’s common to find several species living in sympatry. Indeed, in the area that seems to be the centre of pygopodid distribution (the lower west coast of Western Australia), as many as ten species can be found in the same area (Shea 1989).
While New Guinea is home to pygopodids, only the two Lialis species occur there. Of those, one of them – Burton’s snake-lizard L. burtonis – is tremendously widespread across the pygopodid range in general, occurring right across mainland Australia and also being found on islands in the Torres Strait and on the Aru Islands (Kluge 1974) [L. burtonis shown above; image by Smacdonald, from wikipedia]. The other – L. jicari – is unknown from Australia; as well as mainland New Guinea it’s also present on New Britain (Kluge 1974).
Some pygopodids (like the Delma species) can be regarded as ‘primitive’ within the group as they have external ear openings, relatively large hindlimbs and a crushing dentition. Others, however, are more specialised and are remarkably convergent with snakes, lacking external ear openings and possessing slim, lengthy skulls and recurved, slender teeth. In fact, the snake-like niches occupied by some pygopodid taxa might explain why certain kinds of snake are low in diversity or absent in parts of arid Australia (Patchell & Shine 1986). Some pygopodid species (including species of Delma, Paradelma and Pygopus) seemingly mimic elapid snakes when threatened, raising their dark-patterned heads, flattening their necks and flicking their tongues (Johnson 1975, Pianka & Vitt 2003). Most pygopodids are convergent with snakes in possessing large head scales (ironically, the especially snake-like Lialis is the exception). We’ll be having a more detailed look at phylogeny and evolutionary history in the next article. [Adjacent photo shows a juvenile Py. schraderi. Photo by Henry Cook, from the Aussie pythons & snakes forum.]
Partly because limblessness is assumed to be disadvantageous to a tetrapod, it’s sometimes been regarded as paradoxical that pygopodids are extremely diverse in ecology and behaviour. Indeed, they do several things that ‘normal’ gekkotans don’t. Rather than being inhibitive to diversification and speciation, it seems that the evolution of limblessness and a snake-like body plan allowed pygopodids to undergo a fairly impressive radiation. Or, to quote Webb & Shine (1994): “For reasons that are unclear, the evolution of an elongate limb-reduced morphology in early pygopodids appears to have opened the floodgates for subsequent evolutionary modifications of an astonishing scale” (p. 397).
Some basics of anatomy, behaviour and biology
The pygopodid pectoral girdle is a vestigial, V- or U-shaped structure arranged ventral to the fourth, fifth and sixth vertebrae (Stokely 1947). There is never any external trace whatsoever of forelimbs, but a humerus is present internally in Aprasia, Pletholax and Ophidiocephalus (Kluge 1976). The humerus is a ‘floating’ structure: it doesn’t articulate with the scapula.
In the pelvis, the ilium has remained large (often, but not always, maintaining a contact with a single vertebra) and it still has the recognisable form typical of squamates. The hindlimb is variable. In some taxa (e.g., some species of Aprasia), just a vestigial, rod-like femur is present, while in others (e.g., some species of Pygopodus) the hindlimb is complete and still has four digits [hindlimb of Py. lepidopodus shown above; from Shea (1989)]. However reduced it is, this limb skeleton forms the core of the flap-like hindlimb that explains some of the common names used for members of this group. These limbs are quite flexible and can be abducted to a degree normal for a lizard’s hindlimb (the animals sometimes do this by choice, as if it helps them to ‘stand’ on the substrate). Most sources state that males use these limbs to help grip females during mating.
However, little mentioned is that males of at least some species (or all species?) also possess paracloacal spurs, one on each side of the cloaca (and normally hidden from view by the hindlimbs) [adjacent photo shows paracloacal spur (in box) of Py. schraderi, as revealed by lifting hindlimb. Photo by Henry Cook, from the Aussie pythons & snakes forum]. They look much like the far better known spurs of male boas and pythons. Evidently, the pygopodid ‘spurs’ are nothing to do with the hindlimbs – they’re neomorphs (and they aren’t unique to pygopodids: they also occur in carphodactylid and diplodactylid gekkotans). This got me thinking.
It’s widely thought that the cloacal spurs of boas and pythons are relictual hindlimb remnants – but could they actually be neomorphs too, and not genuine hindlimbs? Well, no. Embryological work demonstrates pretty convincingly that the ‘relictual hindlimbs’ of certain modern snakes really are relictual hindlimbs (Cohn & Tickle 1999) (this issue was previously discussed in Monster pythons of the Everglades: Inside Nature’s Giants series 2, part II). On a more speculative note, does the presence of cloacal spurs mean that pygopodids have the evolutionary potential to evolve an extra set of posterior limbs?
Like other gekkotans, pygopodids possess cloacal bones (also known as post-cloacal bones). These curved, serrated structures project from the tips of the everted hemipenes in males and various roles in copulation have been suggested.
Tail length is highly variable in pygopodids: in some species the tail is as much as four times as long as snout-vent length (SVL), while in others it’s much less than SVL. As we’ll see later, at least one species uses the tail tip as a lure.
Some pygopodids are able to jump: to literally lift the entire body and tail off the substrate and repeatedly move upwards and forwards in a weird, jerky manner. A 74-cm-long Delma got its whole body 7 cm off the ground (Bauer 1986). They do this to startle or disorientate potential predators. A few other limbless squamates (including some amphisbaenians, vipers, gymnophthalmids and glass lizards) can do the same trick. When climbing in shrubs, Delma is able (in emergencies) to use the tail to leap, at the same time straightening its body. The result is that individuals “thrust … through vegetation like arrows!” (Pianka & Vitt 2003, p. 27). Caudal autotomy is common in pygopodids, even in those saltating species. [Adjacent photo shows D. inornata; photo by Damian Michael, from Michael et al. (2010).]
Comparatively little is known about the life history of pygopodids. Data from individuals kept in captivity suggests that they are not long-lived (that it, not living for more than seven years or so. If correct, this is a massive contrast with Northern Hemisphere limbless squamates like anguids. They live for a few decades at least). We do know that females are larger than males: you might think that this is unusual for lizards, but it actually seems to be normal for gekkotans. Pygopodids are also typical among gekkotans in being oviparous and in only producing two eggs per clutch (though one or three eggs are sometimes produced by aberrant members of some species). Sexual dimorphism isn’t limited to size: in Aprasia, males have teeth in their premaxillae while females (usually) don’t (Aprasia also lacks teeth in the maxillae, so has a strongly reduced dentition overall: more on this later). This doesn’t seem related to differences in diet, so might be the result of sexual selection pressure.
Some species are reported to emit buzzing and rattling noises when startled (Kluge 1976), most typically the Delma species. Squeaks have also been reported from some pygopodids. These are true vocalizations, and at least some of these noises might be employed in intraspecific communication. D. butleri is said to be able to rapidly brighten the yellow colour of its belly when stressed. [Image below shows a fairly scary-looking individual of L. burtonis; photo by Damian Michael, from Michael et al. (2010). This species is famously variable in pigmentation and patterning.]
I didn’t get to cover pygopodid diversity much in this article, nor look at phylogenetic hypotheses proposed for the group. This is what we’ll be covering next.
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)
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 – –
Bauer, A. M. 1986. Saltation in the pygopodid lizard, Delma tincta. Journal of Herpetology 20, 462-463.
Cogger, H. G. 2000. Reptiles & Amphibians of Australia (Sixth Edition). New Holland Publishers, Sydney.
Cohn, M. J. & Tickle, C. 1999. Developmental basis of limblessness and axial patterning in snakes. Nature 399, 474-479.
Johnson, C. R. 1975. Defensive display behaviour in some Australian and Papuan-New Guinean pygopodid lizards, boid, colubrid and elapid snakes. Zoological Journal of the Linnean Society 56, 265-282.
Kluge, A. G. (1974). A taxonomic revision of the lizard family Pygopodidae. Miscellaneous Publications, Museum of Zoology, University of Michigan, 147, 1-221 [free pdf available here!]
– . 1976. Phylogenetic relationships in the lizard family Pygopodidae: an evaluation of theory, methods and data. Miscellaneous Publications, Museum of Zoology, University of Michigan 152, 1-72.
Michael, D., Lindenmayer, D., Crane, M., Herring, M. & Montague-Drake, R. 2010. Reptiles of the NSW Murray Catchment: A Guide to Their Identification, Ecology and Conservation. CSIRO Publishing, Collingwood (Vic.).
Patchell, F. C. & Shine, R. 1986. Food habits and reproductive biology of the Australian legless lizards (Pygopodidae). Copeia 1986, 30-39.
Pianka, E. R. & Vitt, L. J. 2003. Lizards: Windows the Evolution of Diversity. University of California Press, Berkeley.
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.]
Stokely, P. S. 1947. The post-cranial skeleton of Aprasia repens. Copeia 1947, 22-28.
Webb, J. K. & Shine, R. 1994. Feeding habit and reproductive biology of Australian pygopodid lizards of the genus Aprasia. Copeia 1994, 390-398.