Climate and predation dominate juvenile and adult recruitment in a turtle with temperature‐dependent sex determination (original) (raw)
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Climate change increases the production of female hatchlings at a northern sea turtle rookery
Ecology, 2016
The most recent climate change projections show a global increase in temperatures, along with major adjustments to precipitation, throughout the 21st century. Species exhibiting temperature-dependent sex determination are highly susceptible to such changes since the incubation environment influences critical offspring characteristics such as survival and sex ratio. Here we show that the mean incubation duration of loggerhead sea turtle (Caretta caretta) nests from a high-density nesting beach on Bald Head Island, North Carolina, USA has decreased significantly over the past 25 yr. This decrease in incubation duration is significantly positively correlated with mean air temperature and negatively correlated with mean precipitation during the nesting season. Additionally, although no change in hatching success was detected during this same period, a potentially detrimental consequence of shorter incubation durations is that they lead to the production of primarily female offspring. Given that global temperatures are predicted to increase by as much as 4°C over the next century, the mass feminization of sea turtle hatchlings is a high-priority concern. While presently limited in number, studies using long-term data sets to examine the temporal correlation between offspring characteristics and climatic trends are essential for understanding the scope and direction of climate change effects on species persistence.
Proceedings of The Royal Society B: Biological Sciences, 2010
Nesting behaviour is critical for reproductive success in oviparous organisms with no parental care. In organisms where sex is determined by incubation temperature, nesting behaviour may be a prime target of selection in response to unbalanced sex ratios. To produce an evolutionary change in response to sex-ratio selection, components of nesting behaviour must be heritable. We estimated the field heritability of two key components of nesting behaviour in a population of painted turtles (Chrysemys picta) with temperature-dependent sex determination by applying the 'animal model' to a pedigree reconstructed from genotype data. We obtained estimates of low to non-detectable heritability using repeated records across all environments. We then determined environment-specific heritability by grouping records with similar temperatures for the winter preceding the nesting season, a variable known to be highly associated with our two traits of interest, nest vegetation cover and Julian date of nesting. The heritability estimates of nest vegetation cover and Julian date of nesting were qualitatively highest and significant, or nearly so, after hot winters. Additive genetic variance for these traits was not detectable after cold winters. Our analysis suggests that the potential for evolutionary change of nesting behaviour may be dependent on the thermal conditions of the preceding winter, a season that is predicted to be especially subject to climate change.
Global Change Biology, 2017
The study of temperature-dependent sex determination (TSD) in vertebrates has attracted major scientific interest. Recently, concerns for species with TSD in a warming world have increased because imbalanced sex ratios could potentially threaten population viability. In contrast, relatively little attention has been given to the direct effects of increased temperatures on successful embryonic development. Using 6603 days of sand temperature data recorded across 6 years at a globally important loggerhead sea turtle rookery-the Cape Verde Islands-we show the effects of warming incubation temperatures on the survival of hatchlings in nests. Incorporating published data (n = 110 data points for three species across 12 sites globally), we show the generality of relationships between hatchling mortality and incubation temperature and hence the broad applicability of our findings to sea turtles in general. We use a mechanistic approach supplemented by empirical data to consider the linked effects of warming temperatures on hatchling output and on sex ratios for these species that exhibit TSD. Our results show that higher temperatures increase the natural growth rate of the population as more females are produced. As a result, we project that numbers of nests at this globally important site will increase by approximately 30% by the year 2100. However, as incubation temperatures near lethal levels, the natural growth rate of the population decreases and the long-term survival of this turtle population is threatened. Our results highlight concerns for species with TSD in a warming world and underline the need for research to extend from a focus on temperature-dependent sex determination to a focus on temperature-linked hatchling mortalities.
Functional Ecology, 2010
1. Maternal and environmental factors influence embryo development and offspring phenotypes in ways that are likely to impact fitness. Most studies that address this issue, however, fail to mimic the complexities of natural environmental parameters and only quantify selection during a single season. 2. In this study, we examined year-to-year variation in how maternal factors (egg mass, nesting phenology and nest-site choice) and external abiotic factors (temperature and precipitation) impact egg survival and hatchling morphology in the painted turtle (Chrysemys picta) over seven nesting seasons in the field. In addition, we quantify annual variation in the strength and form of selection operating on maternal factors. 3. Overall, our results demonstrated very low, if any, consistency in how maternal and environmental factors impact egg survival and hatchling size in the field. That is, different variables had different effects in different years. Accordingly, the strength and form of natural selection operating on egg size, nesting phenology and nest-site choice were inconsistent across years, suggesting low potential for substantive or directional evolutionary shifts in these maternal effects. 4. These results may partially explain why traits like egg size and nest-site choice exhibit variation (i.e. are not perfectly optimized), and highlight the importance of multiyear field studies in gaining a more complete picture of the factors driving variation in critical early life-history events and demographic parameters.
Copeia, 2008
Painted Turtles (Chrysemys picta) are often used to test life-history theory. However, within populations, the factors that contribute to among-individual variation in egg size and clutch size are poorly understood, and an understanding of the biotic and abiotic parameters that contribute to this variation is important when framing patterns of maternal investment in a life-history context. We examined proximate sources of reproductive variation in a northern population of Painted Turtles, we attempted to frame these sources of variation in a lifehistory context, and we evaluate which optimality model most adequately explains patterns of reproductive allocation in populations of small-bodied turtles. We used multiple linear regression on data from 168 first clutches of marked females that nested at a long-term study site in Algonquin Park, Ontario, Canada, in 2004. We found that mean egg mass was positively related to maximum plastron length (MPL) and female age, and negatively related to clutch size and water temperature prior to oviposition. Clutch size was positively related to MPL and carapace height, and negatively related to mean egg mass, and the number of clutches laid in the season. Body size (MPL) was the most important predictor of each reproductive parameter, and residual analysis indicated that egg mass was more conserved than clutch size across the range of female body sizes sampled in this study. Thus, egg size may be optimized as a body size-specific function, and in light of this, we suggest that 'phenotype-habitat matching' may occur in C. picta. If a female's phenotype (e.g., body size) influences the selective environment of her eggs and hatchlings (e.g., if larger females generally nest farther away from water), then the optimal strategy of maternal investment should vary among maternal phenotypes. The positive correlation between egg mass and body size that was observed in the present study can be explained in adaptive terms under hypotheses based on the concept of phenotype-habitat matching.
Incubation temperature in the wild influences hatchling phenotype of two freshwater turtle species
Background: The nest environment influences phenotypic traits of hatchling turtles. Female turtles select nest sites that promote hatchling survival, and alter nesting behaviour in response to changing environments. Differences in phenotype generated by incubation environment could provide variation in traits that natural selection can act upon. The relationship between incubation temperature in the laboratory and post-hatching phenotype is well documented, but whether incubation in nature generates biologically meaningful levels of phenotypic variation is less well studied. Questions: (1) What are the effects of canopy cover, laying date, and nest depth on incubation temperature? (2) What are the relationships between incubation temperature, egg mass, and hatchling phenotype? (3) What are the sex-specific effects of incubation temperature on phenotypic variation in two turtles with temperature-dependent sex determination? Organisms: Painted turtle (Chrysemys picta) and snapping turtle (Chelydra serpentina) nests and hatchlings from Algonquin Park, Ontario, Canada. Methods: In 2010 and 2011, we measured canopy cover at nests and hourly temperatures within nests throughout incubation. Post-parturition, we measured egg mass of each clutch. After emergence, we measured hatchling righting response (time taken to flip from carapace to plastron), carapace length, and mass. Conclusions: Canopy cover and oviposition date did not affect nest temperature, but nest depth influenced daily temperature variance in snapping turtle nests. However, limited variation in environmental characteristics suggests that a female's ability to select microhabitats that adaptively affect offspring survivorship or phenotype is limited. Female painted turtles with heavier eggs selected nest sites that were warmer. Nest incubation temperature was related to multiple hatchling characteristics. Painted turtle hatchling carapace length was positively related to mean incubation temperature, but snapping turtle hatchling size was not related to incubation temperature. Painted turtle hatchling righting response was not related to incubation temperature, but snapping turtle hatchlings from warmer nests righted themselves more quickly and hatchlings from nests with greater temperature variance righted more slowly. Our predicted nest sex ratios suggested that warmer nests with heavier eggs would produce female hatchlings. Also, in both species, carapace length was greater for hatchlings from nests
Endangered Species Research
Projected climate change is forecasted to have significant effects on biological systems worldwide. Marine turtles in particular may be vulnerable, as the sex of their offspring is determined by their incubating temperature, termed temperature-dependent sex determination. This study aimed to estimate historical, and forecast future, primary sex ratios of hawksbill turtle Eretmochelys imbricata hatchlings at an important nesting ground in northeastern Qatar. Incubation temperatures from the Arabian/Persian Gulf were measured over 2 nesting seasons. Climate data from same period were regressed with nest temperatures to estimate incubation temperatures and hatchling sex ratios for the site from 1993 to 2100. Future hatchling sex ratios were estimated for 2 climate forecasts, one mid-range (SSP245) and one extreme (SSP585). Historical climate data showed female-biased sex ratios of 73.2 ± 12.1% from 1993 to 2017. Female biases from 2018 to 2100 averaged 85.7% ± 6.7% under the mid-range ...
Biological Journal of the Linnean Society, 2004
Despite the importance of maternal effects in evolution, and knowledge of links among nest site choice, timing of nesting, offspring sex, and reproductive success in animals with environmental sex determination, these attributes have not been rigorously studied in a combined and natural context. To address this need we studied the relationships between three maternal traits (nest site choice, lay date, and nest depth) and two fitness-related attributes of offspring (hatchling sex and embryonic survival) in the riverine turtle Carettochelys insculpta, a species with temperature-dependent sex determination, for four years. Predation and flooding were the major sources of embryonic mortality in 191 nests. Embryonic survival was influenced by both lay date and nest site choice: in one year when nesting began later than average, nests laid later and at lower elevations were destroyed by early wet season river rises. In other years early nesting precluded flood mortality. However, turtles did not nest at the highest available elevations, and a field experiment confirmed that turtles were constrained to nest at lower elevations where they could construct a nest chamber. The principal determinant of hatchling sex in 140 nests was lay date, which in turn was apparently related to the magnitude of the previous wet season(s). Clutches laid earlier in the season (a female's first clutch) produced mainly males, while later clutches (her second clutch) yielded mostly females, due to seasonal increases in air temperatures. Accordingly, later nesting produced female-biased hatchling sex ratios in 1996, while earlier nesting resulted in sex ratios near unity in the other years. However, all-female nests were more likely to be flooded than mixed-sex or all-male nests in years when nesting was late. In conclusion, we found evidence that the position of two maternal trait distributions (elevation of the nest site and lay date), associated with the reproductive strategy of C. insculpta, reflect a combination of natural selection, physical constraints, and phenotypic plasticity.
Canadian Journal of Zoology, 2010
Evolutionary theory predicts that when phenotypic variation arises during development that differently influences the fitness of each sex, selection should favor the maternal ability to match offspring phenotype to the sex that incurs a fitness benefit from that phenotype. In reptiles with temperature-dependent sex determination, the temperatures experienced during incubation can influence numerous phenotypic parameters, including sex. To mimic more naturalistic conditions, this experiment examined how variation in temperature fluctuations affects offspring sex as well as a suite of phenotypic parameters having putative fitness consequences in the Northern Painted Turtle ( Chrysemys picta (Schneider, 1783)). We also characterized variation in natural nest temperatures, including the daily temperature range, related to the vegetation cover surrounding the nest. We found that temperature fluctuations did not affect hatchling morphology, immune response, or behavior, but did significan...