A potential tool to mitigate the impacts of climate change to the caribbean leatherback sea turtle

Global Change Biology

Volumn 18, Issue 2, 2012, Pages 401-411

  Patino Martinez, Juan ^a,b   Marco, Adolfo ^a   Quiñones, Liliana ^a   Hawkes, Lucy ^c  

^a DEPARTMENT OF CONSERVATION BIOLOGY   (Spain)

^b ARANZADI Zientzia Elkartea Society of Science   (Spain)

^c BANGOR UNIVERSITY   (United Kingdom)

Author keywords

Colombia; Conservation; Global change; Hatchery; Leatherback; Panama; Reproduction; Sea turtles; Sex ratio; Temperature

Indexed keywords

AIR TEMPERATURE; BIODIVERSITY; CLIMATE CHANGE; CLIMATE EFFECT; CONSERVATION; FEMINIZATION; GLOBAL CHANGE; HATCHING; INCUBATION; REPRODUCTION; SEX RATIO; SPATIOTEMPORAL ANALYSIS; SURVIVORSHIP; TURTLE;

COLOMBIA; PANAMA [CENTRAL AMERICA];

CHELONIIDAE; DERMOCHELYIDAE; DERMOCHELYS CORIACEA; TESTUDINES;

EID: 84855826063     PISSN: 13541013     EISSN: 13652486     Source Type: Journal    
DOI: 10.1111/j.1365-2486.2011.02532.x     Document Type: Article

References (113)

1. Alfaro-Shigueto J, Dutton PH, Van Bressem M, Mangel J (2007) Interactions between leatherback turtles and Peruvian artisanal fisheries. Chelonian Conservation and Biology, 1, 129-134.
2. Angeles ME, Gonzalez JE, Erickson DJ, Hernandez JL (2007) Predictions of future climate change in the Caribbean region using global general circulation models. International Journal of Climatology, 27, 555-569.
3. Araujo MB, Rahbek C (2006) How does climate change affect biodiversity? Science, 313, 1396-1397.
4. Baker JD, Littnan CL, Johnston DW (2006) Potential effects of sea level rise on the terrestrial habitats of endangered and endemic megafauna in the Northwestern Hawaiian Islands. Endangered Species Research, 4, 21-30.
5. Baskale E, Kaska Y (2005) Sea turtle nest conservation techniques on southwestern beaches in Turkey. Israel Journal of Zoology, 51, 13-26.
6. Bell G, Collins S (2008) Adaptation, extinction and global change. Evolutionary Applications, 1, 3-16.
7. Bilinski JJ, Reina RD, Spotila JR, Paladino FV (2001) The effects of nest environment on calcium mobilization by leatherback turtle embryos (Dermochelys coriacea) during development. Comparative Biochemistry and Physiology. Part A, Molecular & Integrative Physiology, 130, 151-162.
8. Binckley CA, Spotila J, Wilson KS, Paladino F (1998) Sex determination and sex ratios of Pacific leatherback turtles, Dermochelys coriacea. Copeia, 2, 291-300.
9. Blanvillain G, Pease AP, Segars AL, Rostal DC, Richards AJ, Owens DW (2008) Comparing methods for the assessment of reproductive activity in adult male loggerhead sea turtles Caretta caretta at Cape Canaveral, Florida. Endangered Species Research, 6, 75-85.
10. Booth DT, Freeman C (2006) Sand and nest temperatures and an estimate of hatchling sex ratio from the Heron Island green turtle (Chelonia mydas) rookery, Southern Great Barrier Reef. Coral Reefs, 25, 629-633.
11. Booth DT, Burgess E, McCosker J, Lanyon JM (2005) The influence of incubation temperature on post-hatching fitness characteristics of turtles. Animals and Environments Book Series: International Congress Series, 1275, 226-233, doi: 10.1016/j.ics.2004.08.057.
12. Both C, van Asch M, Bijlsma RG, van den Burg AB, Visser ME (2009) Climate change and unequal phenological changes across four trophic levels: constraints or adaptations? Journal of Animal Ecology, 78, 73-83.
13. Broderick AC, Godley BJ, Hays GC (2001) Metabolic heating and the prediction of sex ratios for green turtles (Chelonia mydas). Physiological and Biochemical Zoology, 74, 161-170.
14. Chaloupka M, Kamezaki N, Limpus C (2008) Is climate change affecting the population dynamics of the endangered Pacific loggerhead sea turtle? Journal of Experimental Marine Biology and Ecology, 356, 136-143.
15. Chan EH, Liew HC (1995) Incubation temperatures and sex ratios in the Malaysian leatherback turtle Dermochelys coriacea. Biological Conservation, 74, 169-174.
16. Chevalier J, Godfrey MH, Girondot M (1999) Significant difference of temperature-dependent sex determination between French Guiana (Atlantic) and Playa Grande (Costa-Rica, Pacific) leatherbacks (Dermochelys coriacea). Annales des Sciences Naturelles-Zoologie et Biologie Animale, 20, 147-152.
17. Congdon JD, Nagle RD, Dunham AE, Beck CW, Kinney OM, Yeomans SR (1999) The relationship of body size to survivorship of hatchling snapping turtles (Chelydra serpentina): an evaluation of the "bigger is better"'hypothesis. Oecologia, 121, 224-235.
18. Dalrymple GH, Hampp JC, Wellins DJ (1985) Male-biased sex-ratio in a cold nest of a hawksbill sea turtle (Eretmochelys-Imbricata). Journal of Herpetology, 19, 158-159.
19. Davenport J (1989) Sea turtles and the greenhouse effect. British Herpetological Society Bulletin, 29, 11-15.
20. Davenport J (1997) Temperature and the life-history strategies of sea turtles. Journal of Thermal Biology, 22, 479-488.
21. Delgado C, Canario AVM, Dellinger T (2010) Sex ratios of loggerhead sea turtles Caretta caretta during the juvenile pelagic stage. Marine Biology, 157, 979-990.
22. Doody JS, Guarino E, Georges A, Corey B, Murray G, Ewert M (2006) Nest site choice compensates for climate effects on sex ratios in a lizard with environmental sex determination. Evolutionary Ecology, 20, 307-330.
23. Drake DL, Spotila JR (2002) Thermal tolerances and the timing of sea turtle hatchling emergence. Journal of Thermal Biology, 27, 71-81.
24. Dutton DL, Dutton PH, Chaloupka M, Boulon RH (2005) Increase of a Caribbean leatherback turtle Dermochelys coriacea nesting population linked to long-term nest protection. Biological Conservation, 126, 186-194.
25. Edwards M, Richardson AJ (2004) Impact of climate change on marine pelagic phenology and trophic mismatch. Nature, 430, 881-884.
26. Ferraroli S, Georges JY, Gaspar P, Le Maho Y (2004) Endangered species - where leatherback turtles meet fisheries. Nature, 429, 521-522.
27. Fish MR, Cote IM, Gill JA, Jones AP, Renshoff S, Watkinson AR (2005) Predicting the impact of sea-level rise on Caribbean sea turtle nesting habitat. Conservation Biology, 19, 482-491.
28. Fish MR, Cote IM, Horrocks JA, Mulligan B, Watkinson AR, Jones AP (2008) Construction setback regulations and sea-level rise: mitigating sea turtle nesting beach loss. Ocean & Coastal Management, 51, 330-341.
29. Fuentes M, Abbs D (2010) Effects of projected changes in tropical cyclone frequency on sea turtles. Marine Ecology Progress Series, 412, 283-292.
30. Fuentes M, Bateman BL, Hamann M (2011a) Relationship between tropical cyclones and the distribution of sea turtle nesting grounds. Journal of Biogeography, 38, 1886-1896.
31. Fuentes M, Cinner JE (2010) Using expert opinion to prioritize impacts of climate change on sea turtles' nesting grounds. Journal of Environmental Management, 91, 2511-2518.
32. Fuentes M, Dawson JL, Smithers SG, Hamann M, Limpus CJ (2010a) Sedimentological characteristics of key sea turtle rookeries: potential implications under projected climate change. Marine and Freshwater Research, 61, 464-473.
33. Fuentes M, Limpus CJ, Hamann M (2011b) Vulnerability of sea turtle nesting grounds to climate change. Global Change Biology, 17, 140-153.
34. Fuentes M, Limpus CJ, Hamann M, Dawson J (2010b) Potential impacts of projected sea-level rise on sea turtle rookeries. Aquatic Conservation: Marine and Freshwater Ecosystems, 20, 132-139.
35. Fuentes MMPB, Hamann M, Limpus CJ (2009a) Past, current and future thermal profiles of green turtle nesting grounds: implications from climate change. Journal of Experimental Marine Biology and Ecology, 383, 56-64.
36. Fuentes MMPB, Maynard JA, Guinea ML, Bell IP, Werdell PJ, Hamann M (2009b) Proxy indicators of sand temperature help project impacts of global warming on sea turtles in northern Australia. Endangered Species Research, 9, 33-40.
37. Garcon JS, Grech A, Moloney J, Hamann M (2010) Relative Exposure Index: an important factor in sea turtle nesting distribution. Aquatic Conservation: Marine and Freshwater Ecosystems, 20, 140-149.
38. Girondot M, Godfrey MH, Ponge L, Rivalan P (2007) Modeling approaches to quantify leatherback nesting trends in French Guiana and Suriname. Chelonian Conservation and Biology, 6, 37-46.
39. Glen F, Broderick AC, Godley BJ, Hays GC (2005) Patterns in the emergence of green (Chelonia mydas) and loggerhead (Caretta caretta) turtle hatchlings from their nests. Marine Biology, 146, 1039-1049.
40. Glen F, Mrosovsky N (2004) Antigua revisited: the impact of climate change on sand and nest temperatures at a hawksbill turtle (Eretmochelys imbricata) nesting beach. Global Change Biology, 10, 2036-2045.
41. Godfrey MH, Barreto R, Mrosovsky N (1997) Metabolically-generated heat of developing eggs and its potential effect on sw ratio of sea turtle hatchlings. Journal of Herpetology, 31, 616-619.
42. Godley BJ, Broderick AC, Downie JR et al. (2001) Thermal conditions in nests of loggerhead turtles: further evidence suggesting female skewed sex ratios of hatchling production in the Mediterranean. Journal of Experimental Marine Biology and Ecology, 263, 45-63.
43. Hamann M, Godfrey MH, Seminoff JA et al. (2010) Global research priorities for sea turtles: informing management and conservation in the 21st century Endangered Species Research, 11, 245-269.
44. Hampe A, Petit RJ (2005) Conserving biodiversity under climate change: the rear edge matters. Ecology Letters, 8, 461-467.
45. Hawkes LA, Broderick AC, Godfrey MH, Godley BJ (2007) Investigating the potential impacts of climate change on a marine turtle population. Global Change Biology, 13, 923-932.
46. Hawkes LA, Broderick AC, Godfrey MH, Godley BJ (2009) Climate change and marine turtles. Endangered Species Research, 7, 137-154.
47. Hawkes LA, Witt MJ, Broderick AC et al. (2011) Home on the range: spatial ecology of loggerhead turtles in Atlantic waters of the USA Diversity and Distributions, 17, 624-640.
48. Hays GC, Adams CR, Mortimer JA, Speakman JR (1995) Inter-beach and intra-beach thermal variation for green turtle nests on Ascension Island, South-Atlantic. Journal of the Marine Biological Association of the United Kingdom, 75, 405-411.
49. Hays GC, Ashworth JS, Barnsley MJ et al. (2001) The importance of sand albedo for the thermal conditions on sea turtle nesting beaches. Oikos, 93, 87-94.
50. Hays GC, Broderick AC, Glen F, Godley BJ (2003) Climate change and sea turtles: a 150-year reconstruction of incubation temperatures at a major marine turtle rookery. Global Change Biology, 9, 642-646.
51. Hays GC, Fossette S, Katselidis KA, Schofield G, Gravenor MB (2010) Breeding Periodicity for Male Sea Turtles, Operational Sex Ratios, and Implications in the Face of Climate Change. Conservation Biology, 24, 1636-1643.
52. Hays GC, Godley BJ, Broderick AC (1999) Long-term thermal conditions on the nesting beaches of green turtles on Ascension Island. Marine Ecology Progress Series, 185, 297-299.
53. Heller NE, Zavaleta ES (2009) Biodiversity management in the face of climate change: a review of 22 years of recommendations. Biological Conservation, 142, 14-32.
54. Hirayama R (1998) Oldest known sea turtle. Nature, 392, 705-708.
55. Hoegh-Guldberg O (2011) Coral reef ecosystems and anthropogenic climate change. Regional Environmental Change, 11, S215-S227.
56. Hoegh-Guldberg O, Mumby PJ, Hooten AJ et al. (2007) Coral reefs under rapid climate change and ocean acidification. Science, 318, 1737-1742.
57. Houghton JDR, Myers AE, Lloyd C, King RS, Isaacs C, Hays GC (2007) Protracted rainfall decreases temperature within leatherback turtle (Dermochelys coriacea) clutches in Grenada, West Indies: ecological implications for a species displaying temperature dependent sex determination. Journal of Experimental Marine Biology and Ecology, 345, 71-77.
58. Hulin V, Delmas V, Girondot M, Godfrey MH, Guillon JM (2009) Temperature-dependent sex determination and global change: are some species at greater risk? Oecologia, 160, 493-506.
59. IPCC (2007) Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge.
60. IUCN (2008) Red list of Threatened Species. Available at: (accessed 4 January 2009).
61. Janzen FJ (1994) Climate change and temperature-dependent sex determination in reptiles. Proceedings of the National Academy of Sciences of the United States of America, 91, 7487-7490.
62. Johnson GC, Purkey SG (2009) Deep Caribbean sea warming. Deep-Sea Research. Part I, Oceanographic Research Papers, 56, 827-834.
63. Jribi I, Echwikhi K, Bradai MN, Bouain A (2008) Incidental capture of sea turtles by longlines in the Gulf of Gabes (South Tunisia): a comparative study between bottom and surface longlines. Scientia Marina, 72, 337-342.
64. Kamel SJ, Mrosovsky N (2006) Deforestation: risk of sex ratio distortion in hawksbill sea turtles. Ecological Applications, 16, 923-931.
65. Kaschner K, Tittensor DP, Ready J, Gerrodette T, Worm B (2011) Current and future patterns of global marine mammal biodiversity. PLoS ONE, 6, 1-13.
66. Magrin GC, Gay García D, Cruz Choque JC et al. (2007) Latin America. Climate Change 2007. Cambridge University Press, Cambridge, UK. pp. 581-615.
67. Mazaris AD, Matsinos G, Pantis JD (2009) Evaluating the impacts of coastal squeeze on sea turtle nesting. Ocean & Coastal Management, 52, 139-145.
68. McGowan A, Broderick AC, Frett G et al. (2008) Down but not out: marine turtles of the British Virgin Islands. Animal Conservation, 11, 92-103.
69. McMahon CR, Hays GC (2006) Thermal niche, large-scale movements and implications of climate change for a critically endangered marine vertebrate. Global Change Biology, 12, 1330-1338.
70. Miller JD (1985) Embryology of marine turtles. In: Biology of the Reptilia, Vol 14, (eds Gans C, Billett F), pp. 269-328. Wiley Interscience, New York.
71. Morjan CL (2003a) How rapidly can maternal behavior affecting primary sex ratio evolve in a reptile with environmental sex determination? The American Naturalist, 162, 205-219.
72. Morjan CL (2003b) Variation in nesting patterns affecting nest temperatures in two populations of painted turtles (Chrysemys picta) with temperature-dependent sex determination. Behavioral Ecology and Sociobiology, 53, 254-261.
73. Mrosovsky N (1994) Sex ratios of sea turtles. Journal of Experimental Zoology, 270, 16-27.
74. Mrosovsky N, Provancha J (1992) Sex-ratio of Hatchling Loggerhead Sea-Turtles - data and estimates from a 5-year study. Canadian Journal of Zoology, 70, 530-538.
75. Mrosovsky N, Yntema CL (1980) Temperature-dependence of sexual-differentiation in sea turtles - implications for conservation practices. Biological Conservation, 18, 271-280.
76. Mumby PJ, Hastings A, Edwards HJ (2007) Thresholds and the resilience of Caribbean coral reefs. Nature, 450, 98-101.
77. Naro-Maciel E, Mrosovsky N, Marcovaldi MA (1999) Thermal profiles of sea turtle hatcheries and nesting areas at Praia do Forte, Brazil. Chelonian Conservation and Biology, 3, 407-413.
78. Patino-Martinez J (2010) Factores Ambientales que Influyen sobre la Reproducción de la Tortuga Laúd (Dermochelys coriacea) en Colombia y Sur de Panamá. Aplicación a Programas de Manejo y Conservación. PhD thesis. Universidad de Salamanca. Salamanca, España.
79. Patino-Martinez J, Marco A, Quinones L, Godley B (2008) Globally significant nesting of the leatherback turtle (Dermochelys coriacea) on the Caribbean coast of Colombia and Panama. Biological Conservation, 141, 1982-1988.
80. Pike DA, Antworth RL, Stiner JC (2006) Earlier nesting contributes to shorter nesting seasons for the Loggerhead Seaturtle, Caretta caretta. Journal of Herpetology, 40, 91-94.
81. Pike DA, Stiner JC (2007) Sea turtle species vary in their susceptibility to tropical cyclones. Oecologia, 153, 471-478.
82. Pilcher NJ, Enderby S (2001) Effects of prolonged retention in hatcheries on green turtle (Chelonia mydas) hatchling swimming speed and survival. Journal of Herpetology, 35, 633-638.
83. Poloczanska ES, Hawkins SJ, Southward AJ, Burrows MT (2008) Modeling the response of populations of competing species to climate change. Ecology, 89, 3138-3149.
84. Rahmstorf S, Cazenave A, Church JA, Hansen JE, Keeling RF, Parker DE, Somerville RCJ (2007) Recent climate observations compared to projections. Science, 316, 709.
85. Read AJ (2007) Do circle hooks reduce the mortality of sea turtles in pelagic longlines? A review of recent experiments. Biological Conservation, 135, 155-169.
86. Reece SE, Broderick AC, Godley BJ, West SA (2002) The effects of incubation environment, sex and pedigree on the hatchling phenotype in a natural population of loggerhead turtles. Evolutionary Ecology Research, 4, 737-748.
87. Rees AF, Al Saady S, Broderick AC, Coyne MS, Papathanasopoulou N, Godley BJ (2010) Behavioural polymorphism in one of the world's largest populations of loggerhead sea turtles Caretta caretta. Marine Ecology Progress Series, 418, 201-212.
88. Reina RD, Mayor PA, Spotila JR, Piedra R, Paladino FV (2002) Nesting ecology of the leatherback turtle, Dermochelys coriacea, at Parque Nacional Marino Las Baulas, Costa Rica: 1988-1989 to 1999-2000. Copeia, 3, 653-664.
89. Rimblot F, Fretey J, Mrosovsky N, Lescure J, Pieau C (1985) Sexual differentiation as a function of the incubation temperature of eggs in the sea-turtle Dermochelys coriacea (Vandelli, 1761). Amphibia-Reptilia, 6, 83-92.
90. Robinson RA, Crick HQP, Learmonth JA et al. (2009) Travelling through a warming world: climate change and migratory species. Endangered Species Research, 7, 87-99.
91. Rumbold DG, Davis PW, Perretta C (2001) Estimating the effect of beach nourishment on Caretta caretta (loggerhead sea turtle) nesting. Restoration Ecology, 9, 304-310.
92. Saba VS, Shillinger GL, Swithenbank AM, Block BA, Spotila JR, Musick JA, Paladino FV (2008) An oceanographic context for the foraging ecology of eastern Pacific leatherback turtles: consequences of ENSO (vol 55, pg 646, 2008). Deep-Sea Research. Part I, Oceanographic Research Papers, 55, 646-660.
93. Sandoval S, Gomez-Munoz V, Gutierrez J, Porta-Gandara MA (2011) Metabolic heat estimation of the sea turtle Lepidochelys olivacea embryos. Journal of Thermal Biology, 36, 138-141.
94. Schofield G, Hobson VJ, Lilley MKS, Katselidis KA, Bishop CM, Brown P, Hays GC (2010) Inter-annual variability in the home range of breeding turtles: implications for current and future conservation management. Biological Conservation, 143, 722-730.
95. Schwanz LE, Janzen FJ (2008) Climate change and temperature-dependent sex determination: can individual plasticity in nesting phenology prevent extreme sex ratios? Physiological and Biochemical Zoology, 81, 826-834.
96. Selkoe KA, Halpern BS, Toonen RJ (2008) Evaluating anthropogenic threats to the Northwestern Hawaiian Islands. Aquatic Conservation: Marine and Freshwater Ecosystems, 18, 1149-1165.
97. Seminoff JA, Shanker K (2008) Marine turtles and IUCN Red Listing: a review of the process, the pitfalls, and novel assessment approaches. Journal of Experimental Marine Biology and Ecology, 356, 52-68.
98. Spotila JR, Dunham AE, Leslie AJ, Steyermark AC, Plotkin PT, Paladino FV (1996) Worldwide population decline of Dermochelys coriacea: are leatherback turtles going extinct? Chelonian Conservation and Biology, 2, 209-222.
99. Spotila JR, Reina RD, Steyermark AC, Plotkin PT, Paladino FV (2000) Pacific leatherback turtles face extinction. Nature, 405, 529-530.
100. Spotila JR, Standora EA, Morreale SJ, Ruiz GJ (1987) Temperature-dependent sex determination in the green turtle (Chelonia mydas) - effects on the sex-ratio on a natural nesting beach. Herpetologica, 43, 74-81.
101. Standora EA, Spotila JR (1985) Temperature dependent sex determination in sea turtles. Copeia, 1985, 711-722.
102. Theissinger K, FitzSimmons NN, Limpus CJ, Parmenter CJ, Phillott AD (2009) Mating system, multiple paternity and effective population size in the endemic flatback turtle (Natator depressus) in Australia. Conservation Genetics, 10, 329-346.
103. Tucker JK, Dolan CR, Lamer JT, Dustman EA (2008a) Climatic warming, sex ratios, and red-eared sliders (Trachemys scripta elegans) in Illinois. Chelonian Conservation and Biology, 7, 60-69.
104. Tucker JK, Paukstis GL, Janzen FJ (2008b) Does predator swamping promote synchronous emergence of turtle hatchlings among nests? Behavioral Ecology, 19, 35-40.
105. Uller T, Olsson M (2008) Multiple paternity in reptiles: patterns and processes. Molecular Ecology, 17, 2566-2580.
106. van de Merwe J, Ibrahim K, Whittier J (2005) Effects of hatchery shading and nest depth on the development and quality of Chelonia mydas hatchlings: implications for hatchery management in Peninsular, Malaysia. Australian Journal of Zoology, 53, 205-211.
107. Weishampel JF, Bagley DA, Ehrhart LM (2004) Earlier nesting by loggerhead sea turtles following sea surface warming. Global Change Biology, 10, 1424-1427.
108. Willis KJ, Bhagwat SA (2009) Biodiversity and climate change. Science, 326, 806-807.
109. Witt MJ, Akesson S, Broderick AC et al. (2010a) Assessing accuracy and utility of satellite-tracking data using Argos-linked Fastloc-GPS. Animal Behaviour, 80, 571-581.
110. Witt MJ, McGowan A, Blumenthal JM et al. (2010b) Inferring vertical and horizontal movements of juvenile marine turtles from time-depth recorders. Aquatic Biology, 8, 169-177.
111. Yntema CL, Mrosovsky N (1980) Sexual-differentiation in hatchling loggerheads (Caretta caretta) incubated at different controlled temperatures. Herpetologica, 36, 33-36.
112. Zbinden JA, Largiader AR, Leippert F, Margaritoulis D, Arlettaz R (2007) High frequency of multiple paternity in the largest rookery of Mediterranean loggerhead sea turtles. Molecular Ecology, 16, 3703-3711.
113. Zbinden JA, Margaritoulis D, Arlettaz R (2006) Metabolic heating in Mediterranean loggerhead sea turtle clutches. Journal of Experimental Marine Biology and Ecology, 334, 151-157.