How do we know...? (Part I: Head in the Clouds)

To kick off this topical series looking at how we know what we claim to know about temnospondyls, we'll start with the most recognizable part of any animal: the head! Lots of important things happen up at the head - breathing, eating, and plenty of sensory functions from smell to hearing. So it stands to reason that the skull might offer us a good deal of insight into the lifestyle and ecology of temnospondyls.

Shapes and sizes

Temnospondyls are well-known for a diversity of skull shapes, some of which look an awful lot like other animals (which are really copycats of temnospondyls, who did it first). Often we assume that like modern tetrapods, this has something to do with what you ate and where you lived. Long-snouted crocodilian-like taxa probably ate primary smaller, agile fish; this is something that long snouts (or beaks) have evolved repeatedly to do very well. It isn't perhaps so great for sucking in a large fish, something that a wide skull with a big gape is better equipped to do. To get at the question of whether general skull shapes might line up with general ecologies, we have to come up with some categories.

Temnospondyl phylogeny showing different temnospondyl skull shapes; figure is not to scale with respect to different species' skulls (source: Schoch, 2013).

The first is in relation to the snout: long- versus short-snouted forms. Of course, this begs the question of what really is a snout. Do all animals have snouts? We often associate snouts with mammals and many reptiles, but what about other animals? Do birds have snouts? Or just beaks? No modern amphibian has a long skull today, so do any of them have snouts? What about fish? Well, there is no standard, which is just like most other things in paleontology, but most people use 'snout' to refer to what is technically called the 'preorbital region,' or the amount of skull that is in front of the eyes. In this sense, all animals have a snout, it may just be really short in some.

The long-snouted Permian stereospondylomorph Archegosaurus decheni from Germany (source: Witzmann, 2005).

The short-snouted Triassic plagiosaurid Gerrothorax pulcherrimus from Europe (source: Schoch & Witzmann, 2012).

Short- and long-snouted should not be conflated with short-skulled (brachycephalic) and long-skulled (dolichocephalic); a taxon can have a long skull but a short snout, as with Erpetosaurus below (from Romer, 1930). Probably the closest thing to a taxon with the inverse - a short skull but a long snout - is a zatracheid, like Acanthostomatops below (from Witzmann & Schoch, 2006).

Most of what we infer about general skull shapes' relevance for inferring paleoecology is based on what we have today. So we assume that long-snouted taxa like Archegosaurus were crocodile analogues and probably spent more time in water, at least when it came to feeding. Other animals with long snouts that hang out in water are obligately aquatic (i.e. they die if they're out of water) like dolphins/porpoises and some fish like gar and needlefish. There aren't many terrestrial animals with long snouts, and those are weirdos with specialized lifestyles like anteaters and echidnas who use their snouts to get into places where termites and ants live. A cautionary tale comes in the most relevant case study: modern amphibians. There are no long-snouted modern amphibians, let they live in all sorts of different habitats.

One promising type of analysis that has been applied to the entire skull to infer feeding behaviour is called finite element analysis (FEA). This method measures stress buildup in different regions based on the type of stress applied (e.g., from one side or evenly distributed). A number of studies have used this method to examine different feeding strategies in temnospondyls (e.g., Fortuny et al., 2011, 2017), with the idea that strategies that produce high degrees of stress are unlikely to have been used. You can see in the above example that the same stress produces different stress distribution patterns in different skulls (warm colours = more stress). However, much of the determination about possible feeding style and habitat is influenced by nuances of the skull like the exact shape of the tabular horns (the backward projections), not just its general shape. For example, not all of the taxa that lack the long crocodilian-like snout are inferred as terrestrial here.

Lapillopsis, from the Triassic of Australia, is one of the smallest temnospondyls, with a skull barely exceeding 2 cm in length (scale bar is 1 cm; from Yates, 1999).

Mastodonsaurus, from the Triassic of Germany, is conversely one of the largest, with a skull that could reach up to 125 cm in length (source: Schoch, 1999).

What about size? Well size fundamentally constrains at least what you can eat and how you can eat it, though not necessarily where you eat it. Temnospondyl skulls range from about 2 cm in length to well over 100 cm. We can presume that small temnospondyls are eating mostly invertebrates like insects, much as the vast majority of modern amphibians (mostly small) do today, simply because there aren't many small vertebrates that would fit in the mouth of a 2 cm long skull. We run into more uncertainty as they start increasing in size because we just don't have great modern analogues. Asian giant salamanders, which approach about 2 meters in total body length, still eat mostly invertebrates as well as fish; they just tend to be larger invertebrates (e.g., crayfish). Just because you have a big mouth doesn't mean you eat big food. So there is really a lot of uncertainty for large temnospondyls - did any of them specialize in eating other tetrapods or perhaps very large fish, or were they just sizing up at the local crab shack?

I spy, with my little eye...

One of the general attributes of skulls that may confer pretty good insight is one of the primary sensory features - the eyes! Obviously, which way your eyes face is a major constraint on how well you can catch other animals, avoid predators, etc. Temnospondyls exhibit lots of variation in the position of the orbits (the eye socket), from facing mostly outward to the site to facing entirely upward.

Compare these two examples, Cacops morrisi on the left, which has orbits that face mostly laterally and which thus has a correspondingly tall skull, and Metoposaurus krasiejowensis on the right, which has only dorsally facing orbits and a correspondingly flat skull; you basically can't even see the orbits when looking from the side (sources: Reisz et al., 2009 and Sulej, 2007).

The Atlantic halibut (source: Marcus Elieser Bloch via Wikimedia)

The flat skulls and dorsally facing orbits of Metoposaurus and a lot of other Triassic temnospondyls may remind some people of some modern fish like the halibut, which sit on the ocean floor and look upward, waiting for food to pass. This is a classic ambush strategy and one best employed when sitting on the bottom of something where you only need to focus on looking up.

Indeed, convention favours interpretation of flat-headed temnospondyls with dorsally facing orbits as being primarily aquatic and specializing in ambush modes of predation. Conversely, we have assumed that temnospondyls with taller skulls and laterally facing orbits were more terrestrial and had better range of vision. An important caveat in all of this is that the orbit may only be a crude proxy for the actual eyeball. As occurs in lots of modern animals, the orbit can be much larger than the actual eyeball. A great example of this is the hellbender, a modern salamander found in North America, which has large orbits but very tiny eyes (source: Schoch et al., 2014). Therefore, there is a lot of uncertainty about how big the eyes were (a certain small size renders them pretty useless for discerning fine shapes) or how they were oriented.

Comparison of differently sized scleral rings that are associated with different activity patterns (when an animal is most active; source: Schmitz & Motani, 2011).

One proxy that we do have for eyeball size is the scleral ring. I've blogged about this weird ossification before, but the gist is that the ring is a series of bony plates that are within the eyeball itself and that act as a support structure and to help with visual acuity. We know that at least some temnospondyls had scleral rings of a similar size to the orbit, which suggests a close correspondence in eyeball-to-orbit size, but for most taxa, we have no information on whether this ring was even present (it is absent in many non-reptiles and non-birds today, including humans).

There's also the question of how much the eyeballs protrude and in what direction. In most animals, including flat-headed fish like the halibut, the eyes protrude above the skull, being held up by soft tissue, not bone. There isn't, for example, an elevated rim along one side of the orbit that might offer a hint of which way the eyes faced. So while we as humans are accustomed to thinking of forward-facing vision, in fact many animals have eyes that face more to the sides, and there is a blind spot directly in front of the animal where there is no coverage. Fish and modern amphibians, among some other animals, have this type of vision, which is often why they turn slightly to face you because their forward vision is more limited than ours.

Most temnospondyl paleoart to date has borrowed from modern amphibians, with more laterally facing orbits supported by a soft tissue on the inner edge, like this Eryops by Liam Elward.

In tune

Like vision, hearing is another sensory structure that varies substantially in air versus in water, and there are a number of bony components of the ear. But unlike eyes, there are many different ways to "hear," and not all of them involve the kind of ear that you might expect. Humans, of course, have prominent external ears. Sound waves go in (perhaps past your piercings), hit the eardrum, and are then transmitted through an attached series of bones (the incus, malleus, and stapes) on the other side of the eardrum to the brain. Most mammals have very prominent ears, which can sometimes tell us other things about them like their mood. This type of ear has three parts - outer (the fleshy part); middle (the three bones); and inner (the fluid-filled canals that pass vibrations to the brain).

Amphibians though have a very different ear. For one, no amphibian has a fleshy ear sticking off of their head. Instead, some of them, like frogs, have the equivalent of our eardrum right on the outside of their head. This is called the tympanum or the tympanic membrane and is often quite large. Because people aren't used to seeing an eardrum, it's often confusing what this large structure is, but it sits right behind the eyes similar to where our ears sit. However, the frog ear is not the same as the salamander ear or the caecilian ear. Salamanders and caecilians actually don't have external ears - if you look at the head, there isn't even a small hole, let alone a large membrane or fleshy structure.

Most mammals, like dogs, have very prominent ears, although these can take on very different shapes (source: Bryan Gee).

A green frog from eastern North America (source: Bryan Gee)

An eastern newt from eastern North America (source: u/cotinis via Flickr)

Toph Beifong, a blind girl, is able to "see" by using her feet to sense vibrations in the ground when people or objects move (source: Nickelodeon)

This doesn't mean that salamanders and caecilians can't hear though! Sound waves are ultimately transmitted as vibrations, which means that if you can pick up vibrations, you can "hear." Of course, audible sound is not the only vibrations that we are able to sense either; you can feel vibrations in the ground when a large truck drives by or an earthquake strikes. Other parts of our body can sense vibration, they just aren't always as sensitive (this is the idea behind how Toph from Avatar: the Last Airbender can "see"); this is one form of what we call mechanoreception. In a similar fashion, salamanders have developed a variety of ways to "hear" without a tympanic membrane, some of which involve muscles attached to the shoulder, lungs, and their mouth.

All of this is to say that it is quite hard to actually figure out what kind of auditory capabilities temnospondyls had and in turn whether a given species was better at hearing on land or underwater. We know that at least some temnospondyls had a tympanic membrane, which suggests that they were capable of detecting airborne sounds and thus probably spent at least some time on land. This evidence comes from a well-developed otic notch, a large opening in the skull behind the orbit and adjacent to the braincase. Whereas most of the temnospondyl skull is covered in pits, ridges, and grooves, this otic notch sometimes has a large unornamented flange in it that is thought to have been the spot where a tympanum would have attached (the gray shading and 'ty' label in the figure on the bottom left). Often times, one of the bones of the inner ear (the stapes), is preserved with one end pointing outwards into the notch and the other end articulated with the braincase. This suggests that these temnospondyls could hear airborne sound.

The Permian dissorophid Cacops morrisi from Oklahoma. The otic notches are the large openings behind the eyes that are more visible from the side than from above (source: Reisz et al., 2009).

The Triassic capitosaur Stanocephalosaurus amenasensis from Algeria. The otic notches are the semi-enclosed openings at the back of the skull and face upward, not to the side, in contrast to Cacops (source: Arbez et al., 2017).

However, most temnospondyls have an otic notch, and the majority of those do not have this large flange within their otic notch - many have no flange at all, particular those in which the otic notch doesn't face out to the side, but upward. Species without a flange do still have a stapes that points towards the notch, but the key is that it is unknown whether a tympanic membrane stretched across the otic notch or whether it was merely covered in other soft tissues like the rest of the head. It has been suggested that the otic notch in these taxa was indeed covered by some soft tissue and thus formed an enclosed air pocket that was impermeable to water. If the stapes projected into this pocket, then it would be operating in an airborne setting, not an underwater setting, so vibrations transmitted through water would be converted to sound waves inside of this air pocket and then be conducted to the brain in the same fashion as animals with a tympanum. This is the best guess for what many of these taxa with otic notches but no tympanum were doing (e.g., Schoch, 2000; Arbez et al., 2017).

Then there are some temnospondyls with no otic notches. These usually still have a stapes, but we are left with more uncertainty regarding their hearing capacities and how they did it if so. The figure on the right shows nine different dvinosaurs (from Schoch & Voigt, 2019), some of which have an otic notch at the back of the skull like Stanocephalosaurus above. In these taxa (e.g., A-D), the same principle of an air pocket may have been present, implying they lived underwater. No tympanum is known from any dvinosaur. However, some taxa have no otic notch (e.g., E-F, H-I). What these taxa did, and how they heard if they could hear, is less clear.

Slimy senses

Reconstruction of the Permian dvinosaur Dvinosaurus by Bystrow (1939), labels added to show the infraorbital (io), postorbital (po), and the supraorbital (so) canals.

The final sensory system that is recorded in fossils is one that I've blogged about before at length: lateral line canals! Preserved as a series of grooves on top of the skull and sometimes along the side of the lower jaw and on the underside of the shoulder girdle, this is a specialized system of mechanoreceptors that is often found in aquatic animals and that allows them to detect slight movements like an approaching predator, even when they can't see them. Historically, we have assumed that anything with these canals on the skull was aquatic because the organ would dry out and then die if exposed to air for too long. It is probably more complicated than this because we don't know, for example, whether an animal needed these sensory organs for its entire life. If it intentionally moved onto land and had other means of sensing (like ground vibrations), then it may not have mattered as much if the organ dried up - it's not like the animal would automatically die with it. Many temnospondyls do have these grooves, and this tends to correlate with flatter heads and dorsally facing orbits (= aquatic). It's less clear what to make of temnospondyls that have only one or two grooves, a middle ground of sorts. Having fewer grooves doesn't make the organ less at risk of drying out on land, so does that mean the animal just couldn't detect vibrations as well in water? Or merely that the organ was present and just didn't carve a groove into the top of the skull (a bony impression of the lateral line is rare in modern animals).

Something to chew on

The jaw sadly does not tell us much about temnospondyl ecology so much as what sits on the jaw does: the teeth. Temnospondyls do have a variety of different jaw anatomies, and it's clear that some features, like the size of the cavity where muscles would have been packed in or the length of a long protrusion off the back end (the retroarticular process), have functional implications related to bite force, gape (how big the mouth can open), and jaw-opening mechanics (did the head raise up or did the jaw lower). Most of the studies that look at the role of the jaw do so only in a conjectural sense of attempting to reconstruct the arrangement of muscles (e.g., Witzmann & Schoch, 2013) or a modeling sense of attempting to predict where stress would have built up during a bite (e.g., Fortuny et al., 2011). Early histological work has identified complex articulations between different bones in the jaw (e.g., Gruntmejer et al., 2019), some of which are set up for tension (pulling apart) and others of which are set up for compression (pushing together), but we don't have enough data yet for comparative purposes to really know what this means other than that some parts of the jaw were under different stress than others (this is true of pretty much any animal's jaw). There is clearly a lot of room to work on jaw biomechanics because at present, we pretty much assume a lot of things didn't vary much between temnospondyls.

Inferred head-raising capability in the Triassic plagiosaurid Gerrothorax pulcherrimus from Europe. Head-raising is very atypical among vertebrates - you will notice that when you open your mouth, your head doesn't move, and your jaw moves down. In head-raising (also known as the "toilet seat mechanism," the head moves up while the jaw stays still (source: Jenkins et al., 2008)

Reconstruction of cranial and jaw musculature associated with feeding in the Triassic plagiosaurid Gerrothorax. Because we have no true temnospondyls alive today, most of our interpretations are based on what we observe in dissections of salamanders (source: Witzmann & Schoch, 2013)

Tale of the teeth

One would assume that the teeth of temnospondyls should tell us quite a lot about what they ate; after all, this is often how we infer what modern animals are up to. Alas, the teeth of temnospondyls are about as basic as they come. Practically all temnospondyls have the stock model of tooth: a single cone. This type of unspecialized dentition is common of many fish and early tetrapods, although there are always exceptions that end up being unusually specialized. Many modern amphibians also have only conical teeth. One thing that we know that conical teeth are good for is eating fish; cones are great for piercing and stabbing prey, and something slippery like a fish that's hard to hold often requires a firm grasp. You can see this in many modern predatory fish as well as in crocodilians (which of course eat pretty much anything, not just fish).

A variety of temnospondyl teeth from Middle Triassic sites in Germany: (a-d) Mastodonsaurus giganteus; (e-f) Callistomordax kugleri; (g) Marginal tooth of Trematolestes hagdorni; (h) Gerrothorax pulcherrimus; (i) Plagiosternum granulosum; (j) Plagiosuchus pustuliferus (source: Schoch et al., 2018)

Crocodile sunning itself (source: u/Dushybusy via Wikimedia)

This is not to say that every temnospondyls with conical teeth (the overwhelming majority) were fish-eaters. Some of them were almost certainly too small to be eating fish unless they were eating guppies, and because amphibians lack true necks, it would be difficult for many land-dwelling temnospondyls to eat much of anything in the water. There are also nuances to conical teeth - some area straight while others are curved; some have cutting edges while others are entirely smooth. One might assume, for example, that the ones with cutting edges are eating some beefier items (say, other temnospondyls). Most are not perfect cones. Size differences were probably also a big factor, mainly in controlling the number of teeth that fit in the mouth - some taxa had fewer than 30 teeth along the outer margin, while others exceeded 130.

Finally, we have teeth in different parts of the mouth, which is a strange concept for people to think about (you can read more about the very large teeth of many temnospondyls here). In addition to the outer tooth row ('marginal teeth'), temnospondyls almost always had large accessory teeth on the roof of their mouth that we call 'fangs' or 'tusks.' Whether these were used to impale prey isn't clear; the bone under these teeth is often quite thin, so it may have been pretty bad at bearing a lot of bite force on those teeth. Then we have very small teeth, often found by the hundreds, called denticles. These covered the roof of the mouth in early temnospondyls (like Cochleosaurus, above on left; Sequeira, 2003) but gradually become reduced and eventually disappear in later temnospondyls (like in Mastodonsaurus, above on right; Schoch, 1999). Presumably, having the roof of your mouth was useful for prey capture by making a giant gripping surface (imagine a sandpaper-like covering). This would be great for slippery prey or anything that would try to make an escape from the literal jaws of death. So it isn't clear then whether the loss of these denticles had any measurable effect on a temnospondyl's ability to eat, and if so, why these tiny teeth were lost. There is no clear correlation with any other skull feature (e.g., being short-snouted) that might indicate a particular need for denticles in one type of environment versus another.

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That wraps up what was a much longer blog post than I anticipated (and which is hardly exhaustive). The TLDR is that there are few simple ways to infer a temnospondyl's ecology based on singular features, like whether it had a wide head or curved teeth. We can make educated guesses of course (and often do), but most of this is based on the limited sample of what we can parallel to today, like crocodiles or frogs. We could be entirely wrong for all we know! That's why it's important to look at all parts of the skeleton, not just the head. Up next week: limbs!