What makes marine turtles go: A review of metabolic rates and their consequences

Journal of Experimental Marine Biology and Ecology

Volumn 356, Issue 1-2, 2008, Pages 8-24

  Wallace, Bryan P ^a   Jones, T Todd ^b  

^a DUKE UNIVERSITY MARINE LABORATORY   (United States)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Diving physiology; Doubly labeled water; Energetics; Leatherbacks; Marine turtles; Metabolic rate; Respirometry; Thermoregulation

Indexed keywords

BIOENERGETICS; BODY MASS; DIVING BEHAVIOR; LIFE HISTORY; LITERATURE REVIEW; METABOLISM; PHYSIOLOGY; THERMOREGULATION; TURTLE;

ANIMALIA; CHELONIA MYDAS; CHELONIIDAE; DERMOCHELYIDAE; DERMOCHELYS CORIACEA; MAMMALIA; REPTILIA; TESTUDINES; VERTEBRATA;

EID: 39549083024     PISSN: 00220981     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jembe.2007.12.023     Document Type: Article

References (109)

1. Bennett A.F. Activity metabolism of the lower vertebrates. Annu. Rev. Physiol. 400 (1978) 447-469
2. Bennett A.F. The energetics of reptilian activity. In: Gans C., and Pough F.H. (Eds). Biology of the Reptilia vol. 13 (1982), Academic Press, New York 155-199
3. Berkson H. Physiological adjustements to prolonged diving in the Pacific green turtle (Chelonia mydas agassizii). Comp. Biochem. Physiol. 18 (1966) 101-119
4. Bjorndal K.A. The consequences of herbivory for the life history pattern of the Caribbean green turtle, Chelonia mydas. In: Bjorndal K.A. (Ed). Biology and Conservation of Sea Turtles (1982), Smithsonian Institution Press, Washington, D.C. 111-116
5. Bleakney J.S. Reports of sea turtles from New England and eastern Canada. Can. Field-Nat. 79 (1965) 120-128
6. Block B.A., Finnerty J.R., Stewart A.F.R., and Kidd J. Evolution of endothermy in fish: mapping physiological traits on a molecular phylogeny. Science 260 (1993) 210-213
7. Bostrom B.L., and Jones D.R. Exercise warms adult leatherback turtles. Comp. Physiol. Biochem., Part A 147 (2007) 323-331
8. Bradshaw C.J.A., McMahon C.R., and Hays G.C. Behavioral inference of diving metabolic rate in free-ranging leatherback turtles. Physiol. Biochem. Zool. 80 (2007) 209-219
9. Brown J.H., Gillooly J.F., Allen A.P., Savage V.M., and West G.B. Toward a metabolic theory of ecology. Ecology 85 (2004) 1771-1789
10. Butler P.J. Metabolic regulation in diving birds and mammals. Resp. Physiol. Neurobiol., 141 (2004) 297-315
11. Butler P.J., Milsom W.K., and Woakes A.J. Respiratory, cardiovascular and metabolic adjustments during steady state swimming in the green turtle, Chelonia mydas. J. Comp. Physiol., B 154 (1984) 167-174
12. Butler P.J., Green J.A., Boyd I.L., and Speakman J.R. Measuring metabolic rate in the field: the pros and cons of the doubly labelled water and heart rate methods. Funct. Ecol. 18 (2004) 168-183
13. Castellini M.A., Kooyman G.L., and Ponganis P.J. Metabolic rates of freely diving Weddell seals: correlations with oxygen stores, swim velocity and diving duration. J. Exp. Biol. 165 (1992) 181-194
14. Clusella Trullas S., Spotila J.R., and Paladino F.V. Energetics during hatchling dispersal of the olive ridley turtle Lepidochelys olivacea using doubly labeled water. Physiol. Biochem. Zool. 79 (2006) 389-399
15. Colbert E.H., Cowles R.B., and Bogert C.M. Temperature tolerances in the American alligator and their bearing on the habits, evolution, and extinction of the dinosaurs. Bull. Am. Mus. Nat. Hist. 86 (1946) 327-374
16. Congdon J.D. Proximate and evolutionary constraints on energy relations of reptiles. Physiol. Zool. 62 (1989) 356-373
17. Congdon J.D., Dunham A.E., and Tinkle D.W. Energy budgets and life histories of reptiles. In: Gans C., and Pough F.H. (Eds). Biology of the Reptilia vol. 13 (1982), Academic Press, New York 233-271
18. Costa D.P. Methods for studying the energetics of freely diving animals. Can. J. Zool. 66 (1988) 45-52
19. Costa D.P., Gales N.J., and Goebel M.E. Aerobic dive limit: how often does it occur in nature?. Comp. Biochem. Physiol., Part A 129 (2001) 771-783
20. Davenport J. Temperature and the life-history strategies of sea turtles. J. Therm. Biol. 22 (1997) 479-488
21. 2 consumption in hatchling green turtles (Chelonia mydas). Br. J. Herpetol. 4 (1984) 60-63
22. Davenport J., and Scott C.R. Individuality of growth, appetite, metabolic rate, and assimilation of nutrients in young green turtles (Chelonia mydas L.). Herpetol. J. 3 (1993) 26-31
23. Davenport J., Ingle G., and Hughes A.K. Oxygen uptake and heart rate in young green turtles (Chelonia mydas). J. Zool. London 198 (1982) 399-412
24. Davenport J., Holland D.L., and East J. Thermal and biochemical characteristics of the lipids of the leatherback turtle Dermochelys coriacea: evidence of endothermy. J. Mar. Biol. Assoc. U.K. 70 (1990) 33-41
25. Doyle T.K., Houghton J.D.R., McDevitt R., Davenport J., and Hays G.C. The energy density of jellyfish: estimates from bomb-calorimetry and proximate-composition. J. Exp. Mar. Biol. Ecol. 343 (2007) 239-252
26. Dunham A.E., Grant B.W., and Overall K.L. Interfaces between biophysical and physiological ecology and the population ecology of terrestrial verterbrate ectotherms. Physiol. Zool. 62 (1989) 335-355
27. Eckert S.A. Swim speed and movement patterns of gravid leatherback sea turtles (Dermochelys coriacea) at St. Croix, US Virgin Islands. J. Exp. Biol. 205 (2002) 3689-3697
28. Eckert S.A. Distribution of juvenile leatherback sea turtle Dermochelys coriacea sightings. Mar. Ecol. Prog. Ser. 230 (2002) 289-293
29. 2 measuring systems. J. Appl. Physiol. 51 (1981) 772-776
30. Frair W., Ackman R.G., and Mrosovsky N. Body temperature of Dermochelys coriacea: warm turtle from cold water. Science 177 (1972) 791-793
31. Frappell P. Respirometry, the gold standard. The Physiologist 49 (2006) 12
32. Goff G.P., and Lien J. Atlantic leatherback turtles, Dermochelys coriacea, in cold water off Newfoundland and Labrador. Can. Field-Nat. 102 (1988) 1-5
33. Goff G.P., and Stenson G.B. Brown adipose tissue in leatherback sea turtles: a thermogenic organ in an endothermic reptile. Copeia 1988 (1988) 1071-1075
34. Greer A.E., Lazelle J.D., and Wright R.M. Anatomical evidence for a countercurrent heat exchanger in the leatherback turtle (Dermochelys coriacea). Nature 244 (1973) 181
35. Grigg G.C., Drane C.R., and Courtice G.P. Time constants of heating and cooling in the eastern water dragon, Physignathus lesueruii, and some generalizations about heating and cooling in reptiles. J. Therm. Biol. 4 (1979) 95-103
36. Hawkes L.A., Broderick A.C., Coyne M.S., Godfrey M.H., and Godley B.J. Only some like it hot - quantifying the thermal niche of the loggerhead sea turtle. Divers. Distrib 13 (2007) 447-457
37. Hays G.C. The implications of variable remigration intervals for the assessment of population size in sea turtles. J. Theor. Biol. 206 (2000) 221-227
38. Hays G.C., Broderick A.C., Glen F., and Godley B.J. Change in body mass associated with long-term fasting in a marine reptile: the case of green turtles (Chelonia mydas) at Ascension Island. Can. J. Zool. 80 (1992) 1299-1302
39. Hays G.C., Houghton J.D.R., Isaacs C., King R.S., Lloyd C., and Lovell P. First oceanic dive profiles for leatherback turtles, Dermochelys coriacea, indicate behavioural plasticity associated with long-distance migration. Anim. Behav. 67 (2004) 733-743
40. Hays G.C., Houghton J.D.R., and Myers A.E. Pan-Atlantic leatherback turtle movements. Nature 429 (2004) 522
41. Hewavisenthi S., and Parmenter C.J. Egg components and utilization of yolk lipids during development of the flatback turtle Natator depressus. J. Herpetol. 36 (2002) 43-50
42. Hochscheid S., Bentivegna F., and Speakman J.R. Regional blood flow in sea turtles: implications for heat exchange in an aquatic ectotherm. Physiol. Biochem. Zool. 75 (2002) 66-76
43. 10 effects on oxygen consumption of loggerhead sea turtles Caretta caretta. Physiol. Biochem. Zool. 77 (2004) 209-222
44. Hochscheid S., McMahon C.R., Bradshaw C.J.A., Maffucci F., Bentivegna F., and Hays G.C. Allometric scaling of lung volume and its consequences for marine turtle diving performance. Comp. Biochem. Physiol., A 148 (2007) 360-367
45. Hochscheid S., Bentivegna F., Bradai M.N., and Hays G.C. Overwintering behaviour in sea turtles: dormancy is optional. Mar. Ecol. Prog. Ser. 340 (2007) 287-298
46. Jackson D.C., and Prange H.D. Ventilation and gas exchange during rest and exercise in adult green sea turtles. J. Comp. Physiol. 134 (1979) 315-319
47. James M.C., and Mrosovsky N. Body temperatures of leatherback turtles (Dermochelys coriacea) in temperate waters off Nova Scotia, Canada. Can. J. Zool. 82 (2004) 102-106
48. James M.C., Myers R.A., and Ottensmeyer C.A. Behaviour of leatherback sea turtles, Dermochelys coriacea, during the migratory cycle. Proc. Royal Acad. Sci. Lond. 272 (2005) 1547-1555
49. James M.C., Davenport J., and Hays G.C. Expanded thermal niche for a diving vertebrate: a leatherback turtle diving into near-freezing water. J. Exp. Mar. Biol. Ecol. 335 (2006) 221-226
50. Jones D.R., Southwood A.L., and Andrews R.D. Energetics of leatherback sea turtles: a step toward conservation. In: Gordon M.S., and Bartol S.M. (Eds). Experimental Approaches to Conservation Biology (2004), University of California Press, Berkeley, CA 66-82
51. Jones T.T., Seminoff J.A., Hidalgo A., and Lutz P.L. Energetics of the east Pacific green turtle at a Gulf of California for aging habit. NOAA Tech. Memo. NMFS-SEFSC 528 (2005) 198-199
52. Jones T.T., Hastings M., Bostrom B., Andrews R., and Jones D.R. Validation of the use of doubly labeled water in the green turtle (Chelonia mydas): a note of caution. The Physiologist 49 (2006) 31
53. Jones T.T., Reina R.D., Darveau C.-A., and Lutz P.L. Ontogeny of energetics in leatherback (Dermochelys coriacea) and olive ridley (Lepidochelys olivacea) sea turtle hatchlings. Comp. Biochem. Physiol., Part A 147 (2007) 313-322
54. Kaufmann R., Forstner H., and Wieser W. Respirometry - methods and approaches. In: Bridges C.R., and Butler P.J. (Eds). Techniques in Comparative Respiratory Physiology (1989), Cambridge University Press, Cambridge 51-76
55. Kleiber M. The Fire of Life: an Introduction to Animal Energetics (1961), John Wiley and Sons, Inc., New York
56. Kooyman G.L. Diverse divers: physiology and behavior. In: Johansen K., and Farner D.S. (Eds). Zoophysiology Series vol. 23 (1999), Springer-Verlag, New York 216
57. Kooyman G.L., Wahrenbrock E.A., Castellini M.A., Davis R.W., and Sinnett E.E. Aerobic and anaerobic metabolism during voluntary diving in Weddell seals: evidence of preferred pathways from blood chemistry and behavior. J. Comp. Physiol., B 138 (1980) 335-346
58. Kraemer J.E., and Bennett S.H. Utilization of post-hatching yolk in loggerhead sea turtles, Caretta caretta. Copeia 1981 (1981) 406-411
59. 18. J. Appl. Physiol. 7 (1955) 704-710
60. Limpus C.J., and Nicholls N. The southern oscillation regulates the annual numbers of green turtles (Chelonia mydas) breeding around northern Australia. Aust. J. Wildl. Res. 15 (1988) 157-161
61. Lutcavage M.E., and Lutz P.L. Metabolic rate and food energy requirements of the leatherback sea turtle, Dermochelys coriacea. Copeia 1986 (1986) 796-798
62. Lutcavage M.E., and Lutz P.L. Voluntary diving metabolism and ventilation in the loggerhead sea turtle. J. Exp. Mar. Biol. Ecol. 147 (1991) 287-296
63. Lutcavage M.E., and Lutz P.L. Diving physiology. In: Lutz P.L., and Musick J.A. (Eds). The Biology of Sea Turtles vol. 1 (1997), CRC Press, Boca Raton, FL 276-296
64. Lutcavage M.E., Lutz P.L., and Baier H. Gas exchange in the loggerhead sea turtle Caretta caretta. J. Exp. Biol. 131 (1987) 365-372
65. Lutcavage M.E., Bushnell P.G., and Jones D.R. Oxygen transport in the leatherback sea turtle Dermochelys coriacea. Physiol. Zool. 63 (1990) 1012-1024
66. Lutcavage M.E., Bushnell P.G., and Jones D.R. Oxygen stores and aerobic metabolism in the leatherback sea turtle. Can. J. Zool. 70 (1992) 348-351
67. Lutz P.L., and Bentley T.B. Respiratory physiology of diving in the sea turtle. Copeia 1985 (1985) 671-679
68. Lutz P.L., Bergey A., and Bergey M. Effects of temperature on gas exchange and acid-base balance in the sea turtle Caretta caretta at rest and during routine activity. J. Exp. Biol. 144 (1989) 155-169
69. McDonald H.S. Methods for the physiological study of reptiles. In: Gans C., and Dawson W.R. (Eds). The Biology of the Reptilia vol. 5 (1976), Academic Press, London 70-83
70. Myers A.E., and Hays G.C. A novel technique for measuring heart rate in a free swimming marine vertebrate. J. Exp. Mar. Biol. Ecol. 349 (2007) 45-51
71. Musick J.A., and Limpus C.J. Habitat utilization and migration in juvenile sea turtles. In: Lutz P.L., and Musick J.A. (Eds). The Biology of Sea Turtles vol. 1 (1997), CRC Press, Boca Raton, FL 137-164
72. Mrosovsky N., and Pritchard P.C.H. Body temperatures of Dermochelys coriacea and other sea turtles. Copeia 1971 (1971) 624-631
73. O'Connor M.P. Physiological and ecological implications of a simple model of heating and cooling in reptiles. J. Therm. Biol. 24 (1999) 113-136
74. Paladino F.V., O'Connor M.P., and Spotila J.R. Metabolism of leatherback turtles, gigantothermy, and thermoregulation of dinosaurs. Nature 344 (1990) 858-860
75. Paladino F.V., Spotila J.R., O'Connor M.P., and Gatten Jr. R.E. Respiratory physiology of adult leatherback turtles (Dermochelys coriacea) while nesting on land. Chelonian Conserv. Biol. 2 (1996) 223-229
76. Penick D.N., Paladino F.V., Steyermark A.C., and Spotila J.R. Thermal dependence of tissue metabolism in the green turtle, Chelonia mydas. Comp. Biochem. Physiol., Part A 113 (1996) 293-296
77. Penick D.N., Spotila J.R., O'Connor M.P., Steyermark A.C., George R.H., Salice C.J., and Paladino F.V. Thermal independence of tissue metabolism in the leatherback turtle, Dermochelys coriacea. Comp. Biochem. Physiol., Part A 120 (1998) 399-403
78. Prange H.D. Energetics of swimming of a sea turtle. J. Exp. Biol. 64 (1976) 1-12
79. Prange H.D., and Ackerman R.A. Oxygen consumption and mechanisms of gas exchange of green turtle (Chelonia mydas) eggs and hatchlings. Copeia 1974 (1974) 758-763
80. Prange H.D., and Jackson D.C. Ventilation, gas exchange and metabolic scaling of a sea turtle. Res. Physiol. 27 (1976) 369-377
81. Saba V.S., Santidrián Tomillo P., Reina R.D., Spotila J.R., Musick J.A., Evans D.A., and Paladino F.V. The effect of the El Niño Southern Oscillation on the reproductive frequency of eastern Pacific leatherback turtles. J. Appl. Ecol. 44 (2007) 395-404
82. Sato K., Sakamoto W., Matsuzawa Y., Tanaka H., Minamikawa S., and Naito Y. Body temperature independence of solar radiation in free-ranging loggerhead turtles, Caretta caretta, during internesting periods. Mar. Biol. 123 (1995) 197-205
83. Schmidt-Nielsen K. Scaling: Why is Animal Size so Important? (1984), Cambridge Univ. Press, Cambridge
84. Schmidt-Nielsen K. Animal Physiology: Adaptation and Environment. 5th edn. (1997), Cambridge University Press, Cambridge, UK
85. Seebacher F., Grigg G.C., and Beard L.A. Crocodiles as dinosaurs: behavioural thermoregulation in very large ectotherms leads to high and stable body temperatures. J. Exp. Biol. 202 (1999) 77-86
86. Silas E.G., Vijayakumaran M., and Rajagopalan M. Yolk utilization in the egg of the olive ridley Lepidochelys olivacea. CMFRI Bull. 35 (1984) 22-35
87. Smith E.N., Long N.C., and Wood J. Thermoregulation and evaporative water loss of green sea turtles, Chelonia mydas. J. Herpetol. 20 (1986) 325-332
88. Solow A.R., Bjorndal K.A., and Bolten A.B. Annual variation in nesting numbers of sea turtles: the effect of sea surface temperature on re-migration intervals. Ecol. Lett. 5 (2002) 742-746
89. Southwood A.L., Andrews R.D., Lutcavage M.E., Paladino F.V., West N.H., George R.H., and Jones D.R. Heart rates and diving behavior of leatherback sea turtles in the Eastern Pacific Ocean. J. Exp. Biol. 202 (1999) 1115-1125
90. Southwood A.L., Darveau C.A., and Jones D.R. Metabolic and cardiovascular adjustments of juvenile green turtles to seasonal changes in temperature and photoperiod. J. Exp. Biol. 206 (2003) 4521-4531
91. Southwood A.L., Andrews R.D., Paladino F.V., and Jones D.R. Effects of swimming and diving behavior on body temperatures of Pacific leatherbacks in tropical seas. Physiol. Biochem. Zool. 78 (2005) 285-297
92. Southwood A.L., Reina R.D., Jones V.S., Speakman J.R., and Jones D.R. Seasonal metabolism of juvenile green turtles (Chelonia mydas) at Heron Island, Australia. Can. J. Zool. 84 (2006) 125-135
93. Speakman J.R. Doubly Labelled Water: Theory and Practice (1997), Chapman & Hall, London
94. Spotila J.R., and Standora E.A. Energy budgets of ectothermic vertebrates. Am. Zool. 25 (1985) 973-986
95. Spotila J.R., and Standora E.A. Environmental constraints on the thermal energetics of sea turtles. Copeia 1985 (1985) 694-702
96. Spotila J.R., Lommen P.W., Bakken G.S., and Gates D.M. A mathematical model for body temperatures of large reptiles: implications for dinosaur ecology. Am. Nat. 107 (1973) 391-404
97. Spotila J.R., O'Connor M.P., Dodson P., and Paladino F.V. Hot and cold running dinosaurs: body size, metabolism and migration. Mod. Geol. 16 (1991) 203-227
98. Spotila J.R., O'Connor M.P., and Paladino F.V. Thermal biology. In: Lutz P.L., and Musick J.A. (Eds). The Biology of Sea Turtles (1997), CRC Press, Boca Raton, FL 297-314
99. Standora E.A., Spotila J.R., and Foley R.E. Regional endothermy in the sea turtle, Chelonia mydas. J. Therm. Biol. 7 (1982) 159-165
100. Standora E.A., Spotila J.R., Keinath J.A., and Shoop C.R. Body temperatures, diving cycles, and movement of a subadult leatherback turtle, Dermochelys coriacea. Herpetologica 40 (1984) 169-176
101. Thompson D., and Fedak M.A. How long should a dive last? A simple model of foraging decisions by breath-hold divers in a patchy environment. Anim. Behav. 61 (2001) 287-296
102. Wallace B.P., Williams C.L., Paladino F.V., Morreale S.J., Lindstrom R.T., and Spotila J.R. Bioenergetics and diving activity of internesting leatherback turtles Dermochelys coriacea at Parque Nacional Marino Las Baulas, Costa Rica. J. Exp. Biol. 208 (2005) 3873-3884
103. Wallace B.P., Kilham S.S., Paladino F.V., and Spotila J.R. Energy budget calculations indicate resource limitation in Eastern Pacific leatherback turtles. Mar. Ecol. Prog. Ser. 318 (2006) 263-270
104. Watson K.P., and Granger R.A. Hydrodynamic effect of a satellite transmitter on a juvenile green turtle (Chelonia mydas). J. Exp. Biol. 201 (1998) 2497-2505
105. Willmer P., Stone G., and Johnston I. Environmental Physiology of Animals (2000), Blackwell Science, Ltd., MA, USA 141
106. Wilson R.P., White C.R., Quintant F., Halsey L.G., Liebsch N., Martin G.R., and Butler P.J. Moving towards acceleration for estimates of activity-specific metabolic rate in free-living animals: the case of the cormorant. J. Anim. Ecol. 75 (2006) 1081-1090
107. CO2, and evaporative water loss with a flow-through mask. J. Appl. Physiol.: Respir. Environ. Exercise Physiol. 42 (1977) 120-123
108. Wyneken J. Sea turtle locomotion: mechanisms, behavior, and energetics. In: Lutz P.L., and Musick J.A. (Eds). The Biology of Sea Turtles vol. 1 (1997), CRC Press, Boca Raton, FL 165-198
109. Wyneken J., and Salmon M. Frenzy and postfrenzy swimming activity in loggerhead, green, and leatherback hatchling sea turtles. Copeia 1992 (1992) 478-484