On temnos and toilets

Toilet seat currently in stock at Home Depot (in Canada).

Toilet-like gape in a temnospondyl. Modified from Jenkins et al., (2008).

One of the above is a latrine. You may have observed one over the course of your life. The other one is an extinct amphibian. You probably have not observed one over the course of your life. "Toiletheads" and "toilet seat mechanism" are widely used colloquialisms to refer to temnospondyls because of a perception that their mouths opened like a toilet seat, namely by the skull (= the lid) raising up, with little to no movement of the jaw (= the seat). This is in contrast to most other jawed vertebrates, which like us, primarily depress (lower) the jaw to open our mouths. This peculiar attribute of temnospondyls is probably one of the most widely disseminated facts about them among the broader paleontological community. As evidenced by my popular Valentine's rhyme from last week, people think this is hilarious. It makes temnospondyls relatable.  However, most people (scientists or otherwise) don't actually know where this idea comes from, how well it's been tested, or how broadly it may apply within Temnospondyli. So, I thought that I would spend this week going over the evidence, the lack of evidence, and how to interpret it. 

The concept of head raising was first put forward by the classic English paleontologist D.M.S. Watson 100 years (36,363 days) ago, where he suggested that flat-skulled temnospondyls (Mastodonsaurus was his example) would have had a hard time opening their mouth if they spent most of the time resting at the bottom of freshwater habitats like rivers and ponds because of their big heads and small limbs (i.e. they didn't lift themselves off the ground to create room for their lower jaw to open). Therein, he suggested that similar to modern crocodiles, the only way that these temnospondyls could open their mouth in any substantive fashion when lying / sitting on substrate was to lift their skull, rather than to lower the jaw as in most jawed vertebrates. 

Photograph of a crocodile gaping with its skull slightly elevated. Distributed by u/Goutham89 on Wikimedia Commons under a Creative Commons Attribution-Share Alike 4.0 International license.

Skull of the terrestrial temnospondyl Phonerpeton pricei indicating the skull-neck joint (blue line) and the skull-jaw joint (red line). Figure modified from Dilkes (1990).

Skull of the aquatic temnospondyl Gerrothorax pulcherrimus indicating the joints. Figure modified from Jenkins et al. (2008).

Watson reasoned that the relative position of the skull-neck joint to the skull-jaw joint was an important consideration. If the skull-neck joint was well in front of the skull-jaw joint, the animal would have to lift up the front part of its body in order to raise the skull to open its mouth. Conversely, if the two joints were in about the same transverse plane (the same longitudinal position), then the skull could be raised without having to lift the body. Watson also argued that such a method of opening the mouth explained two features of "flattened" temnospondyls: (1) the development of the paired exoccipital condyles and (2) the gradual development of a long process at the back end of the jaw, called the retroarticular process. Because he inferred that the flat skull would have created a mechanical disadvantage for the neck muscles projecting from the back of the skull, he reasoned that the attachment of another muscle (the depressor mandibulae) to the long posterior process would have created a compensatory mechanical advantage. The large condyles would then have permitted great dorsoventral (up and down) flexibility at the skull-neck joint, and the jaw would have moved forward as the mouth opened. This idea was expanded on in later years by Watson (e.g., 1958, 1962) for a number of well-known temnospondyls, always with a focus on the depressor mandibulae as the primary jaw-opening muscle.  A few subsequent workers of the mid-20th century (e.g., Panchen, 1959) extended this model to other groups, retaining the depressor mandibulae as the primary (but not only) muscle involved with this motion. 

Photographs of the occiput of several specimens of the Triassic stereospondyl Metoposaurus krasiejowensis. Arrows indicate the paired exoccipital condyles, which articulate with the first vertebra (the atlas). Figure modified from Sulej (2007).

The mandible of the Triassic chigutisaurid Keratobrachyops australis in medial (internal), dorsal, and ventral profiles. The red brackets indicate the retroarticular process; the blue brackets indicate the articular facets where the jaw and skull would hinge together. Figure modified from Warren (1981).

​Howie (1970) was the first worker to propose a major departure from Watson's original model. Howie utilized brachyopids, whose skull-neck joint is well behind the skull-jaw joint, in contrast to other flat-skulled temnospondyls. In order for the depressor mandibulae to function in the way that Watson proposed, the skull-neck joint (and with it, the vertebral column) would have to be displaced downward by a substantial amount, implying that either (a) the vertebral column was very loosely attached to the shoulder girdle, allowing it to be greatly displaced or (b) the shoulder girdle was not in contact with the ground, an unlikely idea if the jaw had to remain in contact with the ground to act as a fulcrum (think of it as planking with your chin on the ground). This also raises the problem of how could the jaw move forward during a gape if if was needed as a fulcrum. 

Comparison of the classic model of head raising (Watson/Panchen) with that of Howie. (A) resting state; (B) head raising in the classical model by contraction of the depressor mandibulae to open the jaws (in contact with the ground), which also depresses the vertebral column; (C) head raising in Howie's model by contraction of occipital muscles to raise the skull, contraction of the depressor mandibulae to lower the jaw (not in contact with the ground), and the absence of any depression of the vertebral column. Figure from Howie (1970).

Stepwise process of head raising in Parotosaurus pronus based on Howie's model. (A) resting state; (B) head raising by contraction of the cleidomastoideus to raise the skull (and the jaws with it); (C) contraction of the depression mandibulae to lower the jaw back toward the ground. Figure from Howie (1970).

Howie also pointed out that Watson's idea of a depressor attached to the top of the back of the skull was infeasible because of how the hypothesized angle of the muscle would have resulted in opposing forces, a lateral (outward) rotation around the skull-jaw joint with a medial (inward) pull of the depressor. Howie thus proposed a different model (part B on the above left figure), in which two main muscle groups were involved.

• More or less simultaneously, it was occipital muscles from the skull using the exoccipital condyles as the fulcrum (rather than the jaw) and lowering of the jaw (not the raising of the skull) by the depressor mandibulae that produced the head raising phenomenon.
  • With the condyles acting as the fulcrum, the skull would be elevated without the vertebral column having to be depressed, thus freeing the jaw from being in contact with the ground and allowing it to move forward.
  • Using capitosaurs as a model, Howie proposed that the occipital muscle in question was the cleidomastoideus (see below), which would have inserted onto a dorsal process of the clavicle, one of the elements in the shoulder girdle. This process is behind and below the insertion point on the occiput, but is more or less within the same longitudinal plane (in line with each other). Because the occipital muscle would thus extend to the clavicle and not to the jaw, this mitigated the problem of opposing mechanical forces under Watson's model.
  • Howie suggested that the muscles between the occiput and the vertebral column could have played a minor role as well, but that it was limited by the vertical orientation of the occiput. However, in brachyopids in which the occiput slants backwards at at an angle, these muscles would have a greater effective range and thus a probable greater role. The relative role of the muscle inserting onto the clavicle remains difficult to assess, as it was in 1970, because brachyopid postcrania is far and few between and often isolated or fragmentary.  

A reconstruction of the trapeziuscleidomastoideus (now just the cleidomastoideus) of the Permian temnospondyl Eryops by comparison with that of "Megalobatrachus" (=Andrias, the Asian giant salamanders) and Sphenodon (the tuatara). Figure from Miner (1925).

Mandible of the Cretaceous chigutisaurid Koolasuchus cleelandi (the last temnospondyl) showing the long and slightly upturned retroarticular process (bracket colours correspond with above). Figure modified from Warren et al. (1998).

Howie also addressed the role of the retroarticular process. Temnospondyls with a more sloped occiput, like brachyopids, would need a longer retroarticular process. However, an alternative solution would be to have an upturned process that could produce the same mechanical advantage, but without needing to be extensively long. The overall morphology of the jaw articulation probably constrained the gape (degree of opening of the mouth) quite substantially. In particular, the relationship of the quadratojugals to the quadrate (the latter being the skull bone that forms the skull-jaw articulation) would limit the lateral movement of the jaws during opening, which was a result of the morphology of the quadrate condyles (the part that contacts the jaw). Another limitation may have been the position of the orbits; temnospondyls with the eyes far back on the skull would probably have major issues actually seeing much of anything if the skull was raised too far, even if the eyes protruded above the skull to look forward. Subsequent workers have generally proposed gapes around 20-30° (e.g., Shishkin, 1987; Hellrung, 2003), although plenty of other angles (up to a right angle) have been suggested as well. 

Model of head raising in Gerrothorax pulcherrimus. (A-B) resting state; (C-D) gaping state. A and C show the entire skull, mandible, and pectoral girdle, whereas B and D show the skull-neck (atlanto-occipital) joint. (E-J) silhouettes of the curvature of the condyles of three different specimens in medial (internal) view, showing the asymmetry of the dorsal and ventral contours; arrows indicating the margins of the articulating surfaces. Figure from Jenkins et al. (2008).

Work by Jenkins et al. (2008) is the most recent and the most detailed work to explore models of head raising in temnospondyls, using the plagiosaurid Gerrothorax pulcherrimus. 

• Skull-neck (atlanto-occipital) joint: The surface area of the exoccipital condyles is much greater than that of the corresponding articulating facets on the first vertebra (the atlas), providing strong evidence for dorsoventral movement of the skull. These back end of the condyles (that would meet the articulating facets) are also noticeably convex, rather than being flat or concave. During the rest phase, the contact would have been in the lower half of the condyles (B in the above figure), with rotation to the upper half during head raising (D in the above figure). 
• Spinal medulla: An important consideration is that just because a range of motion can be accomplished with the bones does not mean that it is biologically feasible; various soft tissues ranging from organs to ligaments constrain movement. As it relates to movement of the head is the spinal medulla, a nervous tissue structure extending from the brain to the vertebral column. Head lifting could be predicted to substantially deform this structure (not good!), but the space between the exit from the skull (the foramen magnum) and the entrance to the backbone (the atlantal arch) is long and open dorsally. The dorsal margins of both regions are furthermore slightly tilted to face dorsally, further increasing the space and allowing for the medulla to have its deformation distributed along a greater length. Also important is the position of the exoccipital condyles to the foramen magnum. In many temnospondyls, the condyles are fully below the foramen, but in Gerrothorax, the condyles are dorsally shifted, which would allow the axis (the second vertebra) to move dorsally during head raising to minimize deformation of the medulla.
• Skull shortening: Plagiosaurids have relatively short skulls for both temnospondyls and tetrapods in general. This would shift the center of mass pretty close to the skull-neck joint, ideal for rotation around this joint during head raising. Conversely, long-skulled temnospondyls would have a center of mass much farther forward that would be mechanically disadvantageous for this type of 
• The gape angle (i.e. how wide can the mouth open) can be estimated by the difference in heights of the condyles compared to the atlantal facets. A comparable size would indicate a small gape because there would be little room for rotation. Conversely, much smaller facets would indicate a larger gape. The gape is estimated to around 50° in Gerrothorax​. This is nearly double the angle of humans!
• Pectoral (shoulder girdle): In many stereospondyls, the pectoral girdle is massive and robust compared to the limbs, which are small and relatively underdeveloped. The presence of extensive ornamentation on the ventral surface of most pectoral elements also indicates that limb muscles did not originate from the girdle. This provides evidence that the pectoral girdle could have played a role in head raising, as Howie (1970) suggested. Whether it was the clavicle (Howie) or the cleithrum (Jenkins et al.) that the occipital muscles attached to is a bit unclear. 

A lot of the discussion on head raising is inherently linked to other aspects of feeding in stereospondyls. Unfortunately, a lot of that remains poorly resolved or tested only in very specific and isolated groups. For example, were most stereospondyls active swimmers and hunters in the water column (pelagic) or did they prefer ambush tactics at the bottom (benthic)? Did they directly bite prey or attempt to inhale them through suction feeding? Watson's classical model of head raising was predicated on the assumption that the animal sat on the bottom so that its jaw was firmly in contact with the ground and could thus be used as a fulcrum, although a general bottom-dwelling ecology is not incompatible with the more modern concepts of head raising. 

There has been other work done on feeding in temnospondyls, primarily finite element analyses (FEA) by Fortuny and colleagues and reconstructions of muscles systems by Witzmann and colleagues, but these usually are usually intended to assess other aspects of temnospondyl feeding and do not directly inform on the viability and degree of head raising. Some examples:

• Fortuny J, Marcé‐Nogué J, Gil L, Galobart À. 2012. Skull mechanics and the evolutionary patterns of the otic notch closure in capitosaurs (Amphibia: Temnospondyli). The Anatomical Record 295(7):1134-1146.
• Fortuny J, Marcé‐Nogué J, Konietzko‐Meier D. 2017. Feeding biomechanics of Late Triassic metoposaurids (Amphibia: Temnospondyli): a 3D finite element analysis approach. Journal of Anatomy 230(6):752-765. doi: 10.1111/joa.12605
• Witzmann F, Schoch RR. 2013. Reconstruction of cranial and hyobranchial muscles in the Triassic temnospondyl Gerrothorax provides evidence for akinetic suction feeding. Journal of Morphology 274(5):525-542. doi: 10.1002/jmor.20113
• Witzmann F, Werneburg I. 2017. The palatal interpterygoid vacuities of temnospondyls and the implications for the associated eye‐and jaw musculature. The Anatomical Record 300(7):1240-1269. doi: 10.1002/ar.23582

What's it all mean?
Okay, so now that we've gone over all of that, let's sum it all up and debunk some myths and misconceptions:

• All temnospondyls open their mouths by head raising = FALSE
  • ​Even the original model by Watson focused solely on flat-skulled temnospondyls, which are largely aquatic and predominantly stereospondyls, the more derived temnospondyl group that largely shows up in the Mesozoic and that evolves alongside the dinosaurs. Terrestrial temnospondyls don't possess any of the features associated with head raising, nor is there any particular reason to predict this mechanism in the various terrestrial clades. 
• All stereospondyls open their mouths by head raising = INDETERMINATE
  • Evidence against: ​Setting aside the fact that some stereospondyls are terrestrial, the primary test cases for head raising (Gerrothorax, brachyopids, capitosaurs) are not good representatives of all stereospondyls in most aspects. For example, the majority of stereospondyls have vertical occiputs, not the angled occiputs seen in brachyopids and plagiosaurids (among some other temnospondyls). This suggests that most stereospondyls did not have much involvement of muscles between the skull and the neck vertebrae. Furthermore, the dorsal shift of the occipital condyles in Gerrothorax and other plagiosaurids that reduces deformation of the spinal medulla is not typically seen in other stereospondyls. Lastly, the center of mass for most stereospondyls is far anterior to the skull-neck joint because of their long skulls. At minimum, this means that the results of Jenkins et al.'s work on Gerrothorax cannot be paralleled into other stereospondyls, possibly because they were incapable of head-raising to the same degree.
  • ​Evidence for: The postcranial skeleton of stereospondyls is quite conserved, particular with respect to having large pectoral elements with ventral ornamentation and poorly developed limbs. If a requisite for head raising is the insertion of occipital muscles onto the pectoral girdle, especially in taxa with vertical occiputs, presumably that attachment existed in most stereospondyls. 

Illustrations of the skull of Gerrothorax pulcherrimus in dorsal, ventral, and occipital profile. Scale bar equals 1 cm for reference. Figure from Jenkins et al. (2008).

So who can head raising reasonably be inferred to have occurred in?
Realistically, very few taxa have actually been studied with respect to their specific anatomy as it relates to a hypothesis of head raising. Gerrothorax is a pretty peculiar temnospondyl in a lot of regards and takes a lot of stereospondyl features to the extreme (e.g., very flat, wide skull). Based on what we know now, short-faced (short-skulled) aquatic stereospondyls would be my recommendation for limiting the scope of inference. Dvinosaurs are an interesting case within temnospondyls because they are not stereospondyls but look very much like brachyopids (relationships between them are disputed), with short skulls and sloping occiputs. However, a lot of dvinosaurs only have a single occipital condyle down the midline; how this could relate to mobility of the head-neck joint and raising of the head is unclear. 


TLDR: the head raising model should not be automatically inferred to apply to all aquatic stereospondyls and is definitely not applicable to many terrestrial temnospondyls. 

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Refs

• Dilkes DW. 1990. A new trematopsid amphibian (Temnospondyli: Dissorophoidea) from the Lower Permian of Texas. Journal of Vertebrate Paleontology 10(2):222-243. doi: 10.1080/02724634.1990.10011809
• Hellrung H. 2003. Gerrothorax pustuloglomeratus, ein Temnospondyle (Amphibia) mit knöcherner Branchialkammer aus dem Unteren Keuper von Kupferzell (Süddeutschland). Stuttgarter Beiträge zur Naturkunde Serie B (Geologie und Paläontologie) 39:1-130. 
• Howie AA. 1970. A new capitosaurid labyrinthodont from East Africa. Palaeontology 13(2):210-253.
• Jenkins Jr, FA, Shubin NH, Gatesy SM, Warren A. 2008. Gerrothorax pulcherrimus from the Upper Triassic Fleming Fjord Formation of East Greenland and a reassessment of head lifting in temnospondyl feeding. Journal of Vertebrate Paleontology 28(4):935-950. doi: 10.1671/0272-4634-28.4.935
• Miner RW. 1925. The pectoral limb of Eryops and other primitive tetrapods. Bulletin of the American Museum of Natural History 51:7.
• Panchen AL. 1959. A new armoured amphibian from the Upper Permian of East Africa. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 242(6):207-281. doi: 10.1098/rstb.1959.0005
• Shishkin MA. 1987. [Evolution of ancient amphibians (Plagiosauroidea)]. Transactions of the Paleontological Institute, Academy of Sciences of the Union of Soviet Socialist Republics 225:1-144. [Russian] 
• Warren A. 1981. A horned member of the labyrinthodont super-family Brachyopoidea from the Early Triassic of Queensland. Alcheringa 5(4):273-288. doi: ​10.1080/03115518108566995
• Warren A, Rich TH, Vickers-Rich P. 1997. The last last labyrinthodonts. Palaeontographica Abteilung A ​247:1-24.
• Watson DMS. 1919. The structure, evolution and origin of the Amphibia. The "orders' Rachitomi and Stereospondyli. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 209:1-73. doi: 10.1098/rstb.1920.0001
• Watson DMS. 1958. A new labyrinthodont (Paracyclotosaurus) from the Upper Trias of New South Wales. Bulletin of the British Museum of Natural History 3:235-263. 
• Watson DMS. 1962. The evolution of the labyrinthodonts. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 245(723):219-265. doi: 10.1098/rstb.1962.0010