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Tetrapod Zoology

Tetrapod Zoology

Amphibians, reptiles, birds and mammals - living and extinct

Musk turtles and mud turtles: look boring, are secretly hyper-diverse

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In a further effort to relieve Turtle Guilt (see the previous turtle-themed Tet Zoo article), I give you the following article devoted wholly to kinosternids, an exclusively American group of about 25 species of seemingly mundane and unspectacular turtles. Kinosternidae includes turtles that go by two common names: musk turtles (Sternotherus) and mud turtles (Kinosternon)... though things are a little more complex than this, as we'll see below. Musk turtles are also sometimes called stinkpots.

At top: Common musk turtle (Sternotherus odoratus), image by Laurent Lebois (licensed under Creative Commons Attribution 2.0 Generic license). At bottom: Oaxaca mud turtle (Kinosternon oaxacae), image by Vicente Mata Silva (licensed under Creative Commons Attribution 3.0 Unported license).

As a generalisation, kinosternids are amphibious, carnivorous, often nocturnal, turtles that walk and clamber over the bottoms of streams, rivers, lakes and ponds [images above by Laurent Lebois and Vicente Mata Silva/CalPhotos]. Many species spend a lot of time in water but some (like the Common mud turtle K. subrubrum) readily forage on land, and aestivate or hibernate in terrestrial burrows. Insects, snails, worms, crustaceans and fish are all eaten as are carrion, algae, and the seeds and leaves of certain plants. Lovich et al. (2010) reported cases in which mud turtles ate alligator lizards (Elgaria) and ground snakes (Sonora). Predation of this sort might be rare, but its apparent rarity might – Lovich et al. (2010) suggested – be due to under-observation. Kinosternid clutches are often (but not always) small (1-3 eggs), in keeping with their small size.

Captive Loggerhead musk turtle (Sternotherus minor): note the barbels on the chin. Image by Greg Hume, licensed under Creative Commons Attribution-Share Alike 3.0 Unported license.

Kinosternid hindlimbs are often mostly invisible when the turtles are at rest, only the tips of their claws protruding from beneath the shell. A diet that involves grabbing and crushing hard-shelled prey perhaps explains why some old individuals have especially big heads (Ernst & Barbour 1989). Barbels are present on the chins and throats of some Sternotherus species [adjacent image showing barbels by Greg Hume].

Most kinosternids are small, with carapace lengths of 15-20 cm; the biggest reach about 30 cm. If the Mexican giant musk turtle Staurotypus triporcatus is included within Kinosternidae (read on), the very biggest reach 40 cm. The kinosternid carapace is usually solid (that is, it lacks the hinges and mobile or flexible zones present in some turtles), has three longitudinal ridges, and is covered with horny plates that sometimes overlap. Hinges are present in the plastra of some species, however, allowing them to wholly enclose their limbs, neck and tail within the shell. Mud turtles lack an entoplastron (the near-circular plastral bone located along the midline, in between the forelimbs, and in between the epiplastra and hypoplastra). The kinosternid carapace is normally domed, but the aptly named Flattened musk turtle Sternotherus depressus [shown below] has a relatively wide, flat one. It has been suggested that this is an adaptation for hiding in crevices along the banks where it lives.

Flattened musk turtle adult and hatchling; image in public domain. Ontogenetic change in turtle shells... it can be messy.

The most famous and remarkable thing about kinosternids concerns the musk glands located along the bridge section of the shell and which release an incredibly strong musky odour when the turtles feel threatened. Some species also release foul-smelling secretions from the cloaca. These secretions are thought to mostly serve a defensive function, and to repel mammalian (and other?) predators. Musk glands (properly called Rathke's glands) are far from unique to kinosternids; they actually occur in most turtle groups, but the glands and musk secretions produced by kinosternids are most similar to those of snapping turtles. Hold that thought. Incidentally, the idea that evolution might equip turtles, of all things, with vile-smelling, musk-extruding flank glands is surreal and a good example (I think) of one of those things that we wouldn’t predict if we only knew these animals as fossils.

Musk turtles are, as are turtles belonging to many lineages, capable of limited climbing, and they will sometimes ascend steep slopes or sloping branches or logs. There are amusing anecdotes relating cases in which they’ve fallen into boats after being perched on overhanging branches or fallen trees.

Razor-backed musk turtle (Sternotherus carinatus); image by Ltshears, in public domain.

The general impression you might get from the literature on kinosternids is that what I’ve said above more or less applies to all members of the group, and that they’re all samey and pretty much interchangeable (bar minor details of size or shell anatomy). In fact, however, this is one of the most diverse turtle clades when we look at variation in habitat, ecomorphology, biology, anatomy and reproductive behaviour. Iverson et al. (2013) said this of the diversity within the group (note that I’ve deleted the many citations they provided to back up their statements)...

“[Kinosternidae] ranges from north temperate to tropical habitats, and from rain forest to grasslands to desert. It includes totally aquatic to semi-terrestrial species, with adult carapace lengths of 10–38 cm, and female-dominated to male-dominated sexual size dimorphism. At least one species exhibits close to the maximum skeletal mass relative to body mass among all vertebrates. Some species have a greatly reduced plastron, whereas others have a plastron so extensive as to completely close the shell. The group includes members capable of submerged, fully aquatic respiration, and others capable of estivating underground for up to two years. Some species produce a single clutch in the spring, others nest multiple times in the summer, and others nest nearly year-round, with clutches ranging from one or two relatively huge eggs to ten or more relatively tiny eggs. Embryonic development is direct in some species, whereas others exhibit early embryonic diapause and/or late embryonic estivation, with incubation times from 56 to over 366 days. Finally, sex determination in the family ranges from genetic (with sex chromosomes) to temperature-dependent.” (Iverson et al. 2013, pp. 929-930).

In short, this is an impressively diverse set of species, their morphological uniformity obscuring some fascinating weirdness. Because this diversity has gone mostly unappreciated until recently, studies designed to investigate the evolution that led to this diversity have been slow in coming. Things are changing: at least five studies devoted to kinosternid phylogeny, diversity and biology have appeared since the start of 2013, which looks to be about twice the number of papers that generally appeared per year on the group prior to 2013. [Image below by LA Dawson.]

Cute little Eastern or Common mud turtle (Kinosternon subrubrum); image by LA Dawson, licensed under Creative Commons Attribution-Share Alike 2.5 Generic license.

The rise and fall of Cryptochelys

A few studies have led to intimations that musk turtles (Sternotherus) and mud turtles (Kinosternon) are similar enough to be synonymous (see Powell et al. 1998). That idea hasn’t been supported by recent work and in fact it’s flatly contradicted by molecular phylogenies that find both to be well distinct (Iverson et al. 2013, Spinks et al. 2014). Furthermore, Kinosternon sensu lato has been said to include a third group, seemingly outside the clade that includes Sternotherus and all other Kinosternon species. Iverson et al. (2013) named this overlooked group Cryptochelys. If this is valid, kinosternids consist of four major extant groups, not three (read on), all of which have been in existence since the Early Miocene.

However, the validity of Cryptochelys was later tested by Spinks et al. (2014). They argued that Iverson et al.’s analysis was based on unstable and preliminary results, and that Cryptochelys was not a monophyletic entity and hence not deserving of a name. Their study also raised various questions about which kinosternid species were really demarcated and worthy of recognition as distinct taxa... a complex issue that I can’t do justice here.

Mexican musk turtles: reduced plastra, big heads

Mexican giant musk turtle (Staurotypus triporcatus), image by Darren Naish.

You'll have noticed that I just referred to three groups of kinosternids. That third group contains the Mexican giant musk turtle Staurotypus triporcatus, Chiapas giant musk turtle S. salvinii and Narrow-bridged musk turtle Claudius angustatus. Grouped together as the Mexican musk turtles, these are most often classified within Kinosternidae as the ‘subfamily’ Staurotypinae. Some authors, however, have regarded them as a distinct 'family', Staurotypidae. Iverson et al. (2013) found Mexican musk turtles to be the sister-group to the (Cryptochelys + (Kinosternon + Sternotherus)) clade, with the divergence event between both clades dating to the Paleocene. If all of this is accurate, it might indeed be best to use 'Staurotypidae' instead of 'Staurotypinae'.

Alas, Spinks et al. (2014) argued that it made more sense to maintain Staurotypinae as a 'subfamily' given that this is more in keeping with herpetological tradition. In the end, these taxonomic issues are subjective and don’t really matter, so long as we all know what we're talking about.

Narrow-bridged musk turtle (Claudius angustatus); image by Etienne Boncourt, licensed under Creative Commons Attribution-Share Alike 3.0 Unported license.

Anyway, staurotypines have a reduced plastron compared to other kinosternids: it consists of only seven or eight scutes and is cross-shaped. For this reason, the two Staurotypus species are sometimes termed cross-breasted musk turtles. As suggested by its common name, the Narrow-bridged musk turtle also has an extremely narrow bridge (the lateral part of the shell that connects the carapace with the plastron), it being only 5% as long as the plastron (Ernst & Barbour 1989) [adjacent image by Etienne Boncourt]. As Cameron points out in the comments below, the bridge is so weak that Claudius can actually rotate its plastron independently of its carapace. Claudius also has an especially broad and deep head for a kinosternid (the snout and jaws are also proportionally short), so big that it cannot be withdrawn into the shell. It is a ferocious biter, said to cause painful wounds to unwary humans.

Highly simplified cryptodire cladogram, clade names based on those used in Joyce et al. (2013). Mud turtles, musk turtles and Mexican musk turtles - all grouped together as Kinosternoidea - are close to snapping turtles and kin (Chelydroidea). Image by Darren Naish.

Kinosternids are clearly cryptodiran turtles. Beyond this, they have often been included within Trionychoidea or Trionychia, the cryptodire clade that also includes softshells (Trionychidae), since kinosternids are rather softshell-like in cranial characters (Meylan & Gaffney 1989). More recently, however, molecular studies have indicated that kinosternids and chelydrids (snapping turtles) are close relatives (Krenz et al. 2005, Barley et al. 2010), in which case the supposedly convergent similarities shared by the two are not convergent after all. Rather, it’s seemingly the cranial characters that make kinosternids look softshell-like that have deceived us.

Kinosternids don’t, for whatever reason, have a good fossil record. Fossils reveal the presence of several Paleocene and Eocene kinosternid lineages that are outside the crown-clade and were unlike them in character combinations (note that the Eocene was seemingly the ‘golden age’ for turtles, with diversity at an all-time high). There are also mentions here and there of Upper Cretaceous fossils that might be kinosternids (see Joyce et al. 2013). Crown-kinosternids first appear in the fossil record of the Miocene but probably await discovery in the Oligocene. An alleged fossil musk turtle from the Upper Miocene of Kansas was argued by Bourque (2011) to be a misidentified mud turtle, in which case musk turtles still lack a fossil record similar in longevity to that of mud turtles: the oldest mud turtles are from the Hemingfordian (late Early Miocene) – that is, about 17 million years old – while the oldest musk turtles are from the Hemphilian (Late Miocene-early Early Pliocene) – so, between 4.5 and 7 million years old. [Image below by LA Dawson.]

Goodbye from the kinosternids, for now. Common musk turtle (Sternotherus odoratus); image by LA Dawson, licensed under Creative Commons Attribution-Share Alike 2.5 Generic license.

As always with the animal groups I write about, there’s a huge number of things that deserve to be said about kinosternids that I haven’t covered here. Seeing as this was meant to be one of those brief articles consisting of just a few hundred words, I don’t think I’ve done too badly. More turtle coverage to come at some stage...

For previous Tet Zoo articles on turtles, see...

Refs - -

Barley, A. J., Spinks, P. Q, Thomson, R. C. & Shaffer, H. B. 2010. Fourteen nuclear genes provide phylogenetic resolution for difficult nodes in the turtle tree of life. Molecular Phylogenetics and Evolution 55, 1189-1194.

Bourque, J. R. 2011. Reassessment of a putative fossil stinkpot (Kinosternidae: Sternotherus) from the Late Miocene (Clarendonian) of Kansas. Journal of Herpetology 45, 234-237.

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

Iverson, J. B. & Le, M. & Ingram, C. 2013. Molecular phylogenetics of the mud and musk turtle family Kinosternidae. Molecular Phylogenetics and Evolution 69, 929-939.

Joyce, W. G., Parham, J. F., Lyson, T. R., Warnock, R. C. M. & Donoghue, P. C. J. 2013. A divergence dating analysis of turtles using fossil calibrations: an example of best practices. Journal of Paleontology 87, 612-634.

Krenz, J. G., Naylor, G. J. P., Shaffer, H. B. & Janzen, F. J. 2005. Molecular phylogenetics and evolution of turtles. Molecular Phylogenetics and Evolution 37, 178-191.

Lovich, J., Drost, C., Monatesti, A. J., Casper, D., Wood, D. A. & Girard, M. 2010. Reptilian prey of the Sonora mud turtle (Kinosternon sonoriense) with comments on saurophagy and ophiophagy in North American turtles. The Southwestern Naturalist 55, 135-138.

Meylan, P. A. & Gaffney, E. S. 1989. The skeletal morphology of the Cretaceous cryptodiran turtle, Adocus, and the relationships of the Trionychoidea. American Museum Novitates 2941, 1-60.

Powell, R., Collins, J. T. & Hooper, E. D. 1998. A Key to Amphibians and Reptiles of the Continental United States and Canada. University Press of Kansas, Lawrence, Kansas.

Spinks, P. Q., Thomson, R. C., Gidiş, M. & Shaffer, H. B. 2014. Multilocus phylogeny of the New-World mud turtles (Kinosternidae) supports the traditional classification of the group. Molecular Phylogenetics and Evolution 76, 254-260.

The views expressed are those of the author and are not necessarily those of Scientific American.

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