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Nesting beaches of loggerhead and green sea turtles in Turkey (bolds indicate main nesting beaches) and meteorological stations the temperatures of which were obtained from Turkish State Meteorological Service.
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Hatchling sex ratios of loggerhead sea turtles (Caretta caretta) were estimated on two main nesting beaches (Dalyan Beach and Göksu Delta) in Turkey using three methods: nest temperature, incubation period and gonad histology. The electronic temperature recorders were placed in 35 selected nests. The mean nest temperature in the middle third of the...
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... characteristics of sea turtles have generated much interest in the sex ratio of offsprings produced by sea turtles. Survival of sea turtle populations depends on a range of incubation temperatures suitable for the production of offspring of both sexes (Kaska et al. 1998). Under- standing the relationship between temperature and sex ratio on a beach enables protection to be organized in a way that conserves both sexes. The manipulation of hatchling sex ratios can certainly have an effect on the reproductive ecology and recovery of sea turtle populations (Wibbels 2003). Sea turtle species are likely to be impacted by climate change owing to possessing temperature-dependent sex determination. There is an insuffi- ciency of data on the actual sex ratios of offspring produced by regional sea turtle populations. The lack of such information inhibits the ability of researchers to accurately predict how future meteorological and climate- driven changes may affect turtle populations. Further- more, these data are integral for the development of regional and global recovery plans for declining turtle populations (Fuller et al. 2013). Although adult sea turtles possess sexual dimorphism, sea turtle hatchlings do not have physical differences to be able to determine the sex of individual hatchlings (Wibbels 2003; Wyneken et al. 2007). Therefore, several methods can be used to estimate the sex ratios of the hatchlings, such as histological study, examining both tes- tosterone and oestrogen levels in the blood or testing cho- rioallantoic fluid via radioimmunoassay, incubation Temperature is an important factor for sea turtles, since they possess temperature-dependent sex differentiation owing to the absence of their heteromorphic sex chromo- somes (Bull 1980; Wibbels et al. 2000). Previous studies suggest that the temperature-sensitive period of sex differentiation is approximately the middle third of the incubation period in sand (Yntema & Mrosovsky 1982; Kaska et al. 1998; Kaska et al. 2006). The temperature at which an equal sex ratio is produced is called the pivotal temperature. Although evolutionary theory suggests that the primary sex ratio should be 1:1 if parental investment in both sexes is equal (Fisher 1930; Charnov & Bull 1989), incubation above the pivotal temperature results in more females and below the pivotal temperature results in more males (Mrosovsky & Pieau 1991; Kaska et al. 1998; Kaska et al. 2006). Pivotal temperatures for all sea turtle species are reported to exist within a relatively narrow temperature range from approximately 27.7 C to 31 C (Wibbels 2003), and beach temperature variations cause different sex ratios among populations (Mrosovsky 1994). The range of incubation temperature in which both sexes are produced is generally about 2 C–3 C wide, around the pivotal temperature (Mrosovsky 1994). This range of incubation temperature is called the transitional range of temperatures (TRT). Temperatures below the lower limit of the TRT produce only males and temperatures above the upper limit of the TRT produce only females (Mrosovsky & Pieau 1991). durations, beach temperatures and nest incubation temperatures (Yntema & Mrosovsky 1980; Marcovaldi et al. 1997; Kaska et al. 1998; Merchant-Larios 1999; Wibbels 2003). Using some of these methods, various studies on the sex ratio of loggerhead turtles ( Caretta caretta ) have been carried out. In several studies, it was reported that majority of the hatchlings were female due to high nest temperatures. Sex ratios skewed as much as 90% towards females have been found or inferred for loggerhead turtle hatchlings in the USA (Mrosovsky & Provancha 1992; Hanson et al. 1998), in Brazil (Marcovaldi et al. 1997; Mrosovsky et al. 1999) and in the Mediterranean (Kaska et al. 1998; Godley et al. 2001; Mrosovsky et al. 2002; Oz € et al. 2004; Kaska et al. 2006; U car et al. 2012; Jribi et al. 2013). Although the majority of the nesting beaches in the world produce highly female-dominated hatchling sex ratios, there are some key sites having conditions that are biased toward producing male hatchlings (Baptistotte et al. 1999) and some small beaches having nearly 1:1 hatchling sex ratios (Mrosovsky et al. 1984; Marcovaldi et al. 1997; Foley et al. 2000; Hawkes et al. 2007). In this study, we aimed to estimate loggerhead sea turtle hatchling sex ratios on the most eastern and western loggerhead nesting beaches (Dalyan Beach and G oksu Delta, respectively) which are approximately 500 km from each other on the Turkish Mediterranean coast using different methods and to compare the validity of each method. Both beaches are the beaches of prime importance based on the numbers of nests laid there. We believe that this study will contribute to conservation programmes of sea turtle populations nesting on the Mediterranean coasts, since sex ratios of the populations are of great importance, as well as genetic diversity of them, for their management and conservation purposes. The Mediterranean coasts of Turkey are important nesting grounds for both loggerhead and green sea turtles (Groombridge 1990). Based on the nest numbers, Turkey holds the second most important loggerhead sea turtle stocks (Margaritoulis et al. 2003) in the Mediterranean. Female loggerhead sea turtles nest on beaches of Turkey from late April until mid-August. Nests hatch from late June until early October. Dalyan Beach is one of the most important reproductive sites of the loggerhead turtles in terms of annual nest numbers (Table 1), nesting density and regular sea turtle surveys not only for Turkey but also for the Mediterranean region. Dalyan Beach, which has a length of 4.5 km, is located in the south-west of Turkey (Figure 1). G oksu Delta is also one of the most important reproductive sites of the loggerhead turtles in Turkey. The 35-km long beach is located in the south-east of Turkey. The distance between Dalyan Beach and G oksu Delta is roughly 500 km. Both Dalyan Beach and G oksu Delta are beaches of prime importance based on the numbers of nests laid there. The study was conducted from mid-May to mid-Septem- ber in 2010. The beaches were patrolled from 21:00 to 02:00 and early in the morning from 06:00 to 11:00 to record any loggerhead turtle activity. All the activity from the previous night was recorded and evaluated as that day’s activity. Temperatures in loggerhead turtle nests were measured by using electronic “tiny talk” temperature recorders [Orion Components (Chichester) Ltd., Chichester, UK] on both beaches. The device fits into a 35-mm film case. The accuracy of the device was tested under laboratory conditions against a standard mercury ther- mometer and found to have a mean resolution of 0.35 C (minimum 0.3 C, maximum 0.4 C) at temperatures between 4 C and 50 C. We programmed the temperature recorders by computer for a recording period of 70 days; readings were taken at 90-minute intervals. They were recording 16 readings per day. We recorded the temperatures of 35 nests (24 on Dalyan Beach, 11 on G oksu Delta). We aimed to put one temperature recorder into one of every 15 nests on both beaches. The temperature recorders were placed into the centre of new nests during the oviposition. The nests, in which temperature recorders were placed, were screened against predation with ...
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... with a mesh size of 9 cm. The distances (m) of the nests from the sea were measured and recorded. To determine the effect of metabolic heating, temperature recorders were also placed in sand next to two clutches at the same depths. To see the temperature differences within a clutch, three temperature recorders were placed at the top, middle and bottom levels of one nest. The middle third of the incubation period was calculated from the total incubation period representing the numbers of days from the date of egg deposition to the date of the first emergence. Nests were excavated seven days after the first hatchlings emerged; the temperature recorders were taken from the nests and nest depths were measured. The total number of eggs and the hatching success were calculated by counting unhatched eggs and empty egg shells. In order to determine intra-beach thermal variations, sand temperatures were also recorded on Dalyan Beach. For this purpose, four zones were determined with 1-km intervals along the beach. In each zone, three temperature recorders were buried in the sand at nest depth (50 cm) at different distances (10, 20, 30 m) from the sea, and these devices recorded sand temperatures during five days. For the examination of sand temperature at different distances, mean values of four zones at each distance were calculated and used. In order to determine inter-beach thermal variations, six meteorological stations were determined throughout the Mediterranean coastline of Turkey. Of these, three stations (Bodrum, Dat ca and Marmaris) are close to Dalyan Beach, and the others (Anamur, Mersin and Iskenderun) _ to G oksu Delta (Figure 1). Air and sea water temperatures of these stations in 2010 were obtained from Turkish State Meteorological Service, and these temperatures have been recorded automatically once in every minute. The average of obtained temperatures was calculated for each day throughout the year, and these daily averages of air and sea water temperatures were examined using MINITAB 16 statistic programme. The sex ratios of loggerhead turtles on Dalyan Beach and G oksu Delta were estimated using three methods. One of these methods was to use the mean nest temperature during the middle third of incubation period to predict sex ratios of the beaches (Hanson et al. 1998; Kaska et al. 1998; Kaska et al. 2006). Sex ratios of the 35 temperature-recorded nests were calculated using the formula obtained by Kaska et al. (1998). Another method was to use incubation periods (Marcovaldi et al. 1997; Godley et al. 2001). For each nesting beach, we produced the graphic of the relationship between incubation periods and sex ratios (calculated using nest temperature) of temperature-recorded nests and obtained a formula in order to estimate sex ratio from incubation period. The third method was histological analysis of the gonads of all dead hatchlings and late-stage embryos ( > stage 25) found in favourable condition in nests (Yntema & Mrosovsky 1980; Kaska & Downie 1999). For this method, all the dead hatchlings found while patrolling or checking the nest surfaces and any late-stage dead embryos found in the nest during the excavation of the nests were collected. One gonad from each hatchling was cut in half trans- versely and embedded in paraffin wax, sectioned at 8 À 10 m m from the middle of the gonad, and stained with ...
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... Beach is one of the most important reproduc- tive sites of the loggerhead turtles in terms of annual nest numbers (Table 1), nesting density and regular sea turtle surveys not only for Turkey but also for the Mediterranean region. Dalyan Beach, which has a length of 4.5 km, is located in the south-west of Turkey (Figure 1). G€ oksu Delta is also one of the most important reproductive sites of the loggerhead turtles in Turkey. ...
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... G€ oksu Delta (Figure 1). Air and sea water temperatures of these stations in 2010 were obtained from Turkish State Meteorological Service, and these temperatures have been recorded automatically once in every minute. ...
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... light of this finding, we can expect the effect of nest tempera- ture on incubation period to be different on both beaches. The relationship between sex ratio estimated using mean nest temperature during the middle third of incuba- tion period and incubation period in both beaches was analysed, and the results indicated a negative correlation between them on Dalyan Beach (Pearson's correlation, r 2 D 0.79, p < 0.001) (Figure 10(a)) and on G€ oksu Delta (Pearson's correlation, r 2 D 0.84, p < 0.001) (Figure 10(b)). It was also calculated that pivotal incubation periods for Dalyan Beach and G€ oksu Delta were 60.3 and 53.5 days, respectively. ...
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... light of this finding, we can expect the effect of nest tempera- ture on incubation period to be different on both beaches. The relationship between sex ratio estimated using mean nest temperature during the middle third of incuba- tion period and incubation period in both beaches was analysed, and the results indicated a negative correlation between them on Dalyan Beach (Pearson's correlation, r 2 D 0.79, p < 0.001) (Figure 10(a)) and on G€ oksu Delta (Pearson's correlation, r 2 D 0.84, p < 0.001) (Figure 10(b)). It was also calculated that pivotal incubation periods for Dalyan Beach and G€ oksu Delta were 60.3 and 53.5 days, respectively. ...
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... examination, it was seen that only 188 of specimens were male, and the rest (235) were female. The Figure 10. Correlation of sex ratios of the temperature- recorded nests to the total incubation periods on Dalyan Beach (a) and on G€ oksu Delta (b). ...
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... sex ratios in each 15- day period in nesting season were statistically different from each other (x 2 D 35.53, df D 4, p < 0.001). As dem- onstrated in Figure 11, it was determined that there was a positive correlation between the period of nesting and sex ratio of those nests obtained via histological examination (Pearson's correlation, r 2 D 0.85, p < 0.001). ...
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... In addition, some sites with relatively balanced sex ratios have experienced some extreme warming. This was the case in Dalyan (Turkey), one of the most important reproductive sites for loggerheads in the Mediterranean, where histological data revealed 55.6% female-biased sex ratios (Sarı & Kaska, 2015) and we detected high warming (i.e. 1.93°C per century). ...
Climate warming and the feminization of populations due to temperature‐dependent sex determination may threaten sea turtles with extinction. To identify sites of heightened risk, we examined sex ratio data and patterns of climate change over multiple decades for 64 nesting sites spread across the globe. Over the last 62 years the mean change in air temperature was 0.85°C per century (SD = 0.65°C, range = −0.53 to +2.5°C, n = 64 nesting sites). Temperatures increased at 40 of the 64 study sites. Female‐skewed hatchling or juvenile sex ratios occurred at 57 of the 64 sites, with skews >90% female at 17 sites. We did not uncover a relationship between the extent of warming and sex ratio ( r 62 = −0.03, p = .802, n = 64 nesting sites). Hence, our results suggest that female‐hatchling sex ratio skews are not simply a consequence of recent warming but have likely persisted at some sites for many decades. So other factors aside from recent warming must drive these variations in sex ratios across nesting sites, such as variations in nesting behaviour (e.g. nest depth), substrate (e.g. sand albedo), shading available and rainfall patterns. While overall across sites recent warming is not linked to hatchling sex ratio, at some sites there is both is a high female skew and high warming, such as Raine Island (Australia; 99% female green turtles; 1.27°C warming per century), nesting beaches in Cyprus (97.1% female green turtles; 1.68°C warming per century) and in the Dutch Caribbean (St Eustatius; 91.5% female leatherback turtles; 1.15°C warming per century). These may be among the first sites where management intervention is needed to increase male production. Continued monitoring of sand temperatures and sex ratios are recommended to help identify when high incubation temperatures threaten population viability.
... Satellite tracking of post-nesting loggerhead turtles from the northern part of Cyprus has shown a wide geographical distribution. Some individuals have 80 remained along the coast of Cyprus, whereas others have travelled as far as Tunisia. The majority, however, have been shown as residing and utilizing the North African coast lines of Egypt, Libya and Tunisia [10,11,15,16] (Fig 3). ...
... Satellite tracking of post-nesting loggerhead turtles from the northern part of Cyprus has shown a wide geographical distribution. Some individuals have 80 remained along the coast of Cyprus, whereas others have travelled as far as Tunisia. The majority, however, have been shown as residing and utilizing the North African coast lines of Egypt, Libya and Tunisia [10,11,15,16] (Fig 3). ...
... To date, female-biased hatchling sex ratios have been reported for most loggerhead turtle nesting beaches in Turkey (Kaska et al., 1998;Öz et al., 2004;Kaska et al., 2006;Uçar et al., 2012;Candan, 2014;Sarı and Kaska, 2015). This is also the case for other Mediterranean countries Mrosovsky et al., 2002;Rees and Margaritoulis 2004;Zbinden et al., 2007). ...
In this study, we present the first in-water monitoring results of loggerhead turtles (Caretta caretta) in Köyceğiz-Dalyan specially protected area (SPA), Turkey. The capture-mark-recapture (CMR) study encompassed a total of 113 capture events of 88 individuals across two sampling years. The majority of the population was adults (88.6%) with a highly male-biased (70.5%) sex ratio. Our results indicate that some of the overwintering individuals also contribute to the nesting population in the region. Biometric characteristics of captured individuals were also presented. Additionally, we found the population to be under heavy anthropogenic threats with 54.5% of the captured individuals exhibiting results of previous anthropogenically caused injuries. Our results suggest that Köyceğiz-Dalyan SPA is an important overwintering and foraging area for loggerhead turtles, which is currently an indexed nesting site for loggerhead turtles in the Mediterranean. Given the possible feminization effects of climate change on future marine turtle populations, the male-biased population in the study area is of the greatest importance, and together with having an indexed nesting site, the area should therefore be regarded as an important marine turtle area.
... This has often led to the use of the mean nest temperature during the middle third of incubation to predict sex ratios (e.g. Sieg et al. 2011, Fuller et al. 2013, Laloë et al. 2014, Sarı & Kaska 2015, Esteban et al. 2016, Yalçin Özdilek et al. 2016). More recent work shows that (1) the TSP shifts away from the middle third of incubation in field conditions (i.e. ...
... Kaska et al. 1998, Öz et al. 2004, LeBlanc et al. 2012, Patrício et al. 2017 or incubation durations (e.g. Godley et al. 2001, Fuller et al. 2013, dei Marcovaldi et al. 2014, Sarı & Kaska 2015. However, these approaches are likely biased since they do not account for uncontrolled sources of variation (e.g. ...
Climate change is a threat to marine turtles that is expected to affect all 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. 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 on 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.
... Satellite tracking of post-nesting loggerhead turtles from the northern part of Cyprus has shown a wide geographical distribution. Some individuals have 80 remained along the coast of Cyprus, whereas others have travelled as far as Tunisia. The majority, however, have been shown as residing and utilizing the North African coast lines of Egypt, Libya and Tunisia [10,11,15,16] (Fig 3). ...
... Given the difficulty of estimating the TSP for natural regimes of temperature, many authors use the MTID as a proxy for the TSP (e.g. Godley et al., 2002;Hanson et al., 1998;Kamel and Mrosovsky, 2006;LeBlanc et al., 2012;Merchant-Larios et al., 2010;Sarı and Kaska, 2015;Wibbels et al., 1991). However, several authors have proposed methodologies to locate the TSP during incubation at fluctuating temperatures. ...
The sexual phenotype of the gonad is dependent on incubation temperature in many turtles, all crocodilians, and some lepidosaurians. At hatching, identification of sexual phenotype is impossible without sacrificing the neonates. For this reason, a general method to infer sexual phenotype from incubation temperatures is needed. Temperature influences sex determination during a specific period of the embryonic development, starting when the gonad begins to form. At constant incubation temperatures, this thermosensitive period for sex determination (TSP) is located at the middle third of incubation duration (MTID). When temperature fluctuates, the position of the thermosensitive period for sex determination can be shifted from the MTID because embryo growth is affected by temperature. A method is proposed to locate the thermosensitive period for sex determination based on modelling the embryo growth, allowing its precise identification from a natural regime of temperatures. Results from natural nests and simulations show that the approximation of the thermosensitive period for sex determination to the middle third of incubation duration may create a quasi-systematic bias to lower temperatures when computing the average incubation temperature during this period and thus a male-bias for sex ratio estimate.
... The extent to which nest temperature is affected by those meteorological and climatic parameters depends on thermal properties of the incubation substratum and the depth at which the nest is buried. Even when marine turtles bury their eggs deep enough to buffer (Steckenreuter et al., 2010;Sieg et al., 2011;Katselidis et al., 2012;LeBlanc et al., 2012a;LeBlanc et al., 2012b;Maulany et al., 2012;Fuller et al., 2013;Gomuttapong et al., 2013;Jribi et al., 2013a;King et al., 2013;dei Marcovaldi et al., 2014;Jribi and Bradai 2014;Kılıç and Candan 2014;Simões et al., 2014;Stubbs et al., 2014;Rocha et al., 2015;Sarı and Kaska 2015;Tapilatu and Ballamu 2015;Candan and Kolankaya 2016;dei Marcovaldi et al., 2016;Yalç Ii Özdilek et al., 2016). temperature fluctuations, a slight temperature increase or decrease during incubation invalidates methods that approximate the true TSP by the middle third of the whole incubation period. ...
Knowledge of the sex ratio of a population is crucial to understand their structure and dynamics. For species, such as marine turtles, with temperature-dependent sex determination, this knowledge provides a baseline in advance of climate change. Determining the primary sex ratio for marine turtle populations is challenging since offspring lack sexually dimorphic external characteristics. Therefore several proxies have been used to estimate the primary sex ratio of marine turtle populations. However, no study to date has compared estimations of sex ratio when using different proxies to determine the most accurate and to detect potential bias. To address this, we estimated the sex ratio of natural loggerhead, Caretta caretta, nests using 8 different proxies: two based on constant temperature equivalent (average of temperature or average temperature weighted by the growth of embryos during each time step) both for three developmental periods (the whole incubation, the middle third of incubation and the middle third of development) as well as two proxies based on incubation duration (duration of the whole incubation and of the middle third of development). Sex ratio estimates differed greatly depending on the proxy being used. Here we discuss the differences among proxies based on the biological relevance of underlying hypotheses and highlight the need for studies to accurately determine the thermosensitive period and to obtain appropriate estimates of embryo growth rate to estimate marine turtle sex ratio.
... The Mediterranean coasts of Turkey are important nesting grounds for loggerheads. G€ oksu Delta beach on which green turtle (Chelonia mydas) nests as well (Piggelen and Strijbosch, 1993), with an annual mean nest number of 112, is one of the most important loggerhead turtle nesting beaches in the Mediterranean coastline of Turkey, and it marks the eastern edge of the nesting distribution in Turkey for loggerheads (Sarı and Kaska, 2015). Within the Mediterranean, this is one of the few sites, other than Cyprus, where both species nest (Glen et al., 1997), and the beach therefore is of great importance. ...
... We uploaded data recorded by these devices to the computer, and calculated sex ratios of the temperaturerecorded nests using the formula obtained by Kaska et al. (1998). In addition, we estimated the sex ratio from incubation period for these nests using the relationship between incubation periods and sex ratios (calculated using nest temperature) of temperaturerecorded nests as described by Sarı and Kaska (2015). ...
... We also observed that there was a visible increase in hatching success with the increased incubation period and distance from the sea, but hatching success decreased when the distance from the sea was more than 31 m. It is well known that longer incubation periods and lower distances from the sea are two indicators for production of more male hatchlings Sarı and Kaska, 2015). These two findings therefore imply that if the production of male hatchling is high in a nest, hatching success of that nest is high. ...
... While several MP studies were conducted previously in different nesting loggerhead turtle populations (Bollmer et al., 1999;Harry and Briscoe, 1988;Lasala et al., 2013;Moore and Ball, 2002;Tedeschi et al., 2015;Zbinden et al., 2007), there was no MP study carried out in the Mediterranean loggerhead population nesting on not only Dalyan Beach but also any other Turkish beach. Dalyan Beach is one of the most important reproductive sites of the loggerhead turtles in terms of annual nest number (Canbolat, 2004), nesting density (Canbolat, 2004), hatching success and high proportion of male hatchlings produced (Sarı and Kaska, 2015), protection status (Türkozan and Yılmaz, 2008), and regular sea turtle surveys (Sarı and Kaska, 2015) not only for Turkey but for the Mediterranean region. This beach is therefore presumably the most appropriate place for conducting the studies of MP and population size on loggerheads. ...
... While several MP studies were conducted previously in different nesting loggerhead turtle populations (Bollmer et al., 1999;Harry and Briscoe, 1988;Lasala et al., 2013;Moore and Ball, 2002;Tedeschi et al., 2015;Zbinden et al., 2007), there was no MP study carried out in the Mediterranean loggerhead population nesting on not only Dalyan Beach but also any other Turkish beach. Dalyan Beach is one of the most important reproductive sites of the loggerhead turtles in terms of annual nest number (Canbolat, 2004), nesting density (Canbolat, 2004), hatching success and high proportion of male hatchlings produced (Sarı and Kaska, 2015), protection status (Türkozan and Yılmaz, 2008), and regular sea turtle surveys (Sarı and Kaska, 2015) not only for Turkey but for the Mediterranean region. This beach is therefore presumably the most appropriate place for conducting the studies of MP and population size on loggerheads. ...
... Accounting for the male component of the populations has important consequences for determining population viability. Hatchling and juvenile sex ratios in sea turtles are relatively easy to determine, and have been found to be strongly female-biased (Godfrey et al., 1996;Hawkes et al., 2007;Mrosovsky et al., 2002;Sarı and Kaska, 2015), with some exceptions (Baptistotte et al., 1999;Steckenreuter et al., 2010). Apart from these sex ratios, it is critical to understand the OSRs of adult populations. ...
