Turtle mating patterns buffer against disruptive effects of climate change (original) (raw)
Related papers
Frontiers in Marine Science, 2014
The implications of climate change for global biodiversity may be profound with those species with little capacity for adaptation being thought to be particularly vulnerable to warming. A classic case of groups for concern are those animals exhibiting temperature-dependent sex-determination (TSD), such as sea turtles, where climate warming may produce single sex populations and hence extinction. We show that, globally, female biased hatchling sex ratios dominate sea turtle populations (exceeding 3:1 in >50% records), which, at-a-glance, reiterates concerns for extinction. However, we also demonstrate that more frequent breeding by males, empirically shown by satellite tracking 23 individuals and supported by a generalized bio-energetic life history model, generates more balanced operational sex ratios (OSRs). Hence, concerns of increasingly skewed hatchling sex ratios and reduced population viability are less acute than previously thought for sea turtles. In fact, in some scenarios skewed hatchling sex ratios in groups with TSD may be adaptive to ensure optimum OSRs.
2010
Species that have temperature-dependent sex determination (TSD) often produce highly skewed offspring sex ratios contrary to long-standing theoretical predictions. This ecological enigma has provoked concern that climate change may induce the production of single-sex generations and hence lead to population extirpation. All species of sea turtles exhibit TSD, many are already endangered, and most already produce sex ratios skewed to the sex produced at warmer temperatures (females). We tracked male loggerhead turtles ( Caretta caretta) from Zakynthos, Greece, throughout the entire interval between successive breeding seasons and identified individuals on their breeding grounds, using photoidentification, to determine breeding periodicity and operational sex ratios. Males returned to breed at least twice as frequently as females. We estimated that the hatchling sex ratio of 70:30 female to male for this rookery will translate into an overall operational sex ratio (OSR) (i.e., ratio of total number of males vs females breeding each year) of close to 50:50 female to male. We followed three male turtles for between 10 and 12 months during which time they all traveled back to the breeding grounds. Flipper tagging revealed the proportion of females returning to nest after intervals of 1, 2, 3, and 4 years were 0. 21, 0.38, 0.29, and 0.12, respectively (mean interval 2.3 years). A further nine male turtles were tracked for short periods to determine their departure date from the breeding grounds. These departure dates were combined with a photoidentification data set of 165 individuals identified on in-water transect surveys at the start of the breeding season to develop a statistical model of the population dynamics. This model produced a maximum likelihood estimate that males visit the breeding site 2.6 times more often than females (95%CI 2.1, 3.1), which was consistent with the data from satellite tracking and flipper tagging. Increased frequency of male breeding will help ameliorate female-biased hatchling sex ratios. Combined with the ability of males to fertilize the eggs of many females and for females to store sperm to fertilize many clutches, our results imply that effects of climate change on the viability of sea turtle populations are likely to be less acute than previously suspected.
Marine Biology
In a warming climate, male sea turtles may become increasingly rare due to temperature-dependent sex determination with females being produced at warmer temperatures. Hence there is widespread concern that a lack of adult males may impact population viability. However, there is controversy over this scenario and here we review aspects of the biology of male sea turtles that will help mitigate female-biased hatchling sex ratios. In particular, there is strong evidence that males generally breed more frequently than females (i.e. have a shorter remigration interval) and that individual breeding males actively search for females and may mate with multiple females from different nesting sites. These aspects of the biology of male turtles will cause female-biased hatchling sex ratios to translate into more balanced adult sex ratios on the breeding grounds (i.e. operational sex ratios). Sexual dimorphism is widespread with adult male turtles generally being smaller than females. In freshw...
Climate Change Responses, 2014
Background: Quantifying primary sex ratios is essential for assessing how global warming will influence the population dynamics of species with temperature-dependent sex determination (TSD). Process-explicit (mechanistic) models can accurately estimate primary sex ratios but require the resolution of the key physiological parameters that influence sex determination and validation of the model by testing predictions against empirical data.
The Maternal Legacy: Female Identity Predicts Offspring Sex Ratio in the Loggerhead Sea Turtle
Scientific Reports, 2016
In organisms with temperature-dependent sex determination, the incubation environment plays a key role in determining offspring sex ratios. Given that global temperatures have warmed approximately 0.6 °C in the last century, it is necessary to consider how organisms will adjust to climate change. To better understand the degree to which mothers influence the sex ratios of their offspring, we use 24 years of nesting data for individual female loggerhead sea turtles (Caretta caretta) observed on Bald Head Island, North Carolina. We find that maternal identity is the best predictor of nest sex ratio in univariate and multivariate predictive models. We find significant variability in estimated nest sex ratios among mothers, but a high degree of consistency within mothers, despite substantial spatial and temporal thermal variation. Our results suggest that individual differences in nesting preferences are the main driver behind divergences in nest sex ratios. As such, a female's ability to plastically adjust her nest sex ratios in response to environmental conditions is constrained, potentially limiting how individuals behaviorally mitigate the effects of environmental change. Given that many loggerhead populations already show female-biased offspring sex ratios, understanding maternal behavioral responses is critical for predicting the future of long-lived species vulnerable to extinction.
Conservation Biology, 2010
Abstract: Species that have temperature-dependent sex determination (TSD) often produce highly skewed offspring sex ratios contrary to long-standing theoretical predictions. This ecological enigma has provoked concern that climate change may induce the production of single-sex generations and hence lead to population extirpation. All species of sea turtles exhibit TSD, many are already endangered, and most already produce sex ratios skewed to the sex produced at warmer temperatures (females). We tracked male loggerhead turtles (Caretta caretta) from Zakynthos, Greece, throughout the entire interval between successive breeding seasons and identified individuals on their breeding grounds, using photoidentification, to determine breeding periodicity and operational sex ratios. Males returned to breed at least twice as frequently as females. We estimated that the hatchling sex ratio of 70:30 female to male for this rookery will translate into an overall operational sex ratio (OSR) (i.e., ratio of total number of males vs females breeding each year) of close to 50:50 female to male. We followed three male turtles for between 10 and 12 months during which time they all traveled back to the breeding grounds. Flipper tagging revealed the proportion of females returning to nest after intervals of 1, 2, 3, and 4 years were 0.21, 0.38, 0.29, and 0.12, respectively (mean interval 2.3 years). A further nine male turtles were tracked for short periods to determine their departure date from the breeding grounds. These departure dates were combined with a photoidentification data set of 165 individuals identified on in-water transect surveys at the start of the breeding season to develop a statistical model of the population dynamics. This model produced a maximum likelihood estimate that males visit the breeding site 2.6 times more often than females (95%CI 2.1, 3.1), which was consistent with the data from satellite tracking and flipper tagging. Increased frequency of male breeding will help ameliorate female-biased hatchling sex ratios. Combined with the ability of males to fertilize the eggs of many females and for females to store sperm to fertilize many clutches, our results imply that effects of climate change on the viability of sea turtle populations are likely to be less acute than previously suspected.Resumen: Las especies que tienen determinación de sexo dependiente de la temperatura (DST) a menudo producen proporciones de sexo en su descendencia muy sesgadas contrarias las predicciones teóricas prevalecientes. Este enigma ecológico ha motivado preocupación de que el cambio climático puede inducir la producción de generaciones de un solo sexo y por lo tanto conducir a la extirpación de la población. Todas las especies de tortugas marinas presentan DST, muchas ya están en peligro y la mayoría ya producen proporciones de sexos sesgados hacia el sexo producido a temperaturas más cálidas (hembras). Rastreamos tortugas de carey machos (Caretta caretta) de Zakynthos, Grecia, a lo largo de todo el intervalo entre épocas reproductivas sucesivas e identificamos individuos en sus áreas reproductivas, utilizando fotoidentificación, para determinar la periodicidad reproductiva y las proporciones de sexo operacionales. Los machos retornaron para reproducirse por lo menos dos veces más frecuentemente que las hembras. Estimamos que la proporción de sexos de crías de 70:30 hembras a machos en esta colonia se traducirá en una proporción de sexos operacional (PSO) (i.e., la proporción del número total de machos versus hembras en reproducción cada año) cerca de 50:50 hembras a machos. Seguimos a 3 tortugas machos entre 10 y 12 meses durante los cuales todos retornaron al área reproductiva. El marcaje en aletas reveló que la proporción de hembras que retornaron a anidar después de intervalos de 1, 2, 3 y 4 años fue 0.21, 0.38, 0.29 y 0.12, respectivamente (intervalo promedio 2.3 años). Otros 9 machos fueron rastreados por períodos cortos para determinar su fecha de partida del área reproductiva. Esas fechas de partida fueron combinadas con un conjunto datos de la fotoidentificación de 165 individuos identificados en transectos realizados al inicio de la época reproductiva para desarrollar un modelo estadístico de la dinámica poblacional. Este modelo produjo una probabilidad máxima estimada de que los machos visitan el área reproductiva 2.6 veces más a menudo que las hembras (95%IC 2.1, 3.1), que fue consistente con los datos de rastreo por satélite y marcaje de aletas. Una mayor frecuencia de la reproducción de machos ayudará a mejorar las proporciones de sexo de crías sesgadas hacia hembras. En combinación con la habilidad de los machos para fertilizar los huevos de muchas hembras y de las hembras para almacenar esperma para fertilizar muchas puestas, nuestros resultados implican que es probable que los efectos del cambio climático sobre la viabilidad de las poblaciones de tortugas marinas sean menos agudos que lo sospechado previamente.Resumen: Las especies que tienen determinación de sexo dependiente de la temperatura (DST) a menudo producen proporciones de sexo en su descendencia muy sesgadas contrarias las predicciones teóricas prevalecientes. Este enigma ecológico ha motivado preocupación de que el cambio climático puede inducir la producción de generaciones de un solo sexo y por lo tanto conducir a la extirpación de la población. Todas las especies de tortugas marinas presentan DST, muchas ya están en peligro y la mayoría ya producen proporciones de sexos sesgados hacia el sexo producido a temperaturas más cálidas (hembras). Rastreamos tortugas de carey machos (Caretta caretta) de Zakynthos, Grecia, a lo largo de todo el intervalo entre épocas reproductivas sucesivas e identificamos individuos en sus áreas reproductivas, utilizando fotoidentificación, para determinar la periodicidad reproductiva y las proporciones de sexo operacionales. Los machos retornaron para reproducirse por lo menos dos veces más frecuentemente que las hembras. Estimamos que la proporción de sexos de crías de 70:30 hembras a machos en esta colonia se traducirá en una proporción de sexos operacional (PSO) (i.e., la proporción del número total de machos versus hembras en reproducción cada año) cerca de 50:50 hembras a machos. Seguimos a 3 tortugas machos entre 10 y 12 meses durante los cuales todos retornaron al área reproductiva. El marcaje en aletas reveló que la proporción de hembras que retornaron a anidar después de intervalos de 1, 2, 3 y 4 años fue 0.21, 0.38, 0.29 y 0.12, respectivamente (intervalo promedio 2.3 años). Otros 9 machos fueron rastreados por períodos cortos para determinar su fecha de partida del área reproductiva. Esas fechas de partida fueron combinadas con un conjunto datos de la fotoidentificación de 165 individuos identificados en transectos realizados al inicio de la época reproductiva para desarrollar un modelo estadístico de la dinámica poblacional. Este modelo produjo una probabilidad máxima estimada de que los machos visitan el área reproductiva 2.6 veces más a menudo que las hembras (95%IC 2.1, 3.1), que fue consistente con los datos de rastreo por satélite y marcaje de aletas. Una mayor frecuencia de la reproducción de machos ayudará a mejorar las proporciones de sexo de crías sesgadas hacia hembras. En combinación con la habilidad de los machos para fertilizar los huevos de muchas hembras y de las hembras para almacenar esperma para fertilizar muchas puestas, nuestros resultados implican que es probable que los efectos del cambio climático sobre la viabilidad de las poblaciones de tortugas marinas sean menos agudos que lo sospechado previamente.
Global Change Biology, 2015
Temperature-dependent sex determination (TSD) is the predominant form of environmental sex determination (ESD) in reptiles, but the adaptive significance of TSD in this group remains unclear. Additionally, the viability of species with TSD may be compromised as climate gets warmer. We simulated population responses in a turtle with TSD to increasing nest temperatures and compared the results to those of a virtual population with genotypic sex determination (GSD) and fixed sex ratios. Then, we assessed the effectiveness of TSD as a mechanism to maintain populations under climate change scenarios. TSD populations were more resilient to increased nest temperatures and mitigated the negative effects of high temperatures by increasing production of female offspring and therefore, future fecundity. That buffered the negative effect of temperature on the population growth. TSD provides an evolutionary advantage to sea turtles. However, this mechanism was only effective over a range of temperatures and will become inefficient as temperatures rise to levels projected by current climate change models. Projected global warming threatens survival of sea turtles, and the IPCC high gas concentration scenario may result in extirpation of the studied population in 50 years.
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.
Ecology, 2010
Conditions experienced early in life can influence phenotypes in ecologically important ways, as exemplified by organisms with environmental sex determination. For organisms with temperature-dependent sex determination (TSD), variation in nest temperatures induces phenotypic variation that could impact population growth rates. In environments that vary over space and time, how does this variation influence key demographic parameters (cohort sex ratio and hatchling recruitment) in early life stages of populations exhibiting TSD? We leverage a 17-year data set on a population of painted turtles, Chrysemys picta, to investigate how spatial variation in nest vegetation cover and temporal variation in climate influence early life-history demography. We found that spatial variation in nest cover strongly influenced nest temperature and sex ratio, but was not correlated with clutch size, nest predation, total nest failure, or hatching success. Temporal variation in climate influenced percentage of total nest failure and cohort sex ratio, but not depredation rate, mean clutch size, or mean hatching success. Total hatchling recruitment in a year was influenced primarily by temporal variation in climate-independent factors, number of nests constructed, and depredation rate. Recruitment of female hatchlings was determined by stochastic variation in nest depredation and annual climate and also by the total nest production. Overall population demography depends more strongly on annual variation in climate and predation than it does on the intricacies of nest-specific biology. Finally, we demonstrate that recruitment of female hatchlings translates into recruitment of breeding females into the population, thus linking climate (and other) effects on early life stages to adult demographics.