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.


Scientific Reports
| (2023) 13:5277 | https://doi.org/10.1038/s41598-023-31467-1 www.nature.com/scientificreports/ low accuracy 19 . Other approaches which couple LiDAR with biological data 20,21 have higher accuracy, but are also more costly 22 . However, new methodologies, such as the use of open Digital Elevation Models (DEMs) might be a good proxy broadly applicable to assess SLR by satellite images 23 .
Considering that most sea turtle rookeries across the globe are located in remote areas in low and middleincome countries, less costly approaches for field surveys are often preferred and can provide baseline data to identify areas at most risk. Indeed, the few studies assessing the impacts of SLR on sea turtles to date discuss the challenges inherent in successfully predicting shoreline response to SLR and storm activities 17,18 and the inability to couple projections with biological information such as sex ratios and reproductive success 12 . Here we present an assessment of the potential impact of SLR on sea turtle rookeries by applying a low-cost methodology to estimate the probability of flooding of nest locations under multiple IPCC SLR scenarios. This approach combines turtle nest locations, freely available DEMs and Climate Central maps under Coastal DEM predictions 22 . The study considers seven sea turtle rookeries with five nesting species, categorized from vulnerable to critically endangered 24 including leatherback turtles (Dermochelys coriacea), loggerhead turtles (Caretta caretta), hawksbill turtles (Eretmochelys imbricata), olive ridley turtles (Lepidochelys olivacea) and green turtles (Chelonia mydas) ( Fig. 1; Extended Data Table 1). Our study sites encompass some important nesting sites for sea turtles globally (e.g., Raine Island, Australia, the largest green turtle rookery worldwide 25 ) and have different characteristics (i.e., beach width, slope, size), which will allow us to estimate SLR effects on a wide range of nesting rookeries and highlights the broad applicability of our approach.

Vulnerability of sea turtle nests to SLR
From GPS locations of 2835 marine turtle nests belonging to five different species from seven study areas across the globe, we estimated the vulnerability of nests to flooding considering available projections of SLR caused by climate change from 2010 to 2100 (Fig. 1). Firstly, we used data from GPS nest locations + available DEMs + IPCC  www.nature.com/scientificreports/ projections for the seven studied populations across the globe to assess and compare the suitability of the different DEMs to make flooding predictions. The comparison of freely available elevation data shows that the mean estimated elevation for nest sites (and consequently mean proportion of flooded nests) differed substantially between DEM sources for each rookery (Extended Data Fig. 2). It was expected that the highest resolution (30 m) DEMs would be most accurate (compared with lower resolutions of 90-100 m) but there were similarities in accuracy amongst DEMs for each study site ( Fig. 2; Extended Data Figs. 3 and 4). In addition, Cohen's kappa results showed weak relationships between DEM model predictions and the in situ data ( Fig. 3; Supplementary  Table 3). Then, we estimated the probability of flooding from GPS nest locations georeferenced on CoastalDEM maps (e.g., Extended Data Fig. 5) for five of the seven study areas, since CoastalDEM did not provide reliable estimates in Costa Rica and Ecuador (e.g., Extended Data Fig. 6). For the other five study areas, predictions from Coastal DEM maps (Fig. 4) and from basic in situ data (Supplementary Tables 8-15) were reliable to predicting nest flooding under SLR. Raine Island (Australia) and Saona Island (Dominican Republic) are the most vulnerable populations with 100% nest flooding predicted under moderate emissions scenarios for 2050 ( Fig. 1; Supplementary Table 4). For Florida, flooding probability greatly increases after 2050 ( Fig. 2a; Supplementary Table 5). Cuba, probably thanks to their elevated beaches, showed the lowest vulnerability to flooding throughout the twenty-first century ( Fig. 2b; Supplementary Table 6). For St. Eustatius, main differences in flooding vulnerability arise from differences between turtle species (see Fig. 4c and next section).
Overall, our results suggested that flat islands and cays may be highly vulnerable to sea level rise under the moderate IPCC scenario ( Fig. 1; Supplementary Table 4) 7,26 predominantly those in the Caribbean and Pacific 27,28 . Some of these locations are important rookeries 25,29 for species which return every 1-4 years to nest at the beach where they were born 9 . Furthermore, some of them host nestings for more than one species and present several nesting environments and beach characteristics such as different slopes, width, or sand grain size, among others [30][31][32] .
A number of rookeries subjected to beach erosion have already been assessed as vulnerable due to loss of beaches used for nesting 8,33 , nest loss 21,32 and changes in nesting behaviour 16 . The philopatry of leatherbacks 34 and loggerheads is not quite strict 35 and they can move great distances and nest further up the beach in response to SLR depending on future beach availability. However, it has already been reported that 20% of Costa Rican leatherbacks nest in flooded areas when scarp barriers were present 30 . The expected habitat loss rates found in the study areas could have important effects on nesting success since philopatry could lead many individuals to nest www.nature.com/scientificreports/ on inundated beaches. An unknown variable is the potential for sea turtles to adapt to new scenarios. Therefore, their survivorship will depend on their resilience and adaptability to rapid changes within their nesting habitats 36 .

Vulnerability of nests across species
To determine differences between modelled nest flooding probabilities by species we assessed rookeries containing multiple species (i.e., St Eustatius, Dominican Republic and Ecuador rookeries; Fig. 1). Overall, we identified that leatherback turtle nests may be at a higher risk from flooding compared to the rest of the studied species because they tend to nest in open areas near to the high tide line (Fig. 4c). In St Eustatius, significant variation exists between nest flooding probability by species (Supplementary Table 7): leatherback turtle nests are at the highest risk from flooding compared with green turtles (ß = 1.892, p < 0.001; Fig. 4c), and there was no significant difference between flooding risk for hawksbill and green turtle nests (ß = 0.388, p = 0.339; Supplementary Table 3). The model predicted that, on average, 50.0% leatherback, 18.2% hawksbill and 13.1% of green turtle nest locations would be flooded by 2050 ( Fig. 1; Supplementary Table 4). The predicted model accuracy for estimation of likelihood of nest flooding was 79.4%. Leatherback turtle nests in open areas of beaches have been found to already been subject to occasional flooding 30 , whilst hawksbill and green turtles tend to nest at higher elevations closer to dunes and steep cliffs along the coastline 37 and olive ridleys nest at open beaches with low slopes 38 . This difference in nesting location might explain those differences in nest location flooding potential between species. In consequence, leatherback turtle populations as well as other turtles nesting at open beaches (e.g., loggerhead turtles) may be at greater risk from SLR than other species. In Ecuador, no differences in modelled nest flooding severity were found between olive ridley, greens and hawksbill species, potentially due to beaches at this location being steeper 32 (Supplementary Table 15). Similarly, no difference in nest flooding was predicted between nests of different species in the Dominican Republic, although only because all locations were estimated to be inundated by 2050 ( Fig. 1; Supplementary Table 3;  Supplementary Table 4). It is likely that the potential effect of SLR will vary between species, potentially linked to variables such as nesting beach characteristics (e.g., slope, aspect 39 ), nesting habitat preferences and suitable nesting areas 33 .

Conclusions-conservation concerns
Our models of nest flooding validated by field data considered that even a moderate increase in greenhouse emissions (RCP 4.5) 3 might impact the reproductive output of sea turtles at the rookeries included in our study. Recent predictions of accelerating global SLR due to rapid melting of ice in Greenland 40 and the Antarctic 41 in combination with ocean currents 42 indicate that pessimistic scenarios could be more accurate than conservative scenarios 43 . Such scenarios support our projections by indicating that sea turtle nesting populations could be vulnerable to flooding under even moderate scenarios over the next decades. Relatively recent methods of remote sensing and modeling including DEMs 4,43,44 , drones, photogrammetry and GPS have been adopted to assess impacts of SLR on sea turtle populations 12 . However, most highly accurate methodologies entail high costs (e.g., 1500-15,000€ per satellite image) limiting their use to more localised studies. Considering that most sea turtle nesting populations around the world are located in low and middleincome countries, local conservation projects cannot afford the costs of these intensive methodologies to assess the vulnerability of nesting beaches. We have demonstrated that a methodology based on low-cost technological www.nature.com/scientificreports/ models can be a useful tool for predicting possible future SLR scenarios in important sea turtle nesting areas. We highlighted the utility of global open DEM data with high accuracies for remote areas that could assist with estimation of the vulnerability of sea turtle nesting populations worldwide. Scientific assessments are essential for prediction of the impacts of future climate scenarios and to assist stakeholders and managers in anticipating extreme scenarios of coastal erosion or flooding, and to predict areas at higher risk of flooding 45 . Such assessments will help identify conservation refugia and nesting beaches that have greater resilience to climate change 36 . Although sea turtles have been around for millions of years and would be present in several climate change events, we do not know how their populations might be affected by these projected rapid changes of high loss of nesting sites in the study areas by 2050. Thus, this demonstrates the urgency of developing a multi-species assessment at a global scale in order to develop conservation plans for the most vulnerable populations while there is still time. Conservation management strategies are already in place to enhance resilience to SLR at some nesting beaches, including sand refilling of nesting beaches 46 such as in Raine Island, relocation of nests to safe places 47 or the protection of hatcheries for rookeries with extreme erosion and flooding 31 . In addition, we highlighted the need for climate change adaptation measurements to be implemented in management plans considering estimated projections under moderate SLR scenarios.
However, if the world maintains current carbon dioxide emission rates, worst-case scenarios might be vastly underestimated by 3-4 times 48 and existing management strategies may then be insufficient to protect the future of many sea turtle populations worldwide. In summary, our study predicts massive flooding at important rookeries in Australia, Dominican Republic, Costa Rica and the USA. These critical areas will face the effects of SLR in the next few decades, meaning that it is now urgent to reduce anthropogenic emissions to safeguard the future of sea turtle populations against climate change and associated sea level rise.

Data availability
The datasets used and/or analysed during the current study available from the corresponding author on reasonable request.