Despite increasing evidence that some species are adapting to contemporary climate change via genetically driven shifts in thermal traits (Bradshaw & Holzapfel 2006
), long-lived and slow-reproducing reptiles with TSD are unlikely to adapt to the most extreme increases in air temperature, particularly when dealt the additional card of low genetic variation (Janzen 1994
; MacAvoy et al. 2007
). Our analyses demonstrate that without adaptation, extreme climate change will produce fast-developing all-male clutches, resulting in the extinction of smaller tuatara populations as operational sex ratios become increasingly male biased. The time frame over which extinctions could occur under global warming is difficult to predict given the longevity of tuatara (Nelson et al. 2002b
) and that occasional cooler years would produce females.
Given that an evolutionary response to current rates of global warming is unlikely, could tuatara behaviourally compensate for the effects of extreme warming by altering the depth, location or time at which they lay their eggs? Mixed-sex nests are produced at 300
mm depth under maximum warming, but soils on North Brother Island are generally shallow and highly eroded and are likely to prevent females from digging deep nests. Alternatively, the female tuatara could nest on different regions of the island, but our analyses reveal that only limited portions of North Brother Island would produce mixed-sex offspring at current nest depths under maximum warming (5–34%; see figure S1 in the electronic supplementary material). At the typical nest depth of tuatara of 100
mm (Nelson et al. 2004a
), mixed-sex-producing sites are restricted to the south-facing cliff tops, with only the southern face generating females (). Generally, tuatara are scarce on south-facing slopes many of which are probably too steep to allow habitation; hence, females changing nesting locations to female-producing regions of the island is an unlikely response to maximum warming.
A more effective behavioural response to global warming would be to select nest sites that receive less solar radiation. The Australian agamid lizard Physignathus lesueurii
has TSD and selects remarkably similar nest temperatures across a broad latitudinal distribution by preferring more shaded nest sites in warmer parts of its range (Doody et al. 2006
). Although tuatara always nest in open areas (Nelson et al. 2004a
), we simulated the effect of females nesting in partially (75%) shaded sites in response to maximum warming, and found that exclusively mixed-sex nests were produced at depths between 50 and 200
mm, hatching in just under one year (). If female tuatara do not respond to global warming by selecting nest sites receiving relatively low levels of solar radiation, then balanced sex ratios and spring emergence of hatchings could be achieved if humans cover nest sides with shade cloth after oviposition, but before the critical period for sex determination. Considerable disturbance of nesting females would be required to locate nests in large numbers, hence a more practical approach could be to shade entire rookeries at the completion of a nesting season.
Table 2 Proportions and development times of all-female, mixed-sex and all-male clutches predicted under maximum warming with either changed nesting phenology or selection of shaded nest sites. (Percentages were calculated from the combined results of simulations (more ...)
A final mechanism for females to increase the proportion of mixed-sex and all-female offspring is to nest later, in January (; table S3 in the electronic supplementary material). Later nesting means the TSP occurs when soil temperatures are cooler, and the hatching phenology currently seen in the tuatara is restored, with faster developing males hatching in spring, followed by female hatchlings in summer ( and ). Notably, female tuatara from northern populations nest later than those from Cook Strait populations (Tyrrell et al. 2000
), which may be adaptive in the warmer northern climate in ensuring that hatching occurs in the austral spring. It is therefore possible that selection on hatching times could move nesting seasons forward under global warming, but the strength of selection and heritability of the trait would need to be substantial to keep pace with increasing air temperatures. Conversely, warmer winters are predicted in New Zealand under climate change (New Zealand Climate Change Office 2004
), which may lead to earlier vitellogenesis and calcification of eggs, and hence to earlier rather than later nesting. Several studies have documented earlier breeding in oviparous species in response to climate change (Crick & Sparks 1999
; Walther et al. 2002
; Weishampel et al. 2004
; Parmesan 2007
), with one estimate suggesting an advance of 2.8 days per decade (Parmesan 2007
). Our simulations show that earlier nesting by female tuatara would further bias sex ratios towards males and shorten development times (see table S4 in the electronic supplementary material), and may effectively eliminate recruitment of females into the breeding population. Again, partial shading of nest sites could correct the imbalance ().
Our models highlight an additional consequence of extreme global warming for tuatara, in that males developing in all-male-producing nests would complete development five to six months early in autumn, rather than in spring/summer ( and ). Incubation temperature has little effect on body size at hatching in tuatara (Nelson et al. 2004b
), but the energetic consequences of early maturity will depend on whether hatchlings immediately emerge from the nest or overwinter in the nest cavity. Evidence from a review of emergence patterns in turtles that nest in spring and reach hatchling stage in autumn suggests that the phenomenon of overwintering in the nest may be adaptive in ensuring that hatchlings emerge in favourable spring conditions (Gibbons & Nelson 1978
). If maximum warming promotes autumn maturity for tuatara, as our models suggest, then any hatchlings that overwinter will do so under much warmer nest temperatures than they do now, as the 4°C rise in winter air temperatures is predicted to be the most dramatic.
Warmer overwintering temperatures have been correlated with smaller yolk reserves in populations of red-eared slider turtles (Trachemys scripta elegans
) emerging from the nest (Willette et al. 2005
), which is a clear demonstration of a physiological change associated with climate. Using bioenergetic principles (Vleck & Hoyt 1991
; Angilletta et al. 2000
; Mitchell & Seymour 2000
), we can estimate the energy cost of development to hatching stage by averaging the monthly 100
mm CTE for the 52 nest sites, predicting the proportion of development completed on each day using the nonlinear development rate function (figure S2 in the electronic supplementary material), and integrating age-specific rates of oxygen consumption at 20°C (Booth & Thompson 1991
) corrected to the CTE using a Q10
of 3.01 (10–20°C) or 2.34 (20–30°C). The Q10
were calculated from mass-specific rates of carbon dioxide production in S. punctatus
embryos (N. J. Mitchell & N. J. Nelson 2001, unpublished data). The energetic cost of development can be estimated from the volume of oxygen consumed, using the conversion factor 19.64
(Booth & Thompson 1991
). Mean dry yolk mass of S. guntheri
eggs is 1.01
=9; N. J. Mitchell 2002, unpublished data) and, assuming a similar yolk energy density to squamate reptiles (26.7
; Booth & Thompson 1991
), approximately 27
kJ of energy is present in a typical egg at oviposition.
On average, 72% (19.5
kJ out of 27
kJ) of yolk energy would be consumed during development to hatching under current nesting patterns (mid-November oviposition at 100
mm, hatching in 391 days), but this cost would decrease markedly under maximum warming to only 47% (12.7
kJ), because the embryos reach hatching stage in 153 days. If hatching stage is reached when relatively mild autumn weather prevails, then male hatchings may emerge from the nest and begin their growing season in late autumn/early winter, at a time when the invertebrate prey that sustains juvenile tuatara is relatively scarce (Walls 1983
). Conversely, if male hatchings overwinter in the nest cavity, they would consume another 40% of their yolk energy if they emerge in mid-September (early spring), assuming that their metabolic rate remained the same as at hatchling stage, but varied with winter nest temperature. Importantly, under either scenario, the energy reserves of hatchlings from all-male nests under a warmer climate will differ from the reserves of those that hatch under the current climate. The same would apply to males and females completing development in mixed-sex nests in autumn and winter; yet females emerging from all-female-producing nests would retain the current hatchling phenology of spring emergence, and could take advantage of a long growing season. These energetic simulations demonstrate a largely male-biased disruption in emergence time and energy balance, which could have important consequences for sex-specific rates of juvenile activity, growth and mortality.