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

Sea turtles show temperature dependent sex determination. Using an empirical relationship between sand and air temperature, we reconstructed the nest temperatures since 1855 at Ascension Island, a major green turtle (Chelonia mydas) rookery. Our results show that inter‐beach thermal variations, previously ascribed to the albedo of the sand, which varies hugely from one beach to another, have persisted for the last century. Reconstructed nest temperatures varied by only 0.5 °C on individual beaches over the course of the nesting season, while the temperature difference between two key nesting beaches was always around 3 °C. Hence inter‐beach thermal variations are the main factor causing a large range of incubation temperatures at this rookery. There was a general warming trend for nests, with a mean increase in reconstructed nest temperatures for different months of between 0.36 and 0.49 °C for the last 100 years.     

Past, current and future thermal profiles of green turtle nesting grounds: Implications from climate change

Sex determination and hatching success in sea turtles is temperature dependent and as a result global warming poses a threat to sea turtles. Warmer sand temperatures may skew sea turtle population′s sex ratios towards predominantly females and decrease hatching success. Therefore, understanding the rates at which sand temperatures are likely to increase as climate change progresses is warranted. We recorded sand temperature and used historical sea surface and air temperature to model past and to predict future sand temperature under various scenarios of global warming at key sea turtle nesting grounds (n = 7) used by the northern Great Barrier Reef (nGBR) green turtle, Chelonia mydas, population. Reconstructed temperatures from 1990 to the present suggest that sand temperatures at the nesting sites studied have not changed significantly during the last 18 years. Current thermal profile at the nesting grounds suggests a bias towards female hatchling production into this population. Inter-beach thermal variance was observed at some nesting grounds with open areas in the sand dune at northern facing beaches having the warmest incubating environments. Our model projections suggest that a near complete feminization of hatchling output into this population will occur by 2070 under an extreme scenario of climate change (A1T emission scenario). Importantly, we found that some nesting grounds will still produce male hatchlings, under the most extreme scenario of climate change, this finding differs from predictions for other locations. Information from this study provides a better understanding of possible future changes in hatching success and sex ratios at each site and identifies important male producing regions. This allowed us to suggest strategies that can be used at a local scale to offset some of the impacts of warmer incubating temperatures to sea turtles.     

Sand and nest temperatures and an estimate of hatchling sex ratio from the Heron Island green turtle (Chelonia mydas) rookery, Southern Great Barrier Reef

Sand and nest temperatures were monitored during the 2002–2003 nesting season of the green turtle, Chelonia mydas, at Heron Island, Great Barrier Reef, Australia. Sand temperatures increased from ∼ 24°C early in the season to 27–29°C in the middle, before decreasing again. Beach orientation affected sand temperature at nest depth throughout the season; the north facing beach remained 0.7°C warmer than the east, which was 0.9°C warmer than the south, but monitored nest temperatures were similar across all beaches. Sand temperature at 100 cm depth was cooler than at 40 cm early in the season, but this reversed at the end. Nest temperatures increased 2–4°C above sand temperatures during the later half of incubation due to metabolic heating. Hatchling sex ratio inferred from nest temperature profiles indicated a strong female bias.     

Fine-scale thermal adaptation in a green turtle nesting population

The effect of climate warming on the reproductive success of ectothermic animals is currently a subject of major conservation concern. However, for many threatened species, we still know surprisingly little about the extent of naturally occurring adaptive variation in heat-tolerance. Here, we show that the thermal tolerances of green turtle (Chelonia mydas) embryos in a single, island-breeding population have diverged in response to the contrasting incubation temperatures of nesting beaches just a few kilometres apart. In natural nests and in a common-garden rearing experiment, the offspring of females nesting on a naturally hot (black sand) beach survived better and grew larger at hot incubation temperatures compared with the offspring of females nesting on a cooler (pale sand) beach nearby. These differences were owing to shallower thermal reaction norms in the hot beach population, rather than shifts in thermal optima, and could not be explained by egg-mediated maternal effects. Our results suggest that marine turtle nesting behaviour can drive adaptive differentiation at remarkably fine spatial scales, and have important implications for how we define conservation units for protection. In particular, previous studies may have underestimated the extent of adaptive structuring in marine turtle populations that may significantly affect their capacity to respond to environmental change.     

Investigating the potential impacts of climate change on a marine turtle population

Recent increases in global temperatures have affected the phenology and survival of many species of plants and animals. We investigated a case study of the effects of potential climate change on a thermally sensitive species, the loggerhead sea turtle, at a breeding location at the northerly extent of the range of regular nesting in the United States. In addition to the physical limits imposed by temperature on this ectothermic species, sea turtle primary sex ratio is determined by the temperature experienced by eggs during the middle third of incubation. We recorded sand temperatures and used historical air temperatures (ATs) at Bald Head Island, NC, to examine past and predict future sex ratios under scenarios of warming. There were no significant temporal trends in primary sex ratio evident in recent years and estimated mean annual sex ratio was 58% female. Similarly, there were no temporal trends in phenology but earlier nesting and longer nesting seasons were correlated with warmer sea surface temperature. We modelled the effects of incremental increases in mean AT of up to 7.5°C, the maximum predicted increase under modelled scenarios, which would lead to 100% female hatchling production and lethally high incubation temperatures, causing reduction in hatchling production. Populations of turtles in more southern parts of the United States are currently highly female biased and are likely to become ultra‐biased with as little as 1°C of warming and experience extreme levels of mortality if warming exceeds 3°C. The lack of a demonstrable increase in AT in North Carolina in recent decades coupled with primary sex ratios that are not highly biased means that the male offspring from North Carolina could play an increasingly important role in the future viability of the loggerhead turtle in the Western Atlantic.     

Impact of marine heatwaves for sea turtle nest temperatures

There are major concerns about the ecological impact of extreme weather events. In the oceans, marine heatwaves (MHWs) are an increasing threat causing, for example, recent devastation to coral reefs around the world. We show that these impacts extend to adjacent terrestrial systems and could negatively affect the breeding of endangered species. We demonstrate that during an MHW that resulted in major coral bleaching and mortality in a large, remote marine protected area, anomalously warm temperatures also occurred on sea turtle nesting beaches. Granger causality testing showed that variations in sea surface temperature strongly influenced sand temperatures on beaches. We estimate that the warm conditions on both coral reefs and sandy beaches during the MHW were unprecedented in the last 70 years. Model predictions suggest that the most extreme female-biased hatchling sex ratio and the lowest hatchling survival in nests in the last 70 years both occurred during the heatwave. Our work shows that predicted increases in the frequency and intensity of MHWs will likely have growing impacts on sea turtle nesting beaches as well as other terrestrial coastal environments.     

Climate change resilience of a globally important sea turtle nesting population

Few studies have looked into climate change resilience of populations of wild animals. We use a model higher vertebrate, the green sea turtle, as its life history is fundamentally affected by climatic conditions, including temperature‐dependent sex determination and obligate use of beaches subject to sea level rise (SLR). We use empirical data from a globally important population in West Africa to assess resistance to climate change within a quantitative framework. We project 200 years of primary sex ratios (1900–2100) and create a digital elevation model of the nesting beach to estimate impacts of projected SLR. Primary sex ratio is currently almost balanced, with 52% of hatchlings produced being female. Under IPCC models, we predict: (a) an increase in the proportion of females by 2100 to 76%–93%, but cooler temperatures, both at the end of the nesting season and in shaded areas, will guarantee male hatchling production; (b) IPCC SLR scenarios will lead to 33.4%–43.0% loss of the current nesting area; (c) climate change will contribute to population growth through population feminization, with 32%–64% more nesting females expected by 2120; (d) as incubation temperatures approach lethal levels, however, the population will cease growing and start to decline. Taken together with other factors (degree of foraging plasticity, rookery size and trajectory, and prevailing threats), this nesting population should resist climate change until 2100, and the availability of spatial and temporal microrefugia indicates potential for resilience to predicted impacts, through the evolution of nest site selection or changes in nesting phenology. This represents the most comprehensive assessment to date of climate change resilience of a marine reptile using the most up‐to‐date IPCC models, appraising the impacts of temperature and SLR, integrated with additional ecological and demographic parameters. We suggest this as a framework for other populations, species and taxa.     

Predicting the distribution of green turtle nesting sites over the Mediterranean with outcoming climate driven changes

Nesting beaches have a critical role in the life cycle of sea turtles and their survival. Many different factors affect nest site selection, ranging from the composition of the sand to the vegetation of the beach. These factors are subject to change due to the onset of climate change. We aimed to determine the possible changes in nesting beaches according to the future climate scenarios of Chelonia mydas nesting sites in the Mediterranean by ecological niche modeling. Nineteen bioclimatic variables and Representative Concentration Pathway scenarios (RCP2.6 and RCP8.5) were used to generate past, current, and future nesting site projections. The datasets were prepared with ArcGIS v10. and bioclimatic variables were analyzed using the Pearson Correlation Analysis. The ecological niche modeling was made with the MaxEnt v4.1.0. Model outputs, mean temperature of warmest quarter (22.01 %), precipitation of coldest quarter (15.32 %), mean temperature of the driest quarter (13.60 %), isothermality (12.30 %), mean diurnal range (9.22 %), the max temperature of the warmest month (6.60 %), precipitation seasonality (5.87 %) and annual mean temperature (4.73 %) are the parameters that most affect the estimated distribution of the species and the other parameters have the least effect on the estimated distribution (each < 2.60 %). The prediction accuracy of the model is measured by the Area Under the Curve (AUC) values, which is between 0 and 1, where values closer to 1 have a greater prediction accuracy. In our model results, the AUC values vary between 0.961 and 0.990. The majority of current green turtle nesting sites will continue to be suitable for nesting into the 2100′s. But the habitat suitability of the current nesting beaches in Syria and Lebanon will decrease. Conservational efforts should be developed to protect not only the current nesting beaches but also other possible nesting beaches that might become viable in the future.     

Earlier nesting by loggerhead sea turtles following sea surface warming

The onset of spring, noted by the timing of wildlife migratory and breeding behaviors, has been occurring earlier over the past few decades. Here, we examine 15 years of loggerhead sea turtle, Caretta caretta, nesting patterns along a 40.5 km beach on Florida's Atlantic coast. This small section of beach is considered to be the most important nesting area for this threatened species in the western hemisphere. From 1989 to 2003, the annual number of nests fluctuated between 13 000 and 25 000 without a conspicuous trend; however, based on a regression analysis, the median nesting date became earlier by roughly 10 days. The Julian day of median nesting was significantly correlated with near‐shore, May sea surface temperatures that warmed an average of 0.8°C over this period. This marine example from warm temperate/subtropical waters represents another response of nature to recent climate trends.     

Antigua revisited: the impact of climate change on sand and nest temperatures at a hawksbill turtle (Eretmochelys imbricata) nesting beach

Whether a turtle embryo develops into a male or a female depends, as with many other reptiles, on the temperature during incubation of the eggs. With sea turtles, warm temperatures produce 100% females. Therefore, global warming has the potential to drastically alter their sex ratios. Air temperatures on Antigua have increased by 0.7°C over the last 35 years. Measurements in both the sand and the clutches laid by hawksbill turtles (Eretmochelys imbricata) at Pasture Bay, Antigua, show that for important parts of the nesting season temperatures are already above the level producing 50% of each sex (pivotal level). Comparisons are made to sand temperature measurements taken on this beach in 1989 and 1990. It is estimated that fewer males were produced in 2003 than in the previous years. Recommendations are made for close monitoring of the fertility of eggs and for research on any turtles nesting at cooler times of year.     

A potential tool to mitigate the impacts of climate change to the caribbean leatherback sea turtle

It is now well understood that climate change has the potential to dramatically affect biodiversity, with effects on spatio‐temporal distribution patterns, trophic relationships and survivorship. In the marine turtles, sex is determined by incubation temperature, such that warming temperatures could lead to a higher production of female hatchlings. By measuring nest temperature, and using a model to relate the incubation temperature to sex ratio, we estimate that Caribbean Colombian leatherback sea turtles currently produce approximately 92% female hatchlings. We modelled the relationship between incubation, sand and air temperature, and under all future climate change scenarios (0.4–6.0 °C warming over the next 100 years), complete feminization could occur, as soon as the next decade. However, male producing refugia exist in the periphery of smaller nests (0.7 °C cooler at the bottom than at the centre), within beaches (0.3 °C cooler in the vegetation line and inter‐tidal zone) and between beaches (0.4 °C higher on dark beaches), and these natural refugia could be assigned preferential conservation status. However, there exists a need to develop strategies that may ameliorate deleterious effects of climate‐induced temperature changes in the future. We experimentally shaded clutches using screening material, and found that it was effective in reducing nest temperature, producing a higher proportion of male hatchlings, without compromising the fitness or hatching success. Artificial shade in hatcheries is a very useful and simple tool in years or periods of high environmental temperatures. Nevertheless, this is only an emergency response to the severe impacts that will eventually have to be reversed if we are to guarantee the stability of the populations.     

Extreme rainfall events and cooling of sea turtle clutches: Implications in the face of climate warming

Understanding how climate change impacts species and ecosystems is integral to conservation. When studying impacts of climate change, warming temperatures are a research focus, with much less attention given to extreme weather events and their impacts. Here, we show how localized, extreme rainfall events can have a major impact on a species that is endangered in many parts of its range. We report incubation temperatures from the world's largest green sea turtle rookery, during a breeding season when two extreme rainfall events occurred. Rainfall caused nest temperatures to drop suddenly and the maximum drop in temperature for each rain‐induced cooling averaged 3.6°C (n = 79 nests, min = 1.0°C, max = 7.4°C). Since green sea turtles have temperature‐dependent sex determination, with low incubation temperatures producing males, such major rainfall events may have a masculinization effect on primary sex ratios. Therefore, in some cases, extreme rainfall events may provide a “get‐out‐of‐jail‐free card” to avoid complete feminization of turtle populations as climate warming continues.     

An annual cycle,at constant temperature,in a model sandy beach. II. Microbial biology

A model sandy beach successfully mimicking the natural environment has been operated under controlled conditions at a constant temperature (5°C, representative of British winter coastal sea-water temperatures) for a year. During this time the bacterial population of the sand and inundating sea water has been enumerated. Bacterial numbers were highest near the high and low water marks and had a minimum in between on the beach slope; they decreased with depth in the sand profile and showed little variation with time. A number of the bacteria were isolated from the sand system and a preliminary classification attempted. The results are discussed in relation to the meagre literature pertaining to the microbial biology of natural marine sandy beaches.     

Influence of sea turtle nesting on hunting behavior and movements of jaguars in the dry forest of northwest Costa Rica

Jaguars (Panthera onca) are opportunistic predators that prey on large profitable prey items, such as sea turtles at nesting beaches. Here, we use jaguar and sea turtle track-count surveys, combined with satellite telemetry of one jaguar, to evaluate whether jaguar hunting behavior and movements are influenced by seasonal sea turtle nesting in the Sector Santa Rosa of Área de Conservación Guanacaste in northwest Costa Rica. We used generalized linear models to evaluate the effect of moon phase and sea surface temperature on olive ridley (Lepidochelis olivacea) and green turtle (Chelonia mydas) nesting abundance, as well as the combination of these predictors on the frequency of jaguar predation activity (proximity to nesting beaches) and movements. For home-range size and location analyses, we calculated kernel density estimates for each season at three different temporal scales. Sea turtle nesting season influenced jaguar activity patterns, as well as sea turtle abundance was related to jaguar locations and predation events, but jaguar home-range size (88.8 km² overall) did not differ between nesting seasons or among temporal scales. Environmental conditions influenced sea turtle nesting and, as a consequence, also influenced jaguar movements and foraging activity. Our study defined the home range of a female jaguar in the tropical dry forest and its relationship to seasonally abundant turtles. Additional information related to the effect of tourism on jaguar–sea turtle interactions would improve conservation of these species at unique nesting beaches in the area.     

The range implications of lizard traits in changing environments

Aim Most predictions of species ranges are based on correlating current species localities to environmental conditions. These correlative models do not explicitly include a species' biology. In contrast, some mechanistic models link traits to energetics and population dynamics to predict species distributions. These models enable one to ask whether considering a species' biology is important for predicting its range. I implement mechanistic models to investigate how a species' morphology, physiology and life history influence its range. Location North America. Methods I compare the mechanistic model predictions with those of correlative models for eight species of North American lizards in both current environments and following a uniform 3 °C temperature warming. I then examine the implications of superimposing habitat and elevation requirements on constraints associated with environmental tolerances. Results In the mechanistic model, species with a narrower thermal range for activity are both predicted and observed to have more restricted distributions. Incorporating constraints on habitat and elevation further restricts species distributions beyond areas that are thermally suitable. While correlative models generally outperform mechanistic models at predicting current distributions, the performance of mechanistic models improves when incorporating additional factors. In response to a 3 °C temperature warming, the northward range shifts predicted by the mechanistic model vary between species according to trait differences and are of a greater extent than those predicted by correlative models. Main conclusions These findings highlight the importance of species traits for understanding the dynamics of species ranges in changing environments. The analysis demonstrates that mechanistic models may provide an important complement to correlative models for predicting range dynamics, which may underpredict climate‐induced range shifts.     

Estimating the Effect of Beach Nourishment on Caretta caretta (Loggerhead Sea Turtle) Nesting

Caretta caretta (loggerhead sea turtle) nesting activity was recorded daily during three seasons prior to and two seasons immediately following a beach nourishment (replenishment) project in Palm Beach County, Florida. Surveys were done at the nourished beach (Jupiter/Carlin) and at two natural beaches (Juno and Tequesta). The size of the nourishment effect on nesting activity was estimated using Before‐After‐Control‐Impact Paired Series (BACIPS) models. Nesting declined by 4.4 to 5.4 nests km ^{? 1} day ^{? 1} on the nourished beach compared to the two natural beaches in the first season after nourishment. At the same time, false crawls (FC, non‐nesting crawls) increased by 5.0 to 5.6 FC km ^{? 1} day ^{? 1} on the nourished beach. In the second season following nourishment, nesting was reduced by 0.5 to 1.6 nests km ^{? 1} day ^{? 1} on the nourished beach compared to the two natural beaches. The increase in false crawl frequency in the second season following nourishment was 0.7 to 0.9 FC km ^{? 1} day ^{? 1}.These results suggest that beach nourishment significantly decreased loggerhead sea turtle nesting during the first season following the project. However, the size of the effect, in terms of nesting frequency and false crawl frequency, was much reduced by the second season following nourishment.     

Forecasting range expansion into ecological traps: climate‐mediated shifts in sea turtle nesting beaches and human development

Some species are adapting to changing environments by expanding their geographic ranges. Understanding whether range shifts will be accompanied by increased exposure to other threats is crucial to predicting when and where new populations could successfully establish. If species overlap to a greater extent with human development under climate change, this could form ecological traps which are attractive to dispersing individuals, but the use of which substantially reduces fitness. Until recently, the core nesting range for the Critically Endangered Kemp's ridley sea turtle (Lepidochelys kempii) was ca. 1000 km of sparsely populated coastline in Tamaulipas, Mexico. Over the past twenty‐five years, this species has expanded its range into populated areas of coastal Florida (>1500 km outside the historical range), where nesting now occurs annually. Suitable Kemp's ridley nesting habitat has persisted for at least 140 000 years in the western Gulf of Mexico, and climate change models predict further nesting range expansion into the eastern Gulf of Mexico and northern Atlantic Ocean. Range expansion is 6–12% more likely to occur along uninhabited stretches of coastline than are current nesting beaches, suggesting that novel nesting areas will not be associated with high levels of anthropogenic disturbance. Although the high breeding‐site fidelity of some migratory species could limit adaptation to climate change, rapid population recovery following effective conservation measures may enhance opportunities for range expansion. Anticipating the interactive effects of past or contemporary conservation measures, climate change, and future human activities will help focus long‐term conservation strategies.     

Nest temperatures in a loggerhead nesting beach in Turkey is more determined by sea surface than air temperature

While climate change is now fully recognised as a reality, its impact on biodiversity is still not completely understood. To predict its impact, proxies coherent with the studied ecosystem or species are thus required. Marine turtles are threatened worldwide (though some populations are recovering) as they are particularly sensitive to temperature throughout their entire life cycle. This is especially true at the embryo stage when temperature affects both growth rates and sex determination. Nest temperature is thus of prime importance to understand the persistence of populations in the context of climate change. We analysed the nest temperature of 21 loggerheads (Caretta caretta) originating from Dalyan Beach in Turkey using day-lagged generalised mixed models with autocorrelation. Surprisingly, the selected model for nest temperature includes an effect for sea surface temperature 4-times higher than for air temperature. We also detected a very significant effect of metabolic heating during development compatible with what is already known about marine turtle nests. Our new methodology allows the prediction of marine turtle nest temperatures with good precision based on a combination of air temperature measured at beach level and sea surface temperature in front of the beach. These data are available in public databases for most of the beaches worldwide.     

Sea Turtle Nesting as a Process Influencing a Sandy Beach Ecosystem

Sea turtle egg mortality, egg predation, and small organisms associated with turtle nests were studied at Playa Ostional, Costa Rica. Sites with concentrated sea turtle nesting were compared with solitary nesting sites as a function of place and time based on ANOVA, Akaike's Information Criterion, and Bayesian analyses. Results indicate that sea turtle egg mortality was significantly associated (P < 0.005) with flowing water that erodes or saturates nesting sites, and with overlapped nesting in which sea turtles disturb each other's nests. Sarcophagid and calliphorid fly larvae (Bayesian prior = 1.19; posterior = 2.27), fungi (prior = 1.14; posterior = 1.92), mites (prior = 0.51; posterior = 1.15), and several other types of small organisms increased in number after turtle egg laying (N= 303 nests; 34,451 turtle eggs). During peak sea turtle nesting periods, visitation to nesting sites by poachers and vertebrate predators was high, and relative number of nests disturbed by these predators was low (P < 0.02). In multimodel analysis, the three most parsimonious models were: (1) turtle egg mortality and distance from mean high tide; (2) turtle egg predation and distance from mean high tide; and (3) turtle egg mortality and nesting density, with Akaike weights of 0.224, 0.203, and 0.153 respectively. Intensive sea turtle nesting might result in upwelling and turnover of nesting debris and nest organisms, and may influence biotic community structure of sandy beach ecosystems.     

Reconciling Biodiversity with Fishing: A Holistic Strategy for Pacific Sea Turtle Recovery

Recovery of sea turtle populations requires addressing: multiple sources of mortality; nonmarket, diffuse benefits with costs localized on the poor; and a transboundary resource with incomplete jurisprudence, markets, and institutions. Holistic recovery strategies include: beach conservation protecting nesting females, their eggs, and critical breeding habitat to maximize hatchling production; enhanced at-sea survival of turtles on the high seas and in commercial coastal fisheries; and reduced artisanal coastal fisheries mortality of turtles. The traditional approach of focusing long-term sustained conservation efforts on the nesting beaches has by itself led to increases in several sea turtle populations. However, current conservation is inadequate to reverse declines in other cases such as the critically endangered leatherback populations in the Pacific. This article discusses policy instruments comprising a holistic recovery strategy that reconciles fishing with biodiversity conservation.