Agamids are a widespread, diverse iguanian lizard group that I have a special fondness for and consequently have featured several times on Tet Zoo (see links below). Of course, I’ve never featured them enough, nor discussed or even mentioned whole groups of species that really should get adequate coverage here. In a recent article I discussed several taxa within the Australian earless dragon clade Tympanocryptis. Today, I want to expand the discussion somewhat by looking at Australian agamids more generally.

There are about 70 agamid species in Australia (though maybe much more), all belonging to the clade Amphibolurinae and vernacularly termed amphibolurines or amphiboluroids or just dragons (waitaminute... isn't that term in use someplace else?). This group is not endemic to Australia since species also occur in tropical eastern Asia and New Guinea as well. As you’d predict, species also occur on various of the islands between Australia and the Asian mainland.

Amphibolurines include long-tailed, superficially iguana-like rainforest and woodland forms, short-snouted, spiny-bodied animals of dry woodlands and deserts, and a large number of slender, highly gracile semi-arboreal and desert-dwelling specialists. Then there are weirdos like the pebble-mimics, the ant-eaters that are covered in thorn-like spines, and so on. The majority are predators of arthropods. The larger species, however, are capable of tackling and eating other reptiles and even nestling birds and small mammals, and some are omnivorous and will eat flowers and fruits.

Several things make this lizard radiation especially fascinating. For one, it includes a number of morphologically and behaviourally bizarre animals. Perhaps the most familiar is the Frilled lizard, Frilled dragon or Frillynecked dragon Chlamydosaurus kingii, a highly variable, mostly insectivorous agamid that reaches 85 cm in total length and is predominantly arboreal. Its terrestrial bipedal behaviour is well known: TV documentaries often show these lizards sprinting bipedally away from menacing camera-holding humans, but they’re also known to engage in peculiar, prancing bipedal locomotion as their normal method of moving at ground level (Shine & Lambeck 1989). That’s right – this is a (faculatively) bipedal lizard.

The famous frills of these lizards – controlled by massively enlarged hyoid bones and borne on a proportionally long neck (Shine 1990) – are used by the males in dominance battles. Recent work shows that the reddishness of the frill is controlled by the presence of caretenoids, with males judging the quality of opponents based on this reddishness (Hamilton et al. 2013). We know that the frill is used to intimidate would-be predators, but it seems that sexual selection has also contributed to its evolution (Shine 1990). Somebody now needs to test female preference as goes frill ornamentation in these animals (Hamilton et al. 2013).

Moving on -- there’s also the Thorny devil Moloch horridus, sometimes just called the Moloch, a tiny, slow-moving, rather sedentary, spiky, desert-dwelling, myrmecophagous (= ant-eating) amphibolurine that’s strongly convergent with the horned lizard (Phrynosoma) of North America. Thanks mostly to work by Eric Pianka and colleagues, we know a fair bit about the ecology, behaviour and life cycle of this remarkable lizard. Females are bigger than males (a peculiar feature for a lizard) and there are indications that individuals are reasonably long-lived, perhaps surviving into their third decades (remember that this is an animal less than 20 cm long). Females construct a burrow with a large open chamber at the end (about 8 x 13 x 15 cm in size) and the hatchlings apparently eat their eggshells. Both features are also very unusual (if not unique) within lizards (Pianka & Vitt 2003). All populations of Moloch are currently regarded as belonging to the same single species. However, variation in foot anatomy has at times led to the suggestion that there might actually be a set of cryptic species here: a hypothesis that awaits an analysis of variation within Moloch across its range.

Moloch: young, novel and deeply nested, or old, early and independent?

Despite its extreme weirdness, Moloch has been argued by some authors to be a geologically young novelty, deeply nested within the amphibolurine radiation, and specifically within the clade of dry-adapted lineages. A close affinity with the forest and angle-headed dragons (Hypsilurus) has been supported in some studies (Macey et al. 2000, Hugall et al. 2008) and Pyron et al. (2013) even found both Moloch and Chelosania brunnea (the unique Ring-tailed dragon or Chameleon dragon) to be nested within Hypsilurus. Rather than finding Moloch to be a recently evolved ‘core member’ of Amphibolurinae, Hugall et al. (2008) and Pyron et al. (2013) found Moloch, Hypsilurus and Chelosania to belong outside the clade that contains the majority of amphibolurine lineages.

This was also recently supported by Hutchinson & Hutchinson (2011) who showed that Moloch has the 12 chromosome pairs thought primitive for Agamidae. This makes it likely that it’s probably outside the main amphibolurine radiation, the members of which are united by the presence of 10 chromosome pairs. Chelosania also has the primitive 12 chromosome pairs. If Hugall et al. (2008), Hutchinson & Hutchinson (2011) and Pyron et al. (2013) are right, Moloch evidently adapted to desert conditions all on its own, very much independently from the dry-adapted ‘core’ amphibolurines. Intriguingly, Chelosania is an animal of dry woodlands and not rainforest, so it might also be part of an early movement into drier habitats (Hugall et al. 2008).

Forest dragons and angle-headed dragons: there are more than you think

I just mentioned Hypsilurus. This is one of those fantastically ornate iguanian taxa. Boyd’s forest dragon H. boydii, one of the biggest and most ornate of the group, has enlarged cheek plates, tall nuchal and dorsal crests topped with curved, laterally compressed spines, and a giant dewlap, also lined with large spines. If you know the literature on Australian reptiles, you’ll likely think of Hypsilurus as a group that contains just two species: the second being the Southern angle-headed dragon H. spinipes. In fact, there are about 20 of the things, four of which (H. hikidanus, H. magnus, H. ornatus and H. tenuicephalus) were named in 2006 (Manthey & Denzer 2006). These inhabit New Guinea, the Aru Islands, the Bismarck Archipelago, the Solomon Islands and various of the small surrounding islands.

Are there more than just two species in Australia? H. longii has been reported from Cape York Peninsula but this is considered doubtful by some authors. And a very surprising record of the genus is a single photographic record – said to depict H. dilophus – from way out to the west in Sulawesi (Manthey & Denzer 2006). If this record is valid, it suggests the presence of cryptic or extinct populations that must have occurred in between those on and around New Guinea and those on and around Sulawesi. The historical taxonomy of the Hypsilurus species is a fairly complex nightmare, by the way: they have been extensively confused with (and often considered congeneric or synonymous with) the draconine agamid Gonocephalus.

Dissolution of the water dragons

Excluding that weird, wayward record of Hypsilurus, the only amphibolurine outside of Australasia and its surrounding islands is Physignathus, the Green or Chinese water dragon [adjacent image by Marcel Burkhard]. Typically, two extant Physignathus species have been recognised: the superficially iguana-like Eastern or Australian water dragon P. lesueurii of Australia's Pacific seaboard and southern New Guinea, and the Green or Chinese water dragon P. cocincinus, familiar to anyone who's ever walked into a pet shop that sells reptiles.

While both are superficially alike and both lounge around on branches that overhang water (and swim capably when the need arises*), they look extremely different in detail. Are these two really close relatives? Actually, they never group together in phylogenetic studies, the Eastern water dragon being closer to other amphibolurines than is the Chinese water dragon (Honda et al. 2000, Macey et al. 2000, Hugall & Lee 2004, Hugall et al. 2008, Townsend et al. 2011, Pyron et al. 2013). Since the Chinese water dragon is the type species for the name Physignathus (Georges Cuvier came up with the binomial Physignathus cocincinus in 1829), the Eastern water dragon needs a new name. After several false starts, it has been argued (Amey et al. 2012) that a generic name proposed by Wells & Wellington (1985) is the one we have to stick with. Thus the Eastern water dragon is now Intellagama lesueurii. No etymology was ever provided for the name Intellagama: I wonder what it means?

* The Eastern water dragon is even able to remain submerged for a considerable period – an hour or more, apparently. It exhibits a diving response – its heart rate slowing and rate of oxygen consumption decreasing – and is also able to release CO2 cutaneously (Pianka & Vitt 2003). Image of swimming water dragon below by D. Gordon E. Robertson.

There are two main competing phylogenetic hypotheses regarding the position of water dragons relative to other amphibolurines: each implies a different biogeographical scenario for the group. In some studies, the Chinese water dragon is recovered as the sister-taxon to remaining amphibolurines (Macey et al. 2000, Hugall & Lee 2004, Hugall et al. 2008, Pyron et al. 2013) – a topology which suggests that amphibolurines originated in mainland Asia and that all members of the Australasian clade descend from a single ancestor that invaded this region after migrating away from Asia (strengthening this scenario is the fact that all non-amphibolurine agamids are Eurasian or African). In other studies, the species is nested within Amphibolurinae, being closer to Chlamydosaurus and Pogona (a genus we'll look at in part II) than is Lophognathus (Honda et al. 2000). If this is right, Physignathus is of Australian ancestry and members of its lineage moved away at some point, eventually getting as far as mainland Asia. The first scenario is looking more likely.

Intellagama is known from reasonably abundant remains to have been present in the Miocene of Queensland (where its jaws and other bones are preserved at Riversleigh). The fossils – identified by Covacevich et al. (1990) as Physignathus sp. (of course, now this should be Intellagama sp.) – indicate that members of this lineage have therefore been in existence for something like 20 million years. [UPDATE: see comment # 66 below (by John Scanlon). Those Riversleigh fossils may not belong to Intellagama at all.] Phylogenies indicate that Intellagama is outside the clade that contains Ctenophorus and the dry-adapted ‘core’ amphibolurines, so its antiquity is consistent with the idea that most of the amphibolurine radiation occurred some time after the start of the Miocene.

‘Ta ta dragons’: Lophognathus and… Gowidon?

Intellagama is somewhat similar in overall appearance to the several Lophognathus dragons – in fact, both have been considered synonymous by some authors in the recent past*, and at least some species of Lophognathus are sometimes called water dragons too. An alternative vernacular name – Ta ta dragons – refers to their habit of waving their limbs after moving on hot surfaces (‘Ta ta’ is a colloquial term for ‘goodbye’ in some parts of the world). Seeing as I’d like to be able to distinguish these animals from other Aussie dragons, I wonder if we should stick with this term. What the hell; it’s what I’m going to do here. Ta ta dragons occur widely across the upper two-third or so of Australia. L. temporalis inhabits both coastal northern Australia as well as New Guinea while L. maculilabris is unique to the Tanimbar Islands (or Timor Laut) of the Lesser Sundas. Wait a minute... this means it's another non-Australasian amphibolurine, right?

* Lophognathus was also long considered synonymous with Amphibolorus but, then, so were most other amphibolurines, so this doesn’t mean much.

Of the several species, the greyish or reddish-brown Gilbert’s dragon L. gilberti is comparatively short-snouted and hence looks more Intellagama-like than some of the others. However, as is the case with several of the agamids discussed here, L. gilberti seems to be a species complex (Cogger 2000. Melville et al. 2011), and molecular results indicate that some of the populations conventionally included in this species are not close relatives – in fact, one of them is an unnamed taxon within Amphibolurus (another genus we'll look at in part II). Are ta ta dragons really close to the Physignathus water dragons? The phylogenies say no (Honda et al. 2000, Hugall et al. 2008, Melville et al. 2011, Pyron et al. 2013).

And are all of the ta ta dragons close relatives anyway? Gilbert’s dragon looks different from the more boldly striped, generally longer-tailed, longer-snouted species and these differences and others led Wells & Wellington (1983) to propose the new genus Gowidon for L. longirostris and others. Support for this view comes from the fact that Melville et al. (2011) found Lophognathus as most usually conceived to be polyphyletic, with L. longirostris and L. temporalis both grouping as distinct lineages close to a Rankinia + Pogona + Tympanocryptis clade, and L. burnsi and L. gilberti being close to Amphibolurus (and not, incidentally, closer to each other than they were to the included Amphibolurus species) (see also Pyron et al. 2013). A fair bit of work is needed to sort out the phylogeny and systematics of these animals.

We’re not done yet – there’s lot more to say. So stay tuned for part II, coming soon. And I need to finish by saying thank you to the several wonderful individuals who let me use their photos, and thus made this article possible. Thank you Adam Yates (who now blogs at A Fragment of Gondwana), Stephen Zozaya (check out his blog: Saurian Obsessions!) and Tony Gamble. This article literally would not have happened without their help.

For previous Tet Zoo articles on agamids and other iguanian lizards, see…

Refs - -

Amey, A. P., Couper, P. J. & Shea, G. M. 2012. Intellagama lesueurii (Gray, 1831), the correct binomial combination for the Australian Eastern Water Dragon (Sauria, Agamidae). Zootaxa 3390, 65-67.

Covacevich, J. A., Couper, P., Molnar, R. E., Witten, G. & Young, W. 1990. Miocene dragons from Riversleigh: new data on the history of the family Agamidae (Reptilia: Squamata) in Australia. Memoirs of the Queensland Museum 29, 339-360.

Cogger, H. G. 2000. Reptiles and Amphibians of Australia. Reed New Holland, Sydney.

Hamilton, D. G., Whiting, M. J. & Pryke, S. R. 2013. Fiery frills: carotenoid-based coloration predicts contest success in frillneck lizards. Behavioral Ecology 24, 1138-1149.

Honda, M., Ota, H., Kobayashi, M., Nabhitanhata, J., Yong, H.-S., Sengoku, S. & Hikida, T. 2000. Phylogenetic relationships of the family Agamidae (Reptilia: Iguania) inferred from mitochondrial DNA sequences. Zoological Science 17, 527-537.

Hugall, A. F., Foster, R., Hutchinson, M. & Lee, M. S. Y. 2008. Phylogeny of Australasian agamid lizards based on nuclear and mitochondrial genes: implications for morphological evolution and biogeography. Biological Journal of the Linnean Society 93, 343-358.

- . & Lee, M. S. Y. 2004. Molecular claims of Gondwanan age for Australian agamid lizards are untenable. Molecular Biology and Evolution 21, 2102-2110.

Hutchinson, M. N. & Hutchinson, R. G. 2011. Karyotypes of Moloch and Chelosania (Squamata: Acrodonta). Journal of Herpetology 45, 216-218.

Macey, J. R., Schulte, J. A., Larson, A., Ananjeva, N. B., Wang, Y., Pethiyagoda, R., Rastegar-Pouyani, N. & Papenfuss, T. J. 2000. Evaluating trans-Tethyan migration: an example using acrodont lizard phylogenetics. Systematic Biology 49, 233-256.

Manthey, U. & Denzer, W. 2006. A revision of the Melanesian-Australian angle head lizards of the genus Hypsilurus (Sauria: Agamidae: Amphibolurinae), with description of four new species and one new subspecies. Hamadryad 30, 1-40.

Melville, J., Ritchie, E. G., Chapple, S. N. J., Glor, R. E. & Schulte, J. A. 2011. Evolutionary origins and diversification of dragon lizards in Australia’s tropical savannas. Molecular Phylogenetics and Evolution 58, 257-270.

Pianka, E. R. & Vitt, L. J. 2003. Lizards: Windows the Evolution of Diversity. University of California Press, Berkeley.

Pyron, R. A., Burbrink, F. T. & Wiens, J. J. 2013. A phylogeny and revised classification of Squamata, including 4161 species of lizards and snakes. BMC Evolutionary Biology 2013, 13:93 doi:10.1186/1471-2148-13-93

Shine, R. 1990. Function and evolution of the frill of the frillneck lizard, Chlamydosaurus kingii (Sauria: Agamidae). Biological Journal of the Linnean Society 40, 11-20.

Shine, R. & Lambeck, R. 1989. Ecology of Frillneck lizards in tropical Australia. Australian Wildlife 16, 491-500.

Townsend, T. M., Mulcahy, D. G., Noonan, B. P., Sites, J. W., Kuczynski, C. A., Wiens, J. J. & Reeder, T. W. 2011. Phylogeny of iguanian lizards inferred from 29 nuclear loci, and a comparison of concatenated and species-tree approaches for an ancient, rapid radiation. Molecular Phylogenetics and Evolution 61, 363-380.

Wells, R. W. & Wellington, C. R. 1985. A classification of the Amphibia and Reptilia of Australia. Australian Journal of Herpetology, Suppl. Ser. 1, 1-61.