, Volume 149, Issue 1, pp 52–64 | Cite as

Individual variation in feeding habitat use by adult female green sea turtles (Chelonia mydas): are they obligately neritic herbivores?

  • Hideo HataseEmail author
  • Katsufumi Sato
  • Manami Yamaguchi
  • Kotaro Takahashi
  • Katsumi Tsukamoto
Population Ecology


Satellite telemetry and stable isotope analysis were used to confirm that oceanic areas (where water depths are >200 m) are alternative feeding habitats for adult female green sea turtles (Chelonia mydas), which have been thought to be obligate herbivores in neritic areas (where depths are <200 m). Four females were tagged with satellite transmitters and tracked during post-nesting periods from Ogasawara Islands, Japan. Three females migrated to neritic habitats, while transmissions from another female ceased in an oceanic habitat. The overall mean nighttime dive depths during oceanic swimming periods in two females were <20 m, implying that the main function of their nighttime dives were resting with neutral buoyancy, whereas the means in two other females were >20 m, implying that they not only rested, but also foraged on macroplankton that exhibit diel vertical migration. Comparisons of stable carbon and nitrogen isotope ratios between 89 females and the prey items in a three-source mixing model estimated that 69% of the females nesting on Ogasawara Islands mainly used neritic habitats and 31% mainly used oceanic habitats. Out of four females tracked by satellite, two females were inferred from isotope ratios to be neritic herbivores and the two others oceanic planktivores. Although post-nesting movements for four females were not completely consistent with the inferences from isotope ratios, possibly due to short tracking periods (28–42 days), their diving behaviors were consistent with the inferences. There were no relationships between body size and the two isotope ratios, indicating a lack of size-related differences in feeding habitat use by adult female green turtles, which was in contrast with loggerhead sea turtles (Caretta caretta). These results and previous findings suggest that ontogenetic habitat shifts by sea turtles are facultative, and consequently, their life histories are polymorphic.


Life history Ontogenetic habitat shifts Reptile Satellite telemetry Stable isotope analysis 



We thank H. Suganuma and K. Narushima of Everlasting Nature of Asia (ELNA), the staff (Y. Iwata, Y. Horita, and M. Ogasawara) and volunteers of the Ogasawara Marine Center, M. Kaneko and the staff of the Club Noah Hahajima, and the fishermen of Chichijima and Hahajima Islands, for field assistance and logistical support. We also thank the Sea Turtle Association of Japan for supplying tags and equipment, and Y. Matsuzawa for discussion. T. Miyajima and Y. Umezawa of the Biogeochemistry Laboratory, Ocean Research Institute, University of Tokyo, assisted with the stable isotope analysis and allowed us to use their mass spectrometer. G.C. Hays provided useful advice on attachment of the transmitter and data analysis. M.J. Miller helped to improve the manuscript. Figure 1 was created by the Maptool at Two anonymous referees provided constructive comments on the manuscript. This work was partly supported by a Grant-in-Aid from the Japanese Society for the Promotion of Science (No. 15255003) to K.S. and a Grant-in-Aid for Creative Scientific Research (No. 12NP0201) from the Ministry of Education, Culture, Sports, Science and Technology of Japan to K.T. The experiments were conducted under licenses issued by the Ministry of the Environment and complied with the current Japanese laws.

Supplementary material

442_2006_431_MOESM1_ESM.pdf (126 kb)
Supplementary material


  1. Baba N, Kiyota M, Suganuma H, Tachikawa H (1992) Research on migratory routes of loggerhead turtles and green turtles by the Argos system. Report on commissioned project for fishing boat scientist data analysis in 1991. Fisheries Agency of Japan, Tokyo, pp 100–106 (in Japanese)Google Scholar
  2. Baba N, Kiyota M, Suganuma H, Tachikawa H (1993) Research on migratory routes of loggerhead turtles and green turtles by the Argos system. Report on commissioned project for fishing boat scientist data analysis in 1992. Fisheries Agency of Japan, Tokyo, pp 86–99 (in Japanese)Google Scholar
  3. Bjorndal KA (1997) Foraging ecology and nutrition of sea turtles. In: Lutz PL, Musick JA (eds) The biology of sea turtles. CRC, Boca Raton, pp 199–231Google Scholar
  4. Bjorndal KA, Bolten AB, Dellinger T, Delgado C, Martins H (2003) Compensatory growth in oceanic loggerhead sea turtles: responses to a stochastic environment. Ecology 84:1237–1249CrossRefGoogle Scholar
  5. Bolten AB (2003) Variation in sea turtle life history patterns: neritic vs. oceanic developmental stages. In: Lutz PL, Musick JA, Wyneken J (eds) The biology of sea turtles, Vol II. CRC, Boca Raton, pp 243–257Google Scholar
  6. Brockmann HJ (2001) The evolution of alternative strategies and tactics. Adv Stud Behav 30:1–51Google Scholar
  7. Brodeur RD, Sugisaki H, Hunt GL Jr (2002) Increases in jellyfish biomass in the Bering Sea: implications for the ecosystem. Mar Ecol Prog Ser 233:89–103CrossRefGoogle Scholar
  8. Burton RK, Koch PL (1999) Isotopic tracking of foraging and long-distance migration in northeastern Pacific pinnipeds. Oecologia 119:578–585CrossRefGoogle Scholar
  9. Cheng I-J (2000) Post-nesting migrations of green turtles (Chelonia mydas) at Wan-An Island, Penghu Archipealgo, Taiwan. Mar Biol 137:747–754CrossRefGoogle Scholar
  10. Dahlgren CP, Eggleston DB (2000) Ecological processes underlying ontogenetic habitat shifts in a coral reef fish. Ecology 81:2227–2240CrossRefGoogle Scholar
  11. DeNiro MJ, Epstein S (1978) Influence of diet on the distribution of carbon isotopes in animals. Geochim Cosmochim Acta 42:495–509CrossRefGoogle Scholar
  12. Doucett RR, Booth RK, Power G, McKinley RS (1999) Effects of the spawning migration on the nutritional status of anadromous Atlantic salmon (Salmo salar): insights from stable-isotope analysis. Can J Fish Aquat Sci 56:2172–2180CrossRefGoogle Scholar
  13. Grafen A (1988) On the uses of data on lifetime reproductive success. In: Clutton-Brock TH (eds) Reproductive success. Studies of individual variation in contrasting breeding systems. University of Chicago Press, Chicago, pp 454–471Google Scholar
  14. Godley BJ, Thompson DR, Waldron S, Furness RW (1998) The trophic status of marine turtles as determined by stable isotope analysis. Mar Ecol Prog Ser 166:277–284CrossRefGoogle Scholar
  15. Godley BJ, Richardson S, Broderick AC, Coyne MS, Glen F, Hays GC (2002) Long-term satellite telemetry of the movements and habitat utilisation by green turtles in the Mediterranean. Ecography 25:352–362CrossRefGoogle Scholar
  16. Gross MR (1996) Alternative reproductive strategies and tactics: diversity within sexes. Trends Ecol Evol 11:2–98CrossRefGoogle Scholar
  17. Harrison RG (1980) Dispersal polymorphisms in insects. Annu Rev Ecol Syst 11:95–118CrossRefGoogle Scholar
  18. Hatase H, Takai N, Matsuzawa Y, Sakamoto W, Omuta K, Goto K, Arai N, Fujiwara T (2002) Size-related differences in feeding habitat use of adult female loggerhead turtles Caretta caretta around Japan determined by stable isotope analyses and satellite telemetry. Mar Ecol Prog Ser 233:273–281CrossRefGoogle Scholar
  19. Hatase H, Matsuzawa Y, Sato K, Bando T, Goto K (2004) Remigration and growth of loggerhead turtles (Caretta caretta) nesting on Senri Beach in Minabe, Japan: life-history polymorphism in a sea turtle population. Mar Biol 144:807–811CrossRefGoogle Scholar
  20. Hays GC, Adams CR, Broderick AC, Godley BJ, Lucas DJ, Metcalfe JD, Prior AA (2000) The diving behaviour of green turtles at Ascension Island. Anim Behav 59:577–586PubMedCrossRefGoogle Scholar
  21. Hays GC, Åkesson S, Broderick AC, Glen F, Godley BJ, Luschi P, Martin C, Metcalfe JD, Papi F (2001) The diving behaviour of green turtles undertaking oceanic migration to and from Ascension island: dive durations, dive profiles and depth distribution. J Exp Biol 204:4093–4098PubMedGoogle Scholar
  22. Hays GC, Broderick AC, Glen F, Godley BJ, Houghton JDR, Metcalfe JD (2002) Water temperature and internesting intervals for loggerhead (Caretta caretta) and green (Chelonia mydas) sea turtles. J Therm Biol 27:429–432CrossRefGoogle Scholar
  23. Hays GC, Houghton JDR, Isaacs C, King RS, Lloyd C, Lovell P (2004a) First records of oceanic dive profiles for leatherback turtles, Dermochelys coriacea, indicate behavioural plasticity associated with long-distance migration. Anim Behav 67:733–743CrossRefGoogle Scholar
  24. Hays GC, Metcalfe JD, Walne AW (2004b) The implications of lung-regulated buoyancy control for dive depth and duration. Ecology 85:1137–1145CrossRefGoogle Scholar
  25. Hays GC, Metcalfe JD, Walne AW, Wilson RP (2004c) First records of flipper beat frequency during sea turtle diving. J Exp Mar Biol Ecol 303:243–260CrossRefGoogle Scholar
  26. Hirayama R (1998) Oldest known sea turtle. Nature 392:705–708CrossRefGoogle Scholar
  27. Hirth HF (1997) Synopsis of the biological data on the green turtle Chelonia mydas (Linnaeus 1758). US Fish and Wildlife Service Biological Report 97:1–120Google Scholar
  28. Hobson KA (1995) Reconstructing avian diets using stable-carbon and nitrogen isotope analysis of egg components: patterns of isotopic fractionation and turnover. Condor 97:752–762CrossRefGoogle Scholar
  29. Hobson KA, Alisauskas RT, Clark RG (1993) Stable-nitrogen isotope enrichment in avian tissues due to fasting and nutritional stress: implications for isotopic analyses of diets. Condor 95:388–394CrossRefGoogle Scholar
  30. Horning M, Trillmich F (1999) Lunar cycles in diel prey migrations exert a stronger effect on the diving of juveniles than adult Galápagos fur seals. Proc R Soc Lond B 266:1127–1132CrossRefGoogle Scholar
  31. Japan Fisheries Resource Conservation Association (1999) Research on migratory routes and diving ecology of sea turtles. General report on commissioned project for conservation research of aquatic animals in 1994–1998. Vol 1. Japan Fisheries Resource Conservation Association, Tokyo, pp 1–90 (in Japanese)Google Scholar
  32. Kurata Y, Yoneyama S, Tsutsumi S, Kimura J, Hosokawa S (1978) Experiments to increase number of green turtles through the release of the young. Report on fundamental research for fisheries development in Ogasawara Islands. No. 3. Ogasawara Fishery Center, Tokyo Metropolitan Government, Tokyo, pp 58–80 (in Japanese)Google Scholar
  33. Le Boeuf BJ, Crocker DE, Costa DP, Blackwell SB, Webb PM, Houser DS (2000) Foraging ecology of northern elephant seals. Ecol Monogr 70:353–382CrossRefGoogle Scholar
  34. Limpus CJ, Limpus DJ (2001) The loggerhead turtle, Caretta caretta, in Queensland: breeding migrations and fidelity to a warm temperate feeding area. Chelonian Conserv Biol 4:142–153Google Scholar
  35. Lundberg P (1988) The evolution of partial migration in birds. Trends Ecol Evol 3:172–175CrossRefGoogle Scholar
  36. Luschi P, Hays GC, Del Seppia C, Marsh R, Papi F (1998) The navigational feats of green sea turtles migrating from Ascension Island investigated by satellite telemetry. Proc R Soc Lond B 265:2279–2284CrossRefGoogle Scholar
  37. Madsen T, Shine R (2000) Silver spoons and snake body sizes: prey availability early in life influences long-term growth rates of free-ranging pythons. J Anim Ecol 69:952–958CrossRefGoogle Scholar
  38. Maekawa K, Nakano S (2002) To sea or not to sea: a brief review on salmon migration evolution. Fish Sci (suppl I) 68:27–32Google Scholar
  39. McMahon CR, Autret E, Houghton JDR, Lovell P, Myers AE, Hays GC (2005) Animal-borne sensors successfully capture the real-time thermal properties of ocean basins. Limnol Oceanogr Methods 3:392–398Google Scholar
  40. Metcalfe NB, Monaghan P (2001) Compensation for a bad start: grow now, pay later? Trends Ecol Evol 16:254–260PubMedCrossRefGoogle Scholar
  41. Minagawa M, Wada E (1984) Stepwise enrichment of 15N along food chains: further evidence and the relation between δ15N and animal age. Geochim Cosmochim Acta 48:1135–1140CrossRefGoogle Scholar
  42. Minami H, Ogi H (1997) Determination of migratory dynamics of the sooty shearwater in the Pacific using stable carbon and nitrogen isotope analysis. Mar Ecol Prog Ser 158:249–256CrossRefGoogle Scholar
  43. Minamikawa S, Naito Y, Sato K, Matsuzawa Y, Bando T, Sakamoto W (2000) Maintenance of neutral buoyancy by depth selection in the loggerhead turtle Caretta caretta. J Exp Biol 203:2967–2975PubMedGoogle Scholar
  44. Miyawaki I (1994) Sea turtles captured at the coast of Kushimoto Town, Wakayama Prefecture, and their straight carapace lengths. In: Kamezaki N, Yabuta S, Suganuma H (eds) Nesting beaches of sea turtles in Japan. Sea Turtle Association of Japan, Osaka, pp 75–80 (in Japanese)Google Scholar
  45. Mortimer JA, Carr A (1987) Reproduction and migrations of the Ascension Island green turtle (Chelonia mydas). Copeia 1987:103–113CrossRefGoogle Scholar
  46. Musick JA, Limpus CJ (1997) Habitat utilization and migration in juvenile sea turtles. In: Lutz PL, Musick JA (eds) The biology of sea turtles. CRC, Boca Raton, pp 137–163Google Scholar
  47. Nishikawa J, Nishida S, Moku M, Hidaka K, Kawaguchi K (2001) Biomass, abundance, and vertical distribution of micronekton and large gelatinous zooplankton in the subarctic Pacific and the Bering Sea during the summer of 1997. J Oceanogr 57:361–375CrossRefGoogle Scholar
  48. Phillips DL, Gregg JW (2001) Uncertainty in source partitioning using stable isotopes. Oecologia 127:171–179CrossRefGoogle Scholar
  49. Pinnegar JK, Polunin NVC (2000) Contributions of stable-isotope data to elucidating food webs of Mediterranean rocky littoral fishes. Oecologia 122:399–409CrossRefGoogle Scholar
  50. Rostal DC, Owens DW, Grumbles JS, MacKenzie DS, Amoss MS Jr (1998) Seasonal reproductive cycle of the Kemp’s ridley sea turtle (Lepidochelys kempi). General Comp Endocrinol 109:232–243CrossRefGoogle Scholar
  51. Rubenstein DR, Hobson KA (2004) From birds to butterflies: animal movement patterns and stable isotopes. Trends Ecol Evol 19:256–263PubMedCrossRefGoogle Scholar
  52. Sato K, Matsuzawa Y, Tanaka H, Bando T, Minamikawa S, Sakamoto W, Naito Y (1998) Internesting intervals for loggerhead turtles, Caretta caretta, and green turtles, Chelonia mydas, are affected by temperature. Can J Zool 76:1651–1662CrossRefGoogle Scholar
  53. Seminoff JA, Todd Jones T, Eguchi T, Jones DR, Dutton PH (2006) Stable isotope discrimination (δ13C and δ15N) between soft tissues of the green sea turtle Chelonia mydas and its diet. Mar Ecol Prog Ser 308:271–278CrossRefGoogle Scholar
  54. Smit AJ, Brearley A, Hyndes GA, Lavery PS, Walker DI (2005) Carbon and nitrogen stable isotope analysis of an Amphibolis griffithii seagrass bed. Estuar Coast Shelf Sci 65:545–556CrossRefGoogle Scholar
  55. Suganuma H, Horikoshi K, Tachikawa H, Sato F, Yamaguchi M (1996) Reproductive characteristics of the Ogasawara green turtles. In: Keinath JA, Barnard DE, Musick JA, Bell BA (eds) Proceedings of the 15th annual symposium on sea turtle biology and conservation. NOAA Technical Memorandum NMFS-SEFSC-387, pp 318Google Scholar
  56. Tachikawa H, Sasaki A (1990) Tagging study of adult green turtle in Ogasawara Islands. Umigame Newsletter of Japan 6:11–15 (in Japanese)Google Scholar
  57. Troëng S, Evans DR, Harrison E, Lagueux CJ (2005) Migration of green turtles Chelonia mydas from Tortuguero, Costa Rica. Mar Biol 148:435–447CrossRefGoogle Scholar
  58. Tsukamoto K, Nakai I, Tesch W-V (1998) Do all freshwater eels migrate? Nature 396:635–636CrossRefGoogle Scholar
  59. Umezawa Y, Miyajima T, Yamamuro M, Kayanne H, Koike I (2002) Fine-scale mapping of land-derived nitrogen in coral reefs by δ15N in macroalgae. Limnol Oceanogr 47:1405–1416CrossRefGoogle Scholar
  60. Wang WL, Yeh HW (2003) δ13C values of marine macroalgae from Taiwan. Bot Bull Acad Sin 44:107–112Google Scholar
  61. Werner EE, Gilliam JF (1984) The ontogenetic niche and species interactions in size-structured populations. Annu Rev Ecol Syst 15:393–425CrossRefGoogle Scholar
  62. Wilbur HM, Collins JP (1973) Ecological aspects of amphibian metamorphosis. Science 182:1305–1314PubMedCrossRefGoogle Scholar
  63. Wilson RP, Puetz K, Bost CA, Culik BM, Bannasch R, Reins TR, Adelung D (1993) Diel dive depth in penguins in relation to diel vertical migration of prey: whose dinner by candlelight? Mar Ecol Prog Ser 94:101–104CrossRefGoogle Scholar
  64. Wu J, Calvert SE, Wong CS (1997) Nitrogen isotope variations in the subarctic northeast Pacific: relationships to nitrate utilization and trophic structure. Deep Sea Res I 44:287–314CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • Hideo Hatase
    • 1
    Email author
  • Katsufumi Sato
    • 2
  • Manami Yamaguchi
    • 3
  • Kotaro Takahashi
    • 3
  • Katsumi Tsukamoto
    • 1
  1. 1.Ocean Research InstituteUniversity of TokyoTokyoJapan
  2. 2.International Coastal Research Center, Ocean Research InstituteUniversity of TokyoIwateJapan
  3. 3.Sea Turtle Association of Japan and Ogasawara Marine CenterTokyoJapan

Personalised recommendations