Tuatara

While there is currently considered to be only one living species of tuatara, two species were previously identified: Sphenodon punctatus, or northern tuatara, and the much rarer Sphenodon guntheri, or Brothers Island tuatara, which is confined to North Brother Island in Cook Strait.[44] The specific name punctatus is Latin for "spotted",[45] and guntheri refers to German-born British herpetologist Albert Günther.[46] A 2009 paper re-examined the genetic bases used to distinguish the two supposed species of tuatara, and concluded they only represent geographic variants, and only one species should be recognized.[22] Consequently, the northern tuatara was re-classified as Sphenodon punctatus punctatus and the Brothers Island tuatara as Sphenodon punctatus guntheri. Individuals from Brothers Island could also not be distinguished from other modern and fossil samples based on jaw morphology.[33]

The Brothers Island tuatara has olive brown skin with yellowish patches, while the colour of the northern tuatara ranges from olive green through grey to dark pink or brick red, often mottled, and always with white spots.[23][27][47] In addition, the Brothers Island tuatara is considerably smaller.[48] An extinct species of Sphenodon was identified in November 1885 by William Colenso, who was sent an incomplete subfossil specimen from a local coal mine. Colenso named the new species S. diversum.[49] Fawcett and Smith (1970) consider it a synonymous to the subspecies level based on a lack of distinction.[50]

The most abundant LINE element in the tuatara is L2 (10%). Most of them are interspersed and can remain active. The longest L2 element found is 4 kb long and 83% of the sequences had ORF2p completely intact. The CR1 element is the second most repeated (4%). Phylogenetic analysis shows that these sequences are very different from those found in other nearby species such as lizards. Finally, less than 1% are elements belonging to L1, a low percentage since these elements tend to predominate in placental mammals.[12]

Usually, the predominant LINE elements are the CR1, contrary to what has been seen in the tuatara. This suggests that perhaps the genome repeats of sauropsids were very different compared to mammals, birds and lizards.[12]

The genes of the major histocompatibility complex (MHC) are known to play roles in disease resistance, mate choice, and kin recognition in various vertebrate species. Among known vertebrate genomes, MHCs are considered one of the most polymorphic.[51][52] In the tuatara, 56 MHC genes have been identified; some of which are similar to MHCs of amphibians and mammals. Most MHCs that were annotated in the tuatara genome are highly conserved, however there is large genomic rearrangement observed in distant lepidosauria lineages.[12]

Many of the elements that have been analyzed are present in all amniotes, most are mammalian interspersed repeats or MIR, specifically the diversity of MIR subfamilies is the highest that has been studied so far in an amniote. 16 families of SINEs that were recently active have also been identified.[12]

The tuatara has 24 unique families of DNA transposons, and at least 30 subfamilies were recently active. This diversity is greater than what has been found in other amniotes and in addition, thousands of identical copies of these transposons have been analyzed, suggesting to researchers that there is recent activity.[12]

Around 7,500 LTRs have been identified, including 450 endogenous retroviruses (ERVs). Studies in other Sauropsida have recognized a similar number but nevertheless, in the genome of the tuatara it has been found a very old clade of retrovirus known as Spumavirus.[12]

More than 8,000 non-coding RNA-related elements have been identified in the tuatara genome, of which the vast majority, about 6,900, are derived from recently active transposable elements. The rest are related to ribosomal, spliceosomal and signal recognition particle RNA.[12]

The mitochondrial genome of the genus Sphenodon is approximately 18,000 bp in size and consists of 13 protein-coding genes, 2 ribosomal RNA and 22 transfer RNA genes.[12]

DNA methylation is a very common modification in animals and the distribution of CpG sites within genomes affects this methylation. Specifically, 81% of these CpG sites have been found to be methylated in the tuatara genome. Recent publications propose that this high level of methylation may be due to the amount of repeating elements that exist in the genome of this animal. This pattern is closer to what occurs in organisms such as zebrafish, about 78%, while in humans it is only 70%.[12]

Skull of a tuatara, showing the complete temporal arches, and individual bones:

1. premaxilla
2. nasal
3. prefrontal
4. frontal
5. maxilla
6. postfrontal
7. dentary
8. postorbital
9. jugal
10. parietal
11. squamosal
12. quadrate

The ancestor of diapsids had a skull with two openings in the temporal region – upper and lower temporal fenestra on each side of the skull bounded by complete arches. The upper jaw is firmly attached to the posterior of skull.[27] This makes for a very rigid, inflexible construction. The skull of the tuatara has a similar structure, with both upper and lower temporal openings.[10][57]^: 113 However, the lower temporal bar (sometimes called the cheek bone) is incomplete in some fossil Rhynchocephalia, suggesting its presence in the tuatara is a distinctive (autapomorphic) feature rather than one inherited from a common ancestor.[58]

The tip of the upper jaw is beak-like and separated from the remainder of the jaw by a notch.[10] There is a single row of teeth in the lower jaw and a double row in the upper, with the bottom row fitting perfectly between the two upper rows when the mouth is closed.[10] This specific tooth arrangement is not seen in any other reptile;[10] although most snakes have a double row of teeth in their upper jaws, their arrangement and function is different from the tuatara's.

The structure of the jaw joint allows the lower jaw to slide forwards after it has closed between the two upper rows of teeth.[59] This mechanism allows the jaws to shear through chitin and bone. [27] Fossils indicate that the jaw mechanism began evolving at least 200 million years ago.[60] The teeth are not replaced. As their teeth wear down, older tuatara have to switch to softer prey such as earthworms, larvae, and slugs, and eventually have to chew their food between smooth jaw bones.[61] It is a common misconception that tuatara lack teeth and instead have sharp projections on the jaw bone,[62] though histology shows that they have enamel and dentine with pulp cavities.[63]

The brain of Sphenodon fills only half of the volume of its endocranium.[64] This proportion has actually been used by paleontologists trying to estimate the volume of dinosaur brains based on fossils.[64] However, the proportion of the tuatara endocranium occupied by its brain may not be a very good guide to the same proportion in Mesozoic dinosaurs since modern birds are surviving dinosaurs but have brains which occupy a much greater relative volume in the endocranium.[64]

The eyes can focus independently, and are specialised with three types of photoreceptive cells, all with fine structural characteristics of retinal cone cells[65] used for both day and night vision, and a tapetum lucidum which reflects onto the retina to enhance vision in the dark. There is also a third eyelid on each eye, the nictitating membrane. Five visual opsin genes are present, suggesting good colour vision, possibly even at low light levels.[12]

The tuatara has a third eye on the top of its head called the parietal eye. It has its own lens, a parietal plug which resembles a cornea,[66] retina with rod-like structures, and degenerated nerve connection to the brain. The parietal eye is visible only in hatchlings, which have a translucent patch at the top centre of the skull. After four to six months, it becomes covered with opaque scales and pigment.[27] Its use is unknown, but it may be useful in absorbing ultraviolet rays to produce vitamin D,[9] as well as to determine light/dark cycles, and help with thermoregulation.[27]

Of all extant tetrapods, the parietal eye is most pronounced in the tuatara. It is part of the pineal complex, another part of which is the pineal gland, which in tuatara secretes melatonin at night.[27] Some salamanders have been shown to use their pineal bodies to perceive polarised light, and thus determine the position of the sun, even under cloud cover, aiding navigation.[67]

Together with turtles, the tuatara has the most primitive hearing organs among the amniotes. There is no eardrum and no earhole,[62] they lack a tympanum, and the middle ear cavity is filled with loose tissue, mostly adipose (fatty) tissue. The stapes comes into contact with the quadrate (which is immovable), as well as the hyoid and squamosal. The hair cells are unspecialised, innervated by both afferent and efferent nerve fibres, and respond only to low frequencies. Though the hearing organs are poorly developed and primitive with no visible external ears, they can still show a frequency response from 100 to 800 Hz, with peak sensitivity of 40 dB at 200 Hz.[68]

Animals that depend on the sense of smell to capture prey, escape from predators or simply interact with the environment they inhabit, usually have many odorant receptors. These receptors are expressed in the dendritic membranes of the neurons for the detection of odours. The tuatara has several hundred receptors, around 472, a number more similar to what birds have than to the large number of receptors that turtles and crocodiles may have.[12]

The tuatara spine is made up of hourglass-shaped amphicoelous vertebrae, concave both before and behind.[62] This is the usual condition of fish vertebrae and some amphibians, but is unique to tuatara within the amniotes. The vertebral bodies have a tiny hole through which a constricted remnant of the notochord passes; this was typical in early fossil reptiles, but lost in most other amniotes.[69]

The tuatara has gastralia, rib-like bones also called gastric or abdominal ribs,[70] the presumed ancestral trait of diapsids. They are found in some lizards, where they are mostly made of cartilage, as well as crocodiles and the tuatara, and are not attached to the spine or thoracic ribs. The true ribs are small projections, with small, hooked bones, called uncinate processes, found on the rear of each rib.[62] This feature is also present in birds. The tuatara is the only living tetrapod with well-developed gastralia and uncinate processes.

In the early tetrapods, the gastralia and ribs with uncinate processes, together with bony elements such as bony plates in the skin (osteoderms) and clavicles (collar bone), would have formed a sort of exoskeleton around the body, protecting the belly and helping to hold in the guts and inner organs. These anatomical details most likely evolved from structures involved in locomotion even before the vertebrates ventured onto land. The gastralia may have been involved in the breathing process in early amphibians and reptiles. The pelvis and shoulder girdles are arranged differently from those of lizards, as is the case with other parts of the internal anatomy and its scales.[71]

The spiny plates on the back and tail of the tuatara resemble those of a crocodile more than a lizard, but the tuatara shares with lizards the ability to break off its tail when caught by a predator, and then regenerate it. The regrowth takes a long time and differs from that of lizards. Well illustrated reports on tail regeneration in tuatara have been published by Alibardi and Meyer-Rochow.[72][73] The cloacal glands of tuatara have a unique organic compound named tuataric acid.

Currently, there are two means of determining the age of tuatara. Using microscopic inspection, hematoxylinophilic rings can be identified and counted in both the phalanges and the femur. Phalangeal hematoxylinophilic rings can be used for tuatara up to ages 12–14 years, as they cease to form around this age. Femoral rings follow a similar trend, however they are useful for tuatara up to ages 25–35 years. Around that age, femoral rings cease to form.[74] Further research on age determination methods for tuatara is required, as tuatara have lifespans much longer than 35 years (ages up to 60[9] are common, and captive tuatara have lived to over 100 years).[75][76][77] One possibility could be via examination of tooth wear, as tuatara have fused sets of teeth.

A tuatara basking at the West Coast Wildlife Centre, at Franz Josef on the West Coast

Adult tuatara are terrestrial and nocturnal reptiles, though they will often bask in the sun to warm their bodies. Hatchlings hide under logs and stones, and are diurnal, likely because adults are cannibalistic. Juveniles are typically active at night, but can be found active during the day. The juveniles' movement pattern is attributed to genetic hardwire of conspecifics for predator avoidance and thermal restrictions.[78] Tuatara thrive in temperatures much lower than those tolerated by most reptiles, and hibernate during winter.[79] They remain active at temperatures as low as 5 °C (41 °F),[80] while temperatures over 28 °C (82 °F) are generally fatal. The optimal body temperature for the tuatara is from 16 to 21 °C (61 to 70 °F), the lowest of any reptile.[81] The body temperature of tuatara is lower than that of other reptiles, ranging from 5.2–11.2 °C (41.4–52.2 °F) over a day, whereas most reptiles have body temperatures around 20 °C (68 °F).[82] The low body temperature results in a slower metabolism.

Tuatara were once widespread on New Zealand's main North and South Islands, where subfossil remains have been found in sand dunes, caves, and Māori middens.[102] Wiped out from the main islands before European settlement, they were long confined to 32 offshore islands free of mammals.[13] The islands are difficult to get to,[103] and are colonised by few animal species, indicating that some animals absent from these islands may have caused tuatara to disappear from the mainland. However, kiore (Polynesian rats) had recently become established on several of the islands, and tuatara were persisting, but not breeding, on these islands.[104][105] Additionally, tuatara were much rarer on the rat-inhabited islands.[105] Prior to conservation work, 25% of the distinct tuatara populations had become extinct in the past century.[5]

The recent discovery of a tuatara hatchling on the mainland indicates that attempts to re-establish a breeding population on the New Zealand mainland have had some success.[106] The total population of tuatara is estimated to be between 60,000[27] and 100,000.[107]

Tuatara have temperature-dependent sex determination meaning that the temperature of the egg determines the sex of the animal. For tuatara, lower egg incubation temperatures lead to females while higher temperatures lead to males. Since global temperatures are increasing faster than ever, researchers are worried that climate change is skewing the male to female ratio of tuatara and that in a few decades tuatara offspring populations will be all male.[108]

Tuatara were removed from Stanley, Red Mercury and Cuvier Islands in 1990 and 1991, and maintained in captivity to allow Polynesian rats to be eradicated on those islands. All three populations bred in captivity, and after successful eradication of the rats, all individuals, including the new juveniles, were returned to their islands of origin. In the 1991–92 season, Little Barrier Island was found to hold only eight tuatara, which were taken into in situ captivity, where females produced 42 eggs, which were incubated at Victoria University. The resulting offspring were subsequently held in an enclosure on the island, then released into the wild in 2006 after rats were eradicated there.[109]

In the Hen and Chicken Islands, Polynesian rats were eradicated on Whatupuke in 1993, Lady Alice Island in 1994, and Coppermine Island in 1997. Following this program, juveniles have once again been seen on the latter three islands. In contrast, rats persist on Hen Island of the same group, and no juvenile tuatara have been seen there as of 2001. In the Alderman Islands, Middle Chain Island holds no tuatara, but it is considered possible for rats to swim between Middle Chain and other islands that do hold tuatara, and the rats were eradicated in 1992 to prevent this.[6] Another rodent eradication was carried out on the Rangitoto Islands east of D'Urville Island, to prepare for the release of 432 Cook Strait tuatara juveniles in 2004, which were being raised at Victoria University as of 2001.[6]

Sphenodon punctatus guntheri is present naturally on one small island with a population of approximately 400. In 1995, 50 juvenile and 18 adult Brothers Island tuatara were moved to Titi Island in Cook Strait, and their establishment monitored. Two years later, more than half of the animals had been seen again and of those all but one had gained weight. In 1998, 34 juveniles from captive breeding and 20 wild-caught adults were similarly transferred to Matiu/Somes Island, a more publicly accessible location in Wellington Harbour. The captive juveniles were from induced layings from wild females.[6]

In late October 2007, 50 tuatara collected as eggs from North Brother Island and hatched at Victoria University were being released onto Long Island in the outer Marlborough Sounds. The animals had been cared for at Wellington Zoo for the previous five years and had been kept in secret in a specially built enclosure at the zoo, off display.[110]

There is another out of country population of Brothers Island tuatara that was given to the San Diego Zoological Society and is housed off-display at the San Diego Zoo facility in Balboa.[111] No successful reproductive efforts have been reported yet.

S. punctatus punctatus naturally occurs on 29 islands, and its population is estimated to be over 60,000 individuals.[27] In 1996, 32 adult northern tuatara were moved from Moutoki Island to Moutohora. The carrying capacity of Moutohora is estimated at 8,500 individuals, and the island could allow public viewing of wild tuatara.[6] In 2003, 60 northern tuatara were introduced to Tiritiri Matangi Island from Middle Island in the Mercury group. They are occasionally seen sunbathing by visitors to the island.[112][113]

Tuatara at the Karori Sanctuary are given coloured markings on the head for identification.

A mainland release of S.p. punctatus occurred in 2005 in the heavily fenced and monitored Karori Sanctuary.[23] The second mainland release took place in October 2007, when a further 130 were transferred from Stephens Island to the Karori Sanctuary.[114] In early 2009, the first recorded wild-born offspring were observed.[115]

The first successful breeding of tuatara in captivity is believed to have achieved by Sir Algernon Thomas at either his University offices or residence in Symonds Street in the late 1880s or his new home, Trewithiel, in Mount Eden in the early 1890s.

Several tuatara breeding programmes are active in New Zealand. Southland Museum and Art Gallery in Invercargill was the first institution to have a tuatara breeding programme; starting in 1986 they bred S. punctatus and have focused on S. guntheri more recently.[116]

Hamilton Zoo, Auckland Zoo and Wellington Zoo also breed tuatara for release into the wild. At Auckland Zoo in the 1990s it was discovered that tuatara have temperature-dependent sex determination. The Victoria University of Wellington maintains a research programme into the captive breeding of tuatara, and the Pukaha / Mount Bruce National Wildlife Centre keeps a pair and a juvenile.

The WildNZ Trust has a tuatara breeding enclosure at Ruawai. One notable captive breeding success story took place in January 2009, when all 11 eggs belonging to 110 year-old tuatara Henry and 80 year-old tuatara Mildred hatched. This story is especially remarkable as Henry required surgery to remove a cancerous tumour in order to successfully breed.[99]

In January 2016, Chester Zoo, England, announced that they succeeded in breeding the tuatara in captivity for the first time outside its homeland.[117]