A pulse check for trends in sea turtle numbers across the globe.

Population declines of vertebrates are common, but rebuilding marine life may be possible. We assessed trends in sea turtle numbers globally, building 61 time series of abundance extending beyond 2015, representing monitoring in >1200 years. Increases were widespread with significant upward trends, no significant change, and significant downward trends in 28, 28, and 5 time series, respectively. For example, annual nest numbers increased between 1980 and 2018 from around 4,000 to 16,000 for green turtles at Aldabra (Seychelles, Indian Ocean) and between 2008 and 2020 from around 500 to 35,000 for loggerhead turtles in Sal (Cape Verde, north Atlantic). However, conservation concerns remain. Major populations may experience declines, such as loggerhead turtles in Oman, while previous upward trends can be reversed, as with green turtles nesting at Tortuguero (Costa Rica, Caribbean). Further, decreases in abundance were evident in several leatherback turtle time series. These concerns show there is no room for complacency for sea turtle conservation.

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.

The ecological importance of the accuracy of environmental temperature measurements.

The implications of logger accuracy and precision are rarely considered prior to their application in many ecological studies. We assessed the accuracy and precision of three temperature data loggers widely used in ecological studies (Hobo®, iButton® and TinyTag®). Accuracy was highest in TinyTags (95% of readings were within 0.23°C of the true temperature) and lowest in HOBOs and iButtons (95% of were readings within 0.43°C and 0.49°C of the true temperature, respectively). The precision (standard deviation of the repeat measurements) was greatest in TinyTags (0.04°C), followed by iButtons (0.17°C) and then HOBOs (0.22°C). As a case study, we then considered how modelled estimates of sea turtle hatchling sex ratios (derived from temperature), could vary as a function of logger accuracy. For example, at 29°C when the mean sex ratio derived was 0.47 female, the sex ratio estimate from a single logger could vary between 0.40 and 0.50 for TinyTags and 0.29 and 0.56 for both HOBOs and iButtons. Our results suggest that these temperature loggers can provide reliable descriptions of sand temperature if they are not over-interpreted. Logger accuracy must be considered in future ecological studies in which temperature thresholds are important.

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.

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.

High accuracy tracking reveals how small conservation areas can protect marine megafauna.

Space use estimates can inform conservation management but relaying high-accuracy locations is often not straightforward. We used Fastloc-GPS Argos satellite tags with the innovation of additional data relay via a ground station (termed a "Mote") to record high volumes (typically >20 locations per individual per day) of high accuracy tracking data. Tags were attached in the Chagos Archipelago (Indian Ocean) in 2018-2019 to 23 immature turtles of two species for which there have been long-standing conservation concerns: 21 hawksbill turtles (Eretmochelys imbricata) and two green turtles (Chelonia mydas). Over long tracking durations (mean 227.6 d per individual), most turtles moved very little. For example, 17 of 21 hawksbill turtles remained continuously in the lagoon where they were equipped, with 95% and 50% utilization distributions (UDs) averaging only 1.03 and 0.18 km2 , respectively. Many individuals, and both species, could use the same small spaces, i.e., individuals did not maintain unique home ranges. However, three hawksbill turtles travelled hundreds of kilometers from the tagging site. Our results show that, for some large marine vertebrates, even small protected areas of only a few square kilometers can encompass the movements of a large proportion of individuals over long periods. High accuracy tracking may likewise reveal the details of space use for many other animals that move little and/or use important focal areas and where previous low-accuracy tracking techniques have tended to overestimate space use.

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.

Mutualism promotes site selection in a large marine planktivore.

Mutualism is a form of symbiosis whereby both parties benefit from the relationship. An example is cleaning symbiosis, which has been observed in terrestrial and marine environments. The most recognized form of marine cleaning symbiosis is that of cleaner fishes and their clients.Cleaner species set up cleaning stations on the reef, and other species seek out their services. However, it is not well understood how the presence of cleaning stations influence movements of large highly mobile species. We examined the role of cleaning stations as a driver of movement and habitat use in a mobile client species.Here, we used a combination of passive acoustic telemetry and in-water surveys to investigate cleaning station attendance by the reef manta ray Mobula alfredi. We employed a novel approach in the form of a fine-scale acoustic receiver array set up around a known cleaning area and tagged 42 rays. Within the array, we mapped structural features, surveyed the distribution of cleaner wrasse, and observed the habitat use of the rays.We found manta ray space use was significantly associated with blue-streak cleaner wrasse Labroides dimidiatus distribution and hard coral substrate. Cleaning interactions dominated their habitat use at this site, taking precedence over other life history traits such as feeding and courtship.This study has demonstrated that cleaning symbiosis is a driver for highly mobile, and otherwise pelagic, species to visit inshore reef environments. We suggest that targeted and long-term use of specific cleaning stations reflects manta rays having a long-term memory and cognitive map of some shallow reef environments where quality cleaning is provided. We hypothesize that animals prefer cleaning sites in proximity to productive foraging regions.

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.

Human disturbance causes widespread disruption of animal movement.

Disturbance and habitat modification by humans can alter animal movement, leading to negative impacts on fitness, survival and population viability. However, the ubiquity and nature of these impacts across diverse taxa has not been quantified. We compiled 208 studies on 167 species from terrestrial and aquatic ecosystems across the globe to assess how human disturbance influences animal movement. We show that disturbance by humans has widespread impacts on the movements of birds, mammals, reptiles, amphibians, fish and arthropods. More than two-thirds of 719 cases represented a change in movement of 20% or more, with increases in movement averaging 70% and decreases -37%. Disturbance from human activities, such as recreation and hunting, had stronger impacts on animal movement than habitat modification, such as logging and agriculture. Our results point to a global restructuring of animal movement and emphasize the need to reduce the negative impacts of humans on animal movement.

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.

Open Ocean Reorientation and Challenges of Island Finding by Sea Turtles during Long-Distance Migration.

In 1873, Charles Darwin marveled at the ability of sea turtles to find isolated island breeding sites [1], but the details of how sea turtles and other taxa navigate during these migrations remains an open question [2]. Exploring this question using free-living individuals is difficult because, despite thousands of sea turtles being satellite tracked across hundreds of studies [3], most are tracked to mainland coasts where the navigational challenges are easiest. We overcame this problem by recording unique tracks of green turtles (Chelonia mydas) migrating long distances in the Indian Ocean to small oceanic islands. Our work provides some of the best evidence to date, from naturally migrating sea turtles, for an ability to reorient in the open ocean, but only at a crude level. Using individual-based models that incorporated ocean currents, we compared actual migration tracks against candidate navigational models to show that turtles do not reorient at fine scales (e.g., daily), but rather can travel several 100 km off the direct routes to their goal before reorienting, often in the open ocean. Frequently, turtles did not home to small islands with pinpoint accuracy, but rather overshot and/or searched for the target in the final stages of migration. These results from naturally migrating individuals support the suggestion from previous laboratory work [4-6] that turtles use a true navigation system in the open ocean, but their map sense is coarse scale.

Long-term photo-id and satellite tracking reveal sex-biased survival linked to movements in an endangered species.

Sex-biased survival linked to anthropogenic threats places populations at risk. We show the utility of long-term multidecadal photo-identification (photo-id) combined with long-term high-resolution (Fastloc-GPS) satellite telemetry to investigate the links between mortality rates and patterns of movement for a wide-ranging, endangered marine vertebrate. Using a photo-identification database of 947 loggerhead turtles (Caretta caretta) compiled over 18 yr, we estimated greater annual survival rates of females (0.89; 95% confidence interval [CI] 0.87-0.90) compared to males (0.73; 95% CI 0.67-0.78). For males satellite-tracked across multiple breeding seasons, 100% (26 of 26) returned to the same breeding site, suggesting the calculated lower male survival rate was likely not due to emigration to breed elsewhere. 10,111 and 2,524 tracking days for males (n = 39 individuals) and females (n = 18 individuals), respectively, revealed different habitat-use patterns outside the breeding season: males tended to occupy foraging sites closer to shore and closer to breeding sites but, due to their generally annual breeding, compared to biennial breeding for females, males migrated further per year on average. These differences in movement patterns likely contribute to higher mortality in males through increased interaction with anthropogenic threats. Long-term identification coupled with tracking offers great promise for estimating the survival rates of other wide-ranging species.

Fidelity to foraging sites after long migrations.

Patterns of animal movement associated with foraging lie at the heart of many ecological studies and often animals face decisions of staying in an environment they know versus relocating to new sites. The lack of knowledge of new foraging sites means there is risk associated with a decision to relocate (e.g. poor foraging) as well as a potential benefit (e.g. improved foraging). Using a unique long-term satellite tracking dataset for several sea turtle species, combined with capture-mark-recapture data extending over 50 years, we show how, across species, individuals generally maintain tight fidelity to specific foraging sites after extended (up to almost 10,000 km) migration to and from distant breeding sites as well as across many decades. Migrating individuals often travelled through suitable foraging areas en route to their 'home' site and so extended their journeys to maintain foraging site fidelity. We explore the likely mechanistic underpinnings of this trait, which is also seen in some migrating birds, and suggest that individuals will forgo areas of suitable forage encountered en route during migration when they have poor knowledge of the long-term suitability of those sites, making relocation to those sites risky.

The importance of migratory connectivity for global ocean policy.

The distributions of migratory species in the ocean span local, national and international jurisdictions. Across these ecologically interconnected regions, migratory marine species interact with anthropogenic stressors throughout their lives. Migratory connectivity, the geographical linking of individuals and populations throughout their migratory cycles, influences how spatial and temporal dynamics of stressors affect migratory animals and scale up to influence population abundance, distribution and species persistence. Population declines of many migratory marine species have led to calls for connectivity knowledge, especially insights from animal tracking studies, to be more systematically and synthetically incorporated into decision-making. Inclusion of migratory connectivity in the design of conservation and management measures is critical to ensure they are appropriate for the level of risk associated with various degrees of connectivity. Three mechanisms exist to incorporate migratory connectivity into international marine policy which guides conservation implementation: site-selection criteria, network design criteria and policy recommendations. Here, we review the concept of migratory connectivity and its use in international policy, and describe the Migratory Connectivity in the Ocean system, a migratory connectivity evidence-base for the ocean. We propose that without such collaboration focused on migratory connectivity, efforts to effectively conserve these critical species across jurisdictions will have limited effect.