Mating‐induced ovulation in loggerhead sea turtles,Caretta caretta

Mating‐induced ovulation is common in mammals, but has been rarely described in other taxa. Observations of several mature female loggerhead sea turtles, Caretta caretta, held in captivity seemed to indicate that ovulation did not occur in the absence of a male. This study was designed to determine whether this was an effect of captivity or an effect of the absence of a male. Two mature female loggerheads were followed over six annual reproductive cycles. Ultrasound exams were performed approximately every 2 weeks to follow the development of follicles in the ovaries. During the first two seasons, no male was present, in the next two seasons, a mature male was present without mating, and in the final two seasons a mature male was present, mating with one or both females. When no male was present or when present without mating, ovarian follicles developed to full size, but ovulation did not occur and the follicles gradually began to decrease in diameter and undergo changes evident on ultrasound. In the fifth season, only one of the females mated, dropping two eggs after 7 days, and continued to oviposit throughout the following months (total 275 eggs). The unmated female did not ovulate, showing the same pattern as earlier seasons. In the final season, both females mated and ovulated, dropping eggs for the next four months (total 539 eggs). The following year, no males were present and neither female ovulated. This study provides clear evidence that ovulation in loggerhead sea turtles is induced by mating. Zoo Biol 27:213–225, 2008. © 2008 Wiley‐Liss, Inc.     

Strong male‐biased operational sex ratio in a breeding population of loggerhead turtles (Caretta caretta) inferred by paternal genotype reconstruction analysis

Characterization of a species mating systems is fundamental for understanding the natural history and evolution of that species. Polyandry can result in the multiple paternity of progeny arrays. The only previous study of the loggerhead turtle (Caretta caretta) in the USA showed that within the large peninsular Florida subpopulation, multiple paternity occurs in approximately 30% of clutches. Our study tested clutches from the smaller northern subpopulation for the presence of multiple paternal contributions. We examined mothers and up to 20 offspring from 19.5% of clutches laid across three nesting seasons (2008–2010) on the small nesting beach on Wassaw Island, Georgia, USA. We found that 75% of clutches sampled had multiple fathers with an average of 2.65 fathers per nest (1–7 fathers found). The average number of fathers per clutch varied among years and increased with female size. There was no relationship between number of fathers and hatching success. Finally, we found 195 individual paternal genotypes and determined that each male contributed to no more than a single clutch over the 3‐year sampling period. Together these results suggest that the operational sex ratio is male‐biased at this site.     

Multiple paternity in loggerhead turtle (Caretta caretta) nests on Melbourne Beach, Florida: a microsatellite analysis

Many aspects of sea turtle biology are difficult to measure in these enigmatic migratory species, and this lack of knowledge continues to hamper conservation efforts. The first study of paternity in a sea turtle species used allozyme analysis to suggest multiple paternity in loggerhead turtle (Caretta caretta) clutches in Australia. Subsequent studies indicated that the frequency of multiple paternity varies from species to species and perhaps location to location. This study examined fine-scale population structure and paternal contribution to loggerhead clutches on Melbourne Beach, FL, USA using microsatellite markers. Mothers and offspring from 70 nests collected at two locations were analysed using two to four polymorphic microsatellite loci. Fine-scale population differentiation was not evident between the sampled locations, separated by 8 km. Multiple paternity was common in loggerhead nests on Melbourne Beach; 22 of 70 clutches had more than one father, and six had more than two fathers. This is the first time that more than two fathers have been detected for offspring in individual sea turtle nests. Paternal genotypes could not be assigned with confidence in clutches with more than two fathers, leaving the question of male philopatry unanswered. Given the high incidence of multiple paternity, we conclude that males are not a limiting resource for this central Florida nesting aggregate.     

Tetranucleotide microsatellites from the loggerhead sea turtle (Caretta caretta)

We describe primers and polymerase chain reaction conditions to amplify 15 tetranucleotide microsatellite loci from the loggerhead sea turtle (Caretta caretta). The primers were tested on 30 individuals that nested along the Georgia, USA coast. The primer pairs developed in this study yielded an average of 13.9 alleles per locus (range of 10–21), an average observed heterozygosity of 0.91 (range 0.79–1.00), and an average polymorphic information content of 0.88 (range 0.84–0.92).     

Estimating the complex patterns of survey availability for loggerhead turtles

Successful management strategies are important for conservation and allow accurate surveying and monitoring of populations for presence, abundance, and trend. This becomes challenging for cryptic, low-density species, and for animals that have complicated life histories where not every stage of the life cycle can be surveyed effectively. We used information from animal-borne data loggers to characterize the dive-surfacing behavior of cryptic loggerhead turtles (Caretta caretta) in the northwest Atlantic from 2009–2018. Our data covered a large geographic area off the east coast of North America, and allowed us to present estimates for and variation in 3 metrics that can be used to assess availability bias affecting visual surveys: average dive duration, average surface duration, and the proportion of time at the surface. We used a stochastic partial differential equation approach to construct spatiotemporal regression models for the availability bias metrics. Model predictions showed pronounced individual, spatial, and spatiotemporal (seasonal) variation among the 245 turtles. Overall, we estimated an average dive duration of 14.5 ± 1.36 minutes (SE), an average surface duration of 15.1 ± 2.77 minutes, and an average proportion of time at the surface of 0.50 (95% CI = 0.41–0.59). We made predictions of the 3 availability bias metrics on a 20-km × 20-km grid and further used predictions to explore seasonal variations. Our results contribute new insights into loggerhead turtle behavior and provide information that enables survey counts to be translated into more accurate abundance estimates.     

Metabolic heating in Mediterranean loggerhead sea turtle clutches

Offspring sex ratio is an important demographic parameter and, given its determination by incubation temperature in sea turtles, might be a key factor for their conservation under climate warming. An appealing approach to estimate hatchling sex ratios is to measure sand temperatures at nest depth and deduce hatchling sex ratios from a beforehand-established relationship of hatchling sex ratio and sand temperature. Such estimates will only be accurate though if metabolic heat produced by the embryos is considered. Judging whether metabolic heating has a potential effect on hatchling sex ratios without actually measuring temperature within clutches would greatly facilitate monitoring protocols. We tested for a relationship between the amount of metabolic heating and the number of developed embryos as well as clutch size in the largest known loggerhead sea turtle (Caretta caretta) population of the Mediterranean on Zakynthos (Greece). Temperatures were measured within 20 nests as well as at a reference site in the sand at nest depth. Metabolic heating was detected, but only during the last third of the incubation period did nests heat up considerably (1.6 °C on average) above the temperature of the surrounding sand. During the middle third of incubation, when sex is determined, the amount of metabolic heating was negligible. The amount of metabolic heating during the last third of the incubation duration was significantly correlated to the number of offspring developed to at least about 75% of incubation duration. This factor explained nearly 50% of variation in metabolic heating. Metabolic heating was also significantly correlated to clutch size. Given that clutch size within the Mediterranean is largest in Zakynthos loggerheads, we conclude that metabolic heating can be ignored in the estimate of hatchling sex ratios in Mediterranean loggerhead populations. These results thus provide the basis for a feasible monitoring of hatchling sex ratios in the loggerhead sea turtle in the Mediterranean.     

Nest site selection of loggerhead sea turtles: The case of the island of Zakynthos, W Greece

The sandy beaches of Zakynthos Island support the largest single nesting aggregation in the Mediterranean Region of the endangered loggerhead turtle Caretta caretta. The present study attempts to determine possible correlations between a series of habitat variables and nest site selection. Nesting activities, including total and nesting emergences were examined in response to the recorded biotic and abiotic variables. The results of the analysis indicate that beach width is the most critical habitat variable affecting nest site selection. Further analysis of nesting performance implies that sea turtles use multiple environmental cues for nest site selection during the different steps of the nesting processes such as emergence from the surf and nesting. Nevertheless, we caution that a detailed study needs to be conducted over a more extensive period of time to verify these suggestions.     

The frequency of multiple paternity predicts variation in testes size among island populations of house mice

Polyandry generates selection on males through sperm competition, which has broad implications for the evolution of ejaculates and male reproductive anatomy. Comparative analyses across species and competitive mating trials within species have suggested that sperm competition can influence the evolution of testes size, sperm production and sperm form and function. Surprisingly, the intraspecific approach of comparing among population variation for investigating the selective potential of sperm competition has rarely been explored. We sampled seven island populations of house mice and determined the frequency of multiple paternity within each population. Applying the frequency of multiple paternity as an index of the risk of sperm competition, we looked for selective responses in male reproductive traits. We found that the risk of sperm competition predicted testes size across the seven island populations of house mice. However, variation in sperm traits was not explained by sperm competition risk. We discuss these findings in relation to sperm competition theory, and other intrinsic and extrinsic factors that might influence ejaculate quality.     

Heavy metals in marine turtle eggs and hatchlings in the Mediterranean

Abstract

The concentrations of cadmium, lead, iron, copper and zinc were analysed in Loggerhead Turtle (Caretta caretta) hatchling samples (eggshells, remaining yolk, and liver) from beaches of southwest Turkey. Cd, Pb, Fe, and Cu concentrations were higher in embryo liver than in yolk. Zn concentration was higher in yolk. Hg concentrations in all yolk samples were below the detection limit, but levels could be measured in some embryo livers.     

Life‐history constraints on maximum population growth for loggerhead turtles in the northwest Atlantic

Conservation planning for protected species often relies on estimates of life‐history parameters. A commonly used parameter is the instantaneous maximum population growth rate (r_max) that can be used to limit removals and design recovery targets. Estimation of r_max can be challenging because of limited availability of species‐ and population‐specific data and life‐history information. We applied a method proposed by Neil and Lebreton, originally developed for birds, to loggerhead turtles. The method uses age‐at‐first‐reproduction and adult survival to estimate r_max. We used a variety of datasets and matrix population models to confirm an allometric assumption required by the method, and to generate estimates of age‐at‐first‐reproduction and adult survival. A meta‐analysis was applied to parameters from reported growth curves, which were then combined with the size distribution of neophyte nesters to derive estimates of age‐at‐first‐reproduction. Adult survival rates were obtained from an existing matrix population model. Monte Carlo simulation was then used to combine the estimates of the allometric coefficients, age‐at‐first‐reproduction, and adult survival to obtain a probability distribution of approximate r_max values. Estimated annual maximum population growth rates averaged 0.024, with a mode of 0.017 and a 95% highest density interval of 0.006–0.047. These estimates were similar to values reported by others using different methods and captured the variability in positive, annual change estimates across nesting beach sites for the northwest Atlantic loggerhead population. The use of life‐history parameters has a long history in wildlife and fisheries management and conservation planning. Our estimates of r_max, while having some biases and uncertainty, encompassed values presently used in recovery planning for loggerhead turtles and offer additional information for the management of endangered and threatened species.     

Only some like it hot — quantifying the environmental niche of the loggerhead sea turtle

Although the Atlantic waters of North America support hundreds of thousands of loggerhead sea turtles ( Caretta caretta ), remarkably little is known regarding their migratory ecology and habitat use. We integrate satellite tracking with remotely sensed oceanographic data to uncover two different migratory strategies used by loggerhead turtles at the northern part of their range. Most turtles travelled from the nesting beach to forage at higher latitudes in summer, before migrating south to wintering grounds in the autumn. Others moved south after nesting to forage for up to 514 days and did not make an autumn migration. Both groups utilized warm waters at the very edge of the Gulf Stream during winter: for southerly turtles obviating seasonal migration, and for northerly turtles minimizing the distance, time and energy required to reach northern areas for subsequent foraging seasons, avoiding lethally cold winter temperatures in inshore waters at the same latitude, and reducing energy costs that would be incurred within the fast-flowing Gulf Stream. Females made long resting dives of up to 7 h 24 min, effectively hibernating during the colder months. Offshore federal waters of the USA constitute a more important habitat for both foraging and wintering turtles than previously appreciated. These areas are potential hotspots for interaction with fisheries and proposed US military training activities and should receive special monitoring efforts to fully assess the extent of overlap.     

Post-nesting movements and submergence patterns of loggerhead marine turtles in the Mediterranean assessed by satellite tracking

Two female loggerhead turtles (Caretta caretta) were tracked, following nesting at Alagadi Beach (35°33′N, 33°47′E), Northern Cyprus, eastern Mediterranean for 60 and 82 days, respectively. The two individuals showed marked differences in their behaviour. Individual A was tracked to Syrian coastal waters, whereas individual B travelled around the coast of Northern Cyprus to a foraging site in the waters off the east coast of Northern Cyprus. Submergence durations varied markedly during different phases of the migration, suggesting coastal foraging/resting at certain stages en route with sustained directed travelling movements during initial coastal movements and open ocean crossing. Both turtles showed fidelity to foraging grounds for the duration of transmissions (Turtle A: 36 days; Turtle B: 58 days). In both cases, locations were centred in inshore waters although the two individuals exhibited quite different submergence patterns. Individual A carried out very short dives of typical duration <10 min, whereas Individual B carried out longer dives with typical duration >20 min. Diel differences in submergence duration at the foraging grounds suggested longer dives at night/early morning for both turtles. For Turtle A, there was a general reduction in submergence duration as the period of residence increased; a pattern that may have been related to increasing temperature experienced. The total distance travelled by the two turtles (320 and 227 km) was relatively short when compared to satellite tracking studies of conspecifics following nesting in South Africa and USA and tagging studies of nesting loggerhead turtles in Greece and Australia. It is hypothesized that short migratory distance may be correlated with both the small body size and the relatively high frequency of remigration in this population.     

Evidence for transoceanic migrations by loggerhead sea turtles in the southern Pacific Ocean

Post-hatchling loggerhead turtles (Caretta caretta) in the northern Pacific and northern Atlantic Oceans undertake transoceanic developmental migrations. Similar migratory behaviour is hypothesized in the South Pacific Ocean as post-hatchling loggerhead turtles are observed in Peruvian fisheries, yet no loggerhead rookeries occur along the coast of South America. This hypothesis was supported by analyses of the size-class distribution of 123 post-hatchling turtles in the South Pacific and genetic analysis of mtDNA haplotypes of 103 nesting females in the southwest Pacific, 19 post-hatchlings stranded on the southeastern Australian beaches and 22 post-hatchlings caught by Peruvian longline fisheries. Only two haplotypes (CCP1 93% and CCP5 7%) were observed across all samples, and there were no significant differences in haplotype frequencies between the southwest Pacific rookeries and the post-hatchlings. By contrast, the predominant CCP1 haplotype is rarely observed in North Pacific rookeries and haplotype frequencies were strongly differentiated between the two regions (F_st=0.82; p=<0.00001). These results suggest that post-hatchling loggerhead turtles emerging from the southwest Pacific rookeries are undertaking transoceanic migrations to the southeastern Pacific Ocean, thus emphasizing the need for a broader focus on juvenile mortality throughout the South Pacific to develop effective conservation strategies.     

First evidence of multiple paternity in the blue shark (Prionace glauca)

Multiple paternity (MP) is defined as the behaviour in which females successfully mate with multiple males leading to offspring from different sires within the same litter. MP seems to be frequent and an evolutionary advantage in elasmobranchs. Here the authors report for the first time the occurrence of MP in the cosmopolitan blue shark Prionace glauca L. The evidence, gathered via microsatellite genotyping of pregnant females and their embryos, suggests that MP is very frequent in this species. Knowledge of MP in P. glauca should help describe more precisely its reproductive biology and contribute to the management of its populations.     

The genetic structure of the loggerhead sea turtle (Caretta caretta) in the Mediterranean as revealed by nuclear and mitochondrial DNA and its conservation implications

The population genetic structure of the loggerhead sea turtle (Caretta caretta) nesting in the eastern Mediterranean was assessed by sequencing a fragment of the control region of the mitochondrial DNA (n = 190) and seven microsatellites (n = 112). The two types of markers revealed genetic structuring (mtDNA: γ_st = 0.212, P < 0.001; nDNA F _st = 0.006, P < 0.001), thus indicating that both females and males are philopatric and that gene flow between populations is restricted. Mitochondrial DNA data indicate that the female populations nesting on the islands of Crete and Cyprus have suffered a recent bottleneck or colonization event. However, no bottleneck or founder effect was revealed by nuclear markers, thus indicating male-mediated gene flow from other populations that would increase nuclear genetic variability. Crete, and to a lower extent Cyprus, are thought to play a central role in such male-mediated gene flow that may reduce the negative effect of genetic drift or inbreeding on the small populations of Lebanon and Israel. This population structure indicates that assessing population relevance only on the basis of genetic variability and size would be misleading, as some populations not fulfilling those requirements may play a relevant role in genetic exchange and hence contribute to the overall genetic variability.     

Microsatellites indicate a high frequency of multiple paternity in Apodemus (Rodentia)

Microsatellites were employed to estimate frequency of multiple paternity litters of two species of mice (genus Apodemus): striped field mouse (A. agrarius), and wood mouse (A. sylvaticus). Ten pregnant females of A. agrarius and six of A. sylvaticus were collected from natural populations in the northern Ukraine and analysed with 11 and nine microsatellite loci, respectively. Multiple paternity was indicated in eight of 10 litters in A. agrarius and in three of six litters in A. sylvaticus. Multiple paternity was documented at several loci (ranging from two to 10). In two cases (A. agrarius), three males were estimated to have fathered the litter.