Breeding periodicity for male sea turtles, operational sex ratios, and implications in the face of climate change (original) (raw)
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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.
Journal of experimental zoology. Part B, Molecular and developmental evolution, 2015
It has been proposed that because marine turtles have environmentally determined sex by incubation temperature, elevated temperatures might skew sex ratios to unsustainable levels, leading to extinction. Elevated temperatures may also reduce availability of suitable nesting sites via sea level rise. Increased tropical storm activity can directly affect nest site moisture, embryonic development, and the probability that nests will survive. Here, we question some of these assumptions and review the limits of sex ratio estimates. Sea turtles may be more resilient to climate change than previously thought, in part because of hitherto unappreciated mechanisms for coping with variable incubation conditions. J. Exp. Zool. (Mol. Dev. Evol.) 324B: 295-314, 2015. © 2015 Wiley Periodicals, Inc.
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.
Turtle mating patterns buffer against disruptive effects of climate change
Proceedings of the Royal Society B: Biological Sciences, 2012
For organisms with temperature-dependent sex determination (TSD), skewed offspring sex ratios are common. However, climate warming poses the unique threat of producing extreme sex ratio biases that could ultimately lead to population extinctions. In marine turtles, highly female-skewed hatchling sex ratios already occur and predicted increases in global temperatures are expected to exacerbate this trend, unless species can adapt. However, it is not known whether offspring sex ratios persist into adulthood, or whether variation in male mating success intensifies the impact of a shortage of males on effective population size. Here, we use parentage analysis to show that in a rookery of the endangered green turtle (Chelonia mydas), despite an offspring sex ratio of 95 per cent females, there were at least 1.4 reproductive males to every breeding female. Our results suggest that male reproductive intervals may be shorter than the 2 -4 years typical for females, and/or that males move between aggregations of receptive females, an inference supported by our satellite tracking, which shows that male turtles may visit multiple rookeries. We suggest that male mating patterns have the potential to buffer the disruptive effects of climate change on marine turtle populations, many of which are already seriously threatened.
Animal Conservation, 2012
The long-term survival of species with temperature-dependant sex determination requires a sufficient range of incubation temperatures to ensure that both males and females are produced. The primary sex ratio of sea turtles is determined by the temperature experienced by eggs during the middle third of incubation. Here, we investigated the variability in the production of male and female offspring by loggerhead sea turtles Caretta caretta at six nesting beaches in the temperate breeding area of Zakynthos, Greece. Hatchling sex ratios were estimated using incubation durations and sand temperatures for
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.
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...
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.
All marine turtles have temperature-dependent sex determination (TSD), and there is mounting evidence that climate change has increased sand temperatures at some rookeries, leading to pronounced biases in hatchling sex ratios. Quantification of the variation in the key parameters that describe TSD will be essential to our ability to predict the adaptive capacity of marine turtles, and for implementing conservation programs where necessary. Here we integrate field and laboratory data on the embryonic development of a little-studied population of loggerhead turtles (Caretta caretta, Linnaeus 1758) from Western Australia, which is home to a large rookery at the southernmost limit of the species' global range. We determined that the pivotal temperature that produces an equal sex ratio was 29.0°C, centred within a transitional range of temperatures of 0.67°C where both sexes are produced. For the first time for a marine turtle, embryonic development rates were modelled with a nonlinear function, and were used to define the start and end of the thermosensitive period, where bipotential gonads differentiate into testes or ovaries. The period where gonads were sensitive to a masculinizing trigger occurred between 33 and 64% of development. In general, the TSD parameters for this southernmost population of C. caretta were similar to those estimated for other loggerhead populations, reinforcing previous findings that sex determination thresholds and processes are highly conserved.