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Tuatara are rare, medium-sized reptiles, weighing up to 1,300 grams,
that live on cool, windswept islands off the New Zealand coast. They live
in burrows and are most active at night in mist or heavy rain. Their sharp,
shearing teeth are specialised for dismembering the hard, chitinous insects
and for decapitating the seabirds on which they feed. They look like lizards,
but they are not.

In 1878, A K Newman wrote that ‘the tuatara, unlike other lizards, has
no penis, therefore probably small sexual passions ..’ The first of his
errors was to assume that the tuatara (Sphenodon) was a lizard. In fact,
11 years previously, in 1867, Albert Gunther of the British Museum had announced
to a startled scientific community that tuatara were not lizards but the
sole surviving member of an ancient group of reptiles called rhynchocephalians.
Gunther observed that in several ways the anatomy of tuatara appeared intermediate
between crocodilians on the one hand and the lizards and snakes (collectively
know as squamates) on the other. He also noted (as did Newman) that tuatara
were unique among living reptiles in that males lacked an intromittent organ.

Anatomical studies in the 1980s by several British and Canadian zoologists
have substantiated Gunther’s view, although the lineage in which the tuatara
and its closest fossil relatives are placed has been renamed the Order Sphenodontida
(‘wedge-toothed’). Fossil sphenodontidans were small to medium-sized reptiles
that lived in Europe, Africa, Britain and North America between about 120
and 225 million years ago, during the reign of the dinosaurs. Nobody knows
why tuatara survived and all other sphenodontidans became extinct, but the
absence of native land mammals in New Zealand may have been important.

Because of the tuatara’s links with extinct ancient reptiles, it has
sometimes been referred to as a ‘living fossil’. But this claim has been
made on solely anatomical grounds. The question that we pose here is: should
we regard the reproductive biology of tuatara as primitive or simple compared
with that of modern lizards?

Five years ago, almost nothing was known about reproduction in tuatara.
This ignorance sprang from logistical, administrative and biological barriers.
For instance, the 30-odd islands on which tuatara are found are formidably
rugged: they are mostly uninhabited, cliff-bound, cool and windswept, and
access by boat is often impossible because of heavy seas. Even if you get
ashore safely, you may not be able to depart until weeks later. The tuatara
is also protected by New Zealand law and is listed on Appendix 1 of CITES
(Convention on International Trade in Endangered Species of Wild Fauna and
Flora). This means that to study tuatara zoologists must have the permission
of the New Zealand government. Finally, because it is nocturnal, long-lived
(60 or more years) and seemingly inactive, the tuatara has been viewed as
a frustrating and unproductive animal to study.

Since 1985, however, a tuatara research programme based at Victoria
University of Wellington, New Zealand, has overcome these difficulties and
requirements. The research programme was begun by one of us (Charles Daugherty)
and Michael Thompson (now of the University of Sydney), and was later joined
by the second of us (Alison Cree) and many others. By encouraging a number
of scientists from New Zealand and overseas to participate in the project,
we obtained the additional expertise, funding and perspective that an intensive
study must have. Furthermore, because the results of our studies were relevant
to conservation, we were granted permission to carry out our studies.

The research team focused its work on Stephens Island in Cook Strait.
The island, covering 150 hectares, has been staffed as a lighthouse station
since 1894 and has electricity, water and vacant lighthouse-keepers’ houses
for accommodation. It also possesses a helicopter pad, so access does not
depend on calm seas. Perhaps most significantly, it has the world’s largest
population of tuatara. Chris Carmichael of Central Michigan University and
others have found as many as 2,000 tuatara per hectare living in the best
habitat on Stephens Island, and Donald Newman of the New Zealand Department
of Conservation has estimated that at least 30,000 live on the island. Simply
avoiding stepping on tuatara when walking outside at night can be a problem.

The research has revealed the tuatara have superficial similarities
with, and fundamental differences from, the reproductive biology of lizards.
Take reproductive behaviour, for instance. For years it was believed that
the reproductive behaviour of tuatara would never be described because ‘tuatara
never did anything’. It is true that a tuatara caught in the beam of an
enthusiasitc biologist’s headlamp at night will usually freeze or run away.
By using a combination of sophisticated night-vision equipment and enormous
patience, however, James Gillingham of Central Michigan University and his
colleagues have discovered that the reproductive behaviour of tuatara is
neither dull nor non-existent: it involves aggressive interactions within
both sexes, as well as prolonged, ritualistic courtship that culminates
in copulation of a male with one or more females during the breeding season.

Courtship and mating takes place in late summer-autumn (January-March
on Stephens Island). During January the males establish territories, each
including the territories of several resident females. Within their territories,
males engage in a prenuptial display at night in unforested habitats (for
example, sheep pasture – an abundant man-made habitat on Stephens Island)
and also by day in remnant forest. This display involves a stiffening and
erection of the skin and spines down the neck and back, and makes the male
tuatara appear large and fierce to human eyes. Such displays are often carried
out in highly conspicuous locations such as an unvegetated tracks or on
low rocks. The combination of location and appearance suggests that visual
cues are important in the display, which presumably functions both to attract
females and to advertise the male’s presence to other males.

Territorial encounters between males occur frequently and take the form
of ‘face-off’ displays and fights. In face-off displays, the two males line
up parallel to each other about a metre apart, often with their heads facing
in opposite directions, then slowly gape open their mouths and rapidly snap
them shut. Their lungs and throat are inflated, enhancing the impression
of size. One male may eventually be chased away, or a fight may ensue. During
fights, one male locks its jaws around the head or neck of the other male,
and the two tumble and scuffle on the ground, often grunting or croaking
at the same time. Facial wounds, broken jaws and lost tails are not uncommon.

Male tuatara that are successful in attracting receptive females engage
in a stereotyped courtship dance. This stolzer Gang (‘proud walk’) involves
circling the female in a slow, intermittent, stiff-legged walk with the
head held high, crest spines fully erect and the throat skin inflated. The
male may encircle the female several times, or, if he encounters obstructions
such as tree trunks or low branches, he either climbs over or around them
or modifies his stolzer Gang into a figure-of-eight or an arc in front of
the female.

Courtship may continue for about 20 minutes and ends when the female
either disappears down a burrow (if she is unreceptive) or allows the male
to mount her. During copulation, the males lies on top of the flattened
female, using his hind legs and tail to lift her tail so that his vent can
come into contact with hers. As with birds that lack intromittent organs,
the absence of penis or hemipenes in male tuatara does not prevent successful
sperm transfer. Recent anatomical studies by Nick Arnold of the Natural
Histroy Museum in London suggest that in males the common outlet of the
reproductive tract and excretory system, the cloaca, possesses outpouchings
(possibly precursors of the hemipenes seen in lizards) that may be everted
during copulation. Cloacal distension in courting male tuatara has been
confirmed by Gillingham.

The observations made by Gillingham and his colleagues have demonstrated
that, despite the lack of an intromittent organ, the territorial and courtship
behaviour of tuatara is a rich and complex as im many lizards (including
iguanas, which are well-known for their aggressive displays). Furthermore,
with patience and the right equipment, the reproductive behaviour of male
tuatara is readily open to experimental manipulation. Using rubber models
of tuatara, some with movable (and removable) body parts and placed on motorised
trolleys, Gillingham has investigated some of the visual cues that stimulate
a watching male to exhibit either aggressive or courting behaviour. Preliminary
results suggest that, in general, a model with a high head and erect crest
stimulates the watching male to become aggressive towards the model, to
the point where it may rip the model apart. In contrast, a model with a
low, slowly nodding head triggers courtship by the watching male and even
frustrated attempts at copulation with the model.

Nesting, the other major behavioural event in the tuatara’s reproductive
cycle, is more involved and complex than in many lizards. For years, the
nesting behaviour of tuatara was almost entirely unknown, apparently because
nobody knew where tuatara dug their nests. Observations by Thompson demonstrated
that females are highly selective in their choice of nestsites on Stephens
Island. The animals nest at communal sites in spring and early summer (October-December)
and females may travel at least 200 metres to these areas. These are located
in sunny, unforested areas, especially in the sheep pasture and on the cliffs.

Once at the nesting area, nesting females engage in nest-digging, egg-laying
and nest-attendance. The entire sequence may span several weeks. Observations
by Thompson, Louis Guillette of the University of Florida and ourselves
show that many animals dig trial nests, as previously reported in the Galapagos
land iguana. A female tuatara may begin digging a nest in one site, only
to abandon it after a few nights’ digging and begin another a few metres
away. Or, instead of beginning an entirely new nest, she may complete digging
a nest that was begun but abandoned by another female. In some cases the
reason for giving up is obvious (for example, the female strikes a buried
rock), but not in others. When completed, the next hole extends between
10 and 50 centimetres into the sloping hillside. The female deposits her
clutch of up to 19 soft-shelled eggs (with an average of 10) on a single
night and may spend several more nights filling the entrance with soil and
grass. A female may return to her nest for up to eight nights after egg-laying,
even remaining alongside it by day.

Vandals at the nest

Why do females attend their completed nests for so long, sometimes even
exposing themselves to warm, dry, daytime weather and aerial predators,
instead of returning to a cool damp burrow that is their usual daytime retreat?
observations by Thompson, Guillette and ourselves reveal considerable competition
for nest sites. Females often dig up nests that contain eggs laid by other
females, breaking or scattering the previously-laid eggs in the process.
They then lay their own eggs in the same site. By remaining near a nest
for a few days after laying her eggs, a female may minimise the likelihood
of nest ‘vandalism’. Indeed, observations by Gillingham using infared night-viewing
equipment confirm that female tuatara vigorously defend their nests from
other females, their aggression and body inflation every bit as intense
as in territorial males. Similar nest-defence by females has been described
in several species of iguanas.

It is not certain why female tuatara sometimes pick the nests laid by
other females to lay their own eggs in. One possible explanation is that
females prefer sites where the soil is loose and the nest is easy to dig.
This is probably not the entire explanation, however, because females do
not only dig up nests covered with soft soil that contain fresh eggs laid
that nesting season. They also excavate sites with hardened surface soil
in which nesting has occurred the previous season. The latter nests contain
eggs with advanced embryos close to hatching (incubation lasts betweeen
11 and 16 months). Perhaps, then, these sites possess other physical attributes
that make them good spots for incubating eggs. For instance, frequently-dug
nest sites may be warmer or more moist than other sites. Does this mean
that at the time of nesting a female tuatara can accurately predict a site
that will be suitable for incubation over the entire season? Furthermore,
do older, more experienced females wait until near the end of the nesting
period to lay their eggs (thus minimising the chances of nest vandalism
that season) and then pick a relatively warm site that will result in successful
incubation in just under 12 months (and so minimise the chances of vandalism
the next season)? These questions are as yet unanswered.

Experimental studies have provided clues as to why female tuatara nest
on Stephens Island in open areas such as sheep pasture but not in the remnant
forest. Using highly sensitive thermocouple psychrometers, Thompson and
his colleagues Gary C Packard and Mary J Packard of Colorado State University
monitored temperature and moisture conditions in 28 tuatara nests throughout
12 months of incubation. About twice each month, conditions were recorded
every 4 hours for 28 hours, come baking summer days, bitter windswept nights
and the approaches of inquisitive bulls (since removed from Stephens Island).
Conditions in soil at a similar depth in the forest, where no nesting has
been observed, were also monitored for comparison. The results show that
during the summer, soil in the forest is, not surprisingly, much cooler
than in nests in the pasture, and rarely rises above 15 °C. Thompson’s
laboratory studies have shown that a constant temperature of 15 °C is
too cool for successful incubation. Eggs develop successfully, however,
at constant temperatures of 18-22 °C in the laboratory – temperatures
that are more typical of nests in open areas during the summer.

In short, the results suggest that female tuatara do not nest in the
forest because the soil there is too cold for successful incubation. We
and several colleagues recently obtained experimental support for this hypothesis.
We buried eggs in experimental ‘nests’ that we excavated in the pasture
and the forest, and compared their developmental rates. As predicted, those
that hatched in the pasture did so in their second summer (12-15 months
after burial). About 19 per cent hatched, somewhat lower than the figure
of 42 per cent recorded for natural nests by Mary McIntyre of Victoria University
of Wellington; most of the failed eggs in experimental nests probably died
from desication. Those in the forest survived up to 27 months but never
hatched.

Does the presence of sheep pasture explain why tuatara numbers are so
high on Stephens Island? We suspect so. Unfortunately, we have no reliable
estimates of tuatara numbers or their density 100 years ago, and so we have
no data to confirm our inference. Possibly, one (inverse) way of testing
this suggestion will come from proposed moves to revegetate Stephens Island
over future decades. Our prediction is that revegetation of preferred nesting
sites will lead to a gradual decline in tuatara numbers on Stephens Island.
Conservation managers must now address the difficult question of whether
such a decline is in the best interests of the entire community of living
organisms on Stephens Island, which includes rare lizards, a rare giant
cricket, and a frog that may be the rarest in the world.

In any case, with a life-span of at least 60 years, tuatara numbers
on Stephens Island are unlikely to change dramatically in the short term.
This life-span exceeds that of most, if not all, wild lizards. Indeed, the
entire life-history of tuatara occurs at a leisurely pace. We have already
referred to the long incubation period of tuatara eggs. Once hatched, tuatara
take about 13 years to reach maturity on Stephens Island, and although male
tuatara have an annual reproductive cycle, females reproduce on average
only once every four years.

In contrast, most egg-laying lizards produce at least one clutch of
eggs each year. With the possible exception of a large species of chuckwalla,
we know of no lizard with an average interval between nesting bouts as long
as that of female tuatara.

Observations by ourselves, Guillette, John Cockrem (then of the New
Zealand Department of Scientific and Industrial Research, now of Massey
University, New Zealand), Mark Brown (Victoria University of Wellington)
and others demonstrate that the reproductive cycle of female tuatara is
fundamentally different from that of lizards, and probably unique among
reptiles. The essential difference is that in female tuatara, the major
phases of egg production – that is, vitellogenesis, or egg yolk production,
and egg shelling – collectively require several years for a single clutch.

After nesting in spring, most females begin to accumulate yolk in their
developing ovarian follicles during the year that follows. But completion
of the process takes just over three years on average. In other words, if
one examines the reproductive organs of a group of female tuatara in spring,
one finds about 25 per cent in early vitellogenesis, about 25 per cent in
mid-vitellogenesis, about 25 per cent in late vitellogenesis and about 25
per cent carrying shelled eggs in their oviducts. Only those carrying oviducal
eggs will nest that spring.

We used laparoscopy, a technique that involves inserting a sort of medical
telescope into the body cavity under local anaesthesia, to examine the ovaries
of live females. Laparoscopy also enabled us to determine the reproductive
condition of females at mating and the duration of eggshelling. During late
summer, female tuatara mate when vitellogenesis is essentially complete.
The large (16 mm diameter), yolky follicles ovulate within a month or two
of mating, and the eggs then pass into the oviduct where they are fertilised
and shelled. Using scanning electron microscopy to examine the shells of
oviducal eggs collected at various months before laying, we confirmed that
shelling is a slow, gradual process spread over about 6 to 8 months. This
duration of shelling is more than three times as long as reported for any
lizard or indeed any other reptile.

Nobody knows whether female tuatara mate every year, or only in the
years that they carry ovarian follicles ready to ovulate. However, the fluctuations
that we have observed in blood concentrations of sex hormones during the
reproductive cycle suggest that they may be receptive only during the 1-2
months prior to ovulation. Female tuatara show high blood concentrations
of the sex hormones estradiol and testosterone and rising concentrations
of progesterone at this time. Similar hormonal profiles in other female
reptiles have been linked with sexual receptivity.

The high concentrations of testosterone and progesterone seen at the
time of mating or ovulation can be used to estimate the proportion of female
tuatara nesting in any given year. We have since used these criteria to
estimate the proportion of female tuatara nesting on 11 other islands, and
concluded that, as on Stephens, less then half the females are likely to
have nested in the year in question.

Unlike female tuatara, individual male tuatara have an annual reproductive
cycle. Blood concentrations of the sex hormone testosterone are elevated
in males during the mating period and probably help to stimulate territorial
and mating behavior. However, the testosterone cycle in male tuatara appears
to differ from that of lizards. In all male lizards examined, testosterone
levels rise during a relatively brief period (1-3 months) in spring or autumn
when mating occurs, while the levels are low over summer. In contrast, testosterone
levels in male tuatara begin to rise in spring, continue to rise during
early summer, and peak from mid-summer to early autumn. This prolonged period
of rising or elevated testosterone levels is associated with a prolonged
period of sperm production in the testes. In male lizards from other temperate
parts of the world, all stages of sperm production apparently cease for
one or more months of the year during spring or summer when the testes are
regressed in size. Male tuatara differ in that the testes are never fully
regressed and always contain at least the early stages of sperm production.

Why, then, is the reproductive activity of the sex organs of male and
female tuatara so prolonged compared with lizards from other parts of the
world? Are such protracted reproductive cycles ‘primitive’ compared with
those of lizards? We think not. We suggest that the prolonged reproductive
cycles of tuatara are specialisations for a maritime environment that is
cool year-round. On Stephens Island, mean monthly air tempteratures fluctuate
between 9 °C in winter and 16 °C in summer. Tuatara occasionally
reach body temperatures as high as 28 °C during daytime basking, but
most activities are carried out at night with body temperatures between
6-18 °C. These body temperatures are extremely cool compared with lizards
from other parts of the world – many lizards are active at body temperatures
of 20-42 °C, and would retreat into inactivity at the cool temperatures
favoured by tuatara.

In a timely and eloquent article in 1983, Carl Gans of the University
of Michigan discussed the tuatara’s preference for cool temperatures is
well-suited to current environmental conditions, and implied that it might
also be typical of New Zealand lizards from the same environments.

For instance, several species of New Zealand geckos inhabit the same
islands as tuatara and are active at night at similar body temperatures.
The male testicular cycle has been described in one of these (the common
gecko, Hoplodactylus maculatus) and is reported to show the same trend towards
at least partial testicular activity year-round as in tuatara. However,
reproduction in female geckos in New Zealand differs fundamentally from
that in female tuatara. Unlike all but one of the 600-odd geckos fround
elsewhere in the world, New Zealand geckos do not lay eggs. The evolution
of live-bearing in reptiles has frequently been linked with cool temperature,
the inference being that by carrying her young in her body and moving around
to warm sites, a live-bearing reptile can keep her developing young at higher
and more constant temperatures than eggs in a nest would be exposed to.

So female tuatara and nocturnal female geckos in New Zealand appear
to have evolved different ways of coping with a shared environmental ‘restraint’.
If a nocturnal New Zealand gecko was the only surviving lizard and the tuatara
was but one of many surviving sphenodontidans, which would we consider the
‘living fossil’? Michael Benton of Queen’s University in Belfast argued
in 1985 in Nature that the term ‘living fossil’ for tuatara was inaccurate
on anatomical grounds because: (i) there is no fossil record for tuatara,
and thus we have no evidence that the species has remained anatomically
unchanged for millions of years; and (ii) the skull, tooth and jaw structure
of tuatara are clearly specialised in many ways compared with early sphenodontidans.
Gans’ essay on thermal physiology and our recent research on reproductive
biology also suggest that the term ‘living fossil’ is inappropriate, given
its connotations of maladaptiveness, lack of complexity and imminent extinction.
A K Newman was wrong when he wrote in 1878 that the absence of an intromittent
organ in male tuatara implied ‘small sexual passions’. The reproductive
behaviour of both sexes of tuatara is extraorinarily rich, and the reproductive
physiology of females, which is clearly specialised to modern day conditions,
is an example of a strategy that lizards presumably could have, but did
not, evolve.

Saving a slow reproducer from the rat

Tuatara live only in New Zealand. They were once widespread over the
two main islands, but over the past 150 years have become extinct there,
as well as on at least 10 different offshore islands. Habitat destruction,
predation by early Polynesians, and predations by cats, rats, pigs and other
mammals introduced by Polynesians and Europeans are probably the main causes
of extinction.

About 30 populations are thought to survive, but one of these may already
by extinct and a further seven are vulnerable or endangered because of the
presence of an introduced rat (the kiore, Rattus, exulans). On six of the
seven rat-inhabited islands on which tuatara have recently been seen, no
juvenile tuatara have been found. Although experimental evidence is lacking,
kiore probably prey on tuatara eggs and juveniles, and compete for food
with juveniles and adults.

One of the most critically endangered populations is that on Stanley
Island in the Mercury Island group. This forested, medium-sized (100 hectare)
island could potentially support thousands of tuatara, but our recent extensive
surveys have revealed only 18. All are large adults and several appear aged.
The effects of rats on this population are apparently exacerbated by the
presence of rabbits, which were probably introduced by Europeans within
the past 150 years. Rabbits browse the forest floor vegetation, reducing
the habitats and numbers of insects on which tuatara feed. The remaining
adult tuatara may not be able to obtain sufficient food to reproduce. To
make matters worse, the adults are scattered over the island and may never
encounter a mate.

Is there still time to save the Stanley Island tuatara? Given the long
life span of tuatara, we think there is. The greatest chance of success
will come with aggressive management procedures, which could include the
following: (i) captive husbandry of remaining adults to improve their nutritional
condition sufficiently to allow breeding; and (ii) release of captive-bred
juveniles on Stanley Island when the rats and rabbits have been eradicated.
We are currently working with the New Zealand Department of Conservation
and Zoological Society of San Diego to save the Stanley Island tuatara.

Rehabilitating the tuatara populations on islands such as Stanley Island
depends on the eradication of introduced mammals such as kiore. Ten years
ago, eradication of kiore on offshore islands seemed an impossibility, but
recent success with islands up to 31 hectares in area by the New Zealand
Department of Conservation makes it feasible on Stanley Island. In a typical
kiore eradication programme, baits containing an anticoagulant poison are
placed over the island at regular intervals. Poisoning is carried out in
the spring, when the number of rats is low and there is little food available,
increasing the chances of success. Monitoring continues for at least a year
after the poisoning before the island is considered rat-free. The cost of
poisoning the rats on and island the size of Stanley Island is about 5000
Pounds (pds), plus transport and labour costs.

The proposed rehabilitation programmes for Stanley Island also depends
on successful captive breeding of tuatara. To date, the results of past
attempts at captive breeding have been poor: for example, although over
52 adult tuatara have been held in captivity in pairs or groups during the
past 38 years, no captive-bred juvenile has ever been raised to maturitity
and the oldest is only seven years. There are various reasons for this.
For instance, A P W Thomas tried to breed tuatara in 1885, but had to admit
failure when he discovered that the 29 adults he had collected were all
male. Since then, inadequate attention to the animal’s preference for cool
temperatures and its nutritional requirements may explain the poor success
rate. Given the extensive social behaviour of tuatara, lack of social interactions
in captivity may also be significant; captive adult tuatara have often been
maintained in single pairs.

Nevertheless, significant advances have been made. Thompson’s work has
shown that eggs can be collected from wild females by administering a hormone
(oxytocin) that induces laying, and the eggs can be incubated and hatched
successfully in the laboratory. We recently used these techniques to obtain
tuatara hatchlings from a tiny (300+) population on North Brother Island
(4 hectares). This population is of extraordinary conservation significance.
It was named as a separate species, Sphenoden guntheri, during the past
century, but this classificiation was subsequently ignored. Recently, we,
Thompson and Jennifer Hay of Victoria University of Wellington examined
variation in enzymes among 24 populations of tuatara, and concluded that
the North Brother Island population was so distinct from all others that
it should be reinstated as a distinct species (see Nature, 13 September
1990). We are currently working with the New Zealand Department of Conservation
to identify a suitable island for founding a second wild population of this
species using the hatchlings raised in captivity, and to establish a successful
captive breeding stock.

Apart from the species identified on North Brother Island, allozyme
studies revealed two genetic stocks within the more common species, S punctatus
– one present on 19 islands examined from the northeast coast of the North
Island, and one on Stephens Island and three other islands in Cook Strait.
A fourth genetic stocks of tuatara may exist on Little Barrier Island (this
population was described as a separate subspecies of S punctatus half a
century ago), but we were unable to sample it because no tuatara have been
seen on this island for at least 12 years. It may already be extinct. Tuatara
populations must thus be managed as at least three (perhaps four) genetic
stocks, not as a single form as in the past.

Alison Cree and Charles Daugherty are at Victoria University of Wellington,
New Zealand.