Effects of rising temperature on the viability of an important sea turtle rookery

Abstract

A warming world poses challenges for species with temperature-dependent sex determination, including sea turtles, for which warmer incubation temperatures produce female hatchlings. We combined in situ sand temperature measurements with air temperature records since 1850 and predicted warming scenarios from the Intergovernmental Panel on Climate Change to derive 250-year time series of incubation temperatures, hatchling sex ratios, and operational sex ratios for one of the largest sea turtles rookeries globally (Cape Verde Islands, Atlantic). We estimate that light-coloured beaches currently produce 70.10% females whereas dark-coloured beaches produce 93.46% females. Despite increasingly female skewed sex ratios, entire feminization of this population is not imminent. Rising temperatures increase the number of breeding females and hence the natural rate of population growth. Predicting climate warming impacts across hatchlings, male–female breeding ratios and nesting numbers provides a holistic approach to assessing the conservation concerns for sea turtles in a warming world.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Figure 1: Cape Verde is a very important loggerhead rookery with an estimated 10,000–15,000 nests laid annually across the archipelago49,50.
Figure 2: Mean sand temperature versus mean air temperature for nesting beaches on the island of Sal.
Figure 3: Mean metabolic heating of loggerhead eggs on the island of Sal, Cape Verde.
Figure 4: A 250-year incubation temperature time series for the beaches of Sal according to the SRES A2 scenario with the 95% prediction intervals (grey lines).
Figure 5: A 250-year hatchling sex ratio time series for the light sand beaches (lower grey line), dark sand beaches (upper grey line) and all beaches combined (black line) of Sal according to the SRES A2 scenario.
Figure 6: A 250-year operational sex ratio time series (upper line) and expected change in nesting numbers (lower line) for Sal according to the SRES A2 scenario.

References

  1. 1

    Walther, G. R. et al. Ecological responses to recent climate change. Nature 416, 389–395 (2002).

    CAS  Article  Google Scholar 

  2. 2

    Perry, A. L., Low, P. J., Ellis, J. R. & Reynolds, J. D. Climate change and distribution shifts in marine fishes. Science 308, 1912–1915 (2005).

    CAS  Article  Google Scholar 

  3. 3

    Malcolm, J. R., Liu, C., Neilson, R. P., Hansen, L. & Hannah, L. Global warming and extinctions of endemic species from biodiversity hotspots. Conserv. Biol. 20, 538–548 (2006).

    Article  Google Scholar 

  4. 4

    Anderson, J. J., Gurarie, E., Bracis, C., Burke, B. J. & Laidre, K. L. Modeling climate change impacts on phenology and population dynamics of migratory marine species. Ecol. Modell. 264, 83–97 (2013).

    Article  Google Scholar 

  5. 5

    Saba, V. S., Stock, C. A., Spotila, J. R., Paladino, F. V. & Tomillo, P. S. Projected response of an endangered marine turtle population to climate change. Nature Clim. Change 2, 814–820 (2012).

    Article  Google Scholar 

  6. 6

    Thomas, C. D. et al. Extinction risk from climate change. Nature 427, 145–148 (2004).

    CAS  Article  Google Scholar 

  7. 7

    Pounds, J. A. et al. Widespread amphibian extinctions from epidemic disease driven by global warming. Nature 439, 161–167 (2006).

    CAS  Article  Google Scholar 

  8. 8

    Wintle, B. A. et al. Ecological-economic optimization of biodiversity conservation under climate change. Nat. Clim. Change 1, 355–359 (2011).

    Article  Google Scholar 

  9. 9

    Bellard, C. et al. Will climate change promote future invasions? Glob. Chang. Biol. 19, 3740–3748 (2013).

    Article  Google Scholar 

  10. 10

    Davenport, J. Temperature and the life-history strategies of sea turtles. J. Therm. Biol. 22, 479–488 (1997).

    Article  Google Scholar 

  11. 11

    Yntema, C. L. & Mrosovsky, N. Critical periods and pivotal temperatures for sexual differentiation in loggerhead sea turtles. Can. J. Zool. 60, 1012–1016 (1982).

    Article  Google Scholar 

  12. 12

    Mrosovsky, N. Pivotal temperatures for loggerhead turtles (Caretta caretta) from northern and southern nesting beaches. Can. J. Zool. 66, 661–669 (1988).

    Article  Google Scholar 

  13. 13

    Mrosovsky, N. & Pieau, C. Transitional range of temperature, pivotal temperatures and thermosensitive stages for sex determination in reptiles. Amphibia-Reptilia 12, 169–179 (1991).

    Article  Google Scholar 

  14. 14

    Mrosovsky, N., Kamel, S., Rees, A. F. & Margaritoulis, D. Pivotal temperature for loggerhead turtles (Caretta caretta) from Kyparissia Bay, Greece. Can. J. Zool. 80, 2118–2124 (2002).

    Article  Google Scholar 

  15. 15

    Viets, B. E., Tousignant, A., Ewert, M. A., Nelson, C. E. & Crews, D. Temperature-dependent sex determination in the leopard gecko, Eublepharis macularius. J. Exp. Zool. 265, 679–683 (1993).

    CAS  Article  Google Scholar 

  16. 16

    Burke, R. L., Ewert, M. A., McLemore, J. B. & Jackson, D. R. Temperature-dependent sex determination and hatching success in the gopher tortoise (Gopherus polyphemus). Chelon. Conserv. Biol. 2, 86–88 (1996).

    Google Scholar 

  17. 17

    Warner, D. A. & Shine, R. The adaptive significance of temperature-dependent sex determination in a reptile. Nature 451, 566–568 (2008).

    CAS  Article  Google Scholar 

  18. 18

    Hays, G. C., Broderick, A. C., Glen, F. & Godley, B. J. Climate change and sea turtles: A 150-year reconstruction of incubation temperatures at a major marine turtle rookery. Glob. Change Biol. 9, 642–646 (2003).

    Article  Google Scholar 

  19. 19

    Fuentes, M. M. P. B. et al. Proxy indicators of sand temperature help project impacts of global warming on sea turtles in northern Australia. Endang. Species Res. 9, 33–40 (2009).

    Article  Google Scholar 

  20. 20

    Witt, M. J., Hawkes, L. A., Godfrey, M. H., Godley, B. J. & Broderick, A. C. Predicting the impacts of climate change on a globally distributed species: The case of the loggerhead turtle. J. Exp. Biol. 213, 901–911 (2010).

    CAS  Article  Google Scholar 

  21. 21

    Girondot, M. Statistical description of temperature-dependent sex determination using maximum likelihood. Evol. Ecol. Res. 1, 479–486 (1999).

    Google Scholar 

  22. 22

    Hays, G. C., Fossette, S., Katselidis, K. A., Schofield, G. & Gravenor, M. B. Breeding periodicity for male sea turtles, operational sex ratios, and implications in the face of climate change. Conserv. Biol. 24, 1636–1643 (2010).

    Article  Google Scholar 

  23. 23

    Scott, R., Marsh, R. & Hays, G. C. Life in the really slow lane: Loggerhead sea turtles mature late relative to other reptiles. Funct. Ecol. 26, 227–235 (2012).

    Article  Google Scholar 

  24. 24

    Pearse, D. E. & Avise, J. C. Turtle mating systems: Behaviour, sperm storage, and genetic paternity. J. Hered. 92, 206–211 (2001).

    CAS  Article  Google Scholar 

  25. 25

    Ireland, J. S. et al. Multiple paternity assessed using microsatellite markers, in green turtles Chelonia mydas (Linnaeus, 1758) of Ascension Island, South Atlantic. J. Exp. Mar. Bio. Ecol. 291, 149–160 (2003).

    CAS  Article  Google Scholar 

  26. 26

    Lee, P. L. M. & Hays, G. C. Polyandry in a marine turtle: Females make the best of a bad job. Proc. Natl Acad. Sci. USA 101, 6530–6535 (2004).

    CAS  Article  Google Scholar 

  27. 27

    Godley, B. J., Broderick, A. C., Frauenstein, R., Glen, F. & Hays, G. C. Reproductive seasonality and sexual dimorphism in green turtles. Mar. Ecol. Prog. Ser. 226, 125–133 (2002).

    Article  Google Scholar 

  28. 28

    Schofield, G. et al. Evidence-based marine protected area planning for a highly mobile endangered marine vertebrate. Biol. Conserv. 161, 101–109 (2013).

    Article  Google Scholar 

  29. 29

    Plotkin, P. T., Owens, D. W., Byles, R. A. & Patterson, R. Departure of male olive ridley turtles (Lepidochelys olivacea) from a nearshore breeding ground. Herpetologica 52, 1–7 (1996).

    Google Scholar 

  30. 30

    Lee, P. L. M., Luschi, P. & Hays, G. C. Detecting female precise natal philopatry in green turtles using assignment methods. Mol. Ecol. 16, 61–74 (2007).

    Article  Google Scholar 

  31. 31

    Kamel, S. J. Vegetation cover predicts temperature in nests of the hawksbill sea turtle: Implications for beach management and offspring sex ratios. Endanger. Species Res. 20, 41–48 (2013).

    Article  Google Scholar 

  32. 32

    Godley, B. J. et al. Thermal conditions in nests of loggerhead turtles: Further evidence suggesting female skewed sex ratios of hatchling production in the Mediterranean. J. Exp. Mar. Bio. Ecol. 263, 45–63 (2001).

    Article  Google Scholar 

  33. 33

    Zbinden, J. A., Margaritoulis, D. & Arlettaz, R. Metabolic heating in Mediterranean loggerhead sea turtle clutches. J. Exp. Mar. Bio. Ecol. 334, 151–157 (2006).

    Article  Google Scholar 

  34. 34

    DeGregorio, B. A. & Southwood Williard, A. Incubation temperatures and metabolic heating of relocated and in situ loggerhead sea turtle (Caretta caretta) nests at a northern rookery. Chelonian Conserv. Biol. 10, 54–61 (2011).

    Article  Google Scholar 

  35. 35

    Wallace, B. P. et al. Biotic and abiotic factors affect the nest environment of embryonic leatherback turtles, Dermochelys coriacea. Physiol. Biochem. Zool. 77, 423–432 (2013).

    Article  Google Scholar 

  36. 36

    Broderick, A. C., Godley, B. J. & Hays, G. C. Metabolic heating and the prediction of sex ratios for green turtles (Chelonia mydas). Physiol. Biochem. Zool. 74, 161–170 (2001).

    CAS  Article  Google Scholar 

  37. 37

    Rees, A. F. & Margaritoulis, D. Beach temperatures, incubation durations and estimated hatchling sex ratio for loggerhead sea turtle nests in southern Kyparissia Bay, Greece. Testudo 6, 23–36 (2004).

    Google Scholar 

  38. 38

    Hawkes, L. A., Broderick, A. C., Godfrey, M. H. & Godley, B. J. Investigating the potential impacts of climate change on a marine turtle population. Glob. Chang. Biol. 13, 1–10 (2007).

    Article  Google Scholar 

  39. 39

    Houghton, J. D. R. et al. Protracted rainfall decreases temperature within leatherback turtle (Dermochelys coriacea) clutches in Grenada, West Indies: Ecological implications for a species displaying temperature dependent sex determination. J. Exp. Mar. Bio. Ecol. 345, 71–77 (2007).

    Article  Google Scholar 

  40. 40

    Hinder, S. L. et al. Changes in marine dinoflagellate and diatom abundance under climate change. Nat. Clim. Chang. 2, 271–275 (2012).

    Article  Google Scholar 

  41. 41

    Wickramasinghe, R. H. Sea turtles of Sri Lankan waters. Vidurava 13, 20–22 (1991).

    Google Scholar 

  42. 42

    Eckert, K. L., Bjorndal, K. A., Abreu-Grobois, F. A. & Donnelly, M. Research and Management Techniques for the Conservation of Sea Turtles Ch 3, (IUCN/SSC Marine Turtle Specialist Group Publication No 4, 1999).

    Google Scholar 

  43. 43

    Wright, L. I. et al. Turtle mating patterns buffer against disruptive effects of climate change. Proc. R. Soc. B. 279, 2122–2127 (2012).

    Article  Google Scholar 

  44. 44

    Limpus, C. J. The green turtle, Chelonia mydas, in Queensland: Breeding males in the southern Great Barrier Reef. Wildl. Res. 20, 513–523 (1993).

    Article  Google Scholar 

  45. 45

    Houghton, J. D. R. & Hays, G. C. Asynchronous emergence by loggerhead turtle (Caretta caretta) hatchlings. Naturwissenschaften 88, 133–136 (2001).

    CAS  Article  Google Scholar 

  46. 46

    McSweeney, C., New, M., Lizcano, G. & Lu, X. The UNDP climate change country profiles: Improving the accessibility of observed and projected climate information for studies of climate change in developing countries. Bull. Am. Meteorol. Soc. 91, 157–166 (2010).

    Article  Google Scholar 

  47. 47

    Marcovaldi, M. A., Godfrey, M. H. & Mrosovsky, N. Estimating sex ratios of loggerhead turtles in Brazil from pivotal incubation durations. Can. J. Zool. 75, 755–770 (1997).

    Article  Google Scholar 

  48. 48

    Tucek, J., Nel, R., Girondot, M. & Hughes, G. Age-size relationship at reproduction of South African female loggerhead turtles Caretta caretta. Endang. Species Res. 23, 167–175 (2014).

    Article  Google Scholar 

  49. 49

    Lino, S. P. P., Gonccalves, E. & Cozens, J. The loggerhead sea turtle (Caretta caretta) on Sal Island, Cape Verde: Nesting activity and beach surveillance in 2009. Arquipélago: Life Mar. Sci. 27, 59–63 (2010).

    Google Scholar 

  50. 50

    Marco, A. et al. The international importance of the archipelago of Cape Verde for marine turtles, in particular the loggerhead turtle Caretta caretta. Zool. Caboverdiana 2, 1–11 (2011).

    Google Scholar 

Download references

Acknowledgements

G.C.H. was supported by the Climate Change Consortium for Wales (C3W). The authors thank Paolo Luschi and Mariel Murazzi for their help with the sand temperature measurements. We thank SOS Tartarugas for their support to loggerhead conservation in Cape Verde and the numerous volunteers who helped with the fieldwork. J-O.L. thanks Jean-Baptiste Laloë for his help in establishing the mathematical equation to calculate the hatchling sex ratios.

Author information

Affiliations

Authors

Contributions

J.C. initiated the project and completed all the field work. J.C., B.R., and A.T. compiled the data. G.C.H. conceived the manuscript. J-O.L. led the data analysis. J-O.L. and G.C.H. wrote the manuscript with contributions from all authors.

Corresponding author

Correspondence to Jacques-Olivier Laloë.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Laloë, JO., Cozens, J., Renom, B. et al. Effects of rising temperature on the viability of an important sea turtle rookery. Nature Clim Change 4, 513–518 (2014). https://doi.org/10.1038/nclimate2236

Download citation

Further reading

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing