Susan N. Keall

Support for a rare pattern of temperature-dependent sex determination in archaic reptiles: evidence from two species of tuatara (Sphenodon)

BackgroundThe sex of many reptiles is determined by the temperature an embryo experiences during its development. Three patterns of temperature-dependent sex determination (TSD) have been defined, but one pattern where only males are produced above an upper temperature threshold (Type IB) is controversial. Here we report new data on the relationship between constant temperature incubation and sexual phenotype in two species of tuatara (Sphenodon), archaic reptiles of enormous zoological significance as the sole representatives of a once widespread reptilian order.ResultsIn both species, the pattern observed with constant incubation temperatures from 18 to 23°C (or 24°C) supported a female→male (FM or Type IB) pattern of TSD: in Sphenodon guntheri males were produced above a pivotal temperature of 21.6°C, and in S. punctatus (unnamed subspecies on Stephens Island, Cook Strait), males were produced above a pivotal temperature of 22.0°C. The pivotal temperatures and scaling parameters differed between species (p < 0.001). The thermosensitive period (TSP), where temperature influences gonad morphogenesis, occurs between 0.25 and 0.55 of embryonic development. While it is possible that the more common female→male→female (FMF or Type II) pattern exists, with a second pivotal temperature above 23–24°C, we review several lines of evidence to the contrary. Most notably, we show that in S. punctatus, the warmest natural nests during the TSP produce predominantly males.ConclusionAn FM pattern of TSD could be currently adaptive in promoting sexual size dimorphism in tuatara. However, an FM pattern has particularly serious consequences for S. guntheri because current patterns of global warming could exacerbate the male bias already present in the relic population.

Implications of social dominance and multiple paternity for the genetic diversity of a captive-bred reptile population (tuatara)

Captive breeding is an integral part of many species recovery plans. Knowledge of the genetic mating system is essential for effective management of captive stocks and release groups, and can help to predict patterns of genetic diversity in reintroduced populations. Here we investigate the poorly understood mating system of a threatened, ancient reptile (tuatara) on Little Barrier Island, New Zealand and discuss its impact on the genetic diversity. This biologically significant population was thought to be extinct, due to introduced predators, until 8 adults (4 males, 4 females) were rediscovered in 1991/92. We genotyped these adults and their 121 captively-bred offspring, hatched between 1994 to 2005, at five microsatellite loci. Multiple paternity was found in 18.8% of clutches. Male variance in reproductive success was high with one male dominating mating (77.5% of offspring sired) and one male completely restricted from mating. Little Barrier Island tuatara, although clearly having undergone a demographic bottleneck, are retaining relatively high levels of remnant genetic diversity which may be complemented by the presence of multiple paternity. High variance in reproductive success has decreased the effective size of this population to approximately 4 individuals. Manipulation to equalize founder representation was not successful, and the mating system has thus had a large impact on the genetic diversity of this recovering population. Although population growth has been successful, in the absence of migrants this population is likely at risk of future inbreeding and genetic bottleneck.

Egg mass determines hatchling size, and incubation temperature influences post-hatching growth, of tuatara Sphenodon punctatus

The size of reptile hatchlings can be phenotypically plastic in response to incubation temperature, and size is a trait likely to influence fitness – i.e. hatchling size is proposed as an indicator of quality. The parental and incubation temperature effects on the size of one of New Zealands most biologically significant reptile species, the tuatara Sphenodon punctatus are investigated. Artificial incubation at constant temperatures is used to produce founders for new captive and wild populations of tuatara and to augment existing rare populations. We compare size of hatchling tuatara from artificial and natural incubation treatments. The relationship of hatchling size with incubation temperature and sex is examined, and we investigate whether our results support differential fitness models for the evolution of temperature-dependent sex determination in tuatara. Initial egg mass is the most important factor affecting size of hatchling tuatara and is still an important influence at 10 months of age. Incubation temperature does not greatly influence size of hatchlings, but significantly influences size by 10 months of age. Constant artificial incubation conditions result in larger, but possibly less aggressive, juveniles than those from more variable natural incubation conditions by 10 months of age. Evidence from size patterns of tuatara incubated in natural nests supports differential fitness models for the adaptive significance of temperature-dependent sex determination. Thermal variation has little effect on size of male hatchlings, but female embryos that develop in more stable thermal conditions, in more reliable sites for hatching, are bigger and have longer jaws.

Sex Ratio Bias and Extinction Risk in an Isolated Population of Tuatara (Sphenodon Punctatus)

Understanding the mechanisms underlying population declines is critical for preventing the extinction of endangered populations. Positive feedbacks can hasten the process of collapse and create an ‘extinction vortex,’ particularly in small, isolated populations. We provide a case study of a male-biased sex ratio creating the conditions for extinction in a natural population of tuatara (Sphenodon punctatus) on North Brother Island in the Cook Strait of New Zealand. We combine data from long term mark-recapture surveys, updated model estimates of hatchling sex ratio, and population viability modeling to measure the impacts of sex ratio skew. Results from the mark-recapture surveys show an increasing decline in the percentage of females in the adult tuatara population. Our monitoring reveals compounding impacts on female fitness through reductions in female body condition, fecundity, and survival as the male-bias in the population has increased. Additionally, we find that current nest temperatures are likely to result in more male than female hatchlings, owing to the pattern of temperature-dependent sex determination in tuatara where males hatch at warmer temperatures. Anthropogenic climate change worsens the situation for this isolated population, as projected temperature increases for New Zealand are expected to further skew the hatchling sex ratio towards males. Population viability models predict that without management intervention or an evolutionary response, the population will ultimately become entirely comprised of males and functionally extinct. Our study demonstrates that sex ratio bias can be an underappreciated threat to population viability, particularly in populations of long-lived organisms that appear numerically stable.

Securing the Demographic and Genetic Future of Tuatara through Assisted Colonization

Climate change poses a particular threat to species with fragmented distributions and little or no capacity to migrate. Assisted colonization, moving species into regions where they have not previously occurred, aims to establish populations where they are expected to survive as climatic envelopes shift. However, adaptation to the source environment may affect whether species successfully establish in new regions. Assisted colonization has spurred debate among conservation biologists and ecologists over whether the potential benefits to the threatened species outweigh the potential disruption to recipient communities. In our opinion, the debate has been distracted by controversial examples, rather than cases where assisted colonization may be a viable strategy. We present a strategic plan for the assisted migration of tuatara (Sphenodon punctatus), an endemic New Zealand reptile. The plan includes use of extant populations as reference points for comparisons with assisted-colonization populations with respect to demography, phenotypic plasticity, and phenology; optimization of genetic variation; research to fill knowledge gaps; consideration of host and recipient communities; and inclusion of stakeholders in the planning stage. When strategically planned and monitored, assisted colonization could meet conservation and research goals and ultimately result in the establishment of long-term sustainable populations capable of persisting during rapid changes in climate.

Performance of Juvenile Tuatara Depends on Age, Clutch, and Incubation Regime

Abstract We investigated whether incubation treatment or size influence sprint speed of tuatara (Sphenodon punctatus) as artificial incubation is often used to produce founders for new populations of this endangered reptile. Sprint speed was affected by age, clutch and incubation regime (natural vs. artificial incubation). Older juveniles ran faster than younger juveniles. Maternal influence, represented by clutch, accounted for 18% of the variance in sprint speeds at one month of age. Naturally incubated juveniles were the smallest animals of any incubation regime, but at 10 months of age these juveniles were the fastest runners. Naturally incubated juvenile tuatara were more aggressive and faster for their size than artificially incubated juveniles, suggesting they may have higher fitness when released.

Induction of oviposition produces smaller eggs in tuatara (Sphenodon punctatus)

Abstract Induction of oviposition by injection of hormones has been used successfully to collect eggs from at least three orders of reptiles. Eggs of tuatara (Sphenodon spp.) have been collected by induction since 1985. We investigate whether inducing egg laying affects clutch size, egg mass, hatching success, or hatchling size, and describe considerations necessary when deciding whether to induce egg laying or collect eggs from nests. Altogether, 320 tuatara (S. punctatus) eggs were collected for incubation from Stephens Island in November 1998: 166 by induction and 154 from nests. Induced eggs (mean = 4.498 g ± 0.060 SE) were significantly smaller than naturally laid eggs collected within a few days of oviposition (mean = 5.375 g ± 0.070 SE). Induced eggs resulted in significantly smaller hatchlings following incubation in captivity, and the difference was still significant when hatchlings were 10 months old. Reduced size of hatchlings has consequences for long‐term fitness.

Effective partnerships between universities and indigenous communities: A case study in tuatara conservation in Aotearoa

Researchers are increasingly seeking to collaborate cross-culturally, particularly with indig-enous communities. The Kia Mau Te Tītī Mo Ake Tōnu Atu (Keep the Tītī Forever) project is a fantastic example of one such successful effort (Moller et al. 2009). We describe another example of a similarly fruitful relationship between researchers at Victoria University of Wel-lington and Te Atiawa Manawhenua Ki Te Tau Ihu (Te Atiawa)

Nest-site selection and the factors influencing hatching success and offspring phenotype in a nocturnal skink

Nest-site selection in ectothermic animals influences hatching success and offspring phenotype, and it is predicted that females should choose nesting sites that maximise their reproductive fitness, ultimately through the reproductive success of their offspring. We completed nest-site choice experiments on a nocturnal lizard, the egg-laying skink ( Oligosoma suteri ), to determine whether eggs (and subsequent hatchlings) from cooler nests do better at cooler incubation temperatures, and conversely if those laid in warmer nests perform better at warmer incubation temperatures. We provided a simple nest-choice experiment, with oviposition-retreat sites available in either a hot or a cool sector of the enclosure; in the wild females nest under objects. Female O. suteri laid eggs both during the day and night, and nested more in the hot than cool sector. Eggs from each clutch were split across three egg incubation temperatures (18°C, 22°C, 26°C) to decouple the impact of initial nest-site choice from the subsequent incubation temperature regime. Whether eggs were initially laid in the hot or cool sector was not related to hatching success, offspring phenotype or offspring locomotor performance. We conclude that offspring phenotype and performance is primarily influenced by the temperature during incubation, rather than the initial thermal environment of the nest location. Thus, female O. suteri may select warmer nesting sites to ensure higher incubation temperature and enhanced offspring fitness.

Mark–Recapture Accurately Estimates Census for Tuatara, a Burrowing Reptile

Abstract Estimates of population size are necessary for effective management of threatened and endangered species, but accurate estimation is often difficult when species are cryptic. We evaluated effectiveness of mark–recapture techniques using the Lincoln–Peterson estimator for predicting true census size of a population of tuatara (Sphenodon punctatus), a burrowing reptile that is a conservation priority in New Zealand. We found that Lincoln–Peterson estimates (N ˆ  =  85) were accurate for predicting the census size (N  =  87) after only a 3-day mark–recapture survey. We recommend this method as a cost-effective way to accurately estimate population size for isolated, inaccessible tuatara populations, because it requires limited personnel, expertise, and time, and has low environmental impact on fragile sites.