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Journal of Experimental Marine Biology and Ecology 451 (2014) 105–114
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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
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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)
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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]
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