In recent articles I’ve made an effort to review the skinks of the world and today – it’s a momentous occasion – we see the last part of this series. I hope it’s clear that the Tet Zoo skink ‘review’ is very much a simple summary: it really doesn’t do justice to the full diversity of this enormous, globally distributed group of lizards (containing c 1500 species, representing c 25% of all extant lizards). Note that part I is here, part II here. On we go...

Finally, we come to the skink group Scincinae. As used in the ‘conventional’, ‘traditional’ sense, this is by far the most problematic of skink groups since it’s always been understood (Greer 1970) to be paraphyletic with respect to some or all of the others. In other words, this is a ‘grade group’ that simply masses together all those skinks that aren’t (in traditional taxonomy) acontines, feylinines or lygosomines. In addition to Scincus itself (read on), the group is typically considered to include the mostly circum-Mediterranean cylindrical skinks (Chalcides) [adjacent image of C. bedriagai by David Perez], the Eurasian legless skinks Ophiomorus (not all of which are legless), Peters’ banded skink Scincopus fasciatus, and the Eurasian wedge-snouted skinks (Sphenops). All of these skinks have the same sort of gestalt. They’re all long-bodied, brownish lizards with wedge-shaped heads and, often, reduced limbs; Sphenops and Chalcides are much alike and it now seems that the former belongs within the latter, its species actually evolving twice from different Chalcides lineages (Caputo 2004, Carranza et al. 2008).

The ‘classic’ scincine – the skink – is Scincus scincus, the Afroasian sandfish (one of three Scincus species). This streamlined, smooth-scaled lizard is specialised for propelling itself through loose sand. It has a shovel-shaped snout, countersunk lower jaw, reduced ear openings, fringed digits, and a body that’s approximately square in cross-section. A number of recent studies have examined exactly how it swims through sediment. It has usually been thought that these lizards fold their limbs against the body and move via sinusoidal undulation. This idea was challenged by Baumgartner et al. (2008) who showed Scincus moving through sand by almost literally ‘swimming’ with an alternating paddling of the limbs. However, it seems that this technique is only used when the animal is interacting with the surface and other recent studies - involving high-speed x-ray imaging and the use of glass beads as the substrate - confirm use of sinusoidal body-waves (Maladen et al. 2009, 2011a, Ding et al. 2012), not of limbs. The efficiency and shape of the sandfish has in fact resulted in the creation of sand-swimming robots (Maladen et al. 2011b, c) that have many conceivable practical applications.

Catena & Hembree (2014) recently studied the sand-swimming behaviour of the Eurasian-African Ocellated or Eyed skink Chalcides ocellatus, their primary interest being directed toward the sort of traces it left in sediment. It turns out that Chalcides leaves distinctive sinuous surface trails, flame-like traces, U- and V-shaped divots and other structures after moving through sediment. One interesting application of this research is that it might allow us to recognise traces left in ancient sediments by sand-swimming skinks and other lizards and reptiles. The research is also relevant when it comes to what’s known as ecosystem engineering: burrowing skinks loosen, disrupt and aerate sediment layers near the surface, and cause the downward migration of food, skin and faecal particles and other organic debris from the surface (Catena & Hembree 2014). There are already indications that other burrowing tetrapods – caecilians, amphisbaenians and scolecophidian snakes, among others – might be important ecosystem engineers in some habitats and geographical regions. Given how diverse and abundant some fossorial skinks are in some parts of the world, might they play a (mostly hitherto overlooked) role as well? [Photo of Ophiomorus below by Benny Trapp.]

Chalcides skinks were mentioned in the first article of this series since the genus is one of several within the skink assemblage where there are species that exhibit numerous patterns of limb and digit reduction. Species like C. ocellatus are ‘fully limbed’ with reasonably big arms and legs and a full complement of digits but others have slender, miniscule limbs and just three or two digits on their hands and feet (like Armitage’s cylindrical skink C. armitagei of the Sene-Gambian region*). Yet others have stump-like limbs and lack digits entirely (like Günther’s cylindrical skink C. guentheri). Some species are variable with respect to how many phalanges and how many digits they have: there are populations of the Moroccan Mionecton skink C. mionecton, for example, with five digits and others with four (Caputo et al. 2000). Frame-shifts in digit identity are thought to have occurred within this group (a topic that I want to mostly ignore here for reasons of brevity; bring it up in the comments if you want to know more). Incidentally, some of these skinks are pretty big. Large specimens of C. ocellatus can attain a total length of about 30 cm. The far more elongate Three-toed skink C. chalcides can be even longer, sometimes exceeding 40 cm in total.

* Armitage’s cylindrical skink is something of a celebrity within this group, largely because it was once thought to be chronically rare and possibly even extinct. It turns out that people were mostly looking in the wrong place: the species is a specialist of coastal regions and is locally abundant in parts of its range (Wilms et al. 2013). [West Canary skink C. viridanus image below by Guérin Nicolas.]

Chalcides skinks are viviparous, producing between six and 23 babies depending on species and the size of the mother. Chalcides is one of the first skinks in which complex placentation was recognised: that is, they employ a method in which the mother’s circulatory system passes nutrients directly to the developing embryo via a placenta. The anatomy of the placenta, minuscule size of the eggs (they are as tiny as 1 mm in diameter) and way in which the mother's circulation interacts with that of her embryos is strikingly similar to the system present in placental mammals. Indeed, complex, ‘mammal-like’ placentation of this sort is now known for several other skinks, including lygosomines of several groups as well as Chalcides (Blackburn et al. 1984, Blackburn & Flemming 2010).

Oh, it may not be a coincidence that viviparity has evolved repeatedly in long-bodied skinks. Caputo et al. (2000) suggested that body elongation imposes a constraint on the number of eggs that a mother’s body can hold and that the evolution of yolk-less eggs and – eventually – of a placenta and full-blown viviparity is a way of counteracting reduced fecundity. Griffith (1990) said similar things as goes body elongation and fecundity, but this time for Eumeces. By adding four additional vertebrae to the ancestral body plan, Eumeces skinks are able to fit in an additional two or three growing babies. Some long-bodied Chalcides lineages have also evolved sexual size dimorphism, presumably for the same reason (to increase fecundity). In the species concerned, females are much bigger than males and (unlike males) continue growing after reaching sexual maturity.

Given that Scincus is the ‘core scincine’, its phylogenetic position is crucial to the position of scincines as a concept. Annoyingly, markedly different positions have been suggested, in part because different studies have incorporated data from very different sets of taxa. Brandley et al. (2005) and Carranza et al. (2008) found Scincus to belong with a few north African and east Asian taxa (including the Berber or Schneider’s skink E. schneideri and Peters’ banded skink), this small clade being close to a large scincine clade that included Chalcides and – in Brandley et al. (2005) study – Amphiglossus... oh, and Feylinia too. Pyron et al. (2013) produced very similar results. Meanwhile, Whiting et al. (2007) found Scincus to be just outside a big group of lygosomines that includes Australasian Emoia skinks and blue-tongues, and African Mabuya skinks (Whiting et al. 2007).

We saw in one of the previous skink articles that the scincine/scincid Sirenoscincus is weird in lacking hindlimbs while still possessing forelimbs – an anatomical configuration long thought to be unique to the amphisbaenian Bipes. Sirenoscincus was only named in 2003 and thus is a recent addition to our knowledge of skink diversity. Remarkably, another ‘Bipes-style’ skink has also been recently discovered, and it’s not closely related to Sirenoscincus. Termed Jarujinia bipedalis and named in 2011, it’s from Thailand and – though originally said to be a lygosomine (Chan-ard et al. 2011) – also appears to be scincine/scincid of some sort (Pyron et al. 2013).

In the new taxonomic scheme suggested by Hedges (2014), all of the skinks discussed here are include within the new, restricted version of Scincidae. This clade seems to have a sister-group relationship to the lygosomoid clade discussed in the previous article.

Over the years I’ve made a few efforts at Tet Zoo to write about assorted skink lineages, but I’ve never made a proper foray into the diversity of the group as a whole. This article and its two predecessors – together, representing a very brief, cursory and doubtless unsatisfying attempt to summarise skink diversity – is at least a start, and it reminds me why I haven’t attempted such an endeavour before. There are a lot of skinks, and I hope in future to write about them a lot more. Remember that you can help me out by providing photos of the more obscure taxa. Until next time...

Tet Zoo now features some fairly reasonable coverage of squamate diversity, but there is still so much to do.

Dibamids and amphisbaenians

Gekkotans

Iguanians

Lacertids

Skinks and cordylids

Anguimorphs

Snakes

Refs - -

Baumgartner, W., Fidler, F., Weth, A., Habbecke, M., Jakob, P., Butenweg, C. & Böhme, W. 2008. Investigating the locomotion of the sandfish in desert sand using NMR-imaging. PLoS ONE 3(10): e3309. doi:10.1371/journal.pone.0003309

Blackburn, D. G. & Flemming, A. F. 2010. Reproductive specializations in a viviparous African skink and its implications for evolution and conservation. Herpetological Conservation and Biology 5, 263-270.

- ., Vitt, L. J, & Beuchat, C. A. 1984. Eutherian-like reproductive specializations in a viviparous reptiles. Proceedings of the National Academy of Sciences 81, 4860-4863.

Brandley, M. C., Schmitz, A. & Reeder, T. W. 2005. Partitioned Bayesian analyses, partition choice, and the phylogenetic relationships of scincid lizards. Systematic Biology 54, 373-390.

Caputo, V. 2004. The cranial osteology and dentition in the scincid lizards of the genus Chalcides (Reptilia, Scincidae). Italian Journal of Zoology 71, 35-45.

- ., Guarino, F. M. & Angelini, F. 2000. Body elongation and placentome evolution in the scincid lizard genus Chalcides (Squamata, Scincidae). Italian Journal of Zoology 67, 385-391.

Carranza, S., Arnold, E. N., Geniez, Ph., Roca, J. & Mateo, J. A. 2008. Radiation, multiple dispersal and parallelism in the skinks, Chalcides and Sphenops (Squamata: Scincidae), with comments on Scincus and Scincopus and the age of the Sahara Desert. Molecular Phylogenetics and Evolution 46, 1071-1094.

Catena, A. M. & Hembree, D. I. 2014. Swimming through the substrate: the neoichnology of Chalcides ocellatus and biogenic structures of sand-swimming vertebrates. Palaeontologia Electronica Vol. 17, Issue 3;37A; 19p

Chan-ard, T., Makchai, S. & Cota, M. 2011. Jarujinia: a new genus of lygosomine lizard from central Thailand, with a description of one new species. The Thailand Natural History Museum Journal 5, 17-24.

Ding, Y., Sharpe, S. S., Masse, A. & Goldman, D. I. 2012. Mechanics of undulatory swimming in a frictional fluid. PLoS Computational Biology 8(12): e1002810. doi:10.1371/journal.pcbi.1002810

Greer, A. E. 1970. A subfamilial classification of scincid lizards. Bulletin of the Museum of Comparative Zoology 139, 151-183.

Griffith H. 1990. Miniaturization and elongation in Eumeces (Sauria: Scincidae). Copeia 1990, 751-758.

Chan-ard, T., Makchai, S. & Cota, M. 2011. Jarujinia: a new genus of lygosomine lizard from central Thailand, with a description of one new species. The Thailand Natural History Museum Journal 5, 17-24.

Hedges, S. B. 2014. The high-level classification of skinks (Reptilia, Squamata, Scincomorpha). Zootaxa 3765, 317-338.

Maladen, R. D., Ding, Y., Li, C., & Goldman, D. I. 2009. Undulatory swimming in sand: subsurface locomotion of the sandfish lizard. Science 325, 314-318.

- ., Ding, Y., Umbanhowar, P. B., & Goldman, D. I. 2011b. Undulatory swimming in sand: experimental and simulation studies of a robotic sandfish. The International Journal of Robotics Research 30, 793-805.

- ., Ding, Y., Umbanhowar, P. B., Kamor, A. & Goldman, D. I. 2011a. Mechanical models of sandfish locomotion reveal principles of high performance subsurface sand-swimming. Journal of the Royal Society Interface 8, 1332-1345.

- ., Ding, Y., Umbanhowar, P. B., Kamor, A. & Goldman, D. I. 2011c. Biophysically inspired development of a sand-swimming robot. In Robotics: Science and Systems VI, Universidad de Zaragoza, Zaragoza, Spain, June 27-30, 2010; 01/2010.

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

Wilms, T., Chirio, L., Jallow, M. & Wagner, P. 2013. Chalcides armitagei. The IUCN Red List of Threatened Species. Version 2014.2. <www.iucnredlist.org>. Downloaded on 31 October 2014.