Do TSD, sex ratios, and nest characteristics influence the vulnerability of tuatara to global warming?

doi:10.1016/j.ics.2004.08.093

International Congress Series

Volume 1275, December 2004, Pages 250-257

https://doi.org/10.1016/j.ics.2004.08.093 Get rights and content

Abstract

Tuatara (Sphenodon punctatus) are threatened New Zealand reptiles with temperature-dependent sex determination (TSD). Higher incubation temperatures produce males, and less than 1 °C separates production of males and females. We investigated variability in nesting ecology to assess whether global warming is likely to result in increasingly male-biased populations. We examined nesting seasons during 1998/1999 and 2002/2003 in New Zealand's largest tuatara population on Stephens Island, and collected hourly temperature recordings and physical descriptions from 70 nests. Nest depths were not significantly different between years, and ranged from 10 to 230 mm from the soil surface to the top egg. Incubation temperatures in successful nests throughout the year-long incubation period ranged from 1.6 to 38.4 °C. Sex ratios of nests were correlated with incubation temperature: 64% males were produced in 1998/1999, a relatively warm season, but we predict an equal sex ratio was produced in 2002/2003. Although temperatures varied over the 2002/2003 season with respect to monthly long-term averages, 2002 was the second warmest year on record. Stephens Island supports a wide range of nesting habitat, a relatively large population of tuatara, and nest characteristics are highly variable. As such, this population is likely to be resilient to global warming in the short term because an equal sex ratio was predicted from a relatively warm season. However, most other islands where tuatara occur are smaller, have smaller populations, and have fewer open areas for nesting and/or shallower soils. These conditions are more likely to produce a male bias in hatchlings because female tuatara do not appear to vary construction of nests with respect to temperature or location. In the extreme, this could lead to the extinction of small populations.

Introduction

Reptiles with temperature-dependent sex determination (TSD), where embryonic sex is determined by incubation temperatures, have survived extreme climate change before [1]. However, the short time frame and the scale of global temperature increase predicted (+1.4–5.8 °C in the next 100 years)[2] may result in sex ratio imbalances that will threaten population persistence. Species with narrow transitional ranges (the range of incubation temperatures that produce 100% of one sex to 100% of the other sex) and long generation times (indicating limited potential to respond to rapid changes in climate) have four alternatives: to modify their geographic range, to convert to genetic sex determination, to go extinct, or to modify their nesting behaviour [3], [4]. Biased sex ratios are already known for reptiles with TSD [5]. A general warming trend is already evident in sea turtle nests (Chelonia mydas at Ascension Island) over the past 100 years [6]. In addition, findings so far point to nest site selection by female reptiles for hatching success rather than sex ratio manipulation (e.g. Refs. [4], [7], [8]).

Tuatara (Sphenodon), long-lived sole surviving members of the reptilian Order Sphenodontia, are restricted to small off-shore islands of New Zealand [9]. The two species (S. guntheri and S. punctatus) both have the rare Type 1b pattern of TSD, where males are produced from nests with higher incubation temperatures [10], [11]. There is no evidence so far to suggest they exhibit the type II pattern of TSD where females are produced at both extremes and males at intermediate incubation temperatures [11]. The pivotal temperature of the largest population of tuatara (21.7 °C, S. punctatus on Stephens Island) is relatively low for reptiles [12]. In addition, sex determination of embryos from this population occurs over a narrow transitional range of less than 1 °C [11]. The adult sex ratio on Stephens Island is estimated to be 50% males [13]. The only extant population of S. guntheri on North Brother Island comprises 60% adult males [14].

Nesting occurs in spring from early November, and female tuatara lay a clutch of eggs only about every 2–5 years [15], [16]. Shallow subterranean nests are constructed in open areas, not in forest habitat where temperatures are too low for successful development of embryos. On Stephens Island, nesting occurs in paddocks grazed by sheep, open cliff faces and rocky outcrops, and paths [16].

We investigate whether the tuatara's rare pattern of TSD, biased sex ratios, and diversity of nest characteristics and habitat influence the likelihood of male-biased populations that potentially threaten population persistence as a result of global warming. As the first step towards an inventory we ask the following questions: (1) What is the hatchling sex ratio? (2) Are there between-year variations in hatchling sex ratio? (3) Are there between-year variations in nest construction or time of laying?

Section snippets

Methods

Nests of tuatara were investigated during the annual nesting seasons in 1998 (3 weeks, November 1–21)[11] and 2002 (6 weeks, October 28–December 7) on Stephens Island (150 ha), New Zealand. Temperature data loggers (waterproof Stowaway® TidbiT®, dimensions: 30×41×17 mm, Onset Computer, MA, USA) set to record hourly measurements were inserted into nests spread throughout rookeries in sheep paddocks and on rocky outcrops (25 nests in 1998 and 45 nests in 2002). Back-fill of nests was excavated,

Results

Mean depth of nests was 103.5±9.2 mm (range 40–200 mm) in 1998/1999, and was not significantly different from 111.0±6.3 mm (range 10–230 mm) in 2002/2003 (Table 1; F_(1,60)=0.55; P=0.459). Nest depths were not significantly correlated with the date of laying or rookery location (F_(1,60)=0.36; P=0.551 and F_(8,53)=1.10; P=0.377). Depth significantly influenced variability of nest temperatures (minimum: F_(1,60)=28.45; P<0.001; maximum: F_(1,60)=17.25; P<0.001; CTE: F_(1,60)=5.50; P=0.022) but not

Discussion

We found a male-biased sex ratio in our first season of monitoring tuatara nests, but estimated an equal sex ratio from the second season. Several differences exist between the two seasons. Although we encompassed the preponderance of nesting in each instance, nests in the first season in 1998/1999 were marked over 3 weeks compared to 6 weeks in the second season (2002/2003). Temperatures during November, the primary period for laying, were higher in the first season. Warmer weather during nest

Acknowledgements

We thank the Marsden Fund and the Zoological Society of San Diego for funding, Arthur Georges, Brian Gartrell, and Alison Cree for help with techniques, and Victoria University of Wellington Animal Ethics Committee, Te Ngati Koata no Rangitoto ki te Tonga Trust and the New Zealand Department of Conservation for permitting the study.

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In recent decades, changes in climate have caused impacts on natural and human systems on all continents and across the oceans and many species have shifted their geographic ranges, seasonal activities, migration patterns, abundances and interactions in response to these changes. Projections of future climate change are uncertain, but the Earth's warming is likely to exceed 4.8 °C by the end of 21th century. The vulnerability of a population, species, group or system due to climate change is a function of impact of the changes on the evaluated system (exposure and sensitivity) and adaptive capacity as a response to this impact, and the relationship between these elements will determine the degree of species vulnerability. Predicting the potential future risks to biodiversity caused by climate change has become an extremely active field of research, and several studies in the last two decades had focused on determining possible impacts of climate change on Lepidosaurians, at a global, regional and local level. Here we conducted a systematic review of published studies in order to seek to what extent the accumulated knowledge currently allow us to identify potential trends or patterns regarding climate change effects on lizards, snakes, amphisbaenians and tuatara. We conducted a literature search among online literature databases/catalogues and recorded 255 studies addressing the influence of climate change on a total of 1918 species among 49 Lepidosaurian's families. The first study addressing this subject is dated 1999. Most of the studies focused on species distribution, followed by thermal biology, reproductive biology, behavior and genetics. We concluded that an integrative approach including most of these characteristics and also bioclimatic and environmental variables, may lead to consistent and truly effective strategies for species conservation, aiming to buffer the climate change effects on this group of reptiles.
Temperature selection by juvenile tuatara (Sphenodon punctatus) is not influenced by temperatures experienced as embryos
2017, Journal of Thermal Biology
Citation Excerpt :
Furthermore, our gradient only provided temperatures up to 33.5 °C as it was unexpected that they would use such warm temperatures, and thus tuatara may even exceed this temperature if given the opportunity. Temperatures available to eggs in natural nests and juveniles in nature can exceed 33.5 °C (Besson and Cree, 2010; Nelson et al., 2004a). Our observation of a diel cycle in temperature selection in three month old juvenile tuatara with only light cues provides evidence for an innate pattern of thermoregulatory behaviour where there are options for thermoregulation.
Most reptiles thermoregulate to achieve body temperatures needed for biological processes, such as digestion and growth. Temperatures experienced during embryogenesis may also influence post-hatching growth rate, potentially through influencing post-hatching choice of temperatures. We investigated in laboratory settings whether embryonic temperatures (constant 18 °C, 21 °C and 22 °C) influence selected body temperatures (T_sel) of juvenile tuatara (Sphenodon punctatus), providing a possible mechanism for differences in growth rates. We found that incubation temperature does not influence T_sel. Although the average daily mean T_sel was 21.6 ± 0.3 °C, we recorded individual T_sel values up to 33.5 °C in juvenile tuatara, which is higher than expected and above the panting threshold of 31–33 °C reported for adults. We found diel patterns of T_sel of juvenile tuatara, observing a general pattern of two apparent peaks and troughs per day, with T_sel being significantly lower around dawn and at 1500 h than any other time. When comparing our results with other studies on tuatara there is a remarkable consistency in mean T_sel of ~ 21 °C across tuatara of different ages, sizes and acclimatization histories. The ability of juvenile tuatara to withstand a wide range of temperatures supports their former widespread distribution throughout New Zealand and warrants further investigation into their plasticity to withstand climate warming, particularly where they have choices of habitat and the ability to thermoregulate.
Using a microclimate model to evaluate impacts of climate change on sea turtles
2013, Ecological Modelling
Sea turtles are thought to be particularly vulnerable to climate change as projected increases in temperature may skew the sex ratio of their hatchlings, decrease hatchling success and thus threaten population persistence. Given the seriousness of the threat from climate change it is critical to understand the rate at which soil temperatures at sea turtles’ nesting grounds are likely to change. This has stimulated the development of correlative models to assess and project how projected increases in temperature may impact sea turtle's reproductive output. Correlative models correlate climatic variables to soil temperature and hatchling sex ratio. These models have been widely used due to their simplicity and the flexibility of their data requirement. However, outputs are restricted by the environmental conditions used for the model and thus does not allow exploration of daily variation in sand temperature. Further, the potential error inherent in this approach has not been determined.
Researchers working with other animals with temperature-dependent sex determination (TDS) have developed microclimate models to determine nest temperature and potential impacts from climate change. Microclimate models use the interaction between climate, soil, and topography with physiology and nesting behavior of animals to determine future production of hatchling sex ratios. Until now, microclimate models have never been applied to sea turtles and its correlation and consistency with correlative models has never been explored. To address this, we used the Niche Mapper™ microclimate model to project soil temperature at key sea turtle nesting grounds under various scenarios of global warming. Results from the microclimate model are compared to published projections from correlative models. The two approaches accurately and congruently model current soil temperature and project a feminization of the northern Great Barrier Reef green turtle population as climate change progresses. To provide guidance of when to use each approach we also reviewed the applicability and effectiveness of each model. The microclimate model provided a more robust picture of the incubating environment as it has the potential for projecting soil temperature for every hour of the day at various locations and depths within a nesting ground. This allows exploration of whether animals with TDS can counteract the impacts of global warming by changing nest depth and nesting distribution. With time and the validation of the microclimate model with short-term projections, the microclimate model can also be used to refine short-term adaptive management strategies as they can provide explicit recommendations on site-specific scales for translocation of eggs and alteration of the nesting environment.
Behavioural plasticity may compensate for climate change in a long-lived reptile with temperature-dependent sex determination
2012, Biological Conservation
Citation Excerpt :
In species with TSD, the sex-determining pathway is extremely sensitive to temperature: the transitional range of temperatures, within which the complement of offspring sex shifts from 100% male to 100% female (or vice versa), is generally less than 2 °C, and may be less than 1 °C (Ewert et al., 1994). This degree of thermal sensitivity means that a small change in environmental temperature could dramatically alter offspring sex ratio, and potentially result in populations consisting of predominantly one sex (Janzen, 1994a; Nelson et al., 2004). Reptiles with TSD have survived past periods of dramatic global warming and cooling.
How are organisms responding to climate change? The rapidity with which climate is changing suggests that, in species with long generation times, adaptive evolution may be too slow to keep pace with climate change, and that alternative mechanisms, such as behavioural plasticity, may be necessary for population persistence. Species with temperature-dependent sex determination may be particularly threatened by climate change, because altered temperatures could skew sex ratios. We experimentally tested nest-site choice in the long-lived turtle Chrysemys picta to determine whether nesting behaviour can compensate for potential skews in sex ratios caused by rapid climate change. We collected females from five populations across the species′ range and housed them in a semi-natural common garden. Under these identical conditions, populations differed in nesting phenology (likely due to nesting frequency), and in nest depth (possibly due to a latitudinal cline in female body size), but did not differ in choice of shade cover over the nest, nest incubation regime, or in resultant nest sex ratios. These results suggest that choice of nest sites with particular shade cover may be a behaviourally plastic mechanism by which turtles can compensate for change in climatic temperatures during embryonic development, provided that sufficient environmental variation in potential nest microhabitat is available.
Influence of ambient temperature on maternal thermoregulation and neonate phenotypes in a viviparous lizard, Eremias multiocellata, during the gestation period
2011, Journal of Thermal Biology
Citation Excerpt :
For example, there is a general increase in body size with elevated incubation temperature in Cyclura nubila (Alberts et al., 1997) but the reverse situation was found in Sphenomorphus indicus (Ji et al., 2006). In addition to morphology, incubation temperature also influences locomotor performance and early growth rate of some reptile hatchlings (Booth et al., 2004; Nelson et al., 2004); both factors are considered to have great effect on hatchling fitness (Booth, 2006). Many studies investigating the effects of gestation temperature on post-hatchling phenotype have been conducted on oviparous reptile species (Shine and Harlow, 1996; Qualls and Shine, 1998), whereas parallel studies focusing on viviparous species are relatively limited (Beuchat, 1988; Swain and Jones, 2000; Wapstra et al., 2004).
To assess the potential gestational effects on post-hatching morphology, locomotor performance, and early growth rate, we maintained gravid Eremias multiocellata under four constant treatment temperatures (25, 29, 31, and 35 °C). Ambient temperature had significant effects on some morphometric traits of offspring, including tail length, head size, forelimb length and hindlimb length, but not on body mass or snout-vent length. The data of females' body temperature indirectly support the maternal manipulation hypothesis. Juvenile E. multiocellata had better locomotor performance and faster early growth rate at 29 °C than at the other three treatment temperatures (25, 31, and 35 °C). Our results suggest that gestation temperature may be optimized at 29 °C for E. multiocellata from Tianzhu, Gansu Province, China.
No evidence of fine scale thermal adaptation in green turtles
2019, Journal of Experimental Marine Biology and Ecology
Adaptation to increasing temperatures may enable species to mitigate the long-term impacts of climate change. Sea turtles have temperature dependent sex determination (TSD) and variation in the thermal reaction norm, which influences offspring sex ratio, has been suggested as a potential adaptive mechanism to rising global temperatures. Here, we investigate the sex ratio of green turtle Chelonia mydas offspring from nests on beaches with notable differences in their thermal properties, to look for evidence of localised adaptation. We compared pivotal temperatures and hatch success in both the laboratory and in situ using eggs laid on two nesting beaches (dark vs. pale sand) at Ascension Island that represent the extremes of the range of incubation temperatures experienced by this population. We found no effect of beach of origin on pivotal temperatures, hatch success, or hatchling size in the laboratory or the wild. This suggests that turtles from the same rookery are not locally adapted to different thermal conditions experienced during incubation. Under predicted climate change scenarios, this will result in reduced hatch success and an increased proportion of female offspring unless temporal or spatial range shifts occur.

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International Congress Series

Abstract

Introduction

Section snippets

Methods

Results

Discussion

Acknowledgements

References (25)

Nest-site selection in two eublepharid gecko species with temperature-dependent sex determination and one with genotypic sex determination

Biol. J. Linn. Soc.

Tuatara: a survivor from the dinosaur age

N.Z. Geogr.

Climate Change 2001: The Scientific Basis. Inter-Governmental Panel on Climate Change

Environmental sex determination in reptiles: ecology, evolution, and experimental design

Q. Rev. Biol.

How rapidly can maternal behaviour affecting primary sex ratio evolve in a reptile with environmental sex determination

Am. Nat.

Cultural inheritance as a mechanism for population sex-ratio bias in reptiles

Evolution

Climate change and sea turtles: a 150-year reconstruction of incubation temperatures at a major marine turtle rookery

Glob. Chang. Biol.

Beach selection in nesting pig-nosed turtles, Carettochelys insculpta

J. Herpetol.

Tuatara sex determination

Nature

Temperature-dependent sex determination in tuatara

Effects of incubation temperature

Cited by (46)

Unraveling the influences of climate change in Lepidosauria (Reptilia)

Temperature selection by juvenile tuatara (Sphenodon punctatus) is not influenced by temperatures experienced as embryos

Using a microclimate model to evaluate impacts of climate change on sea turtles

Behavioural plasticity may compensate for climate change in a long-lived reptile with temperature-dependent sex determination

Influence of ambient temperature on maternal thermoregulation and neonate phenotypes in a viviparous lizard, Eremias multiocellata, during the gestation period

No evidence of fine scale thermal adaptation in green turtles