skip to main content


Title: Population Viability of Sea Turtles in the Context of Global Warming
Abstract

Sea turtles present a model for the potential impacts of climate change on imperiled species, with projected warming generating concern about their persistence. Various sea turtle life-history traits are affected by temperature; most strikingly, warmer egg incubation temperatures cause female-biased sex ratios and higher embryo mortality. Predictions of sea turtle resilience to climate change are often focused on how resulting male limitation or reduced offspring production may affect populations. In the present article, by reviewing research on sea turtles, we provide an overview of how temperature impacts on incubating eggs may cascade through life history to ultimately affect population viability. We explore how sex-specific patterns in survival and breeding periodicity determine the differences among offspring, adult, and operational sex ratios. We then discuss the implications of skewed sex ratios for male-limited reproduction, consider the negative correlation between sex ratio skew and genetic diversity, and examine consequences for adaptive potential. Our synthesis underscores the importance of considering the effects of climate throughout the life history of any species. Lethal effects (e.g., embryo mortality) are relatively direct impacts, but sublethal effects at immature life-history stages may not alter population growth rates until cohorts reach reproductive maturity. This leaves a lag during which some species transition through several stages subject to distinct biological circumstances and climate impacts. These perspectives will help managers conceptualize the drivers of emergent population dynamics and identify existing knowledge gaps under different scenarios of predicted environmental change.

 
more » « less
NSF-PAR ID:
10364274
Author(s) / Creator(s):
 ;  ;  ;  ;  ;  
Publisher / Repository:
Oxford University Press
Date Published:
Journal Name:
BioScience
Volume:
71
Issue:
8
ISSN:
0006-3568
Page Range / eLocation ID:
p. 790-804
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Climate change is a threat to marine turtles that is expected to affect all of their life stages. To guide future research, we conducted a review of the most recent literature on this topic, highlighting knowledge gains and research gaps since a similar previous review in 2009. Most research has been focused on the terrestrial life history phase, where expected impacts will range from habitat loss and decreased reproductive success to feminization of populations, but changes in reproductive periodicity, shifts in latitudinal ranges, and changes in foraging success are all expected in the marine life history phase. Models have been proposed to improve estimates of primary sex ratios, while technological advances promise a better understanding of how climate can influence different life stages and habitats. We suggest a number of research priorities for an improved understanding of how climate change may impact marine turtles, including: improved estimates of primary sex ratios, assessments of the implications of female-biased sex ratios and reduced male production, assessments of the variability in upper thermal limits of clutches, models of beach sediment movement under sea level rise, and assessments of impacts on foraging grounds. Lastly, we suggest that it is not yet possible to recommend manipulating aspects of turtle nesting ecology, as the evidence base with which to understand the results of such interventions is not robust enough, but that strategies for mitigation of stressors should be helpful, providing they consider the synergistic effects of climate change and other anthropogenic-induced threats to marine turtles, and focus on increasing resilience. 
    more » « less
  2. Abstract

    Global climate is warming rapidly, threatening vertebrates with temperature-dependent sex determination (TSD) by disrupting sex ratios and other traits. Less understood are the effects of increased thermal fluctuations predicted to accompany climate change. Greater fluctuations could accelerate feminization of species that produce females under warmer conditions (further endangering TSD animals), or counter it (reducing extinction risk). Here we use novel experiments exposing eggs of Painted Turtles (Chrysemys picta) to replicated profiles recorded in field nests plus mathematically-modified profiles of similar shape but wider oscillations, and develop a new mathematical model for analysis. We show that broadening fluctuations around naturally male-producing (cooler) profiles feminizes developing embryos, whereas embryos from warmer profiles remain female or die. This occurs presumably because wider oscillations around cooler profiles expose embryos to very low temperatures that inhibit development, and to feminizing temperatures where most embryogenesis accrues. Likewise, embryos incubated under broader fluctuations around warmer profiles experience mostly feminizing temperatures, some dangerously high (which increase mortality), and fewer colder values that are insufficient to induce male development. Therefore, as thermal fluctuations escalate with global warming, the feminization of TSD turtle populations could accelerate, facilitating extinction by demographic collapse. Aggressive global CO2mitigation scenarios (RCP2.6) could prevent these risks, while intermediate actions (RCP4.5 and RCP6.0 scenarios) yield moderate feminization, highlighting the peril that insufficient reductions of greenhouse gas emissions pose for TSD taxa. If our findings are generalizable, TSD squamates, tuatara, and crocodilians that produce males at warmer temperatures could suffer accelerated masculinization, underscoring the broad taxonomic threats of climate change.

     
    more » « less
  3. Premise

    Plant sex is usually fixed, but in rare cases, sex expression is flexible and may be influenced by environmental factors. Theory links female sex expression to better health, but manipulative work involving the experimental change of health via injury is limited, particularly in sexually plastic species. A better understanding of mechanisms influencing shifts in sex is essential to our understanding of life history theory regarding trade‐offs in sex allocation and differential mortality.

    Methods

    We investigated the relationship between physiological stress and sex expression in sexually plastic striped maple trees (Acer pensylvanicum) by inflicting damage of various intensities (crown pruning, defoliation, and hydraulic restriction). We then monitored the sex expression of injured and control individuals for 2 years to assess the extent to which injury may cue changes in sex expression.

    Results

    We found that severe damage such as full defoliation or severe pruning increased odds of changing sex to female and decreased odds of changing to male. In fact, no pruned male trees flowered male 2 years later, while all males in the control group flowered partially or fully male. After full defoliation, trees had 4.5 times higher odds of flowering female. Not all injury is equal; less‐severe physical trauma did not affect the frequency of sex change to femaleness.

    Conclusions

    This work demonstrates that physical trauma in striped maple appears to exhibit a threshold effect in which only the most stressful of physiological cues instigate changes in sex expression, a phenomenon previously unknown, and that damage stress is strongly correlated with switching to femaleness. These findings have implications for population sex ratios and sustainability within an increasing stressful climate regime.

     
    more » « less
  4. Temperature during embryogenesis determines sex and has been shown to influence other physiological traits in reptiles. The common snapping turtle (Chelydra serpentina) is an ideal model for testing how temperature impacts behavior in species that display temperature-dependent sex determination. Behavioral assays are crucial to understanding how a changing climate may affect whole organism function in the snapping turtle. Currently, there are few behavioral assays for semi-aquatic vertebrates like turtles. In this study, we used digital cameras to record behavior of fed and fasted hatchling turtles from different incubation temperatures in an open field setting for 20 minutes in 2018 and repeated the experiment in 2019. Open fields were circular tanks filled with water to a depth of 3.5 cm. Each field was split into four quadrants and two zones (inner and outer). The amount of time turtles spent actively moving, total distance travelled, and several other measures were collected and summarized automatically from videos with open source image analysis software (ImageJ). Satiety and incubation temperature had significant effects on total distance moved, time spent moving, and time moving in the outer zone. These findings indicate that temperature during embryogenesis has a long-lasting effect on neural mechanisms underlying exploratory or general locomotor behavior in turtles. 
    more » « less
  5. Abstract Conservation of thermally sensitive species depends on monitoring organismal and population‐level responses to environmental change in real time. Epigenetic processes are increasingly recognized as key integrators of environmental conditions into developmentally plastic responses, and attendant epigenomic data sets hold potential for revealing cryptic phenotypes relevant to conservation efforts. Here, we demonstrate the utility of genome‐wide DNA methylation (DNAm) patterns in the face of climate change for a group of especially vulnerable species, those with temperature‐dependent sex determination (TSD). Due to their reliance on thermal cues during development to determine sexual fate, contemporary shifts in temperature are predicted to skew offspring sex ratios and ultimately destabilize sensitive populations. Using reduced‐representation bisulphite sequencing, we profiled the DNA methylome in blood cells of hatchling American alligators ( Alligator mississippiensis ), a TSD species lacking reliable markers of sexual dimorphism in early life stages. We identified 120 sex‐associated differentially methylated cytosines (DMCs; FDR < 0.1) in hatchlings incubated under a range of temperatures, as well as 707 unique temperature‐associated DMCs. We further developed DNAm‐based models capable of predicting hatchling sex with 100% accuracy (in 20 training samples and four test samples) and past incubation temperature with a mean absolute error of 1.2°C (in four test samples) based on the methylation status of 20 and 24 loci, respectively. Though largely independent of epigenomic patterning occurring in the embryonic gonad during TSD, DNAm patterns in blood cells may serve as nonlethal markers of hatchling sex and past incubation conditions in conservation applications. These findings also raise intriguing questions regarding tissue‐specific epigenomic patterning in the context of developmental plasticity. 
    more » « less