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.     

Thermal control of hatchling emergence patterns in marine turtles

The emergence patterns of green turtle (Chelonia mydas) hatchlings on two beaches on Ascension Island, South Atlantic were monitored and related to thermal patterns in the sand at 10, 20, 30 and 40 cm depth. A total of 6001 hatchlings were recorded emerging on Long Beach, and 3171 emerged on North East Bay during the study period. No significant difference was observed in the temporal pattern of hatchling emergence among nights, or between the two beaches. Hatchling emergence predominantly occurred at night with over 93% of hatchlings emerging during the hours of darkness. Almost all hatchlings emerging in daylight suffer predation by the Ascension frigatebird (Fregata aquila). Counts of frigatebirds both above the study beaches and offshore were highest just after sunrise, with a smaller peak prior to sunset, when frigatebirds were found to predate hatchlings emerging, crawling down the beach or detected in inshore waters. The likely thermal cues controlling hatchling emergence were investigated (temperature at different depths, thermal gradients in the sand and temperature change). The most plausible thermal factor appears to be the change of temperature at superficial sand depths, with hatchling emergence inhibited when subsurface sand temperatures were increasing. This simple mechanism is likely to ensure predominantly nocturnal hatchling emergence regardless of sand albedo, seasonality or latitude as long as night is relatively cooler than day.     

Water temperature and internesting intervals for loggerhead (Caretta caretta) and green (Chelonia mydas) sea turtles

Temperature loggers were attached to the carapace of green turtles (Chelonia mydas) at Ascension Island and Cyprus and to loggerhead turtles (Caretta caretta) at Cyprus, in order to record the ambient temperature experienced by individuals during the internesting interval, i.e. the period between consecutive clutches being laid. Internesting intervals were relatively short (10–14 days) and mean ambient temperatures relatively warm (27–28°C), compared to previous observations for these species nesting in Japan, although a single internesting interval versus temperature relationship described all the data for these two species from the different areas. The implication is that water temperature has both a common and a profound effect on the length of the internesting interval for these two species: internesting intervals are shorter when the water is warmer.     

Metabolic heating and the prediction of sex ratios for green turtles (Chelonia mydas)

We compared incubation temperatures in nests (n=32) of the green turtle (Chelonia mydas) on Ascension Island in relation to sand temperatures of control sites at nest depth. Intrabeach thermal variation was low, whereas interbeach thermal variation was high in both control and nest sites. A marked rise in temperature was recorded in nests from 30% to 40% of the way through the incubation period and attributed to metabolic heating. Over the entire incubation period, metabolic heating accounted for a mean rise in temperature of between 0.07 degrees and 2.86 degrees C within nests. During the middle third of incubation, when sex is thought to be determined, this rise in temperature ranged between 0.07 degrees and 2.61 degrees C. Metabolic heating was related to both the number of eggs laid and the total number of hatchlings/embryos produced in a clutch. For 32 clutches in which temperature was recorded, we estimate that metabolic heating accounted for a rise of up to 30% in the proportion of females produced within different clutches. Previous studies have dismissed any effect of metabolic heating on the sex ratio of marine turtle hatchlings. Our results imply that metabolic heating needs to be considered when estimating green turtle hatchling sex ratios.     

Potential limitations of behavioral plasticity and the role of egg relocation in climate change mitigation for a thermally sensitive endangered species

Anthropogenic climate change is widely considered a major threat to global biodiversity, such that the ability of a species to adapt will determine its likelihood of survival. Egg‐burying reptiles that exhibit temperature‐dependent sex determination, such as critically endangered hawksbill turtles (Eretmochelys imbricata), are particularly vulnerable to changes in thermal regimes because nest temperatures affect offspring sex, fitness, and survival. It is unclear whether hawksbills possess sufficient behavioral plasticity of nesting traits (i.e., redistribution of nesting range, shift in nesting phenology, changes in nest‐site selection, and adjustment of nest depth) to persist within their climatic niche or whether accelerated changes in thermal conditions of nesting beaches will outpace phenotypic adaption and require human intervention. For these reasons, we estimated sex ratios and physical condition of hatchling hawksbills under natural and manipulated conditions and generated and analyzed thermal profiles of hawksbill nest environments within highly threatened mangrove ecosystems at Bahía de Jiquilisco, El Salvador, and Estero Padre Ramos, Nicaragua. Hawksbill clutches protected in situ at both sites incubated at higher temperatures, yielded lower hatching success, produced a higher percentage of female hatchlings, and produced less fit offspring than clutches relocated to hatcheries. We detected cooler sand temperatures in woody vegetation (i.e., coastal forest and small‐scale plantations of fruit trees) and hatcheries than in other monitored nest environments, with higher temperatures at the deeper depth. Our findings indicate that mangrove ecosystems present a number of biophysical (e.g., insular nesting beaches and shallow water table) and human‐induced (e.g., physical barriers and deforestation) constraints that, when coupled with the unique life history of hawksbills in this region, may limit behavioral compensatory responses by the species to projected temperature increases at nesting beaches. We contend that egg relocation can contribute significantly to recovery efforts in a changing climate under appropriate circumstances.     

Island-finding ability of marine turtles

Green turtles (Chelonia mydas) swim from foraging grounds along the Brazilian coast to Ascension Island to nest, over 2200 km distant in the middle of the equatorial Atlantic. To test the hypothesis that turtles use wind-borne cues to locate Ascension Island we found turtles that had just completed nesting and then moved three individuals 50 km northwest (downwind) of the island and three individuals 50 km southeast (upwind). Their subsequent movements were tracked by satellite. Turtles released downwind returned to Ascension Island within 1, 2 and 4 days, respectively. By contrast, those released upwind had far more difficulty in relocating Ascension Island, two eventually returning after 10 and 27 days and the third heading back to Brazil after failing to find its way back to the island. These findings strongly support the hypothesis that wind-borne cues are used by turtles to locate Ascension Island.     

Metabolic heating in Mediterranean loggerhead sea turtle clutches

Offspring sex ratio is an important demographic parameter and, given its determination by incubation temperature in sea turtles, might be a key factor for their conservation under climate warming. An appealing approach to estimate hatchling sex ratios is to measure sand temperatures at nest depth and deduce hatchling sex ratios from a beforehand-established relationship of hatchling sex ratio and sand temperature. Such estimates will only be accurate though if metabolic heat produced by the embryos is considered. Judging whether metabolic heating has a potential effect on hatchling sex ratios without actually measuring temperature within clutches would greatly facilitate monitoring protocols. We tested for a relationship between the amount of metabolic heating and the number of developed embryos as well as clutch size in the largest known loggerhead sea turtle (Caretta caretta) population of the Mediterranean on Zakynthos (Greece). Temperatures were measured within 20 nests as well as at a reference site in the sand at nest depth. Metabolic heating was detected, but only during the last third of the incubation period did nests heat up considerably (1.6 °C on average) above the temperature of the surrounding sand. During the middle third of incubation, when sex is determined, the amount of metabolic heating was negligible. The amount of metabolic heating during the last third of the incubation duration was significantly correlated to the number of offspring developed to at least about 75% of incubation duration. This factor explained nearly 50% of variation in metabolic heating. Metabolic heating was also significantly correlated to clutch size. Given that clutch size within the Mediterranean is largest in Zakynthos loggerheads, we conclude that metabolic heating can be ignored in the estimate of hatchling sex ratios in Mediterranean loggerhead populations. These results thus provide the basis for a feasible monitoring of hatchling sex ratios in the loggerhead sea turtle in the Mediterranean.     

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.     

Beach erosion and nest site selection by the leatherback sea turtle Dermochelys coriacea (Testudines: Dermochelyidae) and implications for management practices at Playa Gandoca, Costa Rica

Leatherback sea turtles (Dermochelys coriacea) nest on dynamic, erosion-prone beaches. Erosive processes and resulting nest loss have long been presumed to be a hindrance to clutch survival. In order to better understand how leatherbacks cope with unstable nesting beaches, I investigated the role of beach erosion in leatherback nest site selection at Playa Gandoca, Costa Rica. I also examined the potential effect of nest relocation, a conservation strategy in place at Playa Gandoca to prevent nest loss to erosion, on the temperature of incubating clutches. I monitored changes in beach structure as a result of erosion at natural nest sites during the time the nest was laid, as well as in subsequent weeks. To investigate slope as a cue for nest site selection, I measured the slope of the beach where turtles ascended from the sea to nest, as well as the slopes at other random locations on the beach for comparison. I examined temperature differences between natural and relocated nest sites with thermocouples placed in the sand at depths typical of leatherback nests. Nests were distributed non-randomly in a clumped distribution along the length of the beach and laid at locations that were not undergoing erosion. The slope at nest sites was significantly different than at randomly chosen locations on the beach. The sand temperature at nest depths was significantly warmer at natural nest sites than at locations of relocated nests. The findings of this study suggest leatherbacks actively select nest sites that are not undergoing erosive processes, with slope potentially being used as a cue for site selection. The relocation of nests appears to be inadvertently cooling the nest environment. Due to the fact that leatherback clutches undergo temperature-dependent sex determination, the relocation of nests may be producing an unnatural male biasing of hatchlings. The results of this study suggest that the necessity of relocation practices, largely in place to protect nests from erosion, should be reevaluated to ensure the proper conservation of this critically endangered species.     

Warm water and cool nests are best. How global warming might influence hatchling green turtle swimming performance

For sea turtles nesting on beaches surrounded by coral reefs, the most important element of hatchling recruitment is escaping predation by fish as they swim across the fringing reef, and as a consequence hatchlings that minimize their exposure to fish predation by minimizing the time spent crossing the fringing reef have a greater chance of surviving the reef crossing. One way to decrease the time required to cross the fringing reef is to maximize swimming speed. We found that both water temperature and nest temperature influence swimming performance of hatchling green turtles, but in opposite directions. Warm water increases swimming ability, with hatchling turtles swimming in warm water having a faster stroke rate, while an increase in nest temperature decreases swimming ability with hatchlings from warm nests producing less thrust per stroke.     

High thermal variance in naturally incubated turtle nests produces faster offspring

The effects of climate change on populations are complex and difficult to predict, and can result in mismatches between interdependent organisms or between organisms and their environment. Reptiles with temperature-dependent sex determination may be able to compensate for potential skews in offspring sex ratio caused by climate change by selecting cooler (i.e., shadier) nest sites. Although changing nest location may prevent sex ratio skews, it may also affect thermally sensitive performance traits in offspring. I tested righting, sprinting, and swimming performance in hatchling painted turtles (Chrysemys picta), produced by female turtles from five populations across the species’ geographic range, nesting in a common-garden environment. I found that speed of hatchling performance was faster in hatchlings whose mothers originated from warmer climates, and that nests with higher mean daily variation in incubation temperature produced faster hatchlings. These results suggest that the increased temperatures predicted by climate change models could result in hatchling turtles that are faster at sprinting and swimming; however, it is not yet known how these performance measures translate into fitness.     

Navigation by green turtles: which strategy do displaced adults use to find Ascension Island?

Sea turtles are known to perform long-distance, oceanic migrations between disparate feeding areas and breeding sites, some of them located on isolated oceanic islands. These migrations demonstrate impressive navigational abilities, but the sensory mechanisms used are still largely unknown. Green turtles breeding at Ascension Island perform long oceanic migrations (>2200 km) between foraging areas along the Brazilian coast and the isolated island. By performing displacement experiments of female green turtles tracked by satellite telemetry in the waters around Ascension Island we investigated which strategies most probably are used by the turtles in locating the island. In the present paper we analysed the search trajectories in relation to alternative navigation strategies including the use of global geomagnetic cues, ocean currents, celestial cues and wind. The results suggest that the turtles did not use chemical information transported with ocean currents. Neither did the results indicate that the turtles use true bi-coordinate geomagnetic navigation nor did they use indirect navigation with respect to any of the available magnetic gradients (total field intensity, horizontal field intensity, vertical field intensity, inclination and declination) or celestial cues. The female green turtles successfully locating Ascension Island seemed to use a combination of searching followed by beaconing, since they searched for sensory contact with the island until they reached positions NW and N of the Island and from there presumably used cues transported by wind to locate the island during the final stages of the search.     

Natural beaches confer fitness benefits to nesting marine turtles

Coastal ecosystems provide vital linkages between aquatic and terrestrial habitats and thus support extremely high levels of biodiversity. However, coastlines also contain the highest densities of human development anywhere on the planet and are favoured destinations for tourists, creating a situation where the potential for negative effects on coastal species is extremely high. I gathered data on marine turtle reproductive output from the literature to determine whether coastal development negatively influences offspring production. Female loggerhead (Caretta caretta) and green turtles (Chelonia mydas) nesting on natural beaches (as opposed to beaches with permanent development) produce significantly more hatchling turtles per nest; all else being equal, females that successfully produce more offspring will have higher fitness than conspecifics producing fewer offspring. Thus, female marine turtles nesting on natural beaches probably have higher fitness than turtles nesting on developed beaches. Consequently, populations nesting on natural beaches may be able to recover more quickly from the historic population declines that have plagued marine turtles, and some species may recover more quickly than others.     

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.     

Shading and Watering as a Tool to Mitigate the Impacts of Climate Change in Sea Turtle Nests

Increasing sand temperatures resulting from climate change may negatively impact sea turtle nests by altering sex ratios and decreasing reproductive output. We analyzed the effect of nest shading and watering on sand temperatures as climate mitigation strategies in a beach hatchery at Playa Grande, Costa Rica. We set up plots and placed thermocouples at depths of 45cm and 75cm. Half of the plots were shaded and half were exposed to the sun. Within these exposure treatments, we applied three watering treatments over one month, replicating local climatic conditions experienced in this area. We also examined gravimetric water content of sand by collecting sand samples the day before watering began, the day after watering was complete, and one month after completion. Shading had the largest impact on sand temperature, followed by watering and depth. All watering treatments lowered sand temperature, but the effect varied with depth. Temperatures in plots that received water returned to control levels within 10 days after watering stopped. Water content increased at both depths in the two highest water treatments, and 30 days after the end of water application remained higher than plots with low water. While the impacts of watering on sand temperature dissipate rapidly after the end of application, the impacts on water content are much more lasting. Although less effective at lowering sand temperatures than shading, watering may benefit sea turtle clutches by offsetting negative impacts of low levels of rain in particularly dry areas. Prior to implementing such strategies, the natural conditions at the location of interest (e.g. clutch depth, environmental conditions, and beach characteristics) and natural hatchling sex ratios should be taken into consideration. These results provide insight into the effectiveness of nest shading and watering as climate mitigation techniques and illustrate important points of consideration in the crafting of such strategies.     

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.     

Determinants of reproductive success and offspring sex in a turtle with environmental sex determination

Despite the importance of maternal effects in evolution, and knowledge of links among nest site choice, timing of nesting, offspring sex, and reproductive success in animals with environmental sex determination, these attributes have not been rigorously studied in a combined and natural context. To address this need we studied the relationships between three maternal traits (nest site choice, lay date, and nest depth) and two fitness‐related attributes of offspring (hatchling sex and embryonic survival) in the riverine turtle Carettochelys insculpta, a species with temperature‐dependent sex determination, for four years. Predation and flooding were the major sources of embryonic mortality in 191 nests. Embryonic survival was influenced by both lay date and nest site choice: in one year when nesting began later than average, nests laid later and at lower elevations were destroyed by early wet season river rises. In other years early nesting precluded flood mortality. However, turtles did not nest at the highest available elevations, and a field experiment confirmed that turtles were constrained to nest at lower elevations where they could construct a nest chamber. The principal determinant of hatchling sex in 140 nests was lay date, which in turn was apparently related to the magnitude of the previous wet season(s). Clutches laid earlier in the season (a female's first clutch) produced mainly males, while later clutches (her second clutch) yielded mostly females, due to seasonal increases in air temperatures. Accordingly, later nesting produced female‐biased hatchling sex ratios in 1996, while earlier nesting resulted in sex ratios near unity in the other years. However, all‐female nests were more likely to be flooded than mixed‐sex or all‐male nests in years when nesting was late. In conclusion, we found evidence that the position of two maternal trait distributions (elevation of the nest site and lay date), associated with the reproductive strategy of C. insculpta, reflect a combination of natural selection, physical constraints, and phenotypic plasticity. © 2004 The Linnean Society of London, Biological Journal of the Linnean Society, 2004, 81 , 1–16.     

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.     

Female turtles from hot nests: is it duration of incubation or proportion of development at high temperatures that matters?

Summary Mean daily temperature in natural nests of freshwater turtles with temperature-dependent sex determination is known to be a poor predictor of hatchling sex ratios when nest temperatures fluctuate. To account for this, a model was developed on the assumption that females will emerge from eggs when more than half of embryonic development occurs above the threshold temperature for sex determination rather than from eggs that spend more than half their time above the threshold. The model is consistent with previously published data and in particular explains the phenomenon whereby the mean temperature that best distinguishes between male and female nests decreases with increasing variability in nest temperature. The model, if verified by controlled experiments, has important implications for our understanding of temperature-dependent sex determination in natural nests. Both mean nest temperature and hours spent above the threshold will be poor predictors of hatchling sex ratios. Studies designed to investigate latitudinal trends and inter-specific differences in the threshold temperature will need to consider latitudinal and inter-specific variation in the magnitude of diel fluctuations in nest temperature, and variation in factors influencing the magnitude of those fluctuations, such as nest depth. Furthermore, any factor that modifies the relationship between developmental rate and temperature can be expected to influence hatchling sex ratios in natural nests, especially when nest temperatures are close to the threshold.     

Microclimate of American crocodile nests in Banco Chinchorro biosphere reserve, Mexico: Effect on incubation length, embryos survival and hatchlings sex

Crocodilians have temperature-dependent sex determination (TSD) in which incubation temperature determines sex of embryo. Global warming is expected to alter hatchling sex ratio, leading to the extinction of small populations. Regional climate influence on crocodile nest microclimate and hatchlings' characteristics is poorly known. Here, microclimate in natural nests of American crocodile (Crocodylus acutus) and its relation with incubation length, hatchling sex and nesting success was studied in Banco Chinchorro Biosphere Reserve (Mexico) from 2007 to 2010. Temperature and relative humidity in different locations within and outside the nests were registered by data loggers. Incident solar radiation above nest was calculated from hemispheric photographs. Incubation length, proportion of hatchling reaching complete development and hatchling sex were determined at hatching. Nest temperatures exhibited a cyclic daily fluctuation due to solar radiation, which is the major heat source for nests. Clutch temperature was relatively stable and its daily amplitude was negatively correlated with clutch depth and size. Rainfall was the major source of clutch temperature decrease. Clutch and metabolic temperatures increased significantly during incubation. A small sample size failed to demonstrate a statistical relationship between length of incubation and mean clutch temperature. Proportion of embryos reaching complete development depended on maximum and minimum clutch temperature, maximum daily amplitude of clutch temperature and maximum decrease in clutch temperature on a period ≤4 day. Results confirmed a Female-Male-Female TSD pattern for C. acutus, with 31 and 32.5 °C as possible pivotal temperatures. Population and hatchling sex ratios were male-biased and fate of crocodiles of Banco Chinchorro could depend on the magnitude of temperature increase in the future.