Bumps and lumps: a primer on temnospondyl ornamentation

If you look at a temnospondyl skull, it is decidedly not smooth like our own. Instead, it may be covered by any (or all) of the following: pits, grooves, ridges, tubercles, or nodules. Don't confuse this for pebbly or bumpy skin texture like in some modern reptiles that are formed by separate scales or osteoderms that sit on the skull (or other parts of the body) - these bumps develop as part of the skull! This week's blog post is covering dermal ornamentation, naturally with a focus on temnospondyls. A lot of this week's blog is derived / inspired by work by Florian Witzmann at the Museum für Naturkunde in Berlin who has done lots of very cool work on temnospondyls in general but also with respect to their bones.

Mounted skeleton of the Late Triassic temnospondyl Koskinonodon perfectus from Texas (labeled as Buettneria perfecta) at the American Museum of Natural History in New York. Ornamentation is developed on the top of the skull and the side of the jaw. Photo: Bryan Gee

Photograph of the Gila monster (a lizard from Mexico), which has a pebbly texture as a result of scales and osteoderms rather than well-developed ornamentation. Distributed on Flickr by u/OzinOH under a Attribution-NonCommercial 2.0 Generic (CC BY-NC 2.0) license.

Who has it?
Temnospondyls are well-known for having heavily ornamented skulls, especially when they occur in deposits with other tetrapods that are largely or entirely un-ornamented (e.g., Late Triassic deposits) This can make it pretty easy to tell whether a temnospondyl was around and who it was, even just from small fragments. However, they are not the first or the last tetrapods to be ornamented - many Paleozoic tetrapods (e.g., stem tetrapods, seymouriamorphs), including some amniotes (e.g., captorhinids, crocs [both living and extinct]), are ornamented to various degrees. Below are some examples of ornamented non-temnospondyls.

Where is it?
In temnospondyls, the most apparent ornamentation is found across the skull, in which most to all of the elements are ornamented on their dorsal (top) or lateral (external side) surfaces. This is the most common place for ornamentation in non-temnos as well. Temnospondyls also have ornamentation on parts of the jaw (again, common for early tetrapods), particularly along the ventral (bottom) margin and toward the back on the lateral (outer) surface. Lastly, many (but hardly all) temnospondyls have ornamentation covering the ventral (bottom) surface of the main plate-like pectoral (shoulder) elements, specifically the interclavicle (a bone not found in mammals) and the clavicle (the collarbone). These pectoral bones face downward in quadrapeds (4-legged locomotion) and towards the front in bipeds (2-legged locomotion). A few temnospondyls have osteoderms (bony armour plates), which also ornamented (osteoderms are typically ornamented in non-temnos). Ornamentation can differ within the same animal at virtually every scale - between skeletal regions (skull vs. osteoderms), within regions (snout vs. back of skull), and within element (e.g., parietals).

​What's it for?
Because ornamentation is so ubiquitous, it has been widely (although not extensively or conclusively) speculated on. Below are some of the main ideas behind ornamentation:

• Housing of a complex network of blood vessels for facilitating cutaneous respiration (breathing through the skin), which is seen in modern amphibians (e.g., Bystrow, 1947). 
  • Increased surface area for cutaneous respiration (e.g., Cosgriff & Zawiskie, 1979).
• Buffer against acidosis (Janis et al., 2012).
• Housing of a complex network of blood vessels for thermoregulation.
• Increased complexity of the skull roof improved the distribution of stresses on the roof, particularly during feeding (e.g., Coldiron, 1974; Rinehart & Lucas, 2013).
• Tight attachment of the integument (skin) to the sculpturing (e.g., Romer, 1947; Witzmann & Soler-Gijón, 2010).
• Indicator of metamorphosis (e.g., Boy & Sues, 2000).

Some of these ideas hold more water than others, and a number of them are related to the widespread consensus that a complex and well-developed vascular network was integrated with the ornamentation. Evidence for the vasculature is evidenced through small foramina that are found throughout the ornamentation (see figures below). 

Examples of temnospondyl ornamentation from Witzmann et al. (2010). (A) Mastodonsaurus giganteus; (B) Gerrothorax pustuloglomeratus; (C) Metoposaurus fraasi; (D) Wetlugasaurus samarensis.

More examples of temnospondyl ornamentation from Witzmann et al. (2010). (A) Zatrachys serratus; (B) Lanthanosuchus watsoni (a parareptile, not a temnospondyl); (C) Cochleosaurus bohemicus; (D) Vigilius wellesi; (E) Melosaurus uralensis; (F) Gerrothorax pustuloglomeratus.

Cutaneous respiration
Breathing through the skin, or cutaneous respiration, is a common physiological attribute of modern amphibians, hence why they often need to keep their skin wet and usually do not do too hot in deserts and other arid climates. Other animals (including humans) are capable of cutaneous respiration, but this typically is responsible for a very small amount of our total respiration, whereas it is pretty important for amphibians. The most speciose group of salamanders (plethodontids) are called lungless salamanders because they actually lack lungs and more or less rely entirely on cutaneous respiration (e.g., below on left)! Bystrow (1947) was one of the first proponents of the idea that ornamentation of various tetrapods was primarily for cutaneous respiration. There are a few problems with this however...

• Size: Modern amphibians are small, and this is in part based on constraints on physiological functions associated with size. Many regulatory processes (e.g., heat and gas exchange) are directly affected by an animal's surface-area-to-volume ratio. Smaller animals have a larger ratio (proportionately more surface area), which facilitates exchanges of energy and gas. This is not always a good thing - too much heat exchange means that small mammals have to eat extensive amounts of food relative to their body weight in order to maintain a body temperature that can be several times that of the external environment. Plethodontids are able to rely entirely on cutaneous respiration because they are pretty small. Larger amphibians with lungs can still rely heavily on cutaneous respiration, hence why some of them are very wrinkly (e.g., the hellbender on the below right). The first is that a lot of temnospondyls are a lot larger than modern salamanders, so they already have unfavourable surface-area-to-volume ratios.
• (Naked) skin: Most modern amphibians have what we called "naked skin," which like humans, is not covered in scales or feathers or other hard tissues that directly intercede between the skin and the external environment. However, a lot of early tetrapods, including many temnospondyls, have different flavours of scales and osteoderms (e.g., Witzmann, 2007) that would have further reduced the exposed surface available for direct gas exchange. 

Verdict: Unlikely but not impossible in very small and unscaled temnospondyls

Photograph of an Ensatina salamander by Brian Gratwicke, distributed on Flickr under a CC BY 2.0 License.

Photograph of an Eastern hellbender by Freshwaters Illustrated/Dave Herasimtschuk, distributed on Flickr by the Department of Agriculture under a CC BY 2.0 license.

Buffer against gas buildup
This is a relatively novel idea put forward by Janis et al. (2012) that ornamented dermal bone is more effective at buffering acidosis (buildup of acids in the blood), primarily of carbon dioxide (turns to carbonic acid in the blood) and lactic acid. The idea is based on modern vertebrates and largely (well-supported) conjecture about the evolution of early tetrapods and the associated physiological challenges. As pointed out by the authors, fish (living in a lower-oxygen environment) need more ventilation to pull in oxygen through their gills and thus get rid of carbon dioxide much faster due to high ventilation rates. Conversely, terrestrial animals (living in a higher-oxygen environment) ventilate at lower rates and thus accumulate more carbon dioxide. This is a particular problem for larger animals. Various authors have speculated on how early tetrapods eliminated carbon dioxide (e.g., Packard, 1976). Although some of the more aquatic early tetrapods may have retained external gills and been able to dump CO2 by returning to the water, this would not work for a fully terrestrial animal. Costal (rib-driven) respiration like that seen in reptiles also seems unlikely because a mobile ribcage had not evolved. They also probably lacked other mechanisms seen in amniotes (e.g., buffering with the kidneys); modern amphibians are not very efficient at compensating for acidosis. In modern tetrapods, mobilization of calcium deposits from bone tissues can be used to buffer acidosis.

In general, predicted patterns are supported by the fossil record. Terrestrial tetrapods have more pronounced ornamentation on the whole compared to aquatic forms, except for ones that are comparably small to modern amphibians and that probably could buffer through increased gas exchange through un-scaled skin. Ornamentation is also rare in early amniotes, indicating that costal respiration may have evolved by this time. A few problems:

• Data don't match: Of course there are taxa that don't fit the pattern. Some definitely aquatic taxa that were probably bottom-feeders have very pronounced ornamentation that may have served another purpose (ballast?).
• Hard proof: The most prominent challenge to testing this hypothesis is that even in modern animals, virtually no histological signal reflecting mineral mobilization and release is apparent at peak acidosis, and it may thus not be possible to detect this in extinct tetrapods.

Verdict: Appealing but difficult to test.

 Thermoregulation
Based on the strong evidence for a well-developed vascular network, an idea examined by Witzmann et al. (2010) was the potential for temperature regulation to have driven the development of ornamentation. This idea hasn't strictly speaking been directly implicated with respect to ornamentation, but it follows from the support for a complex vascular network associated with the ornamentation. A number of modern animals, particularly reptiles (see on right), bask in order to increase their body temperature, and do so by increasing blood flow through the skin, increasing the heat transmission to the body. Basking was also suggested to have facilitated the evolution of terrestriality (Carroll et al., 2005) because an animal could warm up faster by sitting in the sun than in the water. 

However, there just isn't any hard evidence to support this. The vascularization of bones is pretty similar between areas of varying degrees of ornamentation (including smooth regions) on the skull, and there is still very pronounced ornamentation on areas that would have been facing downward (pectoral girdle, underside of mandibles) that would not have been exposed to the sun.
​
Verdict: Unlikely

Photograph of an Eastern Collard Lizard thermoregulating by basking in the hot summer sun at Petrified Forest National Park. Whether early tetrapods also utilized this behaviour is unknown. Photo by Bryan Gee.

Improved stress distribution
Coldiron (1974) was the first major proponent of the hypothesis that developed ornamentation helped to better distribute stresses, particularly during feeding. This is an attractive idea with respect to the skull, but it does not account for ornamentation on other elements (particularly the postcranial ones) that are not exposed to similar stresses. Additionally, the directionality of ornamentation with a particular orientation (e.g., ridges) does not align with predicted stresses but rather with the development of the vascular network.

A more recent study by Rinehart and Lucas (2013) used a more unusual analytical method to survey two Triassic temnospondyls (Eocyclotosaurus, Koskinonodon): beam mechanics. Modeling two main types of ornamentation, reticulate (honeycomb pitting), and ridge-and-groove, they showed that these types of sculpturing provide different resistances to various stresses and proposed that distribution may relate to muscle attachments (extending to the pectoral elements). This is an interesting finding based on an entirely different approach (P.S. I know nothing about beam mechanics), but it assumes more about temnospondyl musculature than is presently known and certainly requires more testing and taxon sampling. 

Verdict: Unlikely but needs more testing

Tight connection between bone and skin
​Romer's classic 1947 work on the "labyrinthodonts" included a brief mention that the ornamentation was presumably for a firm attachment between the skin and the ornamented elements. In spite of not really having much evidence on hand, Romer was right! Extensive Sharpey's fibers, originally of the dermis and eventually incorporated into the bone, are found in the ornamentation (e.g., Witzmann et al., 2010; Gruntmejer et al., 2016). These are typical histological markers of a tight connection between tissues. The presence of metaplastic bone (a particular type of bone) is also good evidence, as fibers in the soft tissue are confluent with those in the bone. 

Verdict: Likely

Example of Sharpey's fibers (abbreviated ShF) from a cross-section of a "sculptural saddle" of the temnospondyl Edops craigi. Figure from Witzmann (2009).

Thin sections of sculptural ridges in temnospondyls showing Sharpey’s fibres (ShF) penetrating the bone. A, Chenoprosopus milleri; B, Plagiosternum granulosum. Figure from Witzmann et al. (2010).

Indicator of metamorphosis
Boy & Sues (2000) found a correlation with development of polygonal ornamentation with remodelling of the hyobranchial apparatus, which occurs during metamorphosis. This sort of makes sense - many parts of the skeleton change in various ways during metamorphosis in modern amphibians, and this may well have been true for temnospondyls. Metamorphosis has been documented in a number of temnospondyls (e.g., Schoch, 2002, 2009). A few problems...

• Data deficient: We have no data on growth and development of most temnospondyls, so we don't actually know how many went through metamorphosis or how similar that metamorphosis was to modern amphibians. As with many modern amphibians, larval forms (e.g., tadpoles), juveniles, and adults may have lived in different environments, so they aren't often fossilized together, and it can be difficult to definitively recognize juveniles of a species only known from adults if they underwent drastic skeletal changes.
• Paedomorphism: Additionally, many of the large aquatic temnospondyls probably did not go through metamorphosis (like the modern axolotl) and retained larval features as adults (paedomorphism) or underwent a different transformation than modern amphibians, and yet many of them develop polygonal ornamentation.

Verdict: ​Possible but only for particular clades for which metamorphosis is documented.

Photograph of an axolotl (Ambystoma mexicanum), a paedomorphic aquatic salamander that retains external gills as an adult. Distributed on Flickr by Seánín Óg under a Attribution-NonCommercial-NoDerivs 2.0 Generic (CC BY-NC-ND 2.0) license.

Developmental trajectories of some temnospondyls from Schoch (2009). Taxa that undergo metamorphosis into a terrestrial form extend into the beige space, while those that remain aquatic are in the blue-grey space.

Is temnospondyl ornamentation diagnostic?
Yes and no. Some temnospondyls have pretty weird ornamentation. For example, plagiosaurids (e.g., Plagiosuchus pustuliferus, see higher up the slideshow on temno ornamentation) have a pretty recognizable pustulated texture on their elements that is formed by densely packed tubercles (pustules are supposed to have pus in them), in contrast to the more typical pitting and grooving of other temnospondyls. Isolated, ornamented temno chunks can still be diagnostic or at least informative as well, either for guessing at what genus or species the fragment belongs to or what element(s) it comprises. For example, metoposaurid ornamentation is mostly honeycomb patterning made of semi-circular pits, but elongate grooves are found on the parietals. In general though, it can take a lot of observations and practice in the field to be able to identify fragments on the fly, and good luck if you get a random frag with just a few circular pits on it.

Is temnospondyl ornamentation difficult to prepare?
Sometimes accretion of hard minerals to ornamented pieces makes it hard to prepare, especially with ridges and tubercles (3D projections). This is why a lot of the specimens collected in the 19th and early 20th centuries don't have well-preserved ornamentation (it can also be weathered to be flatter when exposed). Pitting (3D depression) is usually a little easier to prepare because sometimes the infilling just pops out. I've actually exposed entire skulls in which the impression was preserved as a single piece on the rock that was lying on top of it. Conversely, sometimes you spend weeks just scraping the pits and grooves to get out residual pieces of matrix from when you put too much glue on the specimen...

This block was yanked (yes, literally) off of the skull seen in the photo on the right. If you play with your screen settings enough, you'll see the faint outlines of the ornamentation in the grey area.

Skull of a small metoposaurid I found while working with the UW Madison Paleo crew in the Popo Agie this past summer. Hopefully you can see the ornamentation...

Closing thoughts
Like most things in paleontology, it isn't easy to conclusively say what led to the evolution of ornamentation in early tetrapods, and there are probably a multiplicity of environmental and ecological factors at play in addition to phylogenetic constraints that produce the diverse array of ornamentation that we observe in the fossil record.

Up next week: TBD, some kind of profile on a particular temno group

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Edit (1/22): minor corrections based on comments by D. Marjanović.