[In image above, Usambara three-horned chameleon Trioceros deremensis at top left, photographed by Benjamin Klingebiel, CC BY-SA 2.0; Lance-nosed or Blade chameleon Calumma gallus at top right, photo by Brian Gratwicke, CC BY 2.0; the spiny-backed Madagascan chameleon below is, I think, Furcifer verrucosus, photo by Andy Farke, used with permission.]

In that previous article I mentioned James Martin’s 1992 book Chameleons: Nature’s Masters of Disguise (Martin 1992) and said that it was pretty much the only thing approaching a comprehensive chameleon-themed volume on the market.

Cover of Tolley & Herrel (2013), another must-have.

How wrong I was. It turns out that there’s an excellent multi-authored technical tome on chameleons: Krystal Tolley and Anthony Herrel’s 2013 The Biology of Chameleons (Tolley & Herrel 2013). I must get it, and until I do I can’t say any more about it. Anyway…

We saw in the previous article that Klaver & Böhme (1986) used data from hemipenis and (to a lesser extent) lung morphology to show that the taxonomic scheme used prior to their study did not accurately reflect the morphological variation or evolutionary history of chameleons. Accordingly, they resurrected the name Rhampholeon for the African leaf chameleons. And, later on, Rieppeleon was coined for species previously included, erroneously, within Rhampholeon.

But Klaver & Böhme (1986) did so much more than resurrect Rhampholeon. They also proposed that Chamaeleo of tradition was so diverse that it should be split into four distinct genera: Chamaeleo sensu stricto, Calumma, Furcifer and Bradypodion.

Here's that annotated hypothetical chameleon again. Image by Darren Naish.

Calumma and Furcifer are both Madagascan. Both are old names (published in 1865 and 1831, respectively) resurrected from synonymy. While both will, by now, be familiar to you if you know your chameleons, this wasn’t the case until recently and it took a while for them to creep into the non-technical literature.

Calumma tarzan... yes, a chameleon named (by Gehring and colleagues in 2010) after Tarzan. Photo by Sebastian Gehring, CC BY-SA 3.0.

Calumma contains about 30 species, the most familiar of which is the often very large Parson’s chameleon C. parsonii. They’re all mid-sized to large, arboreal, colour-changing chameleons that tend to have sexually dimorphic cranial display structures like rostral appendages, tall casques and occipital lobes. The rostral appendage is comparatively huge in some species, like the spectacular Lance-nosed or Blade chameleon C. gallus.

Lance-nosed or Blade chameleon Calumma gallus. Photo by Brian Gratwicke, CC BY 2.0.

Furcifer chameleons are also arboreal, ‘typical’ chamaleons. About 20 species are currently known, the most familiar of which is the Panther chameleon F. pardalis, a now common animal in the pet trade (insert usual complaint about chameleons being poorly suited for life in captivity). They generally have rounded casques that lack occipital lobes. Rostral appendages are present in the males of some species and are sometimes forked (as in, for example, F. petteri and F. willsii). Gular and ventral crests are often present too.

Up close and personal with a wild Furcifer pardalis on Reunion (yes, Reunion: the species has been introduced here, it seems). Photo by Gunnar M. Kvifte, CC-BY.

Incidentally, some of the key divergences within these two genera are thought, on the basis of molecular distances calibrated on fossils, to have occurred during the Oligocene and even Eocene (that is, anywhere between about 25 and 50 million years ago). This means that some of the lineages within these groups are really very old – old enough that it’s certainly conceivable that some of them might, in future, be considered worthy of generic rank as well.

The African dwarf chameleons. The set of mainland African chamaeleonines grouped together in Bradypodion again required the resurrection of an old name, first published in 1843. The Bradypodion species are generally termed African dwarf chameleons. As suggested by that name, they’re small, with SVLs (snout-to-vent lengths) ranging from 50 to 110 mm.

A Bradypodion montage. Above: B. damaranum, from Stuart-Fox & Moussalli (2008), CC BY 2.5. Below: Namaqua dwarf chameleon B. occidentale, photographed by Javier Abalos Alvarez, CC BY-SA 2.0.

In contrast to the Brookesia, Rhampholeon and Rieppeleon leaf chameleons, the Bradypodion species look like miniature ‘conventional’ chameleons, possessing prehensile tails and being habitual climbers in trees, shrubs and also reeds and grasses. They’re often associated with Mediterranean-style habitats and heathland. Molecular studies indicate that Bradypodion is the sister-group to the chamaeleonine clade that includes Chamaeleo and other ‘conventional’ lineages (Raxworthy et al. 2002, Tolley et al. 2013).

A chameleon cladogram - this time a more complex version... topology based on Tolley et al. (2013). Brookesia by Frank Wouters, CC BY-SA 2.0; Rieppeleon by R. J. Blach, CC BY-SA 3.0; Rhampholeon by Martin Nielsen, CC BY-SA 4.0; Bradypodion by Javier Abalos Alvarez, CC BY-SA 2.0; Chamaeleo by Raju Kasambe, CC BY-SA 3.0; Furcifer by Gunnar M. Kvifte, CC-BY; Calumma by Steve Wilson, CC BY 2.0;Trioceros by Benjamint444, CC BY-SA 3.0.

There are currently about 18 Bradypodion species but the presence of numerous small, poorly studied, isolated populations means that the systematics of the group is somewhat unresolved: these populations tend to prove to be new lineages when analysed, cryptic species seem to abound, and there are several populations that have been confirmed as new species but have yet to be named.

The casque is well developed, prominent gular and dorsal crests are often present, and they all seem to be viviparous, females giving birth to between 5 and 20 babies sometimes 2 or even 3 times during a season (Alexander & Marais 2007). These lizards grow quickly, reaching maturity in a year or two, and only living for between 3 and 5 years. It’s all ‘live fast, die young’, a strategy that’s present in other iguanians (we previously looked at it in Australian dragons) but isn’t generally appreciated as a strategy that lizards have gone in for. Well, they have. Incidentally, one suggested driver of this strategy is the prevalence of fire as a selection agent! There’s some interesting work linking the sexual dimorphism present in Bradypodion with habitat preference (Stuart-Fox & Moussalli 2007).

A Bradypodion pumilum drinking water (chameleons mostly, perhaps exclusively, drink from droplets as shown here). Photo by Michnieuwoudt, CC BY-SA 3.0.

Trioceros chameleons: more than T. jacksonii! Another group only recently (2009) elevated to full ‘generic rank’ is Trioceros, a tropical African chameleon clade endemic to a belt stretching from the Gulf of Guinea to Ethiopia, and south to northern Mozambique (Tilbury & Tolley 2009). Species from the Middle East, India and elsewhere previously included within Trioceros are now placed elsewhere. Trioceros is not a new name (it was first published in 1839) but, after a long period of being out of use, it was resurrected by Klaver & Böhme (1986). They initially proposed that it be recognised as a ‘subgenus’ within Chamaeleo. More recent work shows that Trioceros and Chamaeleo are not only distinct but also might not be especially close (Tilbury & Tolley 2009, Tolley et al. 2013): in these phylogenies, Trioceros is part of a chamaeleonine clade that includes Kinyongia, Calumma and Furcifer but not Chamaeleo.

Like me, you may well imagine Trioceros as ‘that three-horned genus that contains Jackson’s chameleon’. In fact, the long-horned Jackson’s chameleon T. jacksonii (try to find a book that mentions this species and doesn’t also mention Triceratops in the same sentence) is an unusual member of the group. A few others possess short rostral processes, but others don’t. Raised parietal crests, occipital lobes, prominent dorsal and gular crests and heterogenous body scalation are all typical in Trioceros: these are especially showy chameleons. I mean, look at this...

What an unbelievable beast! A male Usambara three-horned chameleon Trioceros deremensis photographed in Tanzania by Benjamin Klingebiel, CC BY-SA 2.0.

In fact a few species here have, additionally, especially tall neural spines which give them a mighty sail. This is especially prominent in the Usambara three-horned chameleon. And here’s where I won’t start talking about the manuscript I was preparing on comparing chameleon dorsal neural spines with those of sail-backed dinosaurs… (an idea since picked up by other authors).

It's now well known among palaeontologists that Trioceros chameleons have tall dorsal neural spines that might be of great interest as goes the also tall neural spines of some dinosaurs. Here are photos I took of a slightly battered T. jacksonii skeleton (University of Portsmouth collection, UK), though note that this is not an especially tall-spined species. Far superior photos and x-rays of chameleon skeletons are available elsewhere online.

Anyway, the Trioceros chameleons are in fact a heterogenous lot and, again, it’s conceivable that splitting up and further taxonomic change might happen down the line. Again, note that some of the divergence dates and morphological and ecological variation present within this group well exceed those present in ‘genera’ elsewhere. Don’t, however, go thinking that this makes the species themselves all that old: the majority of divergences within Trioceros seem to have occurred within the last 5 million years (Ceccarelli et al. 2014).

T. cristatus, one of several Trioceros species famous for being 'sail-backed'. Photo by Benjamin Klingebiel, CC BY-SA 2.0.

Some of these lineages are viviparous. In fact, the so-called ‘bitaeniatus-group’ within Trioceros consists of relatively small, mostly montane, viviparous species, and thus looks likely to be a specialised, err, montane clade, their evolution being strongly linked to the Pliocene development of the Eastern Afromontane Region (Ceccarelli et al. 2014). The members of this lineage tend to have a more triangular parietal crest than species belonging to other lineages. Jackson’s chameleon is part of this particular group.

A selection of books consulted during the making of this article. I don't own all the books, but I'm working on it.

So that’s Bradypodion, Calumma, Furcifer and Trioceros done (I mean, in brief, cursory fashion). But that’s still not it. There are more chameleons yet to talk about. In what should be the third and final part of this series of articles, we’ll look at what the relationships between these different chameleon lineages tell us about the pattern of chameleon evolution overall: is the cryptic, leaf-mimicking morphotype the primitive one for the group, or were ancestral chameleons slender-tailed, arboreal animals of more conventional shape? Until next time.

For previous Tet Zoo articles on iguanian lizards, see...

Refs - -

Alexander, G. & Marais, J. 2007. A Guide to the Reptiles of Southern Africa. Struik Publishers, Cape Town.

Ceccarelli, F. S., Menegon, M., Tolley, K. A., Tilbury, C. R., Gower, D. J., Laserna, M. H., Kasahun, R., Rodriguez-Prieto, A., Hagmann, R. & Loader, S. P. 2014. Evolutionary relationships, species delimitation and biogeography of Eastern Afromontane horned chameleons (Chamaeleonidae: Trioceros). Molecular Phylogenetics and Evolution 80, 125-136.

Klaver, C. J. J. & Böhme, W. 1986. Phylogeny and classification of the Chamaeleonidae (Sauria) with special reference to hemipenis morphology. Bonner Zoologische Monographien 22, 1-64.

Martin, J. 1992. Chameleons: Nature’s Masters of Disguise. Blandford, London.

Raxworthy, C. J., Forstner, M. R. J. & Nussbaum, R. A. 2002. Chameleon radiation by oceanic dispersal. Nature 415, 784-787.

Stuart-Fox, D. & Moussalli, A. 2007. Sex-specific ecomorphological variation and the evolution of sexual dimorphism in dwarf chameleons (Bradypodion spp.). Journal of Evolutionary Biology 20, 1073-1081.

Stuart-Fox, D. & Moussalli, A. 2008. Selection for social signalling drives the evolution of chameleon colour change. PLoS Biology 6 (1): e25. DOI:10.1371/journal.pbio.0060025

Tilbury, C. R. & Tolley, K. A. 2009. A re-appraisal of the systematics of the African genus Chamaeleo (Reptilia: Chamaeleonidae). Zootaxa 2079, 57-68.

Tolley, K. & Herrel, A. 2013. The Biology of Chameleons. University of California Press, Berkeley.