Use of skeletochronological analysis to estimate the age of leatherback sea turtles Dermochelys coriacea in the western North Atlantic

Endangered Species Research

Volumn 8, Issue 3, 2009, Pages 165-177

  Avens, Larisa ^a   Taylor, J Christopher ^b   Goshe, Lisa R ^a   Jones, T Todd ^c   Hastings, Mervin ^c,d  

^a NOAA Fisheries   (United States)

^b NOAA EARTH SYSTEM RESEARCH LABORATORY   (United States)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^d NONE   (United Kingdom)

Author keywords

Dermochelys coriacea; LAG; Leatherback; Line of arrested growth; Sea turtle; Skeletal growth mark; Skeletochronology

Indexed keywords

ACCURACY ASSESSMENT; AGE; AGE AT MATURITY; CONSERVATION MANAGEMENT; CORRECTION; ENDANGERED SPECIES; ESTIMATION METHOD; GROWTH CURVE; GROWTH RATE; LIFE HISTORY; PARAMETERIZATION; POPULATION GROWTH; TURTLE;

ATLANTIC OCEAN; ATLANTIC OCEAN (NORTH);

CHELONIIDAE; DERMOCHELYIDAE; DERMOCHELYS CORIACEA; TESTUDINES;

EID: 70349251393     PISSN: 18635407     EISSN: 16134796     Source Type: Journal    
DOI: 10.3354/esr00202     Document Type: Article

References (101)

1. Ardizzone D, Cailliet GM, Natanson LJ, Andrews AH, Kerr LA, Brown TA (2006) Application of bomb radiocarbon chronologies to shortfin mako ( Isurus oxyrinchus) age validation. Environ Biol Fishes 77:355-366
2. Avens L, Goshe LR (2007) Comparative skeletochronological analysis of Kemp's ridley (Lepidochelys kempii) and logger-head (Caretta caretta) humeri and scleral ossicles. Mar Biol 152:1309-1317
3. Balazs GH, Chaloupka M (2004) Spatial and temporal variability in somatic growth of green sea turtles (Chelonia mydas) resident in the Hawaiian Archipelago. Mar Biol 145:1043-1059
4. Beamish RJ, Fournier DA (1981) A method for comparing the precision of a set of age determinations. Can J Fish Aquat Sci 38:982-983
5. Bels B, Rimbolt-Baly F, Lescure J (1988) Croissance et maintien en captivité, de la tortue luth Dermochelys coriacea (Vandelli, 1761). Rev Fr Aquariol 15:59-64
6. Birke E (1971) Nivenile leathery turtles. Dermochelys coriasea (Linnaeus), in captivity. Brunei Mus J 2:160-172
7. Bishop SDH, Francis MP, Duffy C, Montgomery JC (2006) Age, growth, maturity, longevity, and natural mortality of the shortfin mako shark (Isurus oxyrinchus) in New Zealand waters. Mar Freshw Res 57:143-154
8. Bjorndal KA, Bolten AB, Dellinger T, Delgado C, Martins HR (2003) Compensatory growth in oceanic loggerhead sea turtles: response to a stochastic environment. Ecology 84:1237-1249
9. Bowen BW, Karl SA (2007) Population genetics and phylogeography of sea turtles. Mol Ecol 16:4886-4907
10. Braun-McNeill J, Epperly SE, Avens L, Snover ML, Taylor JC (2008) Growth rates of loggerhead (Caretta caretta) sea turtles from the western North Atlantic. Herpetol Conserv Biol 3:273-281
11. Broderick AC, Glen F, Godley BJ, Hays GC (2003) Variation in reproductive output of marine turtles. J Exp Mar Biol Ecol 288:95-109
12. Cailliet GM, Smith WD, Mollet HF, Goldman KJ (2006) Age and growth studies of chondrichthyan fishes: the need for consistency in terminology, verification, validation, and growth function fitting. Environ Biol Fishes 77:211-228
13. Caldwell D (1962) Growth measurements in young captive Atlantic sea turtles in temperate waters. Los Angel City Mus Contrib Sri 50:1-8
14. Campana SE (1997) Use of radiocarbon from nuclear fallout as a dated marker in the otoliths of haddock Melanogrammus aeglefinus. Mar Ecol Prog Ser 150:49-56
15. Carr A (1967) So excellent a fishe: a natural history of sea turtles. The Natural History Press, New York
16. Casselman JM (1983) Age and growth assessment of fish from their calcified Aructures: techniques and tools. NOAA Tech Rep NMFS 8:1-17
17. Castanet J, Francillon-Viellot H, Meunier FJ, DeRicqles A (1993) Bone and individual aging. In: Hall BK (ed) Bone. Vol 7: bone growth-B. CRC Press, Boca Raton, FL, p 245-283
18. Chaloupka MY, Limpus CJ (1997) Robust statistical modeling of hawksbill sea turtle growth rates (southern Great Barrier Reef). Mar Ecol Prog Ser 146:1-8
19. Chaloupka MY, Musick JA (1997) Age, growth, and population dynamics, In: Lutz P, Musick J (eds) The biology of sea turtles. CRC Press, Boca Raton FL, p 233-276
20. Chan EH, Liew HC (1996) Decline of the leatherback population in Terengganu, Malaysia, 1956-1995. Chelonian Conserv Biol 2:196-203
21. Charnov EL, Turner TF, Winemiller KO (2001) Reproductive constraints and the evolution of life histories with indeterminate growth. Proc Natl Acad Sci USA 98:9460-9464
22. Chinsamy A, Hanrahan SA, Neto RM, Seely M (1995) Skeletochronological assessment of age in Angolosaurus skoogi, a cordylid lizard living in an aseasonal environment. J Herpetol 29:457-460
23. Coropeán-Jimenez G, Bard FX (11983) Growth increments on dorsal spines of eastern Atlantic bluefin tuna, Thunnus thynnus, and their possible relation to migration patterns. In: Prince ED, Pulos LM (eds) Proceedings of the international workshop on age determination of oceanic pelagic fishes: tunas, billfishies, and sharks. NOAA Tech Rep NMFS 8:77-86
24. Deraniyagala PEP (1952) A colored atlas of some vertebrates from Ceylon. Vol I (Fishes). The Ceylon Government Press, Colombo, p 3-21
25. Dunham AE, Miles DB (1485) Patterns of covariation in life history traits of squamate reptiles: the effects of size and playlogeny reconsidered. Am Nat 126:231-257
26. Dutton DL, Dutton PH, Chaloupka M, Boulon RH (2005) Increased of a Caribbean leatherback-turtle. Dermochelys coriacea nesting population linked to long-term nest protection. Biol Conserv 126:186-194
27. Eckert SA (2006) High-use oceanic areas for Atlantic leatherback sea turtles. Mar Biol 149:1257-1267
28. Eckert KL, Luginbuhl C (1988) Death of a giant. Mar Turtle Newsl 43:2-3
29. Frazer NB (1986) Survivorship, of adult female loggerhead sea turtles, Caretta caretta, nesting on Little Cumberland Island, Georgia, USA. Herpetologica 39:436-447
30. Frazer NB (1987) Preliminary estimates of survivorship for wild juvenile loggerhead sea turtles (Caretta caretta). J Herpetol 21:232-235
31. Frazer NB, Ehrhart LM (1985) Preliminary growth models for green, Chelonia mydas, and loggerhead, Caretta caretta, turtles in the wild: Copeia 1985:73-79
32. Frazer NB, Schwartz F (1984) Growth curves of captive loggerhead turtles, Caretta caretta,in North. Carolina, USA. Bull Mar Sci 34:485-489
33. Frazier J (1985) A review of in vivo labels for studies of age determination and growth in amphibians and reptiles. Herpetologica 41:222-227
34. Gadgil M, Bossert WH (1970) Life historical consequences of natural selection. Am Nat 104:1-24
35. Gyuris E (1994) The rate of predation by fishes on hatchlings of the green turtle (Chelonia mydas). Coral Reefs 13: 137-144
36. Hays GC, Houghton JDR, Myers AE (2004) Endangered species: pan-Atlantic leatherback turtle movements. Nature 429:522
37. Hays GC, Hobson VJ, Metcalfe JD, Righton D, Sims DW (2006) Flexible foraging movements of leatherback turtles across the north Atlantic Ocean. Ecology 87:2647-2656
38. Heppell SS, Snover ML, Crowder LB (2003a) Sea turtle population ecology. In: Lutz PL, Musick JA, Wyneken J (eds) The biology of sea turtles, Vol II. CRC Press, Boca Raton, FL, p 275-306
39. Heppell SS, Crowder LB, Crouse DT, Epperly SP, Fraser NB (2003b) Population models for Atlantic loggerheads: past, present, and future. In: Bolten AB, Witherington BE (eds) Loggerhead sea turtles. Smithsonian Books, Washington, DC, p 255-273
40. Hirth HF (1971) Synopsis of biological data on the green turtle, Chelonia mydas (Linnaeus) 1758. Food and Agriculture Organization of the United Nations, Rome
41. Hitipeuw C, Dutton PH, Benson S, Thebu J, Bakarbessy J (2007) Population status and internesting movement of leatherback turtles, Dermochelys coriacea, nesting on the northwest coast of Papua,'Indonesia. Chelonian Conserv Biol 6:28-36
42. Hohn AA (2002) Age estimation. In: Perrin WF, Wursig B, Thewissen HGM (eds) Encyclopedia of marine mammals. Academic Press, London, p 6-13
43. Houghton JDR, Doyle TK, Wilson MW, Davenport J, Hays GC (2006) Jellyfish aggregations and leatherback turtle foraging patterns in a temperate coastal environment. Ecology 87:1967-1972
44. Huppert DD, Mittleman TW (1993) Economic effects of the United Nations moratorium on high seas driftnet fishing. NOAA Tech Memo NMFS-SVIFSC-194
45. Hutton JM (1986) Age determination of living Nile crocodiles from the cortical stratification of bone. Copeia 1986: 332-341
46. IUCN (International Union for the Conservation of Nature and Natural Resources) (2008) IUCN Red List of Threatened Species. Available at: www.iucnredlist.org/
47. James JC, Davenport, J, Hays GC (2006) Expanded thermal niche for a diving-vertebrate: a leatherback turtle diving into near-freezing water. J Exp Biol Ecol 335:221-226
48. Jones TT (2009) Energetics of the leatherback turtle, Dermochelys coriacea. PhD dissertation, University of British Columbia, Vancouver, BC
49. Klevezal CA (1996) Recording structures of mammals: determination of age and reconstruction of life history. A. A. Balkema, Brookfield, VT
50. Klinger RC, Musick JA (1995) Age and growth of loggerhead turtles Caretta caretta from Chesapeake Bay. Copeia 1995:204-209
51. Kusrini MD, Alford RA (2006) The application of skeleto-chronology to estimate ages of three species of frogs in West Java, Indonesia. Herpetol Rev 37:423-425
52. Lagardère F, Chaumillon G, Amara R, Heineman G, Lago JM (1995) Examination of otolith morphology and microstructure using laser scanning microscopy, In: Secor DH, Dean JM, Camapana SE (eds) Recent developments in fish otolith research. University of South Carolina Press, Columbia, SC
53. Law R (1979) Optimal life histories under age-specific predation. Am Nat 114:399-417
54. Leslie AJ, Penick DN, Spotila JR, Paladino FV (1996) Leatherback turtle, Dermochelys coriacea, nesting and nest success at Tortuguero, Costa Rica, in 1990-1991. Chelonian Conserv Biol 2:159-168
55. Limpus C (1979) Notes on growth rates of wild turtles. Mar Turtle Newsl 10:3-5
56. Limpus C, Chaloupka M (1997) Nonparametric regression modeling of green sea turtle growth rates (southern Great Barrier Reef). Mar Ecol Prog Ser 149:23-34
57. Limpus CJ, Walter DG (1980) The growth of immature green turtles ( Chelonia mydas) under natural conditions. Herpetologica 36:162-165
58. Mendonça MT (1981) Comparative growth rates of wild immature Chelonia mydas and Caretta caretta in Florida. J Herpetol 15:447-451
59. Michod RE (1979) Evolution of life histories in response to age-specific mortality factors. Am Nat 113:531-550
60. Myrick MC, Holm AA, Sloan PA, Kimura M, Stanely DD (1983) Estimating age of spotted and spinner dolphins (Stenella attenuate and Stenella longirostris) from teeth. NOAA Tech Memo NMFS-SWFSC-30
61. NMFS SEFSC (National Marine Fisheries Service Southeast Fisheries Science Center) (2001) Stock assessments of loggerhead and leatherback sea turtles and an assessment of the impact of the pelagic longline fishery on the loggerhead and leatherback sea turtles of the Western North Atlantic. NOAA Tech Memo NMFS-SEFSC-455
62. Parham JF, Zug GR (1997) Age and growth of loggerhead sea turtles Caretta caretta of coastal Georgia: an assessment of skeletochronological age-estimates. Bull Mar Sci 61: 287-304
63. Price ER, Wallace BP, Reina RD, Spotila JR, Paladino FV, Piedra R, Vélez E (2006) Size, growth, and reproductive output of adult female leatherback turtles Dermochelys coriacea. Endang Species Res 1:41-48
64. Reznick D, Bryant MJ, Bashey F (2002) r- and K-selection revisited: the role of population regulation in life-history evolution. Ecology 83:1509-1520
65. Rhodin AGJ (1985) Comparative chondro-osseous development and growth of marine turtles. Copeia 1985:752-771
66. Saether BE, Ringsby TH, Roskaft E (1996) Life history variation, population processes and priorities in species conservation: towards a reunion of research paradigms. Oikos 77:217-226
67. Sarti Martínez L, Barragán AR, Muñoz DG, García N, Huerta P, Vargas F (2007) Conservation and biology of the leatherbcck turtle in the Mexican Pacific. Chelonian Conserv Biol 6:70-78
68. Schauble MK (1972) Seasonal variation of newt forelimb regeneration under controlled environmental conditions. J Exp Zool 181:281-286
69. Secor DH, Dean JM, Campana. SE (1995) Recent developments in fish otolith research. University of South Carolina Press, Columbia SC
70. Shine R, Charnov EL (1992) Patterns of surivival, growth, and maturation in snakes and lizards. Am Nat 139:1257-1269
71. Simmons DJ (1992) Circadian aspects of bone biology, In: Hall BK - (ed) Bone. Vol 6: bone growth-A. CRC Press, Boca Raton, FL, p 91-128
72. Sinsch U, Oromi N, Sanuy D (2007) Growth marks in the natterjack toad (Bufo calamita) bones: histological correlates of hibernation and aestivation periods. Herpetol J 17:129-137
73. Snover ML (ZO02) Growth and ontogeny of sea turtles using skeletochronology.: methods, validation, and application to conservation. PhD dissertation, Duke University, Durham, NC
74. Snover ML, Hohn AA (2004) Validation and interpretation of annual skeletal marks in loggerhead (Caretta caretta) and Kemp's ridley (Lepidochelys kempii) sea turtles. Fish Bull 102:682-692
75. Snover ML, Rhodin AGJ (2008) Comparative ontogenetic and phylogenetic aspects of chelonian chondro-osseous growth and skeletochronology. In: Wyneken J, Godfrey MH, Bels V (eds) Biology of turtles. CRC Press, Boca Raton, FL, p 17-43
76. Spotila JR, Reina RD, Steyermark AC, Plotkin PT, Paladino FV (1996) Worldwide population decline of Dermochelys coriacea: Are leatherback turtles going extinct? Chelonian Conserv Biol 2:209-222
77. Spotila JR, O'Connor MP, Paladino FV (1997) Thermal biology. In: Lutz P, Musick J (eds) The biology of sea turtles. CRC Press, Boca Raton, FL, p 297-314
78. Spotila JR, Reina RD, Steyermark AC, Plotkin PT, Paladino FV (2000) Pacific leatherback turtles face extinction. Nature 405:529-530
79. Starck JM, Chinsamy A (2002) Bone microstructure and developmental plasticity in birds and other dinosaurs. J Morphol 254:232-246
80. Stearns SC (1984) The effects of size and phylogeny on patterns of covariation in the life history traits of lizards and snakes. Am Nat 123:56-72
81. Stearns SC (1992) The evolution of life histories. Oxford University Press, Oxford
82. Stewart KR, Wyneken J (2004) Predation risk to loggerhead hatchlings at a high-density nesting beach in southeast Florida. Bull Mar Sci 74:325-335
83. Stewart K, Johnson C, Godfrey MH (2007) The minimum size of leatherbacks at reproductive maturity, with a review of sizes for nesting females from the Indian, Atlantic, and Pacific Ocean basins. Herpetol J 17:123-128
84. Summerfelt RC, Hall GE (1987) Age and growth of fish. Iowa State University Press, Ames, IA
85. Takada T, Caswell H (1997) Optimal size at maturity in size-structured populations. J Theor Biol 187:81-93
86. TEWG (Turtle Expert Working Group) (2007) An assessment of the leatherback turtle population in the Atlantic Ocean. NOAA. Tech Memo NMFS-SEFSC-555'
87. Troëng S, Harrison E, Evans D, de Haro A, Vargas E (2007) Leatherback turtle nesting trends and threats at Tortuguero, Costa Rica. Chelonian Conserv Biol 6:117-122
88. Turvey ST, Green OR, Holdaway RN (2005) Cortical growth marks reveal extended juvenile development in New Zealand moa. Nature 435:940-943
89. Uchida I (1967). On the growth of the loggerhead turtle, Caretta caretta, under rearing conditions. Bull Jpn Soc Sci Fish 33:497-506
90. van Buskirk J, Crowder LB (1994) Life-history variation in marine turtles. Copeia 1994:66-81
91. von Bertalanffy L (1938) A quantitative theory of organic growth (inquiries on growth laws. II). Hum Biol 10:181-213
92. Wallace BP, Jones TT (2008) What makes marine turtles go: a review of metabolic rates and their consequences. J Exp Mar Biol Ecol 356:8-24
93. Wood SN (2001) mgcv: GAMs and Generalized Ridge Regression for R. R News 1:20-25
94. Zar JH (1996) Biostatistical analysis, 3rd edn. Prentice Hall, Upper Saddle River, NJ
95. Zug GR, Glor RE (1998) Estimates of age and growth in a population of green sea turtles Chelonia mydas from the Indian River lagoon system, Florida: a skeletochronological analysis. Can J Zool 76:1497-1506
96. Zug GR, Parham J (1996) Age and growth in leatherback turtles, Dermochelys coriacea (Testudines: Dermochelyidae): a skeletochronological analysis. Chelonian Conserv Biol 2:244-249
97. Zug GR, Rand AS (1987) Estimation of age in nesting female Iguana iguana: testing skeletochronology in a tropical lizard. Amphib-Reptilia 8:237-250
98. Zug GR, Wynn AH, Ruckdeschel C (1986) Age determination of loggerhead sea turtles, Caretta caretta, by incremental growth marks in the skeleton. Smithson Contrib Zool 427: 1-34
99. Zug GR, Balazs GH, Wetherall JA (1995) Growth in juvenile loggerhead seaturtles Caretta caretta in the north Pacific pelagic habitat. Copeia 1995:484-487
100. Zug GR, Balazs GH, Wetherall JA, Parker DM, Murakawa SKK (2002) Age aild growth of Hawaiian green seaturtles Chelonia mydas: an analysis based on skeletochronology. Fish Bull 100:117-127
101. Zug GR, Chaloupka M, Balazs GH (1006) Age and growth in olive ridley sea turtles Lepidochelys olivacea from the North-central Pacific: a skeletochronological analysis. PSZN I Mar Ecol 27:263-270