Figure 1. I took this photo of a tuatara at Zealandia in Wellington, NZ. According to the nature guide at the park, this is an adult male tuatara who came out to sunbathe. Despite a very active tuatara population in the ecosanctuary, it is rare to see one during the day.

A Tuatara's Story

I’m Not a Lizard! But I am a Lepidosaur

Disclaimer - A complete understanding of ecotourism as a conservation strategy necessitates an understanding of ecology and the environment. Much of the information included here assumes, at minimum, some background in biology. For a more succinct summary of the salient points and an overview of why protecting and researching tuatara is important, scroll down to the Conclusions section. Ecotourism can be used to protect vulnerable species and enable invaluable research to continue. Revenue from ecotourism can help support zoos, wildlife preserves, and breeding programs that in turn contribute to research projects like the ones described below.

Introduction

While traveling through New Zealand last summer, I frequently heard tour guides and locals boast of the Kiwi “living dinosaur” or “living fossil.” As one of the most unique examples of New Zealand’s numerous endemic species, the tuatara has achieved a pseudo-cult following. It is even the namesake of one of New Zealand’s largest craft brewing companies, Tuatara Breweries. I was incredibly lucky to see wild tuatara at the Zealandia Ecosanctuary in Wellington, NZ (Fig. 1) which is currently home to New Zealand’s only mainland colony of tuatara in over 200 years (Victoria University 2015).

But besides its rarity, what is the big deal about this little lizard?  While the tuatara is not the oldest living species of vertebrate (that distinction belongs to the coelacanth), it is one of the oldest living species of tetrapods and is the only extant member of the order Rhynchocephalia (Daugherty and Cree 1990). Despite its outward appearance, the tuatara is not a lizard.

The journey of correctly identifying this mysterious little fellow began in the mid-19th century with a series of mistaken identities (Kuschel 1975, 331). Before modern genetics, comparative anatomy of the tuatara relative to lizards, crocodiles, and turtles helped place the tuatara within its own order of ancient reptiles (Kuschel 1975, 331). In particular, the unique structure and low kinesis of the tuatara’s skull separated it from the outwardly similar lizard family (Kuschel 1975, 331). The tuatara has been used to extrapolate feeding mechanism and cranial kinesis of primitive extinct reptiles (Daugherty and Cree 1990). Though recent studies into tuatara DNA suggest that these “fossils” may be evolving at an alarming rate, significantly problematizing prior extrapolations (Hay et al. 2008).

The majority of this article will focus upon the identifying features of the tuatara skull relative to other extant reptiles and how those features in tuatara affect bite function and force.   

History

The modern history of the tuatara all began with unusual skull morphology and a case of mistaken identity. In 1831, John Gray, a scientist at the British Museum, was sent a tuatara skull from New Zealand to identify and classify (Kuschel 1975, 331).  Having never seen a similar specimen, he dubbed the new species Sphenodon from the Latin for “wedge tooth” (Kuschel 1975, 331). Gray noted that the upper jaw of the tuatara looked uniquely beak-like (Kuschel 1975, 331).

Figure 2. This is a photo of a fossilized Homeosaurus pulchellus from the University of Maryland Department of Geology archive. The specimen was found in Germany and is currently in the American Museum of Natural History in New York City.

In 1840, Gray was sent a whole tuatara specimen (Kuschel 1975, 331). Failing to connect the specimen to the skull already in his possession, Gray declared this specimen part of a new species called Hatteria punctata (Kuschel 1975, 331). He determined the specimen belonged to the Agamid lizard family (Kuschel 1975, 331).

In 1845, Sir Richard Owen separately identified the tuatara relative to fossil archives and assigned it the species name Rhynchocephalus from the Latin for “snout head” (Kuschel 1975, 331). Despite Gray and Owen both noting the unusual structure of the skull and jaw, the two scientists failed to associate the three tuatara specimens (Kuschel 1975, 331).

Twenty-two years later, their error was finally corrected (Kuschel 1975, 331). In 1867, Dr. Albert Günther, John Gray’s successor at the British Museum, recognized the confusion and determined the tuatara was not a lizard (Kuschel 1975, 331).  Inspired by Sir Richard Owen’s classification, Günther placed the tuatara in a new order called Rhynchocephalia (Kuschel 1975, 331). He separated the tuatara from the lizard family (order Squamata) primarily due to three reasons: (1) the division of temporal fossae into two parts separated by a ridged bony arch (Fig. 6), (2) the presence of uncinate on the ribs similar to birds and crocodiles but not lizards (Fig. 3), and (3) the similarity with the upper Jurassic fossil of Homoeosaurus (Fig 2.)(Kuschel 1975, 334).

Figure 3. This figure was taken from the 2008 Codd et al. paper. It shows the muscle connections to the uncinate process that Günther used to help separate the tuatara from lizards. This muscle formation is often associated with avian breathing mechanics (Codd et al. 2008).

Günther’s discovery is even more remarkable when one considers that Charles Darwin’s On the Origin of Species was published only seven years prior in 1859.

Since its recognition as a distinct branch of evolutionary history in 1867, the tuatara has been the subject of over 1500 scientific papers (Daugherty and Cree 1990).

Species Background

The ancestors of the tuatara likely separated from other reptiles over 220 million years ago in the Upper Triassic (Hay et al. 2008). Based on the fossil record, the Rhynchocephalia order (Fig. 4), including ancient tuatara, seemed to have been most common around the late Triassic and Jurassic and in South America and Africa (Kuschel 1975, 331). Most of the Rhynchocephalia order became extinct over 60 million years ago, around the fall of the dinosaurs, except for the tuatara (Kuschel 1975, 331)!

Figure 4. This is a table I made showing the classification of the tuatara within the tree of life. There is currently some debate on the number of extant tuatara species and whether or not the different types should distinct species or grouped into one main species with subspecies.

 The tuatara is part of the Lepidosaur superorder, the largest group of non-avian reptiles, and is a sister group to Squamata, which includes lizards and snakes (Fig. 5, Kuschel 1975, 331). The tuatara order is normally referred to as Rhynchocephalia, though it will also sometimes be called Sphenodontidia because the sphenodons (tuatara) are the only extant members. In 2009, research into the DNA of different tuatara island populations implied that the New Zealand tuataras likely all belong to one species (S. punctatus) with distinct geographic variants (NZ Department of Conservation [DOC]). In the next section (Skull Morphology), I will explain how the skull of the tuatara, in particular, was used in the 1800s to separate the tuatara from Squamata and extant lizard species.

The tuatara has uniquely adapted to life in New Zealand. Unlike other land masses, prehistoric New Zealand was void of terrestrial mammals which enabled the tuatara to thrive in the absence of predators (Daugherty and Cree 1990). Tuatara primarily eat earthworms, beetles, lizards, frogs, weta, injured or juvenile prions, and young tuatara (Daugherty and Cree 1990). The cold New Zealand climate poses challenges for most cold-blooded reptiles, but not for the tuatara. In the winter, the tuatara can survive for 6 months without feeding and at 9 °C, the tuatara can survive for over an hour without breathing (Daugherty and Cree 1990). Even at ideal temperatures (15-20 °C), the tuatara’s heart beats at a slow 9-10 beats per minute (Daugherty and Cree 1990).

Figure 5. Phylogeny of vertebrate evolution from the University College London. This image shows the relationship between tuatara and lizards and snakes. Tuatara may be more closely related to crocodiles and birds than this picture shows and turtles are likely in the wrong location.

The tuatara has also adapted its reproductive cycle to the cold climate. Tuatara eggs can incubate for up to 14 months (longer than any other reptile) and completely halt development during cold winter months (Kuschel 1975, 335).

Some researchers argue that the tuatara’s survival is intimately linked to New Zealand burrowing seabird populations, particularly petrels and prions (Kuschel 1975, 347). These seabirds contribute to soil fertility which increases access to the invertebrate and lizard fauna in tuatara’s diet (NZ DOC). The tuatara often share burrows with the seabirds and have been known to prey on sick or injured birds when other food is scarce (NZ DOC).

Sub-fossils show that tuatara were once found on both main islands of New Zealand (Kuschel 1975, 338). When the Maori people came from Polynesia, they unfortunately brought with them the Polynesian rat, which eats tuatara eggs and young (Kuschel 1975, 341). By the time of European settlement in New Zealand, the rats had destroyed all mainland tuatara populations (Kuschel 1975, 341). Luckily, the tuatara was able to survive on a few off-shore islands that stayed mammal-free (Kuschel 1975, 341). Now, the tuatara is a heavily protected species with captive breeding programs around the world. The breeding program at the Zealandia Ecosanctuary in Wellington (where I visited) is perhaps the most successful because the tuataras are breeding in the wild, without human intervention, and they are the first mainland population of tuatara in over 200 years (Victoria University 2015).

The biggest concern for the future of the tuatara in New Zealand is preserving at least one successful breeding population. Captive tuataras unfortunately have low genetic diversity which may lead to difficulties coping with climate change, susceptibility to new pathogens, and a potential for low reproductive success (NZ DOC). However, as I will discuss later, a closer look into the DNA of the tuatara may reveal some hope for the future viability of the species.

Skull Morphology

Figure 6. This image shows different reptilian skull morphologies. The tuatara is represented by the diapsid while the lizard is represented by the lizard and the synapsid. This photo is from the Encyclopedia Britannica 2008.

The tuatara is most readily distinguished from lizards by the number and size of temporal fenestra (the holes in the side of the skull).  Tuatara are characterized by the diapsid condition with two large temporal fenestrae on the dorsal and lateral posterior of the skull separated by a ridged bony arch (Fig. 6-7, Kuschel 1975, 334). The quadrate bone forms a solid union with the rest of the skull and the entire structure is strong and rigid (Fig. 7, Kuschel 1975, 336). Although tuatara and lizards are both considered diapsids, in the case of lizards, this is only a reference to their lineage and is not indicative of the actual number of temporal fenestra (Fig. 6, Kuschel 1975, 336). As shown in Fig. 6, diapsids (like the tuatara) have two fully enclosed fenestrae while lizards demonstrate the synapsid condition and only have one fully enclosed fenestra. The structure of the lizard skull allows for increased cranial kinesis relative to the tuatara (Kuschel 1975, 337). Embryos of tuatara may have some cranial kinesis but lose this ability during development (Kuschel 1975, 337)

The tuatara can also be distinguished from lizards based on its “teeth.” The tuatara does not have teeth in the technical sense, but instead has bony protuberances from mandible and palate that act as teeth (Kuschel 1975, 334). The tuatara has a single row of teeth on lower jaw and two rows on the upper (one on the mandible and one on the palate) (Fig. 8, Daugherty and Cree 1990). The bottom row fits between the top rows and when mouth closes on prey, the lower jaw moves forward in a sheering motion (Fig. 11, Daugherty and Cree 1990). This bite structure is unlike any other known living reptile (Daugherty and Cree 1990). Despite numerous differences, tuatara and lizards both have quadrate-articular jaw joints (Curtis et al. 2011, 2)

Another unique feature of the tuatara skull is the parietal foramen and the pineal eye. Unlike most lizards, tuatara has a parietal foramen on the midline of the skull at the junction of the frontal and parietal bones (Fig. 7, Kuschel 1975, 334). The pineal eye is composed of a retina, lens, and plug of translucent tissue over surface in parietal foramen which may act like a rudimentary cornea (Kuschel 1975, 337). Though it is eventually covered with opaque skin and scales in adults, the pineal eye is clearly visible in juvenile tuatara (Kuschel 1975, 337). There are some signs of degeneration of the pineal eye structures in adults, but many scientists speculate it retains the ability control autonomic functions relative to changes in solar radiation (Kuschel 1975, 337).

Unlike mammals, the skull of tuatara does not have a large vaulted braincase (Curtis et al. 2011, 1). Instead, the small brain leaves extra space for the jaw musculature and aforementioned fenestrae (Curtis et al. 2011, 1). As I will discuss in the next section, the structure of the tuatara skull is particularly suited to generate a strong sheering bite unlike any other reptile.

Figure 7-9. The three images above are all from Gorniak et al. 1982. Fig. 7 shows a lateral view of the tuatara skull. From this angle, one can clearly see the diapsid temporal fenestra and the rigid skull structure. Fig. 8 shows a ventral view of the tuatara skull. From this angle, one can clearly see the unusual double row of “teeth” on the upper jaw. Fig. 9 shows an additional lateral view of the skull with part of the jaw and temporal fenestra removed to show the interior structure of the skull.

Form and Function

The following two studies use three-dimensional computer models of the bones and muscles of the tuatara’s head and neck to estimate bite motion and force (Fig. 10). Due to the conservation status of tuatara, the experimenters cannot use live specimens (Jones et al. 2012, 1077).

Figure 10. This image shows the type of computer model used to model the tuatara skull in the Jones and Curtis et al. papers.

As previously mentioned, the tuatara has a highly specialized feeding action whereby the lower jaw closes between two upper rows of teeth (Jones et al. 2012, 1076). Once the prey is trapped, the lower jaw slides between the two components of the upper jaw to produce a shearing motion similar to a saw (Jones et al. 2012, 1076). Despite their relatively low cranial kinesis compared to other lepidosaurs, this shearing motion requires specialize skull mobility unique to the tuatara among extant reptiles (Fig. 13, Jones et al. 2012, 1076).

Tuatara feeding has five main steps (Jones et al. 2012, 1076). The first step is acquisition, or prey capture, during time which the tuatara either uses its sticky tongue to catch prey or its jaws to clamp down on large prey (Jones et al. 2012, 1076). The second step is immobilization (Jones et al. 2012, 1076). At this point the tuatara traps the prey by using a three-point bending bite (two restraining points come from upper “teeth” and the bending point comes from the pressure of the lower jaw) (Jones et al. 2012, 1076). The third step in tuatara feeding is processing (Jones et al. 2012, 1076). This step is the main focus of the Jones et al. 2008 paper. During processing, the sawing motion of the jaw occurs (Jones et al. 2012, 1076). The fourth and fifth steps are transport and swallowing which involve maneuvering the food so it can enter the stomach (Jones et al. 2012, 1076).

Figure 11. This image from Jones et al. (2012) shows the basic motion of the tuatara skull during the different steps of shearing. 

Tuatara processing occurs via and anteriorly directed proal jaw movement (Fig. 11, Jones et al. 2012, 1076). During shearing, the pterygoideus muscle contracts to pull lower jaw forward 2-3 mm and the lower jaw slides between the two upper tracts (Jones et al. 2012, 1076, 1085). Surprisingly, the computer model demonstrated that flexibility at the mandibular symphysis (Fig. 12) (the cartilaginous joint joining the two halves of the lower jaw) is necessary to replicate the jaw movements observed in the living animal (Fig. 13, Jones et al. 2012, 1082).

The necessity of a mobile symphysis joint is revolutionary to tuatara skull morphology. Not only does this demonstrate previously unknown mobility in the tuatara skull, but it also describes a method of feeding and symphysis movement previously unseen in reptiles (Jones et al. 2012, 1082). Jones and colleagues (2012) hypothesize that tuataras evolved this mechanism in order to expand their food options in times of scarcity (Jones et al. 2012, 1086). For example, tuatara have been known to sheer off the heads of seabirds when other food supplies are limited (Jones et al. 2012, 1086). This highly specialized feeding mechanism may also help explain why the tuatara kept its diapsid skull structure (Jones et al. 2012, 1087). There is a preliminary theory that the lower temporal bar functions to provide structure support to the shearing mechanism (Jones et al. 2012, 1087-88).

Jones and colleagues (2012) believe one can use this data to draw conclusions about the feeding mechanism of other Rhynchocephalia (Jones et al. 2012, 1088). Additionally, a prior study from Curtis and colleagues (2011) provides some support to the conclusions made in the Jones et al. study (2012).

Figure 12. This image from the Jones et al. 2012 paper shows the mobile symphysis (cartilaginous joint) between the two halves of lower jaw below the notch. This joint moves during shearing.

Curtis and colleagues (2011) attempted to test the relationship between tuatara skull structure and feeding forces (i.e. biting, chewing, sheering, etc.). Using the same computer models as the Jones et al. study, they found that the tuatara’s skull is likely optimized to compensate for maximum physiological forces while minimizing volume, weight, and energy for maintenance (Curtis et al. 2011, 1).

At the most posterior bite position, the tuatara’s bite force is 80% greater than at the most anterior position (Curtis et al. 2011, 2). The maximum observed joint force was 540 N and the maximum bite force was 216 N (Curtis et al. 2011, 3). This bite force is four times higher than the maximum force required to bite through any of the tuatara’s primary food sources (Curtis et al. 2011, 5).

Figure 13. This image from the Jones et al. 2012 paper summarizes the movement of the different parts of the jaw during sheering. It is particularly important to note panels E, I, and M which show the bending motion of the symphysis.

As shown in Fig. 14, the compressive and tensile forces are balanced throughout the skull during biting (Curtis et al. 2011, 4). This pattern implies that there is a relationship between structure and function that works to evenly redistribute forces so as to avoid overwhelming any single bone (Curtis et al. 2011, 4).

Figure 14. This image taken from the Curtis et al. 2011 paper shows the even distribution of compression and tension forces throughout the skull. This implies a direct correlation between structure and physiological forces.

In accordance with the findings from the previously mentioned study, the lower temporal bar, is under compressive strain during all bite types (Curtis et al. 2011, 7).  This is consistent with the Jones et al. theory that the tuatara kept the diapsid skull structure because the lower temporal bar was necessary for jaw mechanism.

Aside: DNA Analysis

As “living dinosaurs,” tuatara are often studied as models of ancient reptiles. Many of the papers cited above include theories about how one can apply observations of the tuatara to basal reptile species. Additionally, as described in the “Species Background” section of the paper, tuatara have very slow metabolisms and development which is often correlated with low rates of phenotypic and molecular evolution (Hay et el. 2008, 106). If the rates of evolution are in fact low, then the tuatara would be a good “fossil” model organism.

Figure 15. This image from the Hay et al. 2008 paper shows the tuatara rate of evolution relative to other vertebrate species.

However, recent research into the DNA of tuatara challenges this assumption (Hay et al. 2008). Hay and colleagues used living tuatara DNA and nucleotides of sub-fossil bones to measure the rates of molecular evolution in hypervariable regions (HVRs) (Hay et el. 2008, 106). In contrast to the hypothesized rates of evolution, the analysis of ancient and modern tuatara shows that the tuatara has the highest rate of molecular evolution of any recorded vertebrate (Hay et el. 2008, 106). The tuatara’s mitochondrial HVRs evolve at a rate of 1.56 substitutions per base per million years (Hay et el. 2008, 107).

This is the first study to directly estimate the rate of evolution in a “living fossil” and also the first attempt to quantify the rate of molecular evolutionary changes in the tuatara (Hay et el. 2008, 108).

Conclusions

The classification of the tuatara in the 1800s depended heavily upon skull morphology relative to extant and extinct reptiles. Now, over 150 years later, the mechanisms and structures of the tuatara skull continue to baffle and amaze scientists. Computer modeling has allowed for great advances in modeling the tuatara’s unique jaw structure.

However, studying the tuatara in a laboratory setting will always have inherent weaknesses. For example, as noted in the Jones et al. (2012) and Curtis et al. (2011) studies, they were unable to use live tuatara specimens due to the conservation status of these rare “fossils.” Even if a scientist has access to a tuatara, their growth rate and habits make them difficult to study and work with. From a reproducibility stand point, these factors make tuatara a poor model organism for scientific research.

Additionally, Curtis and colleagues (2011) acknowledge that their computer modelling approach is limited (Curtis et al. 2011, 7). For example, during their test on the correlation between structure and function in bite mechanics, they were unable to model the parietal foramen and membrane (Curtis et al. 2011, 7). There is a developing theory that these structures participate in dissipating force, but this cannot be tested using current models (Curtis et al. 2011, 7).

Using a tuatara as a model for basal reptiles may be also problematic due to the tuatara’s abnormally fast rate of molecular evolution, though it is still unclear if or how these molecular changes correlate with phenotype.

In general, more research needs to be done on the tuatara and new research techniques need to be developed to study the species without harming the population. Regardless of whether or not the tuatara is evolving slightly or is easy to use in experiments, the tuatara is undeniably an important and unique piece of the phylogenetic tree and deserves to be thoroughly understood.

Resources

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