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In sea turtle species, high nest temperatures are associated with decreases in incubation period length, hatch success and locomotor performance (Bustard & Greenham 1968; Valverde et al. 2010; Fisher et al. 2014; Booth 2017). Lethal incubation temperatures, which can result in embryonic death and the loss of entire nests, vary between sea turtle species. The threshold point in olive ridleys (Lepidochelys olivacea) is considered to be 35 °C (Valverde et al. 2010; Hill et al. 2015). As regional temperatures increase, the chance of nest temperatures surpassing this threshold also rises. Incubation temperatures also play an important role in sex determination (Mrosovsky & Yntema 1980; Standora & Spotila 1985), so population demography can be affected by the sand temperatures in which embryos develop (Kaska et al. 2006). Increased incubation temperatures produce higher female to male hatchling sex ratios, a trend that is becoming more pronounced with the continuation of anticipated increases in global temperature (Mrosovsky & Yntema 1980; IPCC 2007; Rogers 2013).

These effects could be particularly severe in western Central America, as the region may be exceptionally susceptible to climate change (Giorgi 2006). Future effects on the area could include warming, increased number of hurricanes and tropical storms, and stronger effects of the El Niño Southern Oscillation (ENSO) (Giorgi 2006). The impacts on ENSO are of significant importance to the region as they are predicted to result in higher sea surface temperatures and less precipitous rainy seasons, followed by periods of drought (Waylen et al. 1996; Santidrián-Tomillo et al. 2012). Other marine reptiles have adaptation strategies to survive these climatic anomalies (Wikelski & Thom 2000), though the same adaptations have not been demonstrated in sea turtles (Hawkes et al. 2009). While sea turtles may be able to adapt strategies to survive gradual environmental changes, by processes such as shifting nesting phenology, it is unlikely these mechanisms will be effective in the fast-paced and far-reaching impacts of current climate change. As the effects of ENSO coincide with the August-January nesting season of olive ridleys on the Pacific coast of Costa Rica (Dornfeld et al. 2014), climate change may have a dramatic impact on population size and nesting levels.

The olive ridley is one of the smallest species of sea turtle and is listed as Vulnerable on the IUCN Red List (Abreu-Grobois & Plotkin 2008). It is also the most abundant sea turtle species worldwide, with its largest rookeries located along the northeast coast of India and the western coasts of Central and North America (Polovina et al. 2004). Olive ridleys engage in a bimodal nesting strategy, with females participating in arribada (mass-arrival) nesting events, or, as is found in other species of sea turtle, solitary nesting (Valverde et al. 2010). During a breeding season, females emerge from the surf to lay a clutch of eggs on approximately 1-3 occasions (Hamel et al. 2008). Each of these clutches has 80-120 eggs and is deposited in a roughly 35 cm-deep cavity, with an incubation period of 45-50 days (Pandav et al. 1998).

Using a long-term dataset, we examined relationships between sand and in-nest temperatures and olive ridley nest success, hatchling sex ratios and incubation periods in a solitary nesting population on Playa Coyote, Costa Rica. While arribada populations of olive ridleys are relatively better documented, this study provides novel information relevant to many locations where the species nests in a solitary fashion.

Figure 1. Location of the study site on the western coast ofthe Nicoya Peninsula in Guanacaste, Costa Rica.

Study site. Playa Coyote, encompassing Playa Costa de Oro and Playa San Miguel, is located in Nandayure, Guanacaste, Costa Rica (Fig.1). Both beaches have a turtle conservation project under the direction of CREMA (Rescue Center for Endangered Marine Species). On Playa San Miguel, this conservation project began in 1998, while the project on Playa Costa de Oro started in 2012 (Viejobueno & Arauz 2015; Beange & Arauz 2017). Both projects involve nightly patrols to locate nesting sea turtles and relocate nests to a hatchery to alleviate poaching pressures. Primarily olive ridley turtles nest on Playa Coyote, however occasional leatherback (Dermochelys coriacea), green (Chelonia mydas) and hawksbill (Eretmochelys imbricata) turtles also come ashore. The monitoring season coincides with the peak-nesting season for olive ridleys on the Nicoya Peninsula, beginning at the start of June and concluding in mid-late December.

Research Techniques. To record sand temperature in the on-beach environment, three HOBO-model pendant-series temperature loggers (Onset, USA), programmed to log temperature hourly, were placed at depths of 25-30 cm below the surface of the sand in order to mimic the mid-nest depth of a natural olive ridley nest. These three loggers were placed at each of the following positions: above the vegetation line (~100% vegetation cover), at a midpoint between the vegetation and the beach (~50% vegetation cover) and on the beach (~0% vegetation cover). In-nest temperatures were also recorded with the use of a similarly programmed HOBO data logger placed at the midpoint (50% of all eggs were placed in the chamber, followed by the logger and remaining eggs) of an olive ridley clutch within the hatchery. The number of these in- nest temperature loggers varied from year to year, with anywhere from 2-6 per year being used on both Playa Costa de Oro and Playa San Miguel between the nesting seasons of 2013-2017 (Table 1). In addition, two HOBO data loggers were placed at depths of 25-30 cm outside of nests within the hatchery to collect sand temperature data throughout the incubation period and control for the thermal production of the incubating eggs. The temperature data collected by the HOBO loggers were then analyzed by either trimester averages for in-nest HOBOs, or monthly and yearly averages for beach and out-of-nest hatchery sensors. The number of hours each nest exceeded the lethal field incubation temperature of 35 °C was also recorded (Hill et al. 2015). Data were recorded to delineate the dates in which the data loggers were placed and when the majority of hatchlings emerged, in order to determine incubation periods.

Upon hatching, each nest was excavated to determine hatching and nest emergence success, and the developmental stage of embryos in eggs that failed to hatch. The incubation period was defined as the date eggs were placed in the hatchery to the date of the major emergence of hatchlings. Trimesters were calculated by dividing the incubation period (in days) by three. Wibbels (2007) reported the thermo-sensitive period of sex determination to fall within the second trimester of incubation, and the pivotal temperature to lie between 30.0-31.0 °C, so we assumed the pivotal temperature was 30.5 °C in this study, and estimated sex ratios using the average temperature of the second trimester of each nest (Valverde et al. 2010). Average temperatures of the second trimester above 30.5 °C were considered to be majority-female nests (greater than 50% female), and majority-male nests were presumed for temperatures below 30.5 °C. While pivotal temperatures may vary geographically and among species, we used similar techniques to those employed by Valverde et al. (2010) on Ostional Beach, the more proximate location studying sex ratios and temperature in olive ridleys (Hernández-Echeagaray et al. 2012; Rogers 2013).

Prior to emergence, plastic mesh was placed on top of the nests so that emerging hatchlings could be corralled and counted. Hatching success was calculated by adding the number of emerged hatchlings to the number of hatchlings found in the nest chamber during excavations and subsequently dividing this sum by the total number of eggs counted at the time of deposition. Linear regression models and associated correlation calculations, including Pearson correlations, linear regression t-tests and 95% confidence intervals for slope, were used to test relationships between average nest temperature and both nest success and incubation period. These calculations were also used to test the association between nest success and the number of hours each nest exceeded the 35 °C lethal temperature threshold. All calculations were performed in Microsoft Excel.

Hatchery and Beach Sand Average Temperatures. Temperature data were recorded from both the hatchery and beach environment on Playa Coyote. Monthly average hatchery and beach temperatures did not show significant correlations to nest success ratios (hatchery R² = 0.17, P = 0.06). As anticipated, incubation period was correlated with out-of-nest hatchery sand temperature (R² = 0.03, P = 0.01).

Table 1. Summary table of nest data by associated nest code. Nest codes beginning with C are from Playa Costa de Oro, while nest codes beginning with S are from Playa San Miguel.

Figure 2. Linear regression for average nest temperatures over the incubation period and nest success; n = 41 and P ≤0.001, with the resulting 95% confidence interval for the slope = -0.046, -0.115.

Figure 3. Simple linear regression for hours per nest exceeding 35 °C and nest success, with n = 41, P ≤ 0.001, and the 95% confidence interval for the slope = -0.00087, -0.0015.

Figure 4. Simple linear regression for the incubation period of nests related to the average nest temperature in °C, with . n = 41, P ≤ 0.001, and the 95% confidence interval for the slope = -1.499, -2.579.

Nest Temperatures. Average nest temperatures from Playa San Miguel and Playa Costa de Oro for the whole incubation period ranged from 28.6 to 34.6 °C (Table 1). Nests that experienced any hours above 35 °C (n = 25) had a significantly lower average emergence success (78.9%, P = 0.03) than nests that did not experience a single hour above 35 °C (89.1%, n = 16). The nest that experienced 374 hours above 35 °C had an emergence success of 5.1%, much lower than the average of 84.8% in the 40 other nests studied. Emergence success was correlated with nest temperature (R² = 0.36, P < 0.001), and hours exceeding 35 °C (R² = 0.58, P < 0.001) (Figs. 2 & 3). Incubation duration was also correlated with nest temperature (R² = 0.60, P < 0.001) (Fig. 4).

We estimated that 78.6% of all nests in both Costa de Oro and San Miguel from 2013-2017 resulted in female-biased hatchling sex ratios. Overall temperature can dramatically impact sex ratios, incubation periods, mortality during incubation and hatching success in species of sea turtles (Matsuzawa et al. 2001; Wibbels 2007; Hawkes et al. 2009; Valverde et al. 2010; Hill et al. 2015). Our results show that an increase in temperature can increase female hatchling production and decrease nest success. This is of substantial importance due to the potentially strong impact of climate change on Costa Rican temperatures and weather conditions in the coming years and decades (Giorgi 2006). While the effect of this female bias on the population is unknown, it is worth noting the potential impact of climate change on olive ridley demography. Given that as little as a 2-3°C increase in nest temperature was shown to significantly decrease incubation period and nest success in this study, the impacts of climate change on the nesting environment is worth rigorous study. Extremely high temperatures during incubation have been associated also with reduced locomotor performance and fitness of hatchlings, which may affect on their survival outside of the nest environment (Maulany et al. 2012; Fisher et al. 2014; Booth 2017). It is important to note that all nests monitored for temperature were located within a hatchery environment and therefore not subject to the impacts of vegetation, wind-erosion and other on-beach conditions that could affect temperature and nest success. Our results suggest that the consistent monitoring of incubation temperatures, both within and outside of the hatchery environment, is imperative to learn and respond to the impacts climate change and temperature anomalies may have on the hatch success and sex ratios of nests.

On top of predicted climate change impacts in Costa Rica, ENSO can exacerbate changes in both temperature and precipitation patterns (Waylen et al. 1996; Santidrián-Tomillo et al. 2012). ENSO can cause periods of drought followed by extended, elevated air temperatures, which can have a great impact on sea turtle nesting. Breeding numbers of green turtles in Australia, for instance, are correlated with ENSO trends, due to the variation in foraging resources associated with sea surface temperature fluctuations (Limpus & Nicholls 2000). Additionally, as our study suggests that nest temperature is negatively correlated with nest success, and that nest success is impacted by the number of hours above 35 °C, temperature anomalies such as ENSO are of significant importance to conservation efforts of olive ridley turtles in Costa Rica.

The correlation between extremely high temperatures and lower nest success suggests that peak temperatures, along with more traditionally monitored trimester and incubation averages, may be imperative to predicting the hatch success and condition of each olive ridley nest. The R² values reported here are the result of 41 data points and suggest the need for continual study of nest response to incubation temperatures. A longer-term dataset needs to be considered to confirm the relationships found in this study, such as temperature’s negative correlation with nest success. As we had only three nests that had temperature averages above 33.5 °C, further study of nests at this high temperature is warranted. In addition, further study is needed to determine the impacts of ENSO on sand temperatures and moisture in future events. Due to the effect of the hydric environment on the sex determination process (Lolavar & Wyneken 2015), weather events such as ENSO may impact nests both by temperature fluctuations and precipitation patterns. With olive ridleys’ bimodal nesting strategy, the study of nest success and sex ratio production in arribada nesting populations is also imperative. As arribada populations have been shown to experience higher incubation temperatures than solitary nests laid at the same time (Honavar et al. 2008; Dornfeld et al. 2015), the impacts on sex ratios and nest success are of extreme importance, especially in regards to ENSO and climate change.

The data presented here support a common concern for sea turtle conservation projects: an increasing feminization of hatchlings (Booth & Astill 2001; Wibbels 2007). We did not verify the sex of each hatchling, instead electing to use an estimation technique, and therefore may have conservatively estimated a female-biased sex ratio of 78.6%. This estimate provides a sense of the sex ratio production from nests, although more complicated mechanisms may be at work in sex determination, such as timing of peak temperatures and moisture content of the sand (Rogers 2013; Lolavar & Wyneken, 2015). The IPCC (2007) suggested a potential increase in temperature of 3.5 °C by the year 2100; thus, sex ratios of sea turtle species worldwide may be impacted significantly. Sand temperature manipulation such as shading and watering (Hill et al. 2015) may be necessary tools to counter the impacts of climate change on populations that experience extremely high temperatures. As Costa Rica may be particularly susceptible to the impacts of climate change (Giorgi 2006), and some olive ridley populations along the Pacific coast have been shown to exceed lethal temperature thresholds during incubation (Valverde et al. 2010; Dornfeld et al. 2014), sand temperature manipulation in this region may be compulsory to ensure hatchling production and mitigate further female bias. As many conservation projects in the area use hatcheries in response to poaching pressures, the infrastructure exists to employ and monitor shading and watering techniques on the ground.

Acknowledgements. This study was conducted under MINAET, SINAC, and ACT research permits [ACT-OR-DR-105-14; ACT- OR-DR-104-13; ACT-OR-DR-145-17; ACT-OR-DR-112-16]. Universally accepted egg and animal handling techniques were strictly adhered to throughout the duration of this study. The project was funded by and conducted under the supervision and guidance of CREMA with particular help from Internship Project Manager Daniela Rojas-Cañizales. Additional help was received in the study from research assistants David Sommers, Megan Fong, Rebecca Trippier and Jean Olivier, as well as local assistant Hernaldo Vargas and volunteer Josh Oleinik. David A. Steen and Barbara A. Pytel provided revision assistance for this manuscript.

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