TURTLES! A section of the montage that's being prepared for the Tet Zoo Big Book (larger version viewable at my patreon). Image in-prep, by Darren Naish.

Every now and again – I would guess once every four months or so – I experience Turtle Guilt... the feeling that I really should post more about turtles at Tet Zoo. Maybe there should be a Turtle Month or something where I write about nothing but turtles. And, hey, World Turtle Day was May 23rd and I totally missed it. I’ll try and remember it for next year... along with World Pangolin Day, World Giraffe Day, World Tapir Day and whatever other World Animal Days there are. I receive constant reminders of my Turtle Guilt. As I wander about the zoos, animal parks and aquaria of the British countryside, turtles haunt me, and taunt me: why won’t you write about us Darren, why???, they say. To alleviate some of the guilt, here are brief words on just a few of the turtles species that have been taunting me recently. Correction: not so brief after all. Damn.

I took about 40 photos of this snake-necked turtle triplet, and none are better than this. They just wouldn't stop moving. Photo by Darren Naish, taken at Chester Zoo, UK.

Obscure snake-necks. This is a Roti Island snake-necked turtle or McCord’s snake-necked turtle Chelodina mccordi, a threatened chelid pleurodire endemic to Rote Island (previously spelt Roti Island) in Indonesia. It doesn’t occur right across Rote Island, but only in an area of about 70 km sq in the island’s central highlands. Its numbers have been substantially reduced by collecting for the pet trade. The conservation status of this turtle has been further compounded by the fact that it was regarded as merely an ‘outpost population’ of the New Guinea snake-necked turtle C. novaeguineae until 2004, at which time it was elevated to species status.

Captive Roti Island snaked-neck turtle at Rotterdam. Photo by Silvain de Munck, CC BY 2.0.

Two subspecies are recognised (the western C. m. mccordi and eastern C. m. roteensis). A third population – endemic to Timor-Leste and named C. m. timorlestensis in 2007 – has been regarded by other authors as another distinct species: C. timorensis McCord et al., 2007 (yes, it was published both as a new subspecies, and as a new species, in the same year, by different sets of authors). What are these small, freshwater-dwelling turtles doing on these separate islands? Have they made bold and daring marine crossings at various points during their history? Or did they use terrestrial connections during the many times when sea levels were lower and various of these islands were connected? Studies of phylogeography in other Chelodina snake-necks have found complex patterns of relatedness and biogeography implying substantial movement during times of lowered Pleistocene sea level (Hodges et al. 2014).

Anyway... I recently watched three of these animals cavorting at Chester Zoo. They never stopped moving and goddam fish kept swimming in the way all the time, so my photos are terrible. The fact that snake-necked turtles are so speedy and manoeuvrable underwater inspires me to say things about their aquatic abilities and extremely interesting necks, but I’ll save those thoughts for another article.

Two taxa typically regarded as subspecies of the same variable species. The two larger animals at the rear are Red-eared sliders; the smaller one at the front is a Yellow-bellied slider. If these were birds or mammals they'd definitely be regarded as different species. Photo by Darren Naish (taken at the Welsh Mountain Zoo, Colwyn Bay, Wales).

The world of sliders. Moving now to cryptodires, we begin with this harmonious scene (err -- the one above). It depicts individuals of one of the most familiar turtles alive – the Red-eared slider Trachemys scripta elegans – as well as a single Yellow-bellied slider T. s. scripta, an extremely common, widespread, and widely kept slider that maybe should be equally familiar but (to me, at least) is not. Red-eared and Yellow-bellied sliders can interbreed; consequently, the release of Red-eared sliders into places inhabited by Yellow-bellied sliders has been the cause of some concern. It’s well known that sliders change their dietary preference substantially as they mature. Juveniles are mostly carnivorous; old adults mostly herbivorous.

Yellow-bellied slider lounging in the water. Like virtually all emydids, sliders are semi-aquatic. The red patch on the cheek stripe indicates that this individual is likely a hybrid with Red-ear ancestry. Photo by Darren Naish.

Trachemys is a deirocheyline emydid, a member of the same group of semi-aquatic turtles as the Painted turtle Chrysemys picta and the many map or sawback turtles (Graptemys). Incidentally, the sprawling polytypic mess that was Trachemys scripta of tradition has proved to be radically polyphyletic.

Box turtles – a fruitful foray into terrestrialisation, plastral kinesis, and convergence. Sticking with emydids, this is a Three-toed box turtle Terrapene carolina triunguis, a box turtle of the south-central USA.

Three-toed box turtle. I know the photo isn't the greatest, but I like the semi-abstract, wet and muddy look captured in the image. Reminds me of a scene from The Never Ending Story. Photo by Darren Naish.

Box turtles are adaptable animals known from marshes, woodlands, grasslands and even semi-deserts. They’re strongly adapted for terrestrial life, with a highly domed carapace, and robust limbs and short manual digits: features that are all typical of terrestrial turtles (a domed carapace shape is thought to be a good indicator of terrestrial specialisation among turtles).

Diagrams from Bramble (1974) showing how the mobile plastral hinge works in a box turtle. Note that the pelvis and scapulocoracoid move when the hinge is flexed and the shell openings are closed.

Box turtles are unusual in possessing mobile hinge zones in the plastron which mean that its separate anterior and posterior parts can be closed tightly against the edges of the carapace. This explains the common name (‘box turtle’) and is generally reckoned to be an anti-predator adaptation for life on land.

Plastral kinesis is present in other emydine turtles (some, not all, of the Emys pond turtles) where it seems to have evolved independently from the kinesis present in Terrapene (Feldman & Parham 2002). Yes, a rare, weirdass feature, and it apparently evolves twice, independently, within this one small turtle group. Plastral kineses has also evolved, independently, in testudinid and geoemydid turtles.

What also interests me in particular about box turtles is that they’re emydine emydids; that is, close relatives of the Spotted turtle Clemmys guttata, pond turtles (Emys), bog and wood turtles (Glyptemys), and Blanding’s turtle Emydoidea blandingii (Bickham et al. 1996, Parham & Feldman 2002, Stephens & Wiens 2003). They’re less closely related to sliders and other deirochelyine emydids. The point is that all of these other emydid lineages are semi-aquatic, meaning that Terrapene is a uniquely terrestrialised, ‘tortoise-like’ turtle completely surrounded by close relatives of far more aquatic nature. In other words, it’s an emydid ‘trying to be’ a testudinid tortoise, and potentially a great example of convergent evolution within turtles.

Captive Leopard tortoise; note the excellent spur-like scales on the forelimbs. Photo by Darren Naish.

Stigmochelys! And that nicely brings us, finally, to tortoises, or testudinids, the most terrestrial of all turtles. Tortoises have the most domed carapaces of all turtles and their limbs are also more specialised for terrestrial life than those of any other turtles. Interesting features of their limbs associated with terrestrial life include enlarged, sometimes thorn-like scales on the anterior surfaces of their forelimbs.

These are shown to good effect here in a Leopard tortoise Stigmochelys pardalis, a spectacular African species, sometimes with an exceptionally tall-domed carapace. Leopard tortoises can be enormous, reaching 70 cm in carapace length (there are rumours of Ethiopian specimens 1 m long) and 54 kg in mass. Leopard tortoises have had a tumultuous taxonomic history and most sources include them in the genus Geochelone. However, it’s been recognised for some time that the most familiar version of this genus is a polyphyletic mess (more kindly, a grade), and major attempts have been made to tidy things up. Fritz & Bininda-Emonds (2007) found leopard tortoises to be most closely related to the southern African Psammobates tortoises and to be well away from Geochelone proper (the type species for which is the Indian star tortoise G. elegans). Accordingly, they followed Gerlach (2001) in advocating use of Stigmochelys Gray, 1873 for leopard tortoises. Stigmochelys, Psammobates and Geochelone all belong to a separate clade from Testudona, the tortoise clade that includes Indotestudo, Testudo and their close relatives (Parham et al. 2006, Fritz & Bininda-Emonds 2007).

Captive Manouria tortoise, photographed at Chester Zoo (UK), with cricket hitch-hiker. Note 'archaic' appearance relative to other tortoises. Photo by Darren Naish.

Archaic Manouria. We end with Manouria, the Asian brown tortoises. There are two extant species: M. emys and M. impressa. These are modern Asia’s largest tortoises, big individuals reaching 60 cm in carapace length and 25 kg or so in mass. As is obvious from the photo above, big, pointed, overlapping scales cover the forelimbs. Manouria is mostly a forest-dwelling tortoise of hilly and mountainous places, but there are some indications that M. emys at least is fairly reliant on freshwater aquatic environments, sometimes foraging in streams and eating aquatic plants (Ernst & Barbour 1989). Manouria tortoises often burrow in moist soil and leaf litter.

This association with moist habitats and aquatic resources is interesting in view of the idea that Manouria is anatomically archaic compared to other tortoises. It has frequently been identified as belonging outside the clade that contains all other crown-tortoises (Crumly 1985, Spinks et al. 2004, Lapparent de Broin et al. 2006a, Parham et al. 2006). 

A picture included to remind you how extreme some tortoises are. At left: battling Galapagos tortoises of saddle-backed and domed forms (drawing by Darren Naish). At right: model of Rodrigues saddle-backed tortoise Cylindraspis vosmaeri, created by Nick Bibby of Rungwe Kingdon and Claude Koenig’s sculpture foundry Pangolin Editions.

Not only do these tortoises look less specialised for dedicated terrestrial life than other members of Testudinidae, they also possess primitive characters that are present in close relatives of tortoises (like geoemydid terrapins) but lacking in other tortoise lineages.

Among the best known of such features are chin or mental glands. Remember that turtles of many lineages possess integumentary organs all over the place. Seems weird maybe, but there it is. However, some sources state that other tortoises, like gopher tortoises (Gopherus), have chin glands too. But, then, some molecular studies find Manouria and Gopherus to be sister-taxa (Fritz & Bininda-Emonds 2007). Manouria also has a lower, less vaulted carapace than other tortoises (Lapparent de Broin et al. 2006b). The ‘archaic’ flavour of Manouria means that it’s sometimes been considered synonymous with the Eocene Euro-American fossil tortoise Hadrianus, or at least very closely related to it (Claude & Tong 2004)... but that’s a complicated issue that I can’t discuss further here.

Gopherus tortoises... are they 'archaic' too? They are according to some molecular studies. This is most likely an Agassiz's desert tortoise G. agassizii. Image by Utahcamera, in public domain.

There are so many things to say about turtles. More soon. For previous Tet Zoo articles on turtles, see...

Refs - -

Bickham, J. W., Lamb, T., Minx, P. & Patton, J. C. 1996. Molecular systematic of the genus Clemmys and the intergeneric relationships of emydid turtles. Herpetologica 52, 89-97.

Bramble, D. M. 1974. Emydid shell kinesis: biomechanics and evolution. Copeia 1974, 707-727.

Claude, J. & Tong, H. 2004. Early Eocene testudinoid turtles from Saint-Papoul, France, with comments on the early evolution of modern Testudinoidea. Oryctos 5, 3-45.

Crumly, C. R. 1985. A hypothesis for the relationships of land tortoise genera (family Testudinidae). In de Broin, F. (ed) First International Symposium of Fossil Turtles. Studias Geologica Salamanticensis, Volumen especial, pp. 115-124.

Ernst, C. H. & Barbour, R. W. 1989. Turtles of the World. Smithsonian Institution Press, Washington, D. C. & London.

Fritz, U. & Bininda-Emonds, O. R. P. 2007. When genes meet nomenclature: tortoise phylogeny and the shifting generic concepts of Testudo and Geochelone. Zoology 110, 298-307.

Gerlach, J. 2001. Tortoise phylogeny and the ‘Geochelone’ problem. Phelsuma 9 (Supp. A), 1-24.

Hodges, K., Donnellan, S & Georges, A. 2014. Phylogeography of the Australian freshwater turtle Chelodina expansa reveals complex relationships among inland and coastal bioregions. Biological Journal of the Linnean Society 111, 789-805.

Lapparent de Broin, F. de, Bour, R., & Perälä, J. 2006b. Morphological definition of Eurotestudo (Testudinidae, Chelonii): first part. Annales de Paléontologie 92, 255-304.

- ., Bour, R., & Perälä, J. 2006a. Morphological definition of Eurotestudo (Testudinidae, Chelonii): second part. Annales de Paléontologie 92, 325-357.

Parham, J. F. & Feldman, C. R. 2002. Generic revisions of emydine turtles. Turtle and Tortoise Newsletter 6, 28-30.

- ., Macey, J. R., Papenfuss, T. J., Feldman, C. R., Türkozan, O., Polymeni, R. & Boore, J. 2006. The phylogeny of Mediterranean tortoises and their close relatives based on complete mitochondrial genome sequences from museum specimens. Molecular Phylogenetics and Evolution 38, 50-64.

Spinks, P. Q., Shaffer, H. B., Iverson, J. B. & McCord, W. P. 2004. Phylogenetic hypotheses for the turtle family Geoemydidae. Molecular Phylogenetics and Evolution 32, 164-182.

Stephens, P. R. & Wiens, J. J. 2003. Ecological diversification and phylogeny of emydid turtles. Biological Journal of the Linnean Society 79, 577-610.