Survey
* Your assessment is very important for improving the workof artificial intelligence, which forms the content of this project
* Your assessment is very important for improving the workof artificial intelligence, which forms the content of this project
Journal of Experimental Marine Biology and Ecology 451 (2014) 105–114 Contents lists available at ScienceDirect Journal of Experimental Marine Biology and Ecology journal homepage: www.elsevier.com/locate/jembe Sun exposure, nest temperature and loggerhead turtle hatchlings: Implications for beach shading management strategies at sea turtle rookeries Apanie Wood a,b, David T. Booth a,⁎, Colin J. Limpus c a b c School of Biological Science, The University of Queensland, Qld 4072, Australia Centre for Tropical Water and Aquatic Ecosystem Research, James Cook University, Townsville, Qld 4811, Australia Aquatic Threatened Species Unit, Queensland Department of Environment and Heritage Protection, P.O. Box 2454, Qld 4001, Australia a r t i c l e i n f o Article history: Received 26 August 2013 Received in revised form 12 November 2013 Accepted 15 November 2013 Available online 12 December 2013 Keywords: Global warming Incubation Marine turtles Nest Reptiles Shade a b s t r a c t Sea turtle incubation biology is tightly linked to nest thermal conditions due to the effect temperature has on hatching success, sex determination, morphology and locomotion performance. Because of this relationship between nest temperature and hatchling outcomes, global warming presents an immediate threat to many sea turtle nesting beaches throughout the world. Even small rises in nest temperatures may skew sex ratios and, raise egg mortality and influence hatchling phenotypes adversely, impacting on hatchling recruitment and ultimately species survival at some rookeries. The development of adaptive management practices capable of minimizing the effects of increasing global temperature on nest temperatures is thus a priority for animals exhibiting temperature-dependent sex-determination, such as sea turtles. Here, the relationship between solar radiation exposure and nest temperatures at the Mon Repos turtle rookery, south east Queensland, Australia was explored and the relationship between nest temperature and hatchling attributes examined. Shading decreased nest temperature, and higher nest temperatures were associated with smaller sized hatchlings that had decreased locomotion performance. The use of shading to minimize nest temperature is a management strategy that may be used to mitigate detrimental effects of increased global temperatures at some rookeries. Here, we explored the viability of natural shading options, such as the planting of trees behind nesting beaches, for combating the adverse effect of increased nest temperature caused by increased air temperatures. © 2013 Elsevier B.V. All rights reserved. 1. Introduction Climate change is widely considered one of the greatest looming threats to global biodiversity (Chaloupka et al., 2008; Poloczanska et al., 2007; Root et al., 2003). Average global temperatures are predicted to increase by between 1.9 and 2.6 °C by the year 2050 (IPCC, 2007; Lough, 2007). The biological consequence of rising global temperatures differs between species (Harley et al., 2006), with the most vulnerable species being those with demonstrated life history ties to environmental temperature such as sea turtles where increased nest temperatures have been associated with increased embryonic mortality, highly female skewed sex ratios, and reduced hatchling locomotion ability (Booth and Evans, 2011; Booth et al., 2004; Booth et al., 2013; Hamann et al., 2007; Hawkes et al., 2007, 2009; Hays et al., 2003; Ischer et al., 2009; Janzen, 1994; Katselidis et al., 2012; Maulany et al., 2012a,b; Tomillo et al., 2012; Valverde et al., 2010). All sea turtle species except the flatback turtle (Natator depresses) are listed on the IUCN red list of threatened species (IUCN, 2009). For this reason, research has focused on identifying the impacts of impending ⁎ Corresponding author. Tel.: +61 7 33652138; fax: +61 7 33651655. E-mail address: [email protected] (D.T. Booth). 0022-0981/$ – see front matter © 2013 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.jembe.2013.11.005 temperature rise associated with climate change on sea turtle biology, such as elevated sea level (Fish et al., 2005; Fuentes et al., 2010a, 2011; Kostas et al., 2014), and increased sand temperatures (Fuentes et al., 2010b; Glen and Mrosovsky, 2004; Hawkes et al., 2007, 2009; Katselidis et al., 2012; Saba et al., 2012). Nest temperatures are influenced by air temperature and the amount of solar radiation received by the sand surface above and close to the nest (Ackerman and Lott, 2004; Standora and Spotila, 1985). Therefore, factors that influence solar radiation exposure, such as nest location, aspect and shading from vegetation, are likely to influence nest temperature. Reducing nest exposure to solar radiation is potentially a way of reducing the adverse impact of increased global temperatures at sea turtle rookeries (Fuentes et al., 2012; Mazaris et al., 2009; Morreale et al., 1982). However, global warming is a generalized prediction, and not all sea turtle rookeries may be adversely affected by temperature changes so before active management strategies at a particular rookery are implemented ground-truth data on actual nest temperatures needs to be gathered. The highest nesting density of the South Pacific population of loggerhead turtles (Caretta caretta) occurs along the Woongarra coast of mainland Australia. Within this region the Mon Repos rookery supports the majority of nesting (Chaloupka and Limpus, 2001; Limpus and Limpus, 2003). Consequently, hatchlings produced at Mon Repos 106 A. Wood et al. / Journal of Experimental Marine Biology and Ecology 451 (2014) 105–114 represent an important contribution to the reproductive output of this population. We examined how nest temperature influences nest emergence success, predicted hatchling sex ratio, hatchling size, self-righting ability and crawling speed, and how shading affects nest temperature. We expected shading to decrease nest temperature and subsequently to increase hatchling quality because nest temperatures would be decreased from sub-lethal to optimal levels. We also developed a model that predicts nest temperature as a function of afternoon shade exposure from trees planted on dunes to demonstrate that shade trees could be used to decrease nest temperatures in response to global warming. 2. Materials and methods 2.1. Study area This study was conducted during the 2009–2010 nesting season at the Mon Repos sea turtle rookery (24°40′S, 152°27′E) a declared conservation park located in southeast Queensland on mainland Australia (Fig. 1). This rookery is an east facing beach, 1.54 km long, consisting of brown siliceous sand. A casuarinas tree (Casuarina equisetifolia) forest fringing the hind dune created shade across the width of the beach late in the afternoon. 2.2. Experimental design To test the effects of solar radiation exposure on loggerhead turtle nest temperature and hatchling quality, four shading treatments were used: no artificial shade hereafter referred to as ‘no shade’ (~9.5 h direct sun exposure per day), eastern row of the shaded hatchery hereafter referred to as ‘least shade’ (~ 4 h direct sun exposure), middle row of the shaded hatchery hereafter referred to as ‘intermediate shade’ (~1.5 h per day direct sun exposure), and western row of the shaded hatchery hereafter referred to as ‘most shade’ (~0.5 h of direct sun per day) (Fig. 2). Extra-light synthetic shade cloth (AS 4174-1994) rated as allowing 70% solar radiation transmission covered a 7.5 × 4.5 m rectangular shade structure that was positioned parallel to the shore on the beach front dune in the zone where most natural nests were constructed. Entire clutches of eggs were collected at random from nesting loggerhead turtles at Mon Repos between 1st and 16th December 2009. All turtles nesting at this rookery were fitted with flipper identity tags and these were used to ensure that no two clutches came from the same female. Clutch relocation was completed within 2 h of oviposition to avoid movement-induced mortality (Limpus et al., 1979) and eggs were buried with the bottom of the egg chamber 60 cm below the sand surface to control variation in nest temperatures resulting from differences in nest depth (Mrosovsky, 1994). Six clutches were included in the no shade treatment, 8 clutches in the least shade treatment, 7 clutches in the intermediate shade treatment, and 7 clutches in the most shade treatment. 2.3. Sand and nest temperature Sand temperatures (between 1 December 2009 and 5 February 2010) and nest temperatures were measured every 2 h using iButton® temperature data loggers (Dallas Semiconductor, Model DS1922 L) accurate to ± 0.5 °C, placed in the middle of egg clutches when the clutch was buried or in sand at 50 cm below the beach surface. Nest data loggers were recovered four days after the emergence of the first hatchlings. Nest incubation period was calculated as the number of days between nest relocation and hatching (detected as an abrupt change in nest temperature as hatchlings dig upward towards the surface (Booth and Freeman, 2006). For nest temperature calculations, if time of hatching was not obvious from the temperature trace, incubation period was estimated as three days prior to the emergence of the first hatchlings at the sand's surface (the mean time taken in nests that did show a clear hatching temperature signal: 3.1 ± 0.4 days, n = 19). Nest temperature was calculated as the mean of all temperatures recorded during the incubation period. When analyzing incubation period data, nests without an obvious time of hatching were excluded from the analysis. 2.4. Exposure of sand surface to solar radiation Fig. 1. Map showing location of the Mon Repos rookery. Maximum (unshaded) energy reaching the sand surface from solar radiation at Mon Repos beach for the months of December, January, February and March was calculated using SolarPathfinder© software (Assistant Version 4.1.31.0 www.solarpathfinder.com). This program uses weather station data, site aspect and geographic coordinates to predict global solar exposure (GSE the total solar energy received on a flat surface per day, MJ m−2 d−1; Bom, 2013). Effective solar radiation received by the sand surface for each shading treatment was calculated by timing shade progression across the floor of the hatchery area at 2 weekly intervals (Table 1), and combining this information with estimated energy inputs from SolarPathfinder© software. To estimate the GSE received at the sand's surface an average daily GSE value at the latitude of Mon Repos was obtained by first calculating the energy reaching the sand surface for each 30 minute period throughout the day. We assumed that when the beach became shaded by the casuarinas trees on the hind dune in the afternoon no further GSE reached the sand surface. We also assumed that the shade cloth permitted only 70% of radiation to reach the sand surface. Daily GSE received by the nest site was then calculated by first determining when the site of interest first became shaded (no shade 15:30 100% shade; least shade 11:00 70% shade, 15:30 100% shade; intermediate shade 7:30 70% shade, 15:30 A. Wood et al. / Journal of Experimental Marine Biology and Ecology 451 (2014) 105–114 107 Fig. 2. Diagram of experimental site illustrating the shaded hatchery, sun positions during the day, and shade progression throughout the day. 100% shade; most shade 6:30 70% shade, 15:30 100% shade) and then summing the 30 minute increments of GSE received for a particular position during the day: 2.6. Hatch and emergence success where USSEn = unshaded solar energy at time n when the nest is unshaded, USSEx = unshaded solar energy at time x when the nest is shaded, and 0.7 is the proportion of solar radiation energy passing through the shade cloth. During the relocation of each clutch, the entire clutch was counted and a sample of 10 eggs was weighed using an electronic balance to ± 0.1 g before being returned to the clutch. Four days after the emergence of the first hatchlings from a nest, the nest was excavated and nest emergence success (%) (100 × (number of eggs in clutch − (unhatched eggs + live hatchlings in nest + dead hatchlings in nest)) / number of eggs in clutch) and hatchling success (%) (100 × (number of eggs in clutch − unhatched eggs) / (number of eggs in clutch)) were calculated. 2.5. Estimation of hatchling sex ratios 2.7. Hatchling morphology To determine the effect of nest shading on hatchling sex ratios, we estimated the proportion of female hatchlings (%) for each clutch by calculating the mean nest temperature for the middle third of incubation and using this temperature in the sigmoid equation that best describes the relationship between incubation temperature and sex ratio for the South Pacific loggerhead turtle population (Chu et al., 2008): After 45 days of incubation, we placed plastic mesh fences (70 cm diameter × 15 cm high) above nests each night to capture emerging hatchlings. Hourly checks of enclosures were conducted throughout the night to record time of emergence. Once hatchlings emerged we collected a haphazard sample of 40–45 hatchlings from the first to emerge from each clutch for measurements. Each hatchling was weighed using an electronic balance (± 0.1 g) and carapace length and width measured using an electronic caliper (±0.1 mm). This data was then used to determine a carapace size index (carapace length (mm) × carapace width (mm)). GSE ¼ ðUSSE1 þ USSE2 þ USSE3…USSEnÞ þ ð0:7 ðUSSE1 þ USSE2 þ USSE3…USSExÞÞ % female ¼ 105:3481=ð1 þ expð−ðTemp−28:5102Þ=1:1379ÞÞ: Table 1 Shade progression times (made by direct observation to the nearest 5 min) for rows within the shade structure and the open beach at 2 weekly intervals throughout the study period. Row times are the time of day the entire row became shaded by the roof of the shade structure. Open beach nests were shaded in the afternoon by casuarinas trees located on a dune on the landward side of the study site. Date Western row shaded Middle row shaded Eastern row shaded Open beach shaded 28 Nov 2009 12 Dec 2009 26 Dec 2009 9 Jan 2010 23 Jan 2010 Mean to (to nearest 30 min) 6:15 6:20 6:25 6:35 6:40 6:30 7:15 7:20 7:25 7:30 7:35 7:30 10:50 10:55 11:00 11:10 11:10 11:00 15:30 15:35 15:40 15:50 15:50 15:30 2.8. Hatchling self-righting A hatchling's self-righting ability was assessed by placing the hatchling up-side-down on its carapace on a flat, smooth area of sand and measuring the time taken to self-right (Booth et al., 2013). If the hatchling failed to right itself within 10 s it was placed right-side-up for another 10 s, a period long enough for hatchlings to become reorientated and begin vigorous crawling behavior, and then turned on its carapace again. We repeated this procedure until the hatchling had successfully righted itself three times, or failed to right itself six times, whichever came first. Hatchlings were only given a maximum of six chances to self-right themselves. For quantifying self-righting ability two separate measures were assessed. The first, ‘self-righting time’ (s) 108 A. Wood et al. / Journal of Experimental Marine Biology and Ecology 451 (2014) 105–114 was calculated as the mean time for the successful self-righting events. Hatchlings that failed to self-right themselves in six attempts were excluded from this analysis because no self-righting time was obtained from these individuals. The second ‘righting propensity’ was a score from 0 to 6 in which 0 = no self-rightings in six attempts, 1 = one self-righting in six attempts, 2 = two self-rightings in 6 attempts, 3 = three self-rightings in six attempts, 4 = three self-rightings in five attempts, 5 = three self-rightings in four attempts, and 6 = three self-rightings in three attempts. Carapace surface temperature of each hatchling was then measured (accuracy ± 2 °C) using an infrared thermometer (Model QM 7222 Digitech) held between 3 and 5 cm above the carapace surface which resulted in a measurement area of approximately 0.8 cm2 in the middle of the carapace. 2.9. Crawling Directly following the self-righting measurement, each hatchling had its crawling speed measured over a 2.9 m raceway constructed from PVC guttering (10 cm × 10 cm) following the method of Read et al. (2012). The base of the raceway was covered with damp sand to simulate natural beach conditions. Both the position on the beach, and the angle of elevation (~15° from horizontal and faced down towards the sea) of the raceway remained constant throughout all measurements. Hatchlings were encouraged to crawl down the raceway by shining a dim light at the ocean end, and times were measured with a stopwatch and then converted into speed (m/s). 2.10. Statistical analysis The relationship between nest temperature and solar energy reaching the sand surface at the nest site was described using linear regression. To test for the effect of shading treatment on nest temperature, incubation duration, predicted sex ratio, hatch success and emergence success one-way ANOVA was used, with nest as the data unit and shade treatment a fixed factor. Sex ratio, hatch success and emergence success data were natural log transformed before analysis to meet the assumption of normality. To test for shading treatment effects on hatchling mass, size, selfrighting ability and crawling speed one-way ANOVA or ANCOVA (with egg mass as the covariate) were used with shade treatment a fixed factor and clutch a random factor nested within shading treatment. Individual hatchlings were used as the data unit in these tests. Differences in initial egg mass between clutches were tested for using one-way ANOVA. Qualitative data collected for righting propensity was log transformed (Natural log (righting propensity + 1)) to meet the assumption of normality and equal variance (Quinn and Keough, 2002). Nest means for hatchling mass, carapace size index, crawling speed and self righting ability were correlated with mean nest temperature. To adjust for possible confounding effects of egg mass on correlations with hatchling mass and carapace size index, nest means for hatchling mass and size index were adjusted using least square covariate means from ANCOVA before analysis was performed. Pearson correlation analysis was used to determine if there was a correlation between body temperature and self-righting ability and crawling speed of hatchlings. Where significant correlations were found, body temperature was included as a covariate in ANCOVAs involving that variable. Results are presented as means ± standard errors. All statistical analyses were performed using Statistica Ver 7.02 software and statistical significance was assumed at P b 0.05. mean value of 26.9 MJ m−2 d−1 measured at Bundaberg airport located 15 km away during this period in 2009–2010 (BOM, 2013). However because all nests were shaded by casuarinas trees from approximately 15:30 onwards (Table 1), nests outside the shade structure received an average of 22.9 MJ m−2 d−1 of GSE. Nests in the least shade treatment received 18.2 MJ m−2 d−1 of GSE, while nests in the intermediate and most shade treatments received 16.2 and 16.1 MJ m−2 d−1 respectively. One nest data logger from the least shade treatment and one from the intermediate shade treatment failed to initiate, however hatchling data from these two nests was included in shade treatment comparison tests. Nest temperature was positively correlated with GSE (Fig. 3). The range in nest temperatures was not substantial (29.6–32.2 °C), however the most shade treatment decreased solar energy exposure by 6.8 MJ m − 2 d− 1 and lowered mean nest temperature by 1.9 °C (Table 2). Both GSE and nest temperatures in the intermediate and most shade treatments were similar (Table 2). Shading had a significant effect on sand temperatures at nest depth with sand temperature being 1 °C warmer in the least shade treatment and 1.9 °C warmer in the no shade treatment compared to the most shade treatment (Fig. 4a, Table 2). The warmest sand temperatures were recorded during the final week of January (Fig. 4a), when sand temperatures in the no shade treatment reached 33.4 °C, and sand temperature in the most shade treatment reached 30.6 °C. GSE was negatively correlated with rainfall (r = − 0.63, P b 0.001, n = 58). Both sand and nest temperatures decreased as a consequence of rainfall and associated decrease in GSE (Fig. 4a,b,d). Sand and nest temperatures were similar for the first four weeks of incubation, but then nest temperature increased above sand temperature, and was 2.5 to 4 °C warmer than sand temperature by the time of hatching (Fig. 4c). 3.2. Hatchling sex ratios Mean nest temperature during the sex determining period differed significantly between shade treatments, resulting in significant variation in predicted hatchling sex ratios between shade treatments (Table 2). Those nests positioned in the no shade treatment were predicted to produce 95% females, while nests in the shaded hatchery were predicted to produce between 55% and 79% females depending upon how much shade they experienced (Table 2). 3.3. Hatching and nest emergence success Mean hatching success for all nests was 80.2 ± 1.4%, and mean emergence success was 78.2 ± 1.4% (Table 2). Hatching success and emergence success were not correlated with nest temperature (Hatch 3. Results 3.1. Nest temperature and solar radiation exposure The calculated mean GSE received at Mon Repos during December and January was 26.0 MJ m− 2 d− 1 which compares well with the Fig. 3. Plot of mean nest temperature against global solar exposure (GSE) for each shade treatment. Numbers associated with each data point indicate number of nests and error represent SE. Linear regression line: y = 25.9 + 0.255x, r2 = 0.99, P = 0.005, n = 4. A. Wood et al. / Journal of Experimental Marine Biology and Ecology 451 (2014) 105–114 109 Table 2 The shade exposure on sand and nest temperature, incubation period and hatchling attributes. ANOVA (sand temperature, nest temperature, proportion females (N = 28), hatch and emergence success (N = 22)) or ANCOVA in which initial egg mass (hatchling mass, hatchling carapace size index, (N = 1165)) or hatchling mass (righting time, righting propensity and crawling speed (N = 1165)) was the covariate, and nest a random factor nested within shade treatment (fixed factor) were used to compare dependent variables between rows. Least-squares means are reported for traits that were ANCOVA adjusted. Means ± SE. No shade (NS) 22.9 MJ m−2 d−1 Least shade (LS) 18.3 MJ m−2 d−1 Intermediate shade (IS) 16.2 MJ m−2 d−1 Most shade (MS) 16.1 MJ m−2 d−1 Probability statistic for comparisons across rows Tukey multiple comparison Mean sand temperature (°C) Mean nest temperature (°C) 30.2 ± 0.1 31.7 ± 0.1 29.4 ± 0.1 30.5 ± 0.1 Logger failed 30.1 ± 0.1 28.4 ± 0.1 29.8 ± 0.1 N/A F3,22 = 56.4, P b 0.001 Mean nest temp during sex determining period (°C) 31.0 ± 0.2 29.8 ± 0.2 29.0 ± 0.3 28.6 ± 0.2 F3,22 = 17.6, P b 0.001 Mean nest temp during final week of incubation (°C) Incubation period (days) Estimated proportion of female hatchlings (%) 34.9 ± 0.3 33.5 ± 0.2 33.6 ± 0.1 33.3 ± 0.1 F3,22 = 13.8, P b 0.001 N/A NS N LS = IS, IS = MS, LS N MS NS N LS N MS, LS = IS, IS = MS NS N LS = IS = MS 49.7 ± 0.9 95.0 ± 1.8 53.9 ± 0.5 79.2 ± 3.6 54.6 ± 0.5 61.1 ± 5.0 56.3 ± 1.2 54.6 ± 4.3 F3,22 = 13.5, P b 0.001 F3,22 = 13.0, P b 0.001 Hatch success (%) Emergence success (%) Egg mass (g) Hatchling mass (g) Carapace size index (mm2) 83.1 ± 7.1 74.6 ± 3.5 36.7 ± 1.5 19.5 ± 0.7 1484.4 ± 3.9 80.3 ± 2.8 78.0 ± 2.8 36.2 ± 1.1 19.6 ± 0.5 1544.5 ± 3.3 81.2 ± 2.4 77.7 ± 2.8 37.6 ± 0.9 20.3 ± 0.5 1564.1 ± 3.4 83.7 ± 1.3 81.5 ± 3.2 38.0 ± 1.0 20.9 ± 0.5 1596.5 ± 3.9 F3,19 F3,19 F3,24 F3,23 F3,23 Crawling speed (cm s−1) Self-righting propensity Self-righting time (s) 3.87 ± 0.07 5.12 ± 0.30 2.93 ± 0.40 5.39 ± 0.07 5.78 ± 0.06 2.31 ± 0.16 5.49 ± 0.12 5.81 ± 0.13 2.17 ± 0.29 5.68 ± 0.09 5.77 ± 0.06 2.51 ± 0.16 F3,23 = 3.7, P = 0.026 F3,23 = 5.1, P = 0.007 F3,23 = 3.0, P = 0.049 success r2 = 0.02, P = 0.51, n = 22; emergence success r2 = 0.04, P = 0.37, n = 22) and they were not affected by shade treatment (Table 2). Incubation period showed a strong negative correlation with nest temperature (r2 = 0.75, P b 0.001, n = 23), and varied across shade treatment (Table 2). 3.4. Hatchling mass and size Egg mass did not differ across shading treatments (Table 2), however there were significant differences in egg mass between clutches (F27,249 = 54.6, P b 0.001). Mean clutch egg mass was correlated with both mean clutch hatchling mass (r2 = 0.48, P b 0.001, n = 28) and mean clutch hatchling carapace size index (r2 = 0.55, P b 0.001, n = 28). Mean clutch hatchling mass was not correlated with nest temperature (r2 = 0.07, P = 0.202, n = 26), even when adjusted by the ANCOVA procedure for differences in initial egg mass (Fig. 5). Mean clutch hatchling carapace size index was negatively correlated with nest temperature (r2 = 0.22, P = 0.016, n = 26), and this correlation was slightly enhanced when carapace size was ANCOVA adjusted to account for differences in initial egg mass (Fig. 5). Hatchling mass (F27,1137 = 134.4, P b 0.001) and hatchling carapace size index (F27,1137 = 86.0, P b 0.001) both varied significantly between clutches and these differences persisted even when initial egg mass was used as a covariate (hatching mass: F27,1136 = 75.3, P b 0.001; carapace size index: F27,1136 = 49.7, P b 0.001). However, only carapace size index differed between shade treatments, with nests receiving less solar energy producing hatchlings with larger carapace size (Table 2). = = = = = 0.2, P 0.7, P 0.2, P 1.0, P 3.4, P = = = = = 0.90 0.55 0.88 0.42 0.035 NS b LS = IS b MS NS N IS = MS, LS N IS, NS = LS, LS = IS NS = LS = IS = MS NS = LS = IS = MS NS = LS = IS = MS NS = LS = IS = MS NS b LS b MS, LS = IS, IS = MS, NS b IS NS b LS = IS = MS NS b LS = IS = MS NS b LS = IS = MS nests receiving less solar energy producing hatchlings that crawled faster although post hoc analysis indicated that there was no difference within the shaded hatchery (Table 2). The same analysis but including nest temperature as a covariate indicated no effect of shade treatment on crawling speed (F3,21 = 1.15, P = 0.352) suggesting that nest temperature was the probable cause for differences in crawling speed. Neither self-righting propensity (r2 b 0.01, P = 0.657, n = 1164) nor self-righting time (r2 b 0.01, P = 0.516, n = 1164) were correlated with carapace surface temperature. Self-righting propensity was negatively and self-righting time positively correlated with nest temperature (Fig. 6b,c). Hatchling self-righting propensity was negatively correlated with self-righting time (r2 = 0.30, P b 0.001, n = 1164), positively correlated with crawling speed (r2 = 0.01, P b 0.001, n = 1164) and selfrighting time was negatively correlated with crawling speed (r2 = 0.003, P = 0.032, n = 1164). Hatchlings from nests in the no shade treatment which received the greatest solar energy had lower self-righting propensities and longer self-righting times than hatchlings from nests within the shaded hatchery (Table 2). The same analysis but including nest temperature as a covariate indicated no effect of shade treatment on self-righting propensity (F3,21 = 0.64, P = 0.597) or self-righting time (F3,21 = 1.54, P = 0.233) suggesting that nest temperature was the probable cause for differences in self-righting ability. 4. Discussion High nest temperatures in loggerhead turtle nests can result in smaller hatchlings having a decreased locomotion performance, and we found that shading is an effective way of decreasing nest temperatures. 3.5. Locomotion performance 4.1. Effect of shading on sand and nest temperatures Hatchling crawling speed was weakly and positively correlated with carapace surface temperature (r2 = 0.04, P b 0.001, n = 1165), so we included carapace surface as a covariate in further analysis involving crawling speed although the same statistical conclusion was reached when carapace temperature was not included as a covariate. Crawling speed was negatively correlated with nest temperature (Fig. 6a), and crawling speed varied significantly between shading treatments with Shading significantly lowered both sand and nest temperatures at Mon Repos (Table 2, Fig. 4). Because of the east-facing aspect of Mon repos beach, the amount of shading and thus the degree of sand and nest cooling varied according to the position that a clutch was placed within the shaded hatchery. In the maximally shaded western row nest temperatures were lowered by 1.9 °C, and 2.4 °C during the sex 110 A. Wood et al. / Journal of Experimental Marine Biology and Ecology 451 (2014) 105–114 Fig. 4. Plots of sand temperature, nest temperature, nest–sand temperature and metrological variables against date over the study. (a) Sand temperature, thick solid line = no shade treatment, dotted line = least shade treatment, thin solid line = most shade treatment. (b) Nest temperatures from nests laid on 1 December 2009, thick solid line = no shaded treatment, dotted line = least shade treatment, thin solid line = most shade treatment. (c) Nest temperature–sand temperature clearly showing an increase in nest temperature above sand temperature after four weeks of incubation. Thick solid line = no shaded treatment, dotted line = least shade treatment, thin solid line = most shade treatment. (d) Metrological variables obtained from Australian Bureau of Meteorology monitoring stations. Solid bars = rainfall data obtained from Bagarra located 2 km from the field site. Solid line = daily global solar exposure (GSE) readings obtained from Bundaberg airport located 15 km from the field site. Dashed line = minimum daily air temperature obtained from Bundaberg airport located 15 km from the field site. Dotted line = maximum daily air temperature obtained from Bundaberg airport located 15 km from the field site. determining period (Table 2). Smaller decreases in nest temperature were achieved by placing nests closer to the eastern edge of the shaded hatchery. If a 1.9 °C decrease was achieved by using 70% shade cloth, then by extrapolation, larger decreases could be achieved by using a heavier grade of shade cloth, such that 50% transmission could cause a 3 °C reduction, 25% transmission a 4.5 °C reduction, and 0% transmission a 6 °C reduction in nest temperature. Predictions of climate change indicate that mean air temperature will increase by up to 2.6 °C by 2050 (IPCC, 2007; Lough, 2007). Such a temperature rise will result in increased sea turtle incubation temperatures because sand and nest temperatures are influenced by air temperature (Chu et al., 2008; Maloney et al., 1990). As a consequence, if sea turtle rookeries are to remain in their current locations, at many rookeries nest temperatures will become unacceptably high and nest shading may be a management option for maintaining nest temperatures within a viable range (Morreale et al., 1982; Patino-Martinez et al., 2012; see below). However, sand temperatures at some sea turtle Fig. 5. (a) Adjusted hatchling mass (using ANCOVA least square means adjusted to an initial egg mass of 37.5 g) has a function of nest temperature. There was no significant correlation between nest temperature and hatchling mass (r2 = 0.07, P = 0.203, n = 26). (b) Adjusted carapace size index (using ANCOVA least square means adjusted to an initial egg mass of 37.5 g) has a function of nest temperature. Regression: y = 3236 − 55.4x, r2 = 0.23, P = 0.015, n = 26. rookeries may not be adversely affected by global warming, and nest temperature data taken over ten or more nesting seasons should be analyzed before implementing shading strategies because this is the minimum time needed to determine reliable rookery specific trends in hatchling sex ratios (Katselidis et al., 2012). If a shading strategy is used, then nest temperatures within the shade and outside the shade need to be monitored to insure that an appropriate mix of nest temperatures and thus male and female hatchlings is achieved. Nest temperature is the result of both sand temperature surrounding the nest and metabolic heat production of the clutch of developing embryos (Booth and Astill, 2001b; Booth and Freeman, 2006; Broderick et al., 2001; Sieg et al., 2011). Early in incubation embryos are tiny and the clutch's metabolic heat production is small and has a negligible effect on nest temperature. However, about half way through incubation the embryos begin their rapid growth phase of development and the clutch's metabolic heat production increases greatly causing a well documented increase in nest temperature during the latter half of incubation (Booth and Astill, 2001b; Booth and Freeman, 2006; Broderick et al., 2001; Chu et al., 2008, Fig. 4c). Nest shading does not abolish the rise in nest temperature caused by embryonic metabolic heat production (Fig. 4c). 4.2. Nest temperatures and hatchling sex ratio The feminization of sea turtle populations due to rising temperatures presented by climate change is predicted to occur at many tropical rookeries both within Australia (Fuentes et al., 2009, 2010a, 2010b) and globally (e.g. Hawkes et al., 2007, 2009; Morreale et al., 1982; Saba et al., 2012). At the Mon Repos rookery, which is located in the A. Wood et al. / Journal of Experimental Marine Biology and Ecology 451 (2014) 105–114 111 year and thus achieve the same result of maintaining viable nest temperatures without shade manipulation. 4.3. Nest temperatures and hatch and nest emergence success Shading lowered nest temperatures throughout incubation including the last two weeks when temperatures were at their highest, however neither hatch success nor nest emergence success varied significantly over the range of temperatures experienced in our study. Early in incubation sea turtle embryos are intolerant to high temperatures, with temperatures above 34 °C being fatal (Ackerman, 1997). The embryos become more tolerant of high temperatures later in development, and many embryos hatch successfully after being exposed to temperatures between 34 and 36 °C for several days during the last two weeks of incubation (Booth et al., 2013; Carthy et al., 2003; Maulany et al., 2012a). However the hatching success of olive ridley (Lepidochelys olivacea) eggs decrease as nest temperature exceeds 34 °C for more than 3 days in a row over the last two weeks of incubation (Maulany et al., 2012a) probably because embryos incubating at temperatures approaching their upper thermal limit have a higher frequency of developmental abnormalities (Deeming and Ferguson, 1991; Reid et al., 2009). In the current study even in the hottest nests, nest temperature only increased above 34 °C for 2–3 days immediately before hatching, a length of time not long enough to have a significant effect on hatching and emergence success. Both hatching success (82%) and nest emergence success (78%) were a little lower than those previously reported for the Mon Repos rookery (85% and 80% respectively, Chu et al., 2008), although a lower nest emergence success (64%) was recorded in the particularly hot 2005–2006 nesting season presumably due to the high nest temperatures experienced at the end of incubation (Chu et al., 2008). If nest temperatures rise in parallel with the predicted 2.6 °C rise in global temperatures by 2050 (IPCC, 2007; Lough, 2007), then nest emergence success at the Mon repos rookery will dramatically decrease unless strategies such as shade provision that lower nest temperatures are introduced or turtles switch from summer nesting to winter nesting. Fig. 6. (a) Relationship between crawling speed (adjusted to a carapace surface temperature of 26.5 °C by ANCOVA) and nest temperature. Regression: y = 36.0 − 1.01x, r2 = 0.39, P b 0.001, n = 26. (b) Relationship between self-righting propensity and nest temperature. Regression: y = 18.3 − 0.41x, r 2 = 0.41, P b 0.001, n = 26. (c) Relationship between self-righting time and nest temperature. Regression: y = 0.45x − 11.1, r2 = 0.23, P = 0.013, n = 26. subtropics, measurements of nest temperatures are generally higher than the pivotal temperature for the east Australian loggerhead turtle stock (Chu et al., 2008; Limpus, 2008). A skewed female sex ratio is consequently common at this beach (Chu et al., 2008; Read et al., 2012) and will likely become more extreme in the future with the predicted global temperature rise. A shift in nest temperature of as little as 1 °C can dramatically alter sex ratios (Janzen, 1994), and, in turn, impact population dynamics and viability (Hulin et al., 2009; Witt et al., 2010). In the current study shading lowered nest temperature by between 1.2 °C and 2.4 °C during the sex determining period and decreased the predicted female bias in loggerhead turtle hatchlings from 95% to 55% for clutches placed in the most shaded region of the hatchery. If a heavier shade cloth was used in the hatchery the proportion of females could be reduced even further. Hence if global warming continues and active management of incubating clutches becomes necessary, it would be possible to produce a wide range of sex ratios from greater than 90% females to greater than 90% males by placing clutches into shaded hatcheries with different grades of shade cloth. However, a decision on whether or not to instigate a shading management strategy should only be made after careful evaluation of rookery specific nest temperature data over at least ten nesting seasons (see for example Katselidis et al., 2012). Also in some rookeries, given enough time, the turtles themselves may adjust their timing of nesting to a cooler time of the 4.4. Nest temperatures and hatchling size There was an inverse correlation between nest temperature and hatching carapace size; shaded, cooler nests produced hatchlings with larger carapaces. This inverse correlation has been reported for sea turtle hatchlings previously (Booth et al., 2013; Ischer et al., 2009; Maulany et al., 2012b; Reece et al., 2002; Read et al., 2012; Stokes et al., 2006). Larger hatchlings are more likely to be ignored by gape limited predators (Bustard, 1972; Janzen et al., 2000a) and to escape other predators by being able to swim and crawl faster (Janzen, 1993; Janzen et al., 2000a, 2000b; Miller, 1993; Wren et al., 1998). Hatchling size has also been found to positively influence swimming thrust in both hatchling loggerhead (Chu et al., 2008), and green turtles (Chelonia mydas) (Burgess et al., 2006; Ischer et al., 2009). It is therefore likely that in the present study the larger hatchlings were better swimmers. Upon entering the ocean, the highest rates of predation on hatchling turtles are in the near shore area (Gyuris, 1994), so larger hatchlings that are stronger swimmers will quickly move offshore and therefore have a greater chance of survival. Despite the influence of nest temperature on hatchling size, nest temperature had no effect on hatchling mass. This supports findings from previous studies on green (Booth et al., 2013; Ischer et al., 2009), olive ridley (Maulany et al., 2012b) and loggerhead (Reece et al., 2002; Read et al., 2012; Stokes et al., 2006) turtle hatchlings emerging from natural nests, where size but not mass was influenced by nest temperature. Artificial incubation experiments indicate that hatchling green turtles from cooler incubation temperatures have similar masses to those incubated at higher temperatures but have larger carapace sizes and smaller residual yolks, as more yolk material is converted into tissue 112 A. Wood et al. / Journal of Experimental Marine Biology and Ecology 451 (2014) 105–114 during embryonic development at cooler temperatures (Booth and Astill, 2001a; Booth et al., 2004; Burgess et al., 2006). It is therefore likely that in the current study larger hatchlings from cooler nests had smaller yolk reserves. Differences in residual yolk may influence hatchling fitness as hatchlings with large residual yolk masses have greater energy reserves (Speake et al., 2003; Thompson et al., 2001) and consequently have increased survivorship in resource poor environments (Reid et al., 2009). High metabolic demand during emergence and dispersal from the nest means hatchlings with small yolk masses will need to feed sooner (Ischer et al., 2009; Reece et al., 2002; Wyneken and Salmon, 1992). The ecological significance of tradeoffs between body size and residual yolk mass in hatchling sea turtles remains unexplored. 4.5. Nest temperatures and hatchling locomotion performance This study found that loggerhead hatchlings emerging from cooler nests had greater locomotion performance as indicated by selfrighting ability and crawling speed. Similar findings have been reported for green (Booth et al., 2013; Ischer et al., 2009) olive ridley (Maulany et al., 2012b) and loggerhead (Read et al., 2012) turtle hatchlings so this relationship appears to be a common phenomenon across sea turtle species. Self-righting ability and crawling speed influence the length of time a hatchling spends on the beach (Paitz et al., 2009). In terrestrial environments, sea turtle locomotion is awkward and inefficient (Davenport, 1997), as a result hatchlings may overturn or become trapped by beach debris (Davenport, 1997; Steyermark and Spotila, 2001). If immobilized a hatchling experiences an increased risk of desiccation, overheating from sun exposure, and predation (Davenport, 1997; Steyermark and Spotila, 2001). This exposure may influence an individual's survival during the early life stage (Dial, 1987; Janzen et al., 2007; Stancyk et al., 1979). Hence if sand temperatures increase with global warming as predicted, any strategy such as nest shading that decreases nest temperatures so that nest temperatures remain within an optimal range will increase the chance of sea turtle hatchlings surviving the transit from nest to sea because hatchlings from optimal temperatures are better and faster at self-righting and faster crawlers. 4.6. Shade as a rookery management strategy Clearly artificial shade structures are effective in reducing sea turtle nest temperature (Morreale et al., 1982; Patino-Martinez et al., 2012; this study) and are a viable management option in the face of rising sand temperatures at rookeries, if these rookeries are to remain at their current locations (but see caveat above about the need for direct monitoring of nest temperatures to insure that conservation management strategies are achieved), and sea turtles are unable to change the time of year that they nest. There are several advantages associated with artificial shade structures including the ability to protect nests relocated into shade structures from human and non-human predation, and the ability to manipulate nest temperature by using a combination of clutch location within a shaded hatchery (if it has an east or west facing aspect) and varying shade cloth covering to allow more or less GSE into the hatchery. In our study a predicted 6 °C decrease in nest temperature might be achievable through total shading and this would result in production of all male hatchlings. For long-term rookery management manipulating nest temperatures around the pivotal temperature is probably desirable because this guarantees the production of both male and female hatchlings and this temperature also appears to produce hatchlings with optimal locomotion performance. As in the current study, artificial nest shading also lowered nest temperature, and increased male hatchling production without compromising the fitness or hatching success at a Caribbean leatherback sea turtle rookery (Patino-Martinez et al., 2012). However there are draw backs to relocating clutches into small managed areas (Mortimer, 1999) including the high cost of collecting and relocating clutches, and the fact that incubating clutches in close proximity to each other can increase nest temperatures (Maulany et al., 2012a; Mortimer, 1999) and that moving eggs into hatcheries often results in decreased hatching success (Mortimer, 1999). Hence when deciding whether or not to move clutches of eggs into hatcheries to be incubated, the nest emergence success of nests left in natural nests and those in the hatchery need to be compared, and only if the nest emergence success is greater in the hatchery should the practice of moving eggs into the hatchery become routine. On east or west facing beaches such as the Mon Repos rookery, another less actively managed way of manipulating nest temperature would be to plant trees that throw a shadow onto the nesting areas for some part of the day. Tree shade has been noted to decrease nest temperatures previously (Spotila et al., 1987). This method has the advantage that it is relatively cheap and aesthetically pleasing when compared with artificial shade structures, and does not require intense on-going management. The higher the tree and or the closer to the nesting area the greater the proportion of the day nests will be shaded. However trees located too close to nests would be detrimental because their roots will penetrate the nesting area and decrease nesting success either via nesting females abandoning nesting attempts because they hit roots (pers. obs.) or through roots penetrating the nest and destroying eggs after the nest is constructed (Leslie et al., 1996) or through decreasing water availability to embryos. Hence further studies are needed to find the most appropriate species of shade tree, preferable indigenous to the area of the rookery, that can provide appropriate shade but whose roots do not adversely affect nests. In rookery regions where trees do not grow naturally on dunes behind beaches, serious consideration about other possible undesirable consequences of tree planting need to be considered before tree planting is instigated. To explore how tree shade might be used to moderate nest temperatures at the Mon Repos rookery a model that predicts nest temperature as a function of the time of day that total shade reaches a nest was developed (Fig. 7). This model uses the relationship between GSE and nest temperature (Fig. 3) and the proportion of daily GSE received during each half hour period of daylight over the peak nesting period (December–March) derived using Solar pathfinder software. Three scenarios were examined: nests constructed in early December 2009, nests constructed in early February 2010, and a climate warming scenario based on a 2 °C increase in temperature above the mean of that recorded in 2009–2010. According to this model, under the 2009–2010 nesting season conditions, nests would need to receive total shading at 15:00 to maintain a mean nest temperature of 32 °C, and under the 2 °C climate warming scenario these nests would need to be totally shaded by 13:00 to maintain a mean nest temperature of 32 °C. These Fig. 7. A nest temperature prediction model for the Mon Repos rookery showing predicted mean nest temperatures under current climatic conditions (thick lines), and with a 2 °C increase in temperature (thin lines) as a function of afternoon shading offering 100% protection from GSE. Solid lines are nests constructed in early December and dashed lines nests constructed in early February. A. Wood et al. / Journal of Experimental Marine Biology and Ecology 451 (2014) 105–114 shading scenarios would also limit the maximum nest temperature during the last week of incubation to around 34 °C thus insuring high nest emergence success. During the 2009–2010 nesting season tree shade reached the high nest density areas of Mon Repos rookery at approximately 15:30 so planting taller growing trees that throw shade onto the nesting area earlier in the day at different intervals along the beach is a management strategy that could be used to produce a relatively wide range of nest temperatures. This strategy could be used at other east or west facing rookeries around the world to counter an increase in nest temperatures, although it is important to note that sand and nest temperature is dependent on the interaction of many variables, including sand color, beach slope and distance from the high water mark (Fuentes et al., 2010a, 2010b; Hays et al., 2001). Sea turtles have demonstrated a remarkable capacity to survive through periods of climatic change over the millions of years they have existed, adapting to changes in temperature and sea level by shifting nesting grounds, foraging distributions and migration routes (Hamann et al., 2007; Hawkes et al., 2009; Limpus, 2008). However the rate of temperature increase is much faster now than in the past (IPCC, 2007) and it remains to be seen if sea turtles can shift the time of year that they nest to winter or shift their nesting grounds to cooler beaches at higher latitudes, and indeed if suitable nesting beaches can be found given that many beaches are now severely altered by human activities. If suitable nesting beaches cannot be successfully utilized and they are unable to change the timing of nesting quickly enough, then the remaining management strategy is to keep rookeries in their current locations but to use active strategies such as shading to ensure that nest temperatures remain within the viable embryonic development range despite increases in air temperatures. The same arguments used here for sea turtles would also apply to many other oviparous reptile species including freshwater turtles, land tortoises, snakes, lizards and crocodilians because incubation temperature has been demonstrated to influence hatching success and hatchling phenotype in all species so far examined (Deeming and Ferguson, 1991) and many of these species also have temperature dependent sex determination. However, from a conservation management point of view, shading strategies would be difficult to implement in many species because they do not aggregate their nesting activity into relatively small areas. In species that are dispersive nesters, nest location and management would require a great deal of effort and resources and therefore might not be practicable. Acknowledgements We thank management and volunteers in the Queensland turtle research program at Mon Repos for their assistance throughout our study. All experimental procedures were approved by a University of Queensland animal ethics committee approval number SBS/405/09/ URG. None of the authors have a conflict of interest in the publication of this research. [RH] References Ackerman, R.A., 1997. The nest environment and the embryonic development of sea turtles. In: Lutz, P.L., Musick, J.A., Wyneken, J. (Eds.), The Biology of Sea Turtles. CRC Press, Boca Raton, pp. 83–106. Ackerman, R.A., Lott, D.B., 2004. Thermal, hydric and respiratory climate of nests. In: Deeming, D.C. (Ed.), Reptilian Incubation: Environment, Evolution and Behaviour. Nottingham University Press, Nottingham, pp. 15–44. Bom, 2013. Commonwealth of Australia Bureau of Meteorology. http://www.bom. gov.au/climate/austmaps/solar-radiation-glossary.shtml (globalexposure Site visited 13 June 2013). Booth, D.T., Astill, K., 2001a. Incubation temperature, energy expenditure and hatchling size in the green turtle (Chelonia mydas), a species with temperature-sensitive sex determination. Aust. J. Zool. 49, 389–396. Booth, D.T., Astill, K., 2001b. Temperature variation within and between nests of the green sea turtle, Chelonia mydas (Chelonia: Cheloniidae) on Heron Island, Great Barrier Reef. Aust. J. Zool. 49, 71–84. Booth, D.T., Evans, A., 2011. Warm water and cool nests are best. how global warming might influence hatchling green turtle swimming performance. PLoS ONE 6 (8), e23262. 113 Booth, D.T., Freeman, C., 2006. Sand and nest temperatures and an estimate of hatchling sex ratio from the Heron Island green turtle (Chelonia mydas) rookery, Southern Great Barrier Reef. Coral Reefs 25, 629–633. Booth, D.T., Burgess, E.A., McCosker, J., Lanyon, J.M., 2004. The influence of incubation temperature on post-hatching fitness characteristics of turtles. Int. Congr. Ser. 1275, 226–233. Booth, D.T., Feeney, R., Shibata, Y., 2013. Nest and maternal origin can influence morphology and locomotor performance of hatchling green turtles (Chelonia mydas) incubated in field nests. Mar. Biol. 160, 127–137. Broderick, A.C., Godley, B.J., Hays, G.C., 2001. Metabolic heating and the prediction of sex ratios for green turtles (Chelonia mydas). Physiol. Biochem. Zool. 74, 161–170. Burgess, E., Booth, D.T., Lanyon, J.M., 2006. Swimming performance of hatchling green turtles is affected by incubation temperature. Coral Reefs 25, 341–349. Bustard, R., 1972. Sea Turtles, Natural History and Conservation. Collins, London. Carthy, R.R., Foley, A.M., Matsuzawa, Y., 2003. Incubation environment of loggerhead turtle nests: effects on hatching success and hatchling characteristics. In: Bolten, A.B., Witherington, B.E. (Eds.), Loggerhead Sea Turtles. Smithsonian Books, Washington, DC, pp. 144–153. Chaloupka, M., Limpus, C.J., 2001. Trends in the abundance of sea turtles resident in southern Great Barrier Reef waters. Biol. Conserv. 102, 235–249. Chaloupka, M., Kamezaki, N., Limpus, C.J., 2008. Is climate change affecting the population dynamics of the endangered Pacific loggerhead sea turtle? J. Exp. Mar. Biol. Ecol. 356, 136–143. Chu, C.T., Booth, D.T., Limpus, C.J., 2008. Estimating the sex ratio of loggerhead turtle hatchlings at Mon Repos rookery (Australia) from nest temperatures. Aust. J. Zool. 56, 57–64. Davenport, J., 1997. Temperature and the life-history strategies of sea turtles. J. Therm. Biol. 22, 479–488. Deeming, D.C., Ferguson, M.W.J., 1991. Physiological effects of incubation temperature on embryonic development in reptiles and birds. In: Deeming, D.C., Ferguson, M.W.J. (Eds.), Egg Incubation: Its Effects on Embryonic Development in Birds and Reptiles. Cambridge University Press, Cambridge, pp. 147–171. Dial, B.E., 1987. Energetics and performance during nest emergence and the hatchling frenzy in loggerhead sea turtles (Caretta caretta). Herpetologica 43, 307–315. Fish, M.R., Cote, I.M., Gill, J.A., Jones, A.P., Renshoff, S., Watkinson, A.R., 2005. Predicting the impact of sea-level rise on Caribbean sea turtle nesting habitat. Conserv. Biol. 19, 482–491. Fuentes, M.M.P.B., Maynard, J.A., Guinea, M., Bell, I.P., Werdell, P.J., Hamann, M., 2009. Proxy indicators of sand temperature help project impacts of global warming on sea turtles. Endanger. Species Res. 9, 33–40. Fuentes, M.M.P.B., Limpus, C.J., Hamann, M., Dawson, J., 2010a. Potential impacts of projected sea-level rise on sea turtle rookeries. Aquat. Conserv. 20, 132–138. Fuentes, M.M.P.B., Hamann, M., Limpus, C.J., 2010b. Past, current and future thermal profiles of green turtle nesting grounds: implications for climate change. J. Exp. Mar. Biol. Ecol. 383, 56–64. Fuentes, M.M.P.B., Limpus, C.J., Hamann, M., 2011. Vulnerability of sea turtle nesting grounds to climate change. Glob. Chang. Biol. 17, 140–153. Fuentes, M.M.P.B., Fish, M.R., Maynard, J.A., 2012. Management strategies to mitigate the impacts of climate change on sea turtle's terrestrial reproductive phase. Mitig. Adapt. Strateg. Glob. Chang. 17, 51–56. Glen, F., Mrosovsky, N., 2004. Antigua revisited: the impact of climate change on sand and nest temperatures at a hawksbill turtle (Eretmochelys imbricata) nesting beach. Glob. Chang. Biol. 10, 2036–2045. Gyuris, E., 1994. The rate of predation by fishes on hatchling of the green turtle (Chelonia mydas). Coral Reefs 13, 137–144. Hamann, M., Limpus, C.J., Read, M.A., 2007. Vulnerability of marine reptiles in the Great Barrier Reef to climate change. In: Johnson, J.E., Marshall, P. (Eds.), Climate Change and the Great Barrier Reef. Great Barrier Reef Marine Park Authority and Australian Greenhouse Office, Australia, pp. 465–496. Harley, C.D.G., Hughes, A.R., Hultgren, K.M., 2006. The impacts of climate change in coastal marine systems. Ecol. Lett. 9, 228–241. Hawkes, L.A., Broderick, A.C., Godfrey, M.H., Godley, B.J., 2007. Investigating the potential impacts of climate change on a marine turtle population. Glob. Chang. Biol. 13, 923–932. Hawkes, L.A., Broderick, A.C., Godfrey, M.H., Godley, B.J., 2009. Climate change and marine turtles. Endanger. Species Res. 7, 137–154. Hays, G.C., Ashworth, J.S., Barnsley, M.J., Broderick, A.C., Emery, D.R., Godley, B.J., Henwood, A., Jones, E.L., 2001. The importance of sand albedo for the thermal conditions on sea turtle nesting beaches. Oikos 93, 87–94. Hays, G.C., Broderick, A.C., Glen, F., Godley, B.J., 2003. Climate change and sea turtles: a 150-year reconstruction of incubation temperatures at a major marine turtle rookery. Glob. Chang. Biol. 9, 642–646. Hulin, V., Delmas, V., Girondot, M., Godfrey, M.H., Guillon, J.M., 2009. Temperaturedependent sex determination and global change: are some species at greater risk? Oecologia 160, 493–506. IPCC, 2007. Climate change 2007: the scientific basis. In: Solomon, S., Qin, D., Manning, M., Chen, Z., Marqui, M., Averyt, K.B., Tignor, M., Miller, H.L. (Eds.), Contributions of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change: “The Physical Science Basis”. Cambridge University Press, Cambridge, pp. 1–18. Ischer, T., Ireland, K., Booth, D.T., 2009. Locomotion performance of green turtle hatchlings from the Heron Island Rookery, Great Barrier Reef. Mar. Biol. 156, 1399–1409. IUCN, 2009. IUCN Red List of Threatened Species. International Union for Conservation of Nature and Natural Resources. Janzen, F.J., 1993. The influence of incubation temperature and family on eggs, embryos, and hatchlings of the smooth softshell turtle (Apalone mutica). Physiol. Zool. 66, 349–373. 114 A. Wood et al. / Journal of Experimental Marine Biology and Ecology 451 (2014) 105–114 Janzen, F.J., 1994. Climate change and temperature dependent sex determination in reptiles. Proc. Natl. Acad. Sci. U. S. A. 91, 7487–7490. Janzen, F.J., Tucker, J.F., Paukstis, G.L., 2000a. Experimental analysis of an early life-history stage: avian predation selects for larger body size of hatchling turtles. J. Evol. Biol. 13, 947–954. Janzen, F.J., Tucker, J.F., Paukstis, G.L., 2000b. Experimental analysis of an early life-history stage: selection on size of hatchling turtles. Ecology 81, 2290–2304. Janzen, F.J., Tucker, J.F., Paukstis, G.L., 2007. Experimental analysis of an early life-history stage: direct or indirect selection on body size of hatchling turtles? Funct. Ecol. 21, 162–170. Katselidis, K.A., Schofield, G., Stamou, G., Dimopoulos, P., Pantis, J.D., 2012. Females first? Past, present and future variability in offspring sex ratio at a temperate sea turtle breeding area. Anim. Conserv. 15, 508–518. Kostas, A., Katselidis, Schofield G., Stamou, G., Dimopoulos, P., Pantis, J.D., 2014. Employing sea-level rise scenarios to strategically select sea turtle nesting habitat important for long-term management at a temperate breeding area. Journal of Experimental Marine Biology and Ecology 450, 47–54. Leslie, A.J., Penick, D.N., Spotila, J.R., Paladino, F.V., 1996. Leatherback turtle, Dermochelys coriacea, nesting and nest success at Tortuguero, Costa Rica in 1990–1991. Chelonian Conserv. Biol. 2, 159–168. Limpus, C.J., 2008. A biological review of Australian marine turtles. Loggerhead Turtle Caretta caretta.Queensland Government Environmental Protection Agency, Brisbane. Limpus, C.J., Limpus, D.J., 2003. Loggerhead turtles in the equatorial and southern Pacific Ocean: a species in decline. In: Bolten, A.B., Witherington, B.E. (Eds.), Loggerhead Sea Turtles. Smithsonian Institution Press, Washington DC., pp. 199–209. Limpus, C.J., Baker, V., Miller, J.D., 1979. Movement induced mortality of loggerhead eggs. Herpetologica 35, 335–338. Lough, J., 2007. Climate and climate change on the Great Barrier Reef. In: Johnson, J.E., Marshall, P. (Eds.), Climate Change and the Great Barrier Reef. Great Barrier Reef Marine Park Authority and Australian Greenhouse Office, Australia, pp. 15–50. Maloney, J.E., Dariansmith, C., Takahashi, Y., Limpus, C.J., 1990. The environment for development of the embryonic loggerhead turtle (Caretta caretta) in Queensland. Copeia 1990, 378–387. Maulany, R.I., Booth, D.T., Baxter, G.S., 2012a. Emergence success and sex ratio of natural and relocated nests of olive ridley turtles from Alas Purwo National Park, East Java, Indonesia. Copeia 738–747. Maulany, R.I., Booth, D.T., Baxter, G.S., 2012b. The effect of incubation temperature on hatchling quality in the olive ridley turtle, Lepidochelys olivacea, from Alas Purwo National Park, East Java, Indonesia: implications for hatchery management. Mar. Biol. 159, 2651–2661. Mazaris, A.D., Matsinos, G., Pantis, J.D., 2009. Evaluating the impacts of coastal squeeze on sea turtle nesting. Ocean Coast. Manag. 52, 139–145. Miller, K., 1993. The improved performance of snapping turtles (Chelydra serpentina) hatched from eggs incubated on a wet substrate persists through the neonatal period. J. Herpetol. 27, 228–233. Morreale, S.J., Ruiz, G.J., Spotila, J.R., Standora, E.A., 1982. Temperature-dependent sex determination—current practices threaten conservation of sea turtles. Science 216, 1245–1247. Mortimer, J.A., 1999. Reducing threats to eggs and hatchlings: hatcheries. In: Eckert, K.L., Bjorndal, K.A., Abreu-Grobois, F.A., Donelly, M. (Eds.), Research and Management Techniques for the Conservation of Sea Turtles. IUCN/SSC Marine Turtle Specialist Group Publication No. 4, pp. 175–178. Mrosovsky, N., 1994. Sex ratios of sea turtles. J. Exp. Zool. 270, 16–27. Paitz, R.T., Gould, A.C., Holgersson, M.C.N., Bowden, R.M., 2009. Temperature, phenotype, and the evolution of temperature dependent sex determination: how do natural incubations compare to laboratory incubations? J. Exp. Zool. 314B, 86–93. Patino-Martinez, J., Marco, A., Quinones, L., Hawkes, L., 2012. A potential tool to mitigate the impacts of climate change to the Caribbean leatherback sea turtle. Glob. Chang. Biol. 18, 401–411. Poloczanska, E.S., Babcock, R.C., Butler, A., 2007. Climate change and Australian marine life. Oceanogr. Mar. Biol. 45, 407–478. Quinn, G.P., Keough, M.J., 2002. Experimental Design and Data Analysis for Biologists. Cambridge University Press, Cambridge. Read, T., Booth, D.T., Limpus, C.J., 2012. Effect of nest temperature on hatchling phenotype of loggerhead turtles (Caretta caretta) from two South Pacific rookeries, Mon Repos and La Roche Percée. Aust. J. Zool. 160, 402–411. Reece, S.E., Broderick, A.C., Godley, B.J., West, S.A., 2002. The effects of incubation environment, sex and pedigree on the hatchling phenotype in a natural population of loggerhead turtles. Evol. Ecol. Res. 4, 737–748. Reid, K.A., Margaritoulis, D., Speakman, J.R., 2009. Incubation temperature and energy expenditure during development in loggerhead sea turtle embryos. J. Exp. Mar. Biol. Ecol. 378, 62–68. Root, T.L., Price, J.T., Hall, K.R., Schneider, S.H., Rosenzweig, C., Pounds, J.A., 2003. Fingerprints of global warming on wild animals and plants. Nature 421, 57–60. Saba, V.S., Stock, C.A., Spotila, J.R., Paladino, F.V., Tomillo, P.S., 2012. Projected response of an endangered marine turtle population to climate change. Nat. Clim. Chang. 2, 814–820. Sieg, A.E., Binckley, C.A., Wallace, B.P., Tomillo, S.P., Reina, R.D., Paladino, F.V., Spotila, J.R., 2011. Sex ratios of leatherback turtles: hatchery translocation decreases metabolic heating and female bias. Endanger. Species Res. 15, 195–204. Speake, B.K., Thompson, M.B., Thacker, F.E., Bedford, G.S., 2003. Distribution of lipids from the yolk to the tissues during development of the water python (Liasis fuscus). J. Comp. Physiol. 173B, 541–547. Spotila, J.R., Standora, E.A., Morreale, S.J., Ruiz, G.J., 1987. Temperature-dependent sex determination in the green turtle (Chelonia mydas)—effects on the sex-ratio on a natural beach. Herpetologica 43, 74–81. Stancyk, S.E., Talbert, O.R., Miller, A.B., 1979. Estimation of loggerhead turtle nesting activity in South Carolina by aerial surveys. Am. Zool. 19, 954. Standora, E.A., Spotila, J.R., 1985. Temperature-dependent sex determination in sea turtles. Copeia 1985, 711–722. Steyermark, A.C., Spotila, J.R., 2001. Effects of maternal identity and incubation temperature on hatching and hatchling morphology in snapping turtles, Chelydra serpentina. Copeia 2001, 129–135. Stokes, L., Wyneken, J., Crowder, L.B., Marsh, J., 2006. The influence of temporal and spatial origin on size and early growth rates in captive loggerhead sea turtles (Caretta caretta) in the United States. Herpetol. Conserv. Biol. 1, 71–80. Thompson, M.B., Speake, B.K., Russell, K.J., McCartney, R.J., 2001. Utilization of lipids, protein, ions and energy during embryonic development of Australian oviparous skinks in the genus Lampropholis. Comp. Biochem. Physiol. 129A, 313–326. Tomillo, P.S., Saba, V.S., Blanco, G.S., Stock, C.A., Paladino, F.V., Spotila, J.R., 2012. Climate driven egg and hatchling mortality threatens survival of eastern Pacific leatherback turtles. PLoS ONE 7 (5), e37602. Valverde, R.A., Wingard, S., Gómez, F., Tordoir, M.T., Orrego, C.M., 2010. Field lethal incubation temperature of olive ridley sea turtle Lepidochelys olivacea embryos at a mass nesting rookery. Endanger. Species Res. 12, 77–86. Witt, M.J., Hawkes, L.A., Godfrey, M.H., Godley, B.J., Broderick, A.C., 2010. Predicting the impacts of climate change on a globally distributed species: the case of the loggerhead turtle. J. Exp. Biol. 213, 901–911. Wren, K., Claussen, D.L., Kurz, M., 1998. The effects of body size and extrinsic mass on the locomotion of the Ornate box turtle, Terrapene ornata. J. Herpetol. 32, 144–150. Wyneken, J., Salmon, M., 1992. Frenzy and postfrenzy swimming activity in loggerhead, green, and leatherback hatchling sea turtles. Copeia 1992, 478–484.