Remote submerged banks and mesophotic ecosystems can provide key habitat for endangered marine megafauna.

The importance of some ecosystems remains poorly understood. We showed that mesophotic ecosystems (30 to 150 m) are a key habitat for a critically endangered species, with strong evidence that a globally important population of adult hawksbill turtles (Eretmochelys imbricata) almost exclusively foraged at these depths on remote submerged banks. This discovery highlights the need for such areas to be included in conservation planning, for example, as part of the United Nations High Seas Treaty. We equipped nesting turtles with Fastloc-GPS (Global Positioning System) satellite tags at an Indian Ocean breeding area and they all traveled to deep foraging sites (6765 days of tracking data across 22 individuals including 183,921 dive-depth measurements) rather than shallow coral reef sites. Both chart depths and depth data relayed from the tags indicated that turtles foraged at mesophotic depths, the modal dive depths being between 35 and 40 m. We calculate that 55,554 km2 of the western Indian Ocean alone consists of submerged banks between 30 and 60 m.

Climate warming and sea turtle sex ratios across the globe.

Climate warming and the feminization of populations due to temperature-dependent sex determination may threaten sea turtles with extinction. To identify sites of heightened risk, we examined sex ratio data and patterns of climate change over multiple decades for 64 nesting sites spread across the globe. Over the last 62 years the mean change in air temperature was 0.85°C per century (SD = 0.65°C, range = -0.53 to +2.5°C, n = 64 nesting sites). Temperatures increased at 40 of the 64 study sites. Female-skewed hatchling or juvenile sex ratios occurred at 57 of the 64 sites, with skews >90% female at 17 sites. We did not uncover a relationship between the extent of warming and sex ratio (r62 = -0.03, p = .802, n = 64 nesting sites). Hence, our results suggest that female-hatchling sex ratio skews are not simply a consequence of recent warming but have likely persisted at some sites for many decades. So other factors aside from recent warming must drive these variations in sex ratios across nesting sites, such as variations in nesting behaviour (e.g. nest depth), substrate (e.g. sand albedo), shading available and rainfall patterns. While overall across sites recent warming is not linked to hatchling sex ratio, at some sites there is both is a high female skew and high warming, such as Raine Island (Australia; 99% female green turtles; 1.27°C warming per century), nesting beaches in Cyprus (97.1% female green turtles; 1.68°C warming per century) and in the Dutch Caribbean (St Eustatius; 91.5% female leatherback turtles; 1.15°C warming per century). These may be among the first sites where management intervention is needed to increase male production. Continued monitoring of sand temperatures and sex ratios are recommended to help identify when high incubation temperatures threaten population viability.

Short-term resilience to climate-induced temperature increases for equatorial sea turtle populations.

Projection models are being increasingly used to manage threatened taxa by estimating their responses to climate change. Sea turtles are particularly susceptible to climate change as they have temperature-dependent sex determination and increased sand temperatures on nesting beaches could result in the 'feminisation' of hatchling sex ratios for some populations. This study modelled likely long-term trends in sand temperatures and hatchling sex ratios at an equatorial nesting site for endangered green turtles (Chelonia mydas) and critically endangered hawksbill turtles (Eretmochelys imbricata). A total of 1078 days of sand temperature data were collected from 28 logger deployments at nest depth between 2018 and 2022 in Papua New Guinea (PNG). Long-term trends in sand temperature were generated from a model using air temperature as an environmental proxy. The influence of rainfall and seasonal variation on sand temperature was also investigated. Between 1960 and 2019, we estimated that sand temperature increased by ~0.6°C and the average hatchling sex ratio was relatively balanced (46.2% female, SD = 10.7). No trends were observed in historical rainfall anomalies and projections indicated no further changes to rainfall until 2100. Therefore, the sex ratio models were unlikely to be influenced by changing rainfall patterns. A relatively balanced sex ratio such as this is starkly different to the extremely female-skewed hatchling sex ratio (>99% female) reported for another Coral Sea nesting site, Raine Island (~850 km West). This PNG nesting site is likely rare in the global context, as it is less threatened by climate-induced feminisation. Although there is no current need for 'cooling' interventions, the mean projected sex ratios for 2020-2100 were estimated 76%-87% female, so future interventions may be required to increase male production. Our use of long-term sand temperature and rainfall trends has advanced our understanding of climate change impacts on sea turtles.

Can a present-day thermal niche be preserved in a warming climate by a shift in phenology? A case study with sea turtles.

How species respond to climate change may impact their extinction probability. Here we link climatology and ecology to tackle a globally important conservation question. For sea turtles, there are concerns that climate warming will cause both the feminization of populations as well as reduced hatchling survival. For 58 nesting sites across the world spanning all seven sea turtle species, we investigated whether warming might be avoided by shifts in nesting phenology to a cooler part of the year. We show that even with the most extreme phenological shift that has been reported to date-an 18-day advance in nesting per °C increase in sea surface temperature (SST)-temperatures will continue to increase at nesting sites with climate warming. We estimate that SST at nesting sites will rise by an average of 0.6°C (standard deviation = 0.9°C, n = 58) when we model a 1.5°C rise in SST combined with a best-case-scenario shift in nesting. Since sea turtles exhibit temperature-dependent sex determination, these temperature rises could lead to increasingly female-biased sex ratios as well as reduced hatchling production at sites across the world. These findings underscore concerns for the long-term survival of this iconic group.

Evidence of adult male scarcity associated with female-skewed offspring sex ratios in sea turtles.

Climate change is a clear and present threat to species survival. For species with temperature-dependent sex determination, including all sea turtles, it has been hypothesised that climate change may drive the creation of sex-ratio biases leading to population extinctions1. Through a global analysis across multiple species, we present the first direct empirical evidence for a demographic consequence of male scarcity in sea turtle populations, with a lower incidence of multiple paternity being found in populations with more extreme female-biased hatchling sex-ratio skews. For green turtles, when the female bias in hatchling sex ratio was >90%, the incidence of multiple paternity was low compared to other nesting sites, being 24.5% in the eastern Mediterranean (Cyprus), 36.4% on Redang Island (Malaysia) and 15.4% on the southern Great Barrier Reef (Heron Island, Australia) compared to higher values (range 61.1-91.7%) at other sites globally. These results suggest that a low incidence of multiple paternity may serve as a harbinger of future problems with egg fertility if males become even scarcer. Assessments of the incidence of multiple paternity at sites where adult males are expected to become scarce, such as Raine Island on the northern Great Barrier Reef in Australia, may help to identify when a lack of males raises the threat of local extinctions. In such cases, intervention to increase the production of male hatchlings may be needed.

Changes in mean body size in an expanding population of a threatened species.

With some taxa, a reduction in the mean size of individuals may reflect over-harvesting and/or trophy hunting. However, we show that in sea turtles, a reduction in the mean size of breeding individuals may be part of the good news story of an expanding population. We describe a 70-fold increase in annual nest numbers on the island of Sal (Cape Verde, North Atlantic) between 2008 and 2020 (from 506 to 35 507 nests), making this now one of the largest loggerhead (Caretta caretta) nesting aggregations in the world. We use 20 128 measurements of the size of nesting turtles to show that their mean annual size has decreased by about 2.4 cm, from 83.2 to 80.8 cm. This decrease in the mean size of nesting turtles was not caused by the removal of larger turtles, for example by selective harvesting. Rather we develop a theoretical model to show than this decrease in mean size can be explained by an influx of first-time nesters, combined with a decrease in the size of those first-time nesters over time. A reduction in mean size of nesting turtles has been reported across the Atlantic, Pacific and Indian Oceans, and may be a common feature of population recoveries in sea turtles.

Travel routes to remote ocean targets reveal the map sense resolution for a marine migrant.

How animals navigate across the ocean to isolated targets remains perplexing greater than 150 years since this question was considered by Charles Darwin. To help solve this long-standing enigma, we considered the likely resolution of any map sense used in migration, based on the navigational performance across different scales (tens to thousands of kilometres). We assessed navigational performance using a unique high-resolution Fastloc-GPS tracking dataset for post-breeding hawksbill turtles (Eretmochelys imbricata) migrating relatively short distances to remote, isolated targets on submerged banks in the Indian Ocean. Individuals often followed circuitous paths (mean straightness index = 0.54, range 0.14-0.93, s.d. = 0.23, n = 22), when migrating short distances (mean beeline distance to target = 106 km, range 68.7-178.2 km). For example, one turtle travelled 1306.2 km when the beeline distance to the target was only 176.4 km. When off the beeline to their target, turtles sometimes corrected their course both in the open ocean and when encountering shallow water. Our results provide compelling evidence that hawksbill turtles only have a relatively crude map sense in the open ocean. The existence of widespread foraging and breeding areas on isolated oceanic sites points to target searching in the final stages of migration being common in sea turtles.

How well do embryo development rate models derived from laboratory data predict embryo development in sea turtle nests?

Development rate of ectothermic animals varies with temperature. Here we use data derived from laboratory constant temperature incubation experiments to formulate development rate models that can be used to model embryonic development rate in sea turtle nests. We then use a novel method for detecting the time of hatching to measure the in situ incubation period of sea turtle clutches to test the accuracy of our models in predicting the incubation period from nest temperature traces. We found that all our models overestimated the incubation period. We hypothesize three possible explanations which are not mutually exclusive for the mismatch between our modeling and empirically measured in situ incubation period: (1) a difference in the way the incubation period is calculated in laboratory data and in our field nests, (2) inaccuracies in the assumptions made by our models at high incubation temperatures where there is no empirical laboratory data, and (3) a tendency for development rate in laboratory experiments to be progressively slower as temperature decreases compared with in situ incubation.

Reconstructing past thermal conditions in beach microclimates.

Reconstruction of past conditions provides important information on how ecosystems have been impacted by climate change, but generally for microhabitats worldwide there are no long-term empirical measurements. In these cases, there has been protracted debate about how various large-scale environmental proxies can best be used to reconstruct local temperatures. Here we help resolve this debate by examining how well environmental proxies hindcast sand temperatures at nest depths for five sea turtle nesting sites across the world. We link instrumental air temperature and sea surface temperature records with empirical sand temperature observations in the Atlantic (Ascension Island and Cape Verde), the Indian Ocean (Chagos Archipelago), the Caribbean (St Eustatius) and the Pacific (French Polynesia). We found strong correlations between sea surface temperatures, air temperatures and sand temperatures at all our study sites. Furthermore, Granger causality testing shows variations in sea surface temperature and air temperature precede variations in sand temperatures. We found that different proxies (air or sea temperature or a combination of both) predicted mean monthly sand temperatures within <0.5°C of empirical observations. Reconstructions of sand temperatures over the last 170 years reveal a slight warming of temperatures (maximum 0.5°C per century). An analysis of 36 published datasets revealed that the gradient of the relationship between sand temperature and air temperature is relatively constant, suggesting long-term changes in sand temperature could be extended around the world to include nesting sites where there are no empirical measurements of sand temperature. Our approaches are likely to have utility for a range of microhabitats where there is an interest in long-term changes in temperature.

Why do Argos satellite tags stop relaying data?

Satellite tracking of animals is very widespread across a range of marine, freshwater, and terrestrial taxa. Despite the high cost of tags and the advantages of long deployments, the reasons why tracking data from tags stop being received are rarely considered, but possibilities include shedding of the tag, damage to the tag (e.g., the aerial), biofouling, battery exhaustion, or animal mortality.We show how information relayed via satellite tags can be used to assess why tracking data stop being received. As a case study to illustrate general approaches that are broadly applicable across taxa, we examined data from Fastloc-GPS Argos tags deployed between 2012 and 2019 on 78 sea turtles of two species, the green turtle (Chelonia mydas) and the hawksbill turtle (Eretmochelys imbricata).Tags transmitted for a mean of 267 days (SD = 113 days, range: 26-687 days, median = 251 days). In 68 of 78 (87%) cases, battery failure was implicated as the reason why tracking data stopped being received. Some biofouling of the saltwater switches, which synchronize transmissions with surfacing, was evident in a few tags but never appeared to be the reason that data reception ceased.Objectively assessing why tags fail will direct improvements to tag design, setup, and deployment regardless of the study taxa. Assessing why satellite tags stop transmitting will also inform on the fate of tagged animals, for example, whether they are alive or dead at the end of the study, which may allow improved estimates of survival rates.

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.

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.

Optimism for mitigation of climate warming impacts for sea turtles through nest shading and relocation.

Increasing incubation temperatures may threaten the viability of sea turtle populations. We explored opportunities for decreasing incubation temperatures at a Caribbean rookery with extreme female-biased hatchling production. To investigate the effect of artificial shading, temperatures were measured under simple materials (white sheet, white sand, palm leaves). To test natural drivers of incubation temperature, temperatures were measured at average nest depths with shading on two beaches. Results from a pilot experiment suggest the most effective material was palm leaves. Shading decreased temperatures by a mean of 0.60 °C (SE = 0.10 °C, N = 20). Variation between beaches averaged 1.88 °C (SE = 0.13 °C, N = 20). We used long-term rookery data combined with experimental data to estimate the effect on sex ratio: relocation and shading could shift ratios from current ranges (97-100% female) to 60-90% female. A conservation mitigation matrix summarises our evidence that artificial shading and nest relocation are effective, low-cost, low-technology conservation strategies to mitigate impacts of climate warming for sea turtles.

Climate change and temperature-linked hatchling mortality at a globally important sea turtle nesting site.

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 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.

Population viability at extreme sex-ratio skews produced by temperature-dependent sex determination.

For species with temperature-dependent sex determination (TSD) there is the fear that rising temperatures may lead to single-sex populations and population extinction. We show that for sea turtles, a major group exhibiting TSD, these concerns are currently unfounded but may become important under extreme climate warming scenarios. We show how highly female-biased sex ratios in developing eggs translate into much more balanced operational sex ratios so that adult male numbers in populations around the world are unlikely to be limiting. Rather than reducing population viability, female-biased offspring sex ratios may, to some extent, help population growth by increasing the number of breeding females and hence egg production. For rookeries across the world (n = 75 sites for seven species), we show that extreme female-biased hatchling sex ratios do not compromise population size and are the norm, with a tendency for populations to maximize the number of female hatchlings. Only at extremely high incubation temperature does high mortality within developing clutches threaten sea turtles. Our work shows how TSD itself is a robust strategy up to a point, but eventually high mortality and female-only hatchling production will cause extinction if incubation conditions warm considerably in the future.

Male hatchling production in sea turtles from one of the world's largest marine protected areas, the Chagos Archipelago.

Sand temperatures at nest depths and implications for hatchling sex ratios of hawksbill turtles (Eretmochelys imbricata) and green turtles (Chelonia mydas) nesting in the Chagos Archipelago, Indian Ocean are reported and compared to similar measurements at rookeries in the Atlantic and Caribbean. During 2012-2014, temperature loggers were buried at depths and in beach zones representative of turtle nesting sites. Data collected for 12,546 days revealed seasonal and spatial patterns of sand temperature. Depth effects were minimal, perhaps modulated by shade from vegetation. Coolest and warmest temperatures were recorded in the sites heavily shaded in vegetation during the austral winter and in sites partially shaded in vegetation during summer respectively. Overall, sand temperatures were relatively cool during the nesting seasons of both species which would likely produce fairly balanced hatchling sex ratios of 53% and 63% male hatchlings, respectively, for hawksbill and green turtles. This result contrasts with the predominantly high female skew reported for offspring at most rookeries around the globe and highlights how local beach characteristics can drive incubation temperatures. Our evidence suggests that sites characterized by heavy shade associated with intact natural vegetation are likely to provide conditions suitable for male hatchling production in a warming world.