Received: 5 March 2017
|
Accepted: 13 April 2017
DOI: 10.1111/gcb.13765
PRIMARY RESEARCH ARTICLE
Climate change and temperature-linked hatchling mortality at a globally important sea turtle nesting site €1,2 Jacques-Olivier Laloe
| Jacquie Cozens3 | Berta Renom3,4 | Albert Taxonera3,4 |
Graeme C. Hays2 1
Department of Biosciences, Swansea University, Swansea, UK 2
Centre for Integrative Ecology, School of Life and Environmental Sciences, Deakin University, Warrnambool, VIC, Australia 3
SOS Tartarugas, Santa Maria, Sal, Cape Verde 4
Project Biodiversity, Santa Maria, Sal, Cape Verde
Abstract The study of temperature-dependent sex determination (TSD) in vertebrates has attracted major scientific interest. Recently, concerns for species with TSD in a warming world have increased because imbalanced sex ratios could potentially threaten population viability. In contrast, relatively little attention has been given to the direct effects of increased temperatures on successful embryonic development. Using 6603 days of sand temperature data recorded across 6 years at a globally
Correspondence €, Centre for Integrative Jacques-Olivier Laloe Ecology, School of Life and Environmental Sciences, Deakin University, Warrnambool, VIC, Australia. Email:
[email protected] Funding information Centre for Integrative Ecology, Deakin University; Alasdair Downes Marine Conservation Fund; Society for Experimental Biology
important loggerhead sea turtle rookery—the Cape Verde Islands—we show the effects of warming incubation temperatures on the survival of hatchlings in nests. Incorporating published data (n = 110 data points for three species across 12 sites globally), we show the generality of relationships between hatchling mortality and incubation temperature and hence the broad applicability of our findings to sea turtles in general. We use a mechanistic approach supplemented by empirical data to consider the linked effects of warming temperatures on hatchling output and on sex ratios for these species that exhibit TSD. Our results show that higher temperatures increase the natural growth rate of the population as more females are produced. As a result, we project that numbers of nests at this globally important site will increase by approximately 30% by the year 2100. However, as incubation temperatures near lethal levels, the natural growth rate of the population decreases and the long-term survival of this turtle population is threatened. Our results highlight concerns for species with TSD in a warming world and underline the need for research to extend from a focus on temperature-dependent sex determination to a focus on temperature-linked hatchling mortalities. KEYWORDS
adaptive significance, conservation, ectotherm, endangered species, environmental sex determination, ESD, evolutionary biology, extinction, reptile, skewed sex ratios
1 | INTRODUCTION
the implications TSD has on sex ratio balance and population viability, the study of TSD quickly became an important topic in evolu-
The discovery of temperature-dependent sex determination (TSD) in
tionary ecology.
a vertebrate species is credited to the work of Charnier (1966). TSD
In the context of climate change, there are concerns that popula-
has since then been documented in all crocodilians, most turtles,
tions with TSD will become biased towards one sex and as a result
some lizards and some fish (Deeming, 2004; Ewert, Etchberger, &
become unviable (Janzen, 1994; Hulin, Delmas, Girondot, Godfrey, &
Nelson, 2004; Harlow, 2004; Conover, 2004, respectively). Given
Guillon, 2009; Mitchell & Janzen, 2010). How these species will cope
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© 2017 John Wiley & Sons Ltd
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Glob Change Biol. 2017;23:4922–4931.
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with the rapid rate of current climatic change is an issue of high con-
middle of a turtle’s nest is found for this population of loggerhead
servation importance, particularly when the species in question is
€ et al., 2014). Temperature was recorded every hour. turtles (Laloe
already threatened. For example, all seven species of sea turtle species exhibit TSD, with males being produced at cool incubation temperatures and females at warm temperatures (Ewert et al., 2004). As
2.2 | Air temperatures
global temperatures warm, there is a concern that populations will
We obtained air temperature data from the International Compre-
be male-depleted in the future (e.g., Davenport, 1989; Mrosovsky &
hensive Ocean Atmosphere Data Set (ICOADS) through the National
Provancha, 1992; Davenport, 1997). These concerns are heightened
Center for Atmospheric Research (http://rda.ucar.edu/datasets/
by the fact that female-biased primary sex ratios (the male-to-female
ds540.1/). We used the Enhanced ICOADS Monthly Summary
ratio of hatchlings in a nest) are already being reported across the
Release 2.5 at 2-degree spatial resolution for the area extending
world (Hays, Mazaris, & Schofield, 2014).
from 14° to 18° N and 22° to 26° W. This 4-degree square region
In contrast to TSD, the study of temperature-dependent hatch-
encompasses all of the Cape Verdean islands. We excluded months
ling mortality has received relatively little attention. The temperature
for which fewer than 30 observations were recorded and checked
range at which turtle eggs develop is relatively narrow and even
that air temperatures within the selected area were homogeneous.
small changes in incubation temperatures can have dramatic effects
IPCC air temperature projections for Cape Verde were obtained
on hatchling mortality within a nest (Bustard & Greenham, 1968).
from the United Nations Development Program (http://www.geog.
Here, we use a recently developed model (Hays, Mazaris, Schofield,
ox.ac.uk/research/climate/projects/undp-cp/). We used the Special
€, 2017) that incorporates temperature impacts on both & Laloe
Report on Emission Scenarios (SRES) A2, A1B and B1. These differ-
embryonic sex and embryonic survival. We parameterize and extend
ent SRES projections are based on different greenhouse emission
this model using empirical data on embryo survival versus incubation
scenarios. We bias-corrected each model’s projection based on the
temperature for a globally important rookery in the Cape Verde
observed ICOADS data for the period of 1854 to 2009: the mean
islands. Cape Verde, a group of islands in the North Atlantic, hosts
was bias-corrected using a delta approach and stochastic variability
the third biggest loggerhead turtle nesting aggregation in the world
consistent with the variability observed between 1854 and 2009
(Marco et al., 2012) with an estimated 10,000–15,000 nests every
was subsequently added.
pez Jurado, Sanz, & Abella, 2007). The effect of warming on year (Lo primary sex ratios was previously reported for this important turtle €, Cozens, Renom, Taxonera, & Hays, 2014). However, rookery (Laloe
2.3 | Hatching and emergence successes
that study did not account for the effect of temperature-linked
Starting in early June every year (from 2008 to 2014), the main
embryonic mortality, which may become an important issue at high
nesting beaches of the island were surveyed for turtle tracks in the
incubation temperatures (Matsuzawa, Sato, Sakamoto, & Bjorndal,
morning (beginning at 07:00). After the first nesting activity was
mez, Tor2002; Chu, Booth, & Limpus, 2008; Valverde, Wingard, Go
recorded, full night surveys (from 20:00 to 07:00) were carried out
doir, & Orrego, 2010; Santidrian Tomillo, Genovart, Paladino, Spotila,
for the rest of the nesting season. Morning surveys (beginning at
& Oro, 2015; Hays et al., 2017). Accordingly, we present sand tem-
07:00) followed the night surveys to guarantee that all nesting activi-
perature data collected over six breeding seasons (2009–2014) and
ties were recorded. Tracks were marked on the beach to prevent
loggerhead nest success data collected over seven breeding seasons
recording nesting activities more than once. The coordinates and
(2008–2014) to examine the relationship between incubation tem-
dates of oviposition of all encountered nests were recorded.
perature and nest success. We then use climate projections from the
Starting 54 days after oviposition, nests were inspected
Intergovernmental Panel on Climate Change (IPCC) to estimate how
nightly for signs of hatchling emergence. After hatchling emer-
hatchling mortalities are likely to change over the course of the
gence, we carried out nest excavations and recorded the numbers
century.
of live hatchlings, dead hatchlings, unhatched eggs (categorized as without an embryo, with an undeveloped embryo or with a fully
2 | MATERIALS AND METHODS 2.1 | Sand temperatures
formed embryo) and predated eggs in each nest. If the number of eggs within a nest was not observed at oviposition, it was estimated by counting the number of egg fragments found in the nest during excavation (Miller, 1999). We defined hatching suc-
We deployed Tinytag Plus 2 loggers (model TGP-4017, Gemini Data
cess as the percentage of hatchlings that successfully hatched
Loggers, UK) on the main turtle nesting beaches of Sal (16°45 N,
from their eggs (i.e., this number includes fully formed hatchlings
22°56 W), Cape Verde, during the 2009–2014 nesting seasons. Log-
found dead inside the nest). We defined emergence success as
gers were deployed at different sites on six of the major nesting
the number of hatchlings that successfully emerged from the
beaches of the island. Loggers were buried at sites where high nest-
nest. As nest excavations were often carried out within 24 hr of
ing activities were recorded. Five loggers were deployed in 2009,
first hatchling emergence, live hatchlings found to be inside the
2010 and 2011, eight in 2012 and 2013 and six in 2014. All loggers
nest during nest excavation were considered as successfully
were buried at 35 cm depth, which is the mean depth at which the
emerged (Miller, 1999).
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2.4 | Relationship between incubation temperature and hatchling mortality
ET AL.
with the mean of the difference being 0.2°C (SD = 0.6°C, n = 24 months). Reconstructing sand temperatures outside of the nesting season reveals that turtles are nesting during the warmest
We estimated the mean incubation temperature of each nest by cal-
months of the year. The difference between the warmest months
culating the mean sand temperature recorded by the logger nearest
and coolest months of the year approximated 5°C (Figure 2b),
to each nest during the incubation duration of the nest. During incu-
although the coolest temperatures were outside of the nesting sea-
bation, metabolic heating of the egg mass can be an important factor
son (December to February).
that increases the temperature of a nest (Broderick, Godley, & Hays, 2001), so we added 0.5°C to the measured sand temperature to represent metabolic heating. This value is the mean metabolic heating
3.3 | Hatching and emergence successes
recorded during the middle third of incubation—that is, during the
Loggerhead nesting season on Sal typically extends from late June
temperature-sensitive period for TSD (Yntema & Mrosovsky, 1982)
(median
€ et al., 2014). —for this population of loggerhead turtles (Laloe
range = 10 days [17/06 to 27/06], n = 7 nesting seasons) to mid-
date
of
first
nest
laid = 22
June,
interquartile
We used the published literature to assemble a database on the
October (median date of last nest laid = 13 October, interquartile
relationship between incubation temperature and hatchling mortality
range = 7 days [11/10 to 18/10], n = 7 nesting seasons). The med-
in sea turtles. To have comparable data points, we only used studies
ian date of the nesting season is 19 August (interquartile
that reported emergence successes against the mean incubation
range = 32 days [05/08 to 06/09], n = 7 nesting seasons).
temperature during the entire incubation process. We used hatching
The hatching season typically extends from late August (median hatch = 26
successes as an estimation of emergence success in studies that
date
reported hatching successes only. Both laboratory studies that mea-
range = 10 days [17/08 to 27/08], n = 7 hatching seasons) to mid-
sured hatchling mortality at fixed incubations temperatures as well
December (median date of last hatchling emergence = 17 December,
of
first
nest
to
August,
interquartile
as field studies that report hatchling mortality vs. mean incubation
interquartile range = 17 days [04/12 to 21/12], n = 7 nesting sea-
temperature were included. We excluded data found for leatherback
sons). The median date for the hatching season is 14 October (in-
turtles (Dermochelys coriacea) as leatherbacks are reported to have
terquartile range = 31 days [30/09 to 31/10], n = 7 hatching
significantly lower hatching success than the hard-shelled turtles
seasons).
(Mrosovsky, 1983; Bell, Spotila, Paladino, & Reina, 2003). Data were
Hatchling mortality data were recorded for 3687 nests. Of these
found for three species: the loggerhead (Caretta caretta), olive ridley
nests, 2162 were left to incubate in situ and 1525 were relocated
(Lepidochelys olivacea) and green turtle (Chelonia mydas).
either to a hatchery (n = 924 nests) or to another site along the beach (n = 601 nests). Hatching and emergence percentages were arcsine-transformed for analysis. Medians and interquartile ranges
3 | RESULTS
were calculated by back-transformation. Nests that incubated in situ
3.1 | Sand temperatures
had a slightly higher hatching success (Δ = 3.0%) than relocated
In total, we obtained 6603 days of sand temperature data across
incubated in situ for further analyses. Hatching success of nests that
6 years. Seasonality was clearly recorded, with sand temperatures on
incubated in situ ranged from 0 to 100% (median = 86.2%,
all beaches increasing from June until September and decreasing
interquartile range = 73.2–93.7%, n = 2162 nests) as did emergence
nests (W = 1943100, p < .001) so we only used natural nests that
(median = 84.6%,
range = 70.0–92.8%,
thereafter (Figure 1). Some beaches recorded markedly higher sand
successes
temperature than others, with the temperature difference between
n = 2162 nests). We found a 1.6% difference between hatching suc-
the warmest and the coolest beach approximating 2.5°C. Mean daily
cesses and emergence successes (W = 2180500, p < .001). In subse-
sand temperatures ranged from 24.4 to 33.7°C during the nesting
quent analyses, we used emergence success as an indicator of
season across all beaches.
hatchling survival as it is a better measure for hatchling production
interquartile
than hatching success (Wallace et al., 2007).
3.2 | Air temperatures We found a strong relationship between monthly mean air temperatures and monthly mean sand temperature (Figure 2a). The least squares fit regression equation is as follows: mean sand temperature = 4.67 + air
temperature 9 0.93
(F1,253 = 385.8,
3.4 | Relationship between incubation temperature and hatchling mortality Mean incubation temperatures were calculated for 893 nests and
r2 = .60,
ranged from 27.8 to 32.5°C (mean = 29.6°C, SD = 0.9°C, n = 893
p < .001). To verify the accuracy and precision of our model, we
nests). To explore the relationship between incubation temperature
hind-casted monthly mean sand temperatures from 2009 to 2014
and emergence success, we ordered our data by increasing incuba-
and compared the reconstructed values to the recorded values
tion temperature and made 27 groups of nests. All groups contained
(Figure 2b). There was no significant difference between recon-
32 nests, bar one group that contained 31 nests (see Supplementary
structed values and observed values (t = 2.01, df = 23, p = .06),
Information Table S1). We calculated the mean emergence success
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30
26
32
(b)
28 40 24
20
Date
04/01
25/11
16/10
06/09
28/07
09/05
01/07/14
01/07/13
01/07/12
01/07/11
01/07/10
0 01/07/09
22
4925
Sand temperature (°C)
80
(a)
18/06
34
Number of clutches
Sand temperature (°C)
€ LALOE
Week starting
F I G U R E 1 (a) Seasonal changes in sand temperatures across years. Sand temperatures were recorded at nest depth during the 2009–2014 loggerhead nesting seasons on Sal, Cape Verde. Individual points represent mean daily sand temperatures recorded by one logger. Different colours indicate different nesting beaches. (b) Weekly number of clutches laid (blue), weekly number of clutches hatched (red) and weekly sand temperatures (black) on Sal, Cape Verde. Error bars are 1 standard error of the mean (n = 7 nesting seasons [2008–2014] for data on number of clutches laid and hatched, and n = 6 nesting seasons [2009–2014] for sand temperature data). Weekly sand temperatures during our study period are sinusoidal (F2,1016 = 3332, r2 = 0.87, p < .001, n = 6 nesting seasons). The solid black line is the regression line, and the dashed lines denote the 95% prediction interval. First clutches are typically laid in late June so the majority of clutches incubate during the warmest weeks of the year
and mean incubation temperature of each group. High emergence successes were found both at the lower and upper thermal ends: at
3.5 | Hatchling output
a mean incubation temperature of 28.5°C, we found a mean emer-
As the mean temperature during the entire incubation period and
gence success equal to 82.6%; at a mean incubation temperature of
the mean temperature during the middle third of incubation are so
32.2°C, we found a mean emergence success equal to 81.3% (Fig-
close in absolute terms in our study (Δ = 0.1°C, t = 9.54, df = 935,
ure 3).
p < .001), we use them interchangeably in our calculations. We used
Using data from published research (see Supplementary Informa-
the method described in 2014 to estimate the number of females
tion Table S1), we fitted a logistic model to this relationship using
€ et al., 2014), with the disrecruiting to the adult population (Laloe
the method of least squares (Figure 3). The equation that best
tinction that we used emergence sex ratios rather than primary sex
describes the relationship between emergence success (H) and incu-
ratios. Whereas primary sex ratios represent the percentage of
bation temperature (t) is:
female hatchlings surviving incubation, emergence sex ratios represent the percentage of female hatchlings emerging from the nest. In HðtÞ ¼
A 1 þ ebðtt0 Þ
(1)
short, this produces a relative index of the number of nests that takes into account temperature-linked hatchling mortality. This calcu-
where the upper asymptote A = 86%, the growth rate constant
lation shows that, as temperatures rise, there will be an increase in
b = 1.7°C1, and the inflection point t0 = 32.7°C (r2 = 0.59,
the number of nests on Sal. Following SRES A2, the number of nests
p < .001). We checked that the function was a good fit for all three
will have increased by approximately 29.1% by 2100. However, as
species by looking at the distribution of residuals. An ANOVA
incubation temperatures near the upper thermal tolerance limit, the
reveals no significant difference in the distribution of residuals
number of nests will begin to decrease at the turn of the century
between all species (F = 1.13, df = 2, p = 0.33). We also checked
and by 2145 the number of nests will in fact be 2.3% lower than
that there was no difference between data based on hatching suc-
the historical mean from 1854 until 2009 (Figure 5). SRES A1B pro-
cess measurements and data based on emergence success measure-
jects a similar but less acute pattern with 28.3% more nests by 2100
ments (t = 0.76, df = 68.27, p = 0.45).
and still 15.3% more nests by 2145. Following SRES B1, the number
Air temperatures during the months of August, September and October (peak incubation time for loggerheads nesting on Sal) are
of nests is projected to increase by 26.9% by 2100 and by 30.5% by 2145.
projected to be between 1.5 and 2.9°C warmer than current recordings at our field site by 2100 (Figure 4a). Using Equation (1), we projected how emergence successes will change as air temperatures,
4 | DISCUSSION
and hence incubation temperatures, warm (Figure 4b). According to SRES A2, emergence successes will fall to 49.1% by the year 2100.
It is now widely understood that the increase in global temperatures
If we consider SRES A1B and SRES B1, emergence successes will fall
threatens many species of plants and animals (Walther et al., 2002;
less dramatically to 66.7% and 80.8%, respectively.
Parmesan & Yohe, 2003; Parmesan, 2006; Bellard, Bertelsmeier,
32
Sand temperature (°C)
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100
(a) Hatchling survival (%)
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30 28 26 24
50
0
22
24
26
28
Air temperature (°C)
Sand temperature (°C)
32
26
30
34
38
Incubation temperature (°C) F I G U R E 3 Hatchling survival decreases with increasing incubation temperature. Data from this study are coloured in red. Data from other field sites were found for loggerhead (circles), olive ridley (diamonds) and green sea turtles (triangles) and are detailed in the Supplementary Information Table S1. Closed symbols represent emergence success data, and open symbols represent hatching success data. A logistic regression was fit using the method of least squares (r2 = 0.59, p < .001)
(b)
30 28 26 24
01/07/14
01/07/13
01/07/12
01/07/11
01/07/10
01/07/09
island of Cape Verde (Abella Perez, Marco, Martins, & Hawkes,
Date F I G U R E 2 Air temperature is a robust proxy for sand temperature. (a) We found a strong linear relationship between monthly mean sand temperature at nest depth and monthly mean air temperature. Individual points represent the monthly mean sand temperature recorded for June, July, August, September or October of 2009, 2010, 2011, 2012, 2013 or 2014. The dashed lines define the 95% prediction interval. (b) Monthly mean sand temperatures for the nesting beaches of Sal, Cape Verde, from 2009 to 2014 were hind-casted (open circles) using the linear regression between monthly mean air temperature and monthly mean sand temperature. Observed monthly mean sand temperatures (closed circles) are not available for all months as the temperature loggers were not left in situ year round
2016), suggesting that the conclusions from our work can likely be extended more broadly across the Cape Verde islands. By deploying temperature loggers over a variety of beach locations, we captured inter- and intra-beach variations and revealed that there was a fairly wide range of sand temperatures, and hence incubation temperatures, throughout the nesting season (Figure 1). Differences in sand temperature between beaches were previously reported at this study site and were linked to sand colour, with dark beaches being warmer € et al., 2014). Sand colour was also shown than light beaches (Laloe to be an important driver of sand temperature at other sites including Ascension Island, where sand temperatures between two beaches with contrasting sand colour differed by up to 4.2°C (Hays, Adams, Mortimer, & Speakman, 1995; Hays et al., 2001). From a conservation perspective, this indicates that the light-coloured beaches, that is the cooler beaches, at a nesting site will become a priority for conservation in a warming world because they will be the ones with higher hatchling production.
Leadley, Thuiller, & Courchamp, 2012). Shifts in distribution and
We recorded similar seasonal patterns of sand temperature
abundance of species are reported across many different taxa
across the six years of measurements (Figure 1), which suggest that
~ uelas & Filella, 2001; Root et al., 2003) including fish (Perry, (Pen
temperature-related hatchling survival and sex ratio are also likely to
Low, Ellis, & Reynolds, 2005), amphibians (Pounds, Fogden, & Camp-
be similar. This lack of inter-annual variability is similar to that
bell, 1999), reptiles (Gibbon et al., 2000; Sinervo et al., 2010), birds
recorded at other rookeries such as Ascension Island (Hays, Godley,
(Maclean et al., 2008) and mammals (Thuiller et al., 2006). Here, we
& Broderick, 1999) where rainfall is minimal during nesting season,
draw attention to a key trait that will limit a species’ ability to cope
but contrasts to the patterns recorded on the east coast of the Uni-
with warming temperatures, namely the increase in embryonic mor-
ted States (e.g., Hawkes, Broderick, Godfrey, & Godley, 2007; Lola-
tality at warmer incubation temperatures.
var & Wyneken, 2015) where rainfall is more important. So at Cape Verde we expect that, over short time periods, the key drivers of
4.1 | Seasonal variation in sand temperatures
variations in hatchling sex ratio production might be seasonal effects (more males at the start and end of the season) and across-beach
Mean incubation temperatures measured at our study were similar
effects rather than cooling produced by rainfall or tidal overwash,
to the values reported for Boa Vista, the primary loggerhead nesting
which may be important at other sites across the world (e.g.,
30
Air temperature (°C)
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29
28
27
26
1.2
1.0
0.8 2020
2040
2060
2080
2100
2050
2075
Year
Emergence success (%)
100
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(a) Relative nest numbers
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(b)
80
60
40 2020
2040
2060
2100
2125
2150
Year
2080
2100
Year F I G U R E 4 Mean emergence successes are projected to decrease on Sal as incubation temperatures warm. We used three SRES projections based on different carbon-emission scenarios: scenarios A2 (red), A1B (blue) and B1 (black). The solid lines represent the means of 1000 stochastic runs, and the dashed lines show single runs (for illustrative purposes). (a) The IPCC projects an increase in air temperatures throughout the 21st century at our field site. (b) Warmer air temperatures will result in a decrease in emergence successes Godfrey, Barreto, & Mrosovsky, 1996; Houghton et al., 2007; Lola€, Esteban, Berkel, & Hays, 2016). var & Wyneken, 2015; Laloe
F I G U R E 5 After an initial increase, the number of nests is predicted to decrease in Cape Verde. We calculated the change in nest numbers by dividing the emergence sex ratios by the mean emergence sex ratio from 1854 until 2009 and then introducing a 45-year lag (time-to-maturity). We used three SRES projections based on different carbon-emission scenarios: scenarios A2 (red), A1B (blue) and B1 (black). The solid lines represent the means of 1000 stochastic runs, and the dashed lines show single runs (for illustrative purposes). The horizontal dotted line represents the mean annual number of nest from 1845 until 2009. The number of nests is projected to increase as temperatures rise and more females are produced. As the incubation temperatures near the upper thermal tolerance limit, the increase in number of nests is projected to slow. Eventually number of nests will decrease due to increased temperature-linked hatchling mortalities months. For species that lack phenological lability (temporal or geographic), genetic shifts may be the only feasible option to maintain population viability (Bradshaw & Holzapfel, 2008). In the event of phenological and genetic inflexibility, conservation measures may have to be put in place to preserve entire populations of threatened species.
4.2 | Hatchling survival The upper thermal limit for sea turtle egg development is often cited
Using air temperature as a proxy, we were able to reconstruct
as 33°C (Miller, 1997) or 35°C (Ackerman, 1997) although it is possi-
sand temperature accurately and relatively precisely, with hind-
ble that for some species the upper thermal tolerance is higher
casted values being on average within fractions of a degree of the
(Howard, Bell, & Pike, 2014, 2015). Additionally, it is now clear that
observed value (Figure 2). Relationships between air temperature
sea turtle embryos become more tolerant of high incubation temper-
and sand temperature were already shown to be fairly robust and
atures as incubation progresses (Maulaney, Booth, & Baxter, 2012).
are commonly used to reconstruct sand temperatures at turtle nest-
For example, early-stage olive ridley turtle embryos are not tolerant
ing sites (e.g., Hays, Broderick, Glen, & Godley, 2003; Hawkes et al.,
of incubation temperatures greater than 34°C, but late-stage
€ et al., 2016; Santidrian Tomillo, 2007; Fuentes et al., 2009; Laloe
embryos exposed to temperatures greater that 36°C during the last
€, Mortimer, Guzman, & Hays, 2016). Saba et al., 2015; Esteban, Laloe
few days of incubation can survive (Maulaney et al., 2012).
Concurrently, this analysis also revealed that turtles nest during the
Using published data, we were able to model the relationship
warmest part of the year in Cape Verde (see also Figure 1b). Some
between incubation temperature and hatchling mortality. Our work
evidence suggests that sea turtles may be able to adapt their nesting
extends earlier research and the relationship we put forward resem-
phenology to warming temperatures (Weishampel, Bagley, & Ehrhart,
bles closely that described previously by Howard et al. (2014). The
2004; Mazaris, Kallimanis, Pantis, & Hays, 2013) so, theoretically,
relationship between hatchling sex ratio and incubation temperature
loggerhead sea turtles nesting in Cape Verde will be able to, at least
seems to be fairly conservative across all sea turtle species (Acker-
temporarily, mitigate the detrimental effects of warming tempera-
man, 1997; Mrosovsky, Kamel, Rees, & Margaritoulis, 2002; Wibbels,
tures by adjusting their nesting phenology and nesting in cooler
2003). Similarly, it seems likely that the relationship between
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hatching success and incubation temperature holds broadly between
according to different IPCC scenarios. We projected that hatching
species. Currently, most of the published data on temperature-linked
successes will drop to 50.95–78.93% by 2100 (Figure 4). This result
mortality stem from studies with loggerhead (e.g., Matsuzawa et al.,
confirms the risks of warming temperatures to sea turtles in the long
2002; Read, Booth, & Limpus, 2013) or green turtles (e.g., Weber
term (Hawkes et al., 2007; Fuentes & Cinner, 2010; Santidrian
et al., 2012), so studying the survival curves of individual species is
Tomillo, Saba et al., 2015). Importantly, we show that the decrease
limited by data availability. Very few data are available for Kemp’s
in hatching successes will be gradual and slow, rather than immedi-
ridley turtles and only a few studies have studied flatback turtles
ate and catastrophic. Considering both TSD and temperature-linked
(e.g., Howard et al., 2015; Van Lohuizen, Rossendell, Mitchell, &
hatchling mortality, our results show that nest numbers initially
Thums, 2016). We reiterate here that there is a need to bridge this
increase with warming incubation temperatures and that a reduction
knowledge gap to assess how climate change will impact different
in nest numbers only occurs once incubation temperatures are so
populations and different species of turtles worldwide (Howard
high as to cause nest failure (Figure 5). In this way, we parameter-
et al., 2014). Only as these new data emerge will we be able to
ized the more general model developed recently by Hays et al.
model the relationships for each species and separate populations
(2017) that combines the impacts of temperature on hatchling sur-
more precisely. In the meantime, the relationship we put forward is
vival and sex. Our findings are in accord with those of Santidrian
broadly applicable to at least three of the seven species of sea tur-
Tomillo, Genovart et al. (2015) who used population simulations to
tles.
show that, although TSD confers sea turtle populations with resili-
Interestingly, most nests on Cape Verde incubate at sufficiently cool temperatures, ensuring high embryonic survival; that is, most
ence in a stochastic environment, as temperatures rise over threshold levels, this mechanism is rendered ineffective.
nests are cooler than the point of inflection denoting the major
Our model assumes there are enough males in the population to
reduction in survival with increasing temperature (Figure 3). Like-
fertilize the eggs of all the females. This assumption is likely to be
wise, this conclusion applies to the available data found in the litera-
robust, as incubation temperatures measured at Cape Verde are
ture. In fact, it is noteworthy that most data on low hatchling
within the male-producing range. Because the proportion of males in
survival (i.e., 32°C) are derived from
the population is likely to decrease throughout the century as the
laboratory incubations (e.g., Bustard & Greenham, 1968; Yntema &
€ et al., 2014), it is urgent to understand if temperatures warm (Laloe
Mrosovsky, 1980; Fisher, Godfrey, & Owens, 2014), and few such
this decrease will limit population persistence. There are already sev-
data are reported from field studies (e.g., Matsuzawa et al., 2002;
eral key biological parameters that suggest that male limitation on
Valverde et al., 2010). In other words, it appears that sea turtles
female fecundity is likely to be low in sea turtles: (i) it is now widely
tend to nest in locations and at times of the year that ensure high
known that male and female sea turtles mate with several partners
hatchling survival. As stated above, if sea turtles are phenologically
during a breeding season (Pearce & Avise, 2001), reducing the need
labile, this would in theory guarantee that they are able to continue
for balanced operational sex ratios—that is, the ratios of males to
to nest in locations and at times that ensure high hatchling survival.
females that are ready to mate in a breeding season; (ii) female sea
This is an important question to address, as it will progress our
turtles have the ability to store sperm to fertilize clutches laid over a
understanding of how future climate change will impact sea turtles
protracted nesting season (Lee, 2008), reducing the need for
and the ecosystems they live in (Schoeman, Schlacher, & Defeo,
repeated contacts with males for the successful fertilization of sev-
2014).
eral clutches of eggs; and (iii) the interval between breeding seasons
While this study focuses on the effect of temperature on hatch-
is different between males and females, with males breeding more
ling survival, there are a number of factors besides temperature that
frequently than females (Hays et al., 2014), leading to more balanced
can contribute to hatchling mortality. For example, tidal overwash
operational sex ratios when hatchling sex ratios are female-biased.
was shown to reduce hatchling survival in leatherback nests in
This suggests that reduced male numbers will not limit population
French Guiana (Caut, Guirlet, & Girondot, 2010). Tropical storms and
persistence in sea turtles and is further supported by theoretical
hurricanes can also reduce hatching success in loggerhead and green
models (Boyle, Hone, Schwanz, & Georges, 2014), but assessing the
turtle nests in Florida (Lindborg, Neidhardt, Witherington, Smith, &
minimum number of males required within a population for it to be
Savage, 2016). In Costa Rica, high abundance of microbes and fungi
viable in the long term remains a conservation priority.
was negatively correlated with hatching success of olive ridley tur-
While the adaptive significance of TSD is still unclear in verte-
zy, Valverde, & Plante, 2015). Investles at a mass-nesting beach (Be
brates, it is becoming clear that TSD may confer an advantage to
tigating how these factors are likely to vary in the future and
sea turtles in a warming world by increasing female output and natu-
estimating how they will impact sea turtle numbers provides for
ral population growth at warmer temperatures (Boyle et al., 2014;
interesting new research.
€ et al., 2014; Santidrian Tomillo, Genovart et al., 2015; Hays Laloe et al., 2017). From a conservation perspective, it is therefore impor-
4.3 | Projections under different warming scenarios
tant to be aware that while nest numbers in Cape Verde (or at any turtle rookery around the world) may seemingly increase throughout
We described the risks of warming temperatures for our study popu-
the century (e.g., 30% increase projected in Cape Verde) there is an
lation by projecting warming incubation temperatures into the future
underlining population feminization and a looming threat brought by
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ET AL.
4929
increased temperature-linked hatchling mortalities. In the future,
the Alasdair Downes Marine Conservation Fund and from the Soci-
extra conservation measures may have to be put in place to safe-
ety for Experimental Biology for his fieldwork in Cape Verde, and
guard sea turtle rookeries against this increase in temperature-linked
from the Centre for Integrative Ecology for an extended research
hatchling mortalities.
visit at Deakin University. The authors thank SOS Tartarugas, Project Biodiversity and the numerous volunteers that helped with data col-
4.4 | Future direction and conclusions
lection. We thank Paolo Luschi and Mariel Murazzi for their help with the sand temperature measurements. The authors thank John
It is important to note that warming temperatures will also have
Davenport, Michael Arendt and two anonymous reviewers for their
influences on the phenotype and survival of hatchlings (Fisher et al.,
helpful comments on an earlier version of this manuscript. The
2014; Kobayashi et al., 2017; Booth, 2017). For example, as well as
authors declare that there is no conflict of interest.
the effects we show on embryonic survival, incubation temperatures have also been shown to affect hatchling size (e.g., Booth & Astill, 2001; Kobayashi et al., 2017), crawling speed across the beach (e.g., Booth, Feeney, & Shibata, 2013; Kobayashi et al., 2017) and swimming speed upon entering the water (e.g., Burgess, Booth, & Lanyon, 2006; Booth & Evans, 2011; Kobayashi et al., 2017). All else being
AUTHOR CONTRIBUTION JC, BR and AT completed the fieldwork and compiled the data. GCH and J-OL conceived the manuscript. J-OL led the data analyses. J-OL and GCH wrote the manuscript with contributions from all the authors.
equal, warmer incubation temperatures will lead to reduced hatchling fitness. Understanding how hatchling fitness will change in the future
REFERENCES
may also be necessary to fully comprehend how warming temperatures will affect the viability of sea turtle populations globally. Our key finding that hatchling survival will decline well before sex ratios are seriously imbalanced reiterates the conclusions of Hays et al. (2017) and underlines that “the effect of reduced embryonic survival at warmer temperatures on populations that produce many females is less obvious than the effects of shortfalls in male abundance” (Boyle et al., 2014). In sea turtle research, the study of TSD has attracted a lot of interest relative to the study of temperature-linked hatchling mortality. While understanding how TSD initially evolved and was subsequently maintained in a wide variety of taxa will certainly continue to be a prolific field of research, from a conservation standpoint it may be necessary to focus research efforts on the study of temperature-linked hatchling mortalities. While TSD has been best studied in turtle species, comparisons with other vertebrate taxa are possible (Girondot et al., 2004). TSD is highly variable, with the transitional range of temperature (the range of temperatures that produce both sexes), the pivotal temperature (the constant temperature that produces sex ratio parity) and mode of TSD differing between taxa (Ewert et al., 2004). Similarly, the thermal tolerance of developing embryos varies between taxa (Deeming & Ferguson, 1991). Taken together, this points to the fact that while the model we put forward in the present study cannot be applied directly to any species with TSD, the approach we use may be transferable. We stress here that monitoring hatchling mortality in species with TSD should be a key conservation priority in order to safeguard the species in a warming world.
ACKNOWLEDGMENTS This research was endorsed by the Ministry of Agriculture and Envirio da Agricultura e Ambiente) of Cape Verde ronment (Ministe through authorizations issued by the National Directorate of the Environment (Direccß~ao Nacional do Ambiente) and complied with all relevant local and national legislation. J-OL received funding from
Abella Perez, E., Marco, A., Martins, S., & Hawkes, L. A. (2016). Is this what a climate change-resilient population of marine turtles looks like? Biological Conservation, 193, 124–132. Ackerman, R. A. (1997). The nest environment and the embryonic development of sea turtles. In P. L. Lutz & J. A. Musick (Eds.), Biology of sea turtles (pp. 83–106). Boca Raton, FL: CRC Press. Bell, B. A., Spotila, J. R., Paladino, F. V., & Reina, R. D. (2003). Low reproductive success of leatherback turtles, Dermochelys coriacea, is due to high embryonic mortality. Biological Conservation, 115, 131–138. Bellard, C., Bertelsmeier, C., Leadley, P., Thuiller, W., & Courchamp, F. (2012). Impacts of climate change on the future of biodiversity. Ecology Letters, 15, 365–377. zy, V. S., Valverde, R. A., & Plante, C. J. (2015). Olive ridley sea turtle Be hatching success as a function of the microbial abundance in nest sand at Ostional, Costa Rica. PLoS ONE, 10, e0118579. Booth, D. T. (2017). The influence of incubation temperature on sea turtle hatchling quality. Integrative Zoology. in press, https://doi.org/10. 1111/1749-4877.12255 Booth, D. T., & Astill, K. (2001). Incubation temperature, energy expenditure and hatchling size in the green turtle (Chelonia mydas), a species with temperature-sensitive sex determination. Australian Journal of Zoology, 49, 389–396. 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, https://doi.org/10.1371/journal.pone. 0023162. 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. Marine Biology, 160, 127–137. Boyle, M., Hone, J., Schwanz, L. E., & Georges, A. (2014). Under what conditions do climate-driven sex ratios enhance versus diminish population persistence? Ecology and Evolution, 4, 4522–4533. Bradshaw, W. E., & Holzapfel, C. M. (2008). Genetic response to rapid climate change: it’s seasonal timing that matters. Molecular Ecology, 17, 157–166. Broderick, A. C., Godley, B. J., & Hays, G. C. (2001). Metabolic heating and the prediction of sex ratios for green turtles (Chelonia mydas). Physiological and Biochemical Zoology, 74, 161–170. Burgess, E. A., Booth, D. T., & Lanyon, J. M. (2006). Swimming performance of hatchling green turtles is affected by incubation temperature. Coral Reefs, 25, 341–349.
4930
|
Bustard, H. R., & Greenham, P. G. (1968). Physical and chemical factors affecting hatching in the green sea turtle, Chelonia mydas (L.). Ecology, 49, 269–276. Caut, S., Guirlet, E., & Girondot, M. (2010). Effect of tidal overwash on the embryonic development of leatherback turtles in French Guiana. Marine Environmental Research, 69, 254–261. rature sur la sex-ratio chez l’emCharnier, M. (1966). Action de la tempe bryon d’Agama agama (Agamidae Lacertilien). Societe de Biologie de l’Ouest Africain, 160, 620–622. 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. Australian Journal of Zoology, 56, 57–64. Conover, D. O. (2004). Temperature-dependent sex determination in fishes. In N. Valenzuela & V. A. Lance (Eds.), Temperature-dependent sex determination in vertebrates (pp. 11–20). Washington, DC: Smithsonian Books. Davenport, J. (1989). Sea turtles and the greenhouse effect. British Herpetological Society Bulletin, 29, 11–15. Davenport, J. (1997). Temperature and the life-history strategies of sea turtles. Journal of Thermal Biology, 22, 479–488. Deeming, D. (2004). Prevalence of TSD in crocodilians. In N. Valenzuela & V. A. Lance (Eds.), Temperature-dependent sex determination in vertebrates (pp. 33–41). Washington, DC: Smithsonian Books. Deeming, D. C., & Ferguson, M. W. J. (1991). Physiological effects of incubation temperature on embryonic development in reptiles and birds. In D. C. Deeming & M. W. J. Ferguson (Eds.), Egg incubation: Its effects on embryonic development in birds and reptiles (pp. 147–171). Cambridge: Cambridge University Press. €, J.-O., Mortimer, J. A., Guzman, A. N., & Hays, G. C. Esteban, N., Laloe (2016). Male hatchling production in sea turtles from one of the world’s largest marine protected areas, the Chagos Archipelago. Scientific Reports, 6, https://doi.org/10.1038/srep20339. Ewert, M. A, Etchberger, C. R., & Nelson, C. E. (2004). Turtle sex-determining modes and TSD patterns, and some TSD pattern correlates. In N. Valenzuela & V. A. Lance (Eds.), Temperature-dependent sex determination in vertebrates (pp. 21–32). Washington, DC: Smithsonian Books. Fisher, L. R., Godfrey, M. H., & Owens, D. W. (2014). Incubation temperature effects on hatchling performance in the loggerhead sea turtle (Caretta caretta). PLoS ONE, 9, e114880. Fuentes, M. M. P. B., & Cinner, J. E. (2010). Using expert opinion to prioritize impacts of climate change on sea turtles’ nesting grounds. Journal of Environmental Management, 91, 2511–2518. 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 in northern Australia. Endangered Species Research, 9, 33–40. Gibbon, J. W., Scott, D. E., Ryan, T. J., Buhlmann, K. A., Tuberville, T. D., Metts, B. S., . . . Winne, C. T. (2000). The global decline of reptiles, ja vu amphibians. BioScience, 50, 653–666. de vot-Julliard, A.Girondot, M., Delmas, V., Rivalan, P., Courchamp, F., Pre C., & Godfrey, M. H. (2004). Implications of temperature-dependent sex determination for population dynamics. In N. Valenzuela & V. A. Lance (Eds.), Temperature-dependent sex determination in vertebrates (pp. 148–155). Washington, DC: Smithsonian Books. Godfrey, M. H., Barreto, R., & Mrosovsky, N. (1996). Estimating past and present sex ratios of sea turtles in Suriname. Canadian Journal of Zoology, 74, 267–277. Harlow, P. S. (2004). Temperature-dependent sex determination in lizards. In N. Valenzuela & V. A. Lance (Eds.), Temperature-dependent sex determination in vertebrates (pp. 42–52). Washington, DC: Smithsonian Books. 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. Global Change Biology, 13, 1–10. Hays, G. C., Adams, C. R., Mortimer, J. A., & Speakman, J. R. (1995). Inter- and intra-beach thermal variation for green turtle nests on
€ LALOE
ET AL.
Ascension Island, South Atlantic. Journal of the Marine Biology Association of the United Kingdom, 75, 405–411. Hays, G. C., Ashworth, J. S., Barnsley, M. J., Broderick, A. C., Emery, D. R., Godley, B. J., . . . 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. Global Change Biology, 9, 642–646. Hays, G. C., Godley, B. J., & Broderick, A. C. (1999). Long-term thermal conditions on the nesting beaches of green turtles on Ascension Island. Marine Ecology Progress Series, 185, 297–299. Hays, G. C., Mazaris, A. D., & Schofield, G. (2014). Different male vs. female breeding periodicities help mitigate offspring sex ratios skews in sea turtles. Frontiers in Marine. Science, 1, 43. €, J.-O. (2017). Population Hays, G. C., Mazaris, A. D., Schofield, G., & Laloe viability at extreme sex-ratio skews produced by temperaturedependent sex determination. Proceedings of the Royal Society of London B, 284, 20162576. Houghton, J. D. R., Myers, A. E., Lloyd, C., King, R. S., Isaacs, C., & Hays, G. C. (2007). Protracted rainfall decreases temperature within leatherback turtle (Dermochelys coriacea) clutches in Grenada, West Indies: ecological implications for a species displaying temperature dependent sex determination. Journal of Experimental Marine Biology and Ecology, 345, 71–77. Howard, R., Bell, I., & Pike, D. A. (2014). Thermal tolerances of sea turtle embryos: current understanding and future directions. Endangered Species Research, 26, 75–86. Howard, R., Bell, I., & Pike, D. A. (2015). Tropical flatback turtle embryos (Natator depressus) are resilient to the heat of climate change. Journal of Experimental Biology, 218, 3330–3335. Hulin, V., Delmas, V., Girondot, M., Godfrey, M. H., & Guillon, J.-M. (2009). Temperature-dependent sex determination and global change: are some species at greater risk? Oecologia, 160, 493–506. Janzen, F. J. (1994). Climate change and temperature-dependent sex determination in reptiles. Proceedings of the National Academy of Sciences, 91, 7487–7490. Kobayashi, S., Wada, M., Fujimoto, R., Kumazawa, Y., Arai, K., Watanabe, G., & Saito, T. (2017). The effects of nest incubation temperature on embryos and hatchlings of the loggerhead sea turtle: implications of sex difference for survival rates during early life stages. Journal of Experimental Marine Biology and Ecology, 486, 274–281. €, J.-O., Cozens, J., Renom, B., Taxonera, A., & Hays, G. C. (2014). Laloe Effects of rising temperature on the viability of an important sea turtle rookery. Nature Climate Change, 4, 513–518. €, J.-O., Esteban, N., Berkel, J., & Hays, G. C. (2016). Sand temperaLaloe tures for nesting sea turtles in the Caribbean: implications for hatchling sex ratios in the face of climate change. Journal of Experimental Marine Biology Ecology, 474, 92–99. Lee, P. L. M. (2008). Molecular ecology of marine turtles: new approaches and future directions. Journal of Experimental Marine Biology and Ecology, 356, 25–42. Lindborg, R., Neidhardt, E., Witherington, B., Smith, J. R., & Savage, A. (2016). Factors influencing loggerhead (Caretta caretta) and green turtle (Chelonia mydas) reproductive success on a mixed use beach in Florida. Chelonian Conservation and Biology, 15, 238–248. Lolavar, A., & Wyneken, J. (2015). Effect of rainfall on loggerhead turtle nest temperatures, sand temperatures and hatchling sex. Endangered Species Research, 28, 235–247. pez Jurado, L. F., Sanz, P., & Abella, E. (2007). Loggerhead nesting on Boa Lo blica de Cabo Verde. In: R. B. Mast, L. M. Bailey & B. J. Vista, Repu Hutchinson (Eds.), SWOT report, Vol. 2 (pp. 22–23). Arlington, VA: SWOT. Maclean, I., Austin, G. E., Rehfisch, M. M., Blew, J. A. N., Crowe, O., Delany, S., . . . Van Roomen, M. (2008). Climate change causes rapid
€ LALOE
|
ET AL.
changes in the distribution and site abundance of birds in winter. Global Change Biology, 14, 2489–2500. pez, O., Jime nezMarco, A., Abella, E., Liria-Loza, A., Martins, S., Lo n, S., . . . Lo pez-Jurado, L. F. (2012). Abundance and exploitaBordo tion of loggerhead turtles nesting in Boa Vista island, Cape Verde: the only substantial rookery in the eastern Atlantic. Animal Conservation, 15, 351–360. Matsuzawa, Y., Sato, K., Sakamoto, W., & Bjorndal, K. A. (2002). Seasonal fluctuations in sand temperature: effects on the incubation period and mortality of loggerhead sea turtle (Caretta caretta) pre-emergent hatchlings in Minabe, Japan. Marine Biology, 140, 639–646. Maulaney, R. I., Booth, D. T., & Baxter, G. S. (2012). Emergence success and sex ratio of natural and relocated nests of olive ridley turtles for Alas Purwo National Park, East Java, Indonesia. Copeia, 2012, 738– 747. Mazaris, A. D., Kallimanis, A. S., Pantis, J. D., & Hays, G. C. (2013). Phenological response of sea turtles to environmental variation across a species’ northern range. Proceedings of the Royal Society of London B, 280, 20122397. Miller, J. D. (1997). Reproduction in sea turtles. In P. L. Lutz & J. A. Musick (Eds.), The biology of sea turtles, Vol. 1 (pp. 51–80). Boca Raton, FL: CRC Press. Miller, J. D. (1999). Determining clutch size and hatching success. In K. L. Eckert, K. A. Bjorndal, F. A. Abreu-Grobois & M. Donnelly (Eds.), Research and management techniques for the conservation of sea turtles (pp. 124– 129). Washington, DC: IUCN/SSC Marine Turtle Specialist Group Publication. Mitchell, N. J., & Janzen, F. J. (2010). Temperature-dependent sex determination and contemporary climate change. Sexual Development, 4, 129–140. Mrosovsky, N. (1983). Ecology and nest-site selection of leatherback turtles Dermochelys coriacea. Biological Conservation, 26, 47–56. Mrosovsky, N., Kamel, S., Rees, A. F., & Margaritoulis, D. (2002). Pivotal temperature for loggerhead turtles (Caretta caretta) from Kyparissia Bay, Greece. Canadian Journal of Zoology, 80, 2118–2124. Mrosovsky, N., & Provancha, J. (1992). Sex ratio of hatchling loggerhead sea turtles: data and estimates from a 5-year study. Canadian Journal of Zoology, 70, 530–538. Parmesan, C. (2006). Ecological and evolutionary responses to recent climate change. Annual Review of Ecology, Evolution, and Systematics, 37, 637–669. Parmesan, C., & Yohe, G. (2003). A globally coherent fingerprint of climate change impacts across natural systems. Nature, 421, 37–42. Pearce, D. E., & Avise, J. C. (2001). Turtle mating systems: behavior, sperm storage, and genetic paternity. Journal of Heredity, 92, 206–211. ~uelas, J., & Filella, I. (2001). Responses to a warming world. Science, Pen 294, 793–795. Perry, A. L., Low, P. J., Ellis, J. R., & Reynolds, J. D. (2005). Climate change and distribution shifts in marine fishes. Science, 308, 1912–1915. Pounds, J. A., Fogden, M. P. L., & Campbell, J. H. (1999). Biological response to climate change on a tropical mountain. Nature, 398, 611–615. Read, T., Booth, D. T., & Limpus, C. J. (2013). Effect of nest temperature on hatchling phenotype of loggerhead turtles (Caretta caretta) from e. Austwo South Pacific rookeries, Mon Repos and La Roche Perce tralian Journal of Zoology, 60, 402–411. 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. Santidri an Tomillo, P., Genovart, M., Paladino, F. V., Spotila, J. R., & Oro, D. (2015). Climate change overruns resilience conferred by temperature-dependent sex determination in sea turtles and threatens their survival. Global Change Biology, 21, 2980–2988.
4931
Santidrian Tomillo, P. S., Saba, V. S., Lombard, C. D., Valiulis, J. M., Robinson, N. J., Paladino, F. V., . . . Nel, R. (2015). Global analysis of the effect of local climate on the hatchling output of leatherback turtles. Scientific Reports, 5. https://doi.org/10.1038/srep16789. Schoeman, D. S., Schlacher, T. A., & Defeo, O. (2014). Climate change impacts on sandy beach biota: crossing a line in the sand. Global Change Biology, 20, 2383–2392. ndez-De-La-Cruz, F., Miles, D. B., Heulin, B., Bastiaans, Sinervo, B., de Me E., Villagr an-Santa Cruz, M., . . . Sites, J. W. Jr. (2010). Erosion of lizard diversity by climate change and altered thermal niches. Science, 328, 894–899. Thuiller, W., Broennimann, O., Hughes, G., Alkmade, J. R. M., Midgley, G. F., & Corsi, F. (2006). Vulnerability of African mammals to anthropogenic climate change under conservative land transformation assumptions. Global Change Biology, 12, 424–440. mez, F., Tordoir, M. T., & Orrego, C. M. Valverde, R. A., Wingard, S., Go (2010). Field lethal incubation temperature of olive ridley sea turtle Lepidochelys olivacea embryos at a mass nesting rookery. Endangered Species Research, 12, 77–86. Van Lohuizen, S., Rossendell, J., Mitchell, N. J., & Thums, M. (2016). The effect of incubation temperatures on nest success of flatback sea turtles (Natator depressus). Marine Biology, 163, 1–12. Wallace, B. P., Sotherland, P. R., Santidrian Tomillo, P., Reina, R. D., Spotila, J. R., & Paladino, F. V. (2007). Maternal investment in reproduction and its consequences in leatherback turtles. Oecologia, 152, 37–47. Walther, G. R., Post, E., Convey, P., Menzel, A., Parmesan, C., Beebee, T. J., . . . Bairlein, F. (2002). Ecological responses to recent climate change. Nature, 416, 389–395. Weber, S. B., Broderick, A. C., Groothuis, T. G. G., Ellick, J., Godley, B. J., & Blount, J. D. (2012). Fine-scale adaptation in green turtle nesting population. Proceedings of the Royal Society of London B, 279, 1077– 1084. Weishampel, J. F., Bagley, D. A., & Ehrhart, L. M. (2004). Earlier nesting by loggerhead sea turtles following sea surface warming. Global Change Biology, 10, 1424–1427. Wibbels, T. (2003). Critical approaches to sex determination in sea turtle biology and conservation. In P. L. Lutz, J. A. Musick & J. Wyneken (Eds.), The Biology of sea turtles, Vol. 2 (pp. 103–134). Boca Raton, FL: CRC Press. Yntema, C. L., & Mrosovsky, N. (1980). Sexual differentiation in hatchling loggerheads (Caretta caretta) incubated at different controlled temperatures. Herpetologica, 36, 33–36. Yntema, C. L., & Mosovsky, N. (1982). Critical periods and pivotal temperatures for sexual differentiation in loggerhead sea turtles. Canadian Journal of Zoology, 60, 1012–1016.
SUPPORTING INFORMATION Additional Supporting Information may be found online in the supporting information tab for this article.
€ J-O, Cozens J, Renom B, How to cite this article: Laloe Taxonera A, Hays GC. Climate change and temperature-linked hatchling mortality at a globally important sea turtle nesting site. Glob Change Biol. 2017;23:4922–4931. https://doi.org/ 10.1111/gcb.13765
