Sex Ratio Estimation of Green Turtle Hatchlings in Kazanlı Beach, Türkiye

Abstract

Sea turtles are distributed worldwide, mostly in the tropical and subtropical waters. All seven species of sea turtles in the world have temperature-dependent sex determination. The pivotal temperature for hatchlings with a female:male ratio of 1:1 is usually around 29°C. Female hatchlings are observed at values higher than the pivotal temperature and male hatchlings at lower values. It is expected that wildlife threatened by global warming will be more severely affected, especially species that sex is determined by temperature. This study was carried out by measuring air, sand and nest temperatures during two nesting seasons at Kazanlı Beach, one of the largest nesting sites of Chelonia mydas (Green turtle) in the Mediterranean. Sand grain size was also measured, and gonads of dead hatchlings were examined histologically. Both sand (n=4) and nest (n=6) temperatures were above the pivotal temperature (between 29.1-31.6°C) in the study area. According to the estimation based on temperatures, hatchlings were female (♀>50%) biased. Of the hatchling samples, 75 were examined histologically. According to histological examination, the female:male ratio was 2:1. According to the direct examination and indirect estimation; the sex ratio of green turtle hatchlings in Kazanlı Beach, one of the highest hatchling producing nesting sites of the Mediterranean, was reported for the first time in this study. There is a need to fill the data gaps regarding sex ratios, especially for major beaches with high hatchling production. Knowing the temperature profiles in and around the nest and sex ratios of hatchlings is critical for the development of conservation measures for endangered sea turtles.

Keywords

• Chelonia mydas
• Mediterranean Sea
• Temperature-dependent sex determination
• Thermal profiles
• Sex ratio
• Gonadal Histology

Ethical Statement

The study is complied with research and publication ethics

Thanks

I thank to volunteers of Sea Turtle Conservation Project of Kazanlı Beach supervised by EKAD (Ecological Research Society) and Güven ARSLAN for mapping. I also thank to anonymous reviewers for their contribution.

References

1. [1] J. W. Moore and D. E. Schindler, “Getting ahead of climate change for ecological adaptation and resilience,” Science no. 376, pp. 1421–1426, 2022, doi: 10.1126/science.abo3608.
2. [2] H. P. Roberts, L. L. Willey, M. T. Jones, T. S. Akre, D. I. King, J. Kleopfer, ... and B. Zarate, “Is the future female for turtles? Climate change and wetland configuration predict sex ratios of a freshwater species,” Glob Chang Biol, vol. 29, no. 10, pp. 2643-2654, 2023, doi: 10.1111/gcb.16625.
3. [3] F. J. Janzen, “Climate change and temperature-dependent sex determination in reptiles,” PNAS, vol. 91, no. 16, pp. 7487-7490, 1994.
4. [4] R. B. Huey, L. Patridge and K. Fowler, “Thermal sensitivity of Drosophila melanogaster responds rapidly to laboratory natural selection,” Evol., vol. 45, no. 3, pp. 751-756, 1991, doi: 10.2307/2409925.
5. [5] N. J. Robinson, J. Aguzzi, S. Arias, C. Gatto, S. K. Mills, A. Monte, ... and P. S. Tomillo, “Global trends in sea turtle research and conservation: Using symposium abstracts to assess past biases and future opportunities,” Glob. Ecol. Conserv., vol. 47, Article no. e02587, 2023, doi: 10.1016/j.gecco.2023.e02587.
6. [6] S. Catron, S. Roth, F. Zumpano, J. Bintz, J. A. Fordyce, S. Lenhart, ... and J. Wyneken, “Modeling the impacts of temperature during nesting seasons on Loggerhead (Caretta caretta) Sea Turtle populations in South Florida,” Ecol Modell, vol. 481, Article no. 110363, 2023, doi: 10.1016/j.ecolmodel.2023.110363.
7. [7] B. J. Godley, A. C. Broderick, R. Frauenstein, F. Glen and G. C. Hays, “Reproductive seasonality and sexual dimorphism in green turtles,” Mar. Ecol. Prog. Ser., vol. 226, pp. 125-133, 2002, doi: 10.3354/meps226125.
8. [8] N. Valenzuela, D. C. Adams, R. M. Bowden and A. C. Gauger, “Geometric morphometric sex estimation for hatchling turtles: a powerful alternative for detecting subtle sexual shape dimorphism,” Copeia, vol. 4, pp. 735-742, 2004, doi: 10.1643/CH-03-248R1.

9. [9] Ç. Kılıç and O. Candan, “Hatchling sex ratio, body weight and nest parameters for Chelonia mydas nesting on Sugözü beaches (Turkey),” Anim Biodivers Conserv, vol. 37, no. 2, pp. 177-182, 2014, doi: 10.32800/abc.2014.37.0177.
10. [10] R. King, W. H. Cheng, C. T. Tseng, H. Chen and I. J. Cheng, “Estimating the sex ratio of green sea turtles (Chelonia mydas) in Taiwan by the nest temperature and histological methods,” J. Exp. Mar. Biol. Ecol., vol. 445, pp. 140-147, 2013, doi: 10.1016/j.jembe.2013.03.016.
11. [11] J. Braun-Mc, S. P. Epperly, D. W. Owens, L. Avens, E. Williams and C. A. Harms, “Seasonal reliability of testosterone radioimmunoassay (RIA) for predicting sex ratios of juvenile loggerhead (Caretta caretta) turtles,” Herpetol., vol. 63, no. 3, pp. 275-284, 2007.
12. [12] S. A. Ceriani and J. Wyneken, “Comparative morphology and sex identification of the reproductive system in formalin-preserved sea turtle specimens,” Zool., vol. 111, no. 3, pp. 179-187, 2008, doi: 10.1016/j.zool.2007.07.007.
13. [13] B. Sönmez, E. Bağda, O. Candan and H. E. Yılmaz, “Sex determination in green turtle hatchlings: geometric morphometry and molecular sex markers,” NESciences, vol. 4, no.1, pp. 42-54, 2019, doi: 10.28978/nesciences.522623.
14. [14] R. Calderón-Peña, R. Betancourt-Avila, E. Rodríguez-Fajardo, Y. Martínez-González and J. Azanza-Ricardo, “Sex ratio of the green sea turtle Chelonia mydas (Testudines: Cheloniidae) hatchlings in the Guanahacabibes Peninsula, Cuba,” Rev. Biol. Trop., vol. 68, no. 3, pp. 777-784, 2020, doi: 10.15517/rbt.v68i3.39033.
15. [15] M. H. Godfrey and N. Mrosovsky, “Pivotal temperature for green sea turtles, Chelonia mydas, nesting in Suriname,” Herpetol. J., vol. 16, no. 1, pp. 55-61, 2006.
16. [16] O. Türkozan and Y. Kaska, “Turkey,” in Sea turtles in the Mediterranean: distribution, threats and conservation priorities, P. Casale and D. Margaritoulis, Eds., Gland, Switzerland: IUCN, 2010, pp. 257-293.
17. [17] O. Candan and D. Kolankaya , "Temperature Profiles And Sex Ratio Estimation For Green Turtle Chelonia mydas Hatchlings On Sugözü Beaches", Hacettepe J. Biol. Chem., vol. 42, no. 4, pp. 531-536, 2014.
18. [18] C. L. Yntema and N. Mrosovsky, “Critical periods and pivotal temperatures for sexual differentiation in loggerhead sea turtles,” Can. J. Zool., vol: 60, no. 5, pp. 1012-1016, 1982, doi:10.1139/z82-141.
19. [19] O. Candan and D. Kolankaya, “Sex ratio of green turtle (Chelonia mydas) hatchlings at Sugözü, Turkey: higher accuracy with pivotal incubation duration,” Chelonian Conserv. Biol., vol. 15, no. 1, pp. 102-108, 2016, doi: 10.2744/CCB-1132.1.
20. [20] C. L. Yntema and N. Mrosovsky, “Sexual differentiation in hatchling loggerheads (Caretta caretta) incubated at different controlled temperatures,” Herpetol., vol. 36, no. 1, pp. 33-36, 1980.
21. [21] B. N. Reid and M. Z. Peery, “Land use patterns skew sex ratios, decrease genetic diversity and trump the effects of recent climate change in an endangered turtle,” Diversity Distrib., vol. 20, pp. 1425-1437, 2014, doi: 10.1111/ddi.12243.
22. [22] M. Kasparek, B. J. Godley and A. C. Broderick, “Nesting of the Green Turtle, Chelonia mydas, in the Mediterranean: a review of status and conservation needs,” Zool Middle East, vol. 24, no. 1, pp. 45-74, 2001, doi: 10.1080/09397140.2001.10637885.
23. [23] L. A. Hawkes, A. C. Broderick, M. H. Godfrey and B. J. Godley, “Climate change and marine turtles,” Endang Species Res, vol. 7, no. 2, pp. 137-154, 2009, doi: 10.3354/esr00198.
24. [24] N. Mrosovsky, S. R. Hopkins-Murphy and J.I. Richardson, “Sex ratio of sea turtles: seasonal changes,” Science, vol. 225, pp. 739–741, 1984.
25. [25] E. A. Standora and J. R. Spotila, “Temperature dependent sex determination in sea turtles,” Copeia, vol. 3, pp. 711–722, 1985.
26. [26] G. Vázquez Luna, R. Sanchez Trejo, R. Márquez Millan and R. Castro Melendez, “Temporal and spatial variation of the hatching temperature in transplanted Lepidochelys kempi nestings and their influence on teh sex ratio, egg survival and mortality,” in The Eighteenth International Sea Turtle Symposium (Mazatlán: NOAA Technical Memorandum NMFS-SEFSC-436), 2000.
27. [27] M. Hamann, M.H. Godfrey, J.A. Seminoff, P.C.R. Barata, K.A. Bjorndal, A.B. Bolten, A.C. Broderick, L.M. Campbell, C. Carreras, P. Casale, M. Chaloupka, S.-K. Chan, M. Coyne, L.B. Crowder, C.E. Diez, P.H. Dutton, S.P. Epperly, N.N. FitzSimmons, A. Formia, M. Girondot, G.C. Hays, I.J. Cheng, Y. Kaska, R. Lewison, J.A. Mortimer, W.J. Nichols, R.D. Reina, K. Shanker, J.R. Spotila, J. Tomás, B.P. Wallace, Thierry M. Work, N. Zbinden, and B.J. Godley, “Global research priorities for sea turtles: informing management and conservation in the 21st century,” Endang Species Res, vol. 11, no. 3, pp. 245-269, 2010, doi: 10.3354/esr00279.
28. [28] N. Mrosovsky, S. Kamel, A. F. Rees and D. Margaritoulis, “Pivotal temperature for loggerhead turtles (Caretta caretta) from Kyparissia Bay, Greece,” Can. J. Zool., vol. 80, no. 12, pp. 2118-2124, 2002, doi: 10.1139/z02-204.
29. [29] G. Arslan, A. Ertürk and O. Candan, “Predicting the distribution of green turtle nesting sites over the Mediterranean with outcoming climate driven changes,” J. Nat. Conserv., vol. 71, no.126320, 2023, doi: 10.1016/j.jnc.2022.126320.
30. [30] J. J. Lembrechts, J. van den Hoogen, J. Aalto, M. B. Ashcroft, P. De Frenne, J. Kemppinen, ... and D. S. Hik, “Global maps of soil temperature,” Glob Chang Biol, vol. 28, no. 9, pp. 3110-3144, 2022, doi: 10.1111/gcb.16060.
31. [31] H. O. Pörtner, D. C. Roberts, M. Tignor, E. S. Poloczanska, K. Mintenbeck, A. Alegría, M. Craig, S. Langsdorf, S. Löschke, V. Möller et al., “Climate change 2022: impact, adaptation, and vulnerability” in Contribution of Working Group II to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change. Summary for Policymakers, H.O. Pörtner, D.C. Roberts, M. Tignor, E.S. Poloczanska, K. Mintenbeck, A. Alegría, M. Craig, S. Langsdorf, S. Löschke, V. Möller, A. Okem and B. Rama Eds., Cambridge, UK, Cambridge University Press, 2023, doi: 10.1017/9781009325844.
32. [32] K. C. Santos, M. Livesey, M. Fish and A. C. Lorences, “Climate change implications for the nest site selection process and subsequent hatching success of a green turtle population,” Mitig Adapt Strateg Glob Chang, vol. 22, pp. 121-135, 2017, doi: 10.1007/s11027-015-9668-6.
33. [33] C. T. Chu, D. T. Booth and C. J. Limpus, “Estimating the sex ratio of loggerhead turtle hatchlings at Mon Repos rookery (Australia) from nest temperatures,” Aust. J. Zool., vol. 56, pp. 57-64, 2008, doi:10.1071/ZO08004.
34. [34] B. F. Önder and O. Candan, “The feminizing effect of metabolic heating in Green Turtle (Chelonia mydas) clutches in the eastern Mediterranean,” Zool Middle East, vol. 62, no. 3, pp. 239-246, 2016, doi: 10.1080/09397140.2016.1202927.
35. [35] N. Mrosovsky and C. L. Yntema, “Temperature dependence of sexual differentiation in sea turtles: implications for conservation practices,” Biol. Conserv., vol. 18, no. 4, pp. 271-280, 1980, doi: 10.1016/0006-3207(80)90003-8.
36. [36] S. S. Heppell, J. Wyneken and S. A. Heppell, “A morphologist, a modeler, and an endocrinologist consider sea turtle sex ratios in a changing climate. Some wine was involved,” Front. Ecol. Evol., vol. 10, no. 952432, 2022, doi: 10.3389/fevo.2022.952432
37. [37] A. D. Mazaris, C. Dimitriadis, M. Papazekou, G. Schofield, A. Doxa, A. Chatzimentor, O. Turkozan, S. Katsanevakis, A. Lioliou, S. Abalo-Morla, M. Aksissou, A. Arcangeli, V. Attard, H. A. El Hili, F. Atzori, E. J. Belda, L. B. Nakhla, A. A. Berbash, K. A. Bjorndal, A. C. Broderick, J.A. Camiñas, O. Candan, L. Cardona, I. Cetkovic, N. Dakik, G. A. de Lucia, P. G. Dimitrakopoulos, S. Diryaq, C. Favilli, C. M. Fortuna, W. J. Fuller, S. Gallon, A. Hamza, I. Jribi, M. B. Ismail, Y. Kamarianakis, Y. Kaska, K. Korro, D. Koutsoubas, G. Lauriano, B. Lazar, D. March, A. Marco, C. Minotou, J. R. Monsinjon, N. M. Naguib, A. Palialexis, V. Piroli, K. Sami, B. Sönmez, L. Sourbès, D. Sözbilen, F. Vandeperre, P. Vignes, M. Xanthakis, V. Köpsel and M. A. Peck, “Priorities for Mediterranean marine turtle conservation and management in the face of climate change,” J. Environ. Manage., vol. 339, no. 117805, 2023, doi: 10.1016/j.jenvman.2023.117805.