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.

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.

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.

How numbers of nesting sea turtles can be overestimated by nearly a factor of two.

Estimating the absolute number of individuals in populations and their fecundity is central to understanding the ecosystem role of species and their population dynamics as well as allowing informed conservation management for endangered species. Estimates of abundance and fecundity are often difficult to obtain for rare or cryptic species. Yet, in addition, here we show for a charismatic group, sea turtles, that are neither cryptic nor rare and whose nesting is easy to observe, that the traditional approach of direct observations of nesting has likely led to a gross overestimation of the number of individuals in populations and underestimation of their fecundity. We use high-resolution GPS satellite tags to track female green turtles throughout their nesting season in the Chagos Archipelago (Indian Ocean) and assess when and where they nested. For individual turtles, nest locations were often spread over several tens of kilometres of coastline. Assessed by satellite observations, a mean of 6.0 clutches (range 2-9, s.d. = 2.2) was laid by individuals, about twice as many as previously assumed, a finding also reported in other species and ocean basins. Taken together, these findings suggest that the actual number of nesting turtles may be almost 50% less than previously assumed.

Use of long-distance migration patterns of an endangered species to inform conservation planning for the world's largest marine protected area.

Large marine protected areas (MPAs), each hundreds of thousands of square kilometers, have been set up by governments around the world over the last decade as part of efforts to reduce ocean biodiversity declines, yet their efficacy is hotly debated. The Chagos Archipelago MPA (640,000 km(2) ) (Indian Ocean) lies at the heart of this debate. We conducted the first satellite tracking of a migratory species, the green turtle (Chelonia mydas), within the MPA and assessed the species' use of protected versus unprotected areas. We developed an approach to estimate length of residence within the MPA that may have utility across migratory taxa including tuna and sharks. We recorded the longest ever published migration for an adult cheloniid turtle (3979 km). Seven of 8 tracked individuals migrated to distant foraging grounds, often ≥1000 km outside the MPA. One turtle traveled to foraging grounds within the MPA. Thus, networks of small MPAs, developed synergistically with larger MPAs, may increase the amount of time migrating species spend within protected areas. The MPA will protect turtles during the breeding season and will protect some turtles on their foraging grounds within the MPA and others during the first part of their long-distance postbreeding oceanic migrations. International cooperation will be needed to develop the network of small MPAs needed to supplement the Chagos Archipelago MPA.

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.

First evidence of marine turtle gastroliths in a fossil specimen: Paleobiological implications in comparison to modern analogues.

Semi-articulated remains of a large chelonioid turtle from the Turonian strata (Upper Cretaceous; ca. 93.9-89.8 Myr) near Sant'Anna d'Alfaedo (Verona province, northeastern Italy) are described for the first time. Together with the skeletal elements, the specimen also preserves pebbles inside the thoracic area which are lithologically distinct from the surrounding matrix. These allochthonous clasts are here interpreted as geo-gastroliths, in-life ingested stones that resided in the digestive tract of the animal. This interpretation marks the first reported evidence of geophagy in a fossil marine turtle. SEM-EDS analysis, together with macroscopic petrological characterization, confirm the presence of both siliceous and carbonatic pebbles. These putative geo-gastroliths have morphometries and size ranges more similar to those of gastroliths in different taxa (fossils and extant) than allochthonous "dropstone" clasts from the same deposit that were carried by floating vegetation A dense pitted pattern of superficial erosion is microscopically recognizable on the carbonatic gastroliths, consistent with surface etching due to gastric acids. The occurrence of a similar pattern was demonstrated by the experimental etching of carbonatic pebbles with synthetic gastric juice. Gut contents of modern green sea turtles (Chelonia mydas) were surveyed for substrate ingestion, providing direct evidence of geophagic behavior in extant chelonioids. Comparison with modern turtle dietary habits may suggests that the pebbles were ingested as a way to supplement calcium after or in preparation for egg deposition, implying that the studied specimen was possibly a gravid female.

Uncertain future for global sea turtle populations in face of sea level rise.

Sea level rise has accelerated during recent decades, exceeding rates recorded during the previous two millennia, and as a result many coastal habitats and species around the globe are being impacted. This situation is expected to worsen due to anthropogenically induced climate change. However, the magnitude and relevance of expected increase in sea level rise (SLR) is uncertain for marine and terrestrial species that are reliant on coastal habitat for foraging, resting or breeding. To address this, we showcase the use of a low-cost approach to assess the impacts of SLR on sea turtles under various Intergovernmental Panel on Climate Change (IPCC) SLR scenarios on different sea turtle nesting rookeries worldwide. The study considers seven sea turtle rookeries with five nesting species, categorized from vulnerable to critically endangered including leatherback turtles (Dermochelys coriacea), loggerhead turtles (Caretta caretta), hawksbill turtles (Eretmochelys imbricata), olive ridley turtles (Lepidochelys olivacea) and green turtles (Chelonia mydas). Our approach combines freely available digital elevation models for continental and remote island beaches across different ocean basins with projections of field data and SLR. Our case study focuses on five of the seven living sea turtle species. Under moderate climate change scenarios, by 2050 it is predicted that at some sea turtle nesting habitats 100% will be flooded, and under an extreme scenario many sea turtle rookeries could vanish. Overall, nesting beaches with low slope and those species nesting at open beaches such as leatherback and loggerheads sea turtles might be the most vulnerable by future SLR scenarios.

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.

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.

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.

Mimicry of emergent traits amplifies coastal restoration success.

Restoration is becoming a vital tool to counteract coastal ecosystem degradation. Modifying transplant designs of habitat-forming organisms from dispersed to clumped can amplify coastal restoration yields as it generates self-facilitation from emergent traits, i.e. traits not expressed by individuals or small clones, but that emerge in clumped individuals or large clones. Here, we advance restoration science by mimicking key emergent traits that locally suppress physical stress using biodegradable establishment structures. Experiments across (sub)tropical and temperate seagrass and salt marsh systems demonstrate greatly enhanced yields when individuals are transplanted within structures mimicking emergent traits that suppress waves or sediment mobility. Specifically, belowground mimics of dense root mats most facilitate seagrasses via sediment stabilization, while mimics of aboveground plant structures most facilitate marsh grasses by reducing stem movement. Mimicking key emergent traits may allow upscaling of restoration in many ecosystems that depend on self-facilitation for persistence, by constraining biological material requirements and implementation costs.

Translating Marine Animal Tracking Data into Conservation Policy and Management.

There have been efforts around the globe to track individuals of many marine species and assess their movements and distribution, with the putative goal of supporting their conservation and management. Determining whether, and how, tracking data have been successfully applied to address real-world conservation issues is, however, difficult. Here, we compile a broad range of case studies from diverse marine taxa to show how tracking data have helped inform conservation policy and management, including reductions in fisheries bycatch and vessel strikes, and the design and administration of marine protected areas and important habitats. Using these examples, we highlight pathways through which the past and future investment in collecting animal tracking data might be better used to achieve tangible conservation benefits.

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.

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.