A Systematic Review of Metabolic Heat in Sea Turtle Nests and Methods to Model Its Impact on Hatching Success

Abstract

Just as organisms do not passively exist in their environment, developing sea turtle embryos affect their own incubation microclimate by producing metabolic heat and other waste products. This metabolic heat ultimately contributes to successful development, but it is unclear how it influences embryonic traits such as hatchling sex, and whether trends exist in the magnitude of metabolic heat produced by different species. In this systematic review, we document all empirical measurements of metabolic heat in sea turtle species, its impact on their development, and explore the methods used to predict nest temperature and how these methods account for metabolic heat. Overall we found metabolic heat increases throughout incubation in all seven species. Typically, the temperature at the center of an egg clutch peaked during the final third of incubation, and exceeded the adjacent sand temperature by 2.5 • C. Metabolic heat was not influenced by species or clutch size (n = 16 studies), but this finding was likely influenced by inconsistency in the methods used to measure metabolic heat, and by localized differences in sand properties, such as moisture, albedo, and thermal conductivity. The influence of metabolic heat on embryo sex determination and survival was dependent on the sand temperature surrounding the nest chamber, and had an appreciable affect only when it caused nest temperatures to exceed key thresholds for sex determination and survival. Methods for modeling nest temperature were either correlative (70% of publications) or mechanistic (30% of publications). Correlative models describe relationships between empirical data to predict sand temperature, while mechanistic models are based on physical laws and do not require extrapolation when predicting novel situations, such as climate change. Most correlative models (74%) accounted for metabolic heat when predicting nest temperatures, but no mechanistic models did-largely because they were developed for predicting primary sex ratios, which are widely believed to be unaffected by metabolic heat. Consequently, developing a generalisable mechanistic model that incorporates metabolic heat will be critical for predicting incubation success as the sand temperatures at sea turtle beaches increase due to anthropogenic climate change.

Impact of marine heatwaves for sea turtle nest temperatures

“…hatchling success), we assumed that metabolic heating within clutches averaged 1.1°C by the middle third of development (i.e. the period when sex is determined during incubation), as reported for hawksbill and green turtles in a recent review [ 17 ]. This value for metabolic heating was added to the mean monthly sand temperatures recorded at nest depths.…”

Global warming facilitates the nesting of the loggerhead turtle on the Mediterranean coast of Spain

“…In this situation, we refrained from estimating the sex ratio of hatchlings and just calculated the proportion of clutches incubated at ≤28°C during the central third of incubation, because this is the lower threshold for the production of females (Mrosovsky et al ., 2002). Studies conducted on Mediterranean nesting beaches usually report no significant metabolic heating during the second third of incubation (Godley et al ., 2001; Zbinden, Margaritoulis & Arlettaz, 2006; Jribi & Bradai, 2014), contrary to the situation in other regions (Gammon et al ., 2020), but González‐Paredes et al . (2021) reported that metabolic heating increased the temperature of an isolated nest by 0.53°C.…”

“…, contrary to the situation in other regions(Gammon et al, 2020), but González-Paredes et al (2021 reported that metabolic heating increased the temperature of an isolated nest by 0.53°C. Accordingly, we calculated the average sand temperature during the central third of the incubation of clutches laid on July 1st, July 15th, and August 1st, considering that incubation lasts for 60 days, and then calculated the proportion of nests reaching the 28°C thresholds in the absence of any significant metabolic heating during the central third of incubation(Godley et al, 2001;Zbinden, Margaritoulis & Arlettaz, 2006; …”

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

“…To estimate hatchling sex ratios, values for metabolic heating (MH) were added to the hindcasted and projected sand temperatures, to estimate nest temperature. We used values of MH equal to 0.5°C (conservative) and 1.1°C (moderate) to capture the likely variations in MH during the sex determination period (Gammon et al, 2020; Laloë et al, 2014; Patrício et al, 2017). The moderate MH estimate was the calculated average from the reported MH temperatures for green turtles during the middle‐third of embryonic development reviewed in Gammon et al (2020).…”

“…We used values of MH equal to 0.5°C (conservative) and 1.1°C (moderate) to capture the likely variations in MH during the sex determination period (Gammon et al, 2020; Laloë et al, 2014; Patrício et al, 2017). The moderate MH estimate was the calculated average from the reported MH temperatures for green turtles during the middle‐third of embryonic development reviewed in Gammon et al (2020). Using the modelled nest temperatures, we estimated the primary hatchling sex ratio of both species for each nesting season using a standardised logistic model described by Hays et al (2017), which assumes a PT = 29.1°C and a transitional range in temperatures (TRT) = 26–32°C.…”