Identifying migrations in marine fishes through stable-isotope analysis

Journal of Fish Biology

Volumn 81, Issue 2, 2012, Pages 826-847

  Trueman, C N ^a   Mackenzie, K M ^a   Palmer, M R ^a  

^a UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

Author keywords

Chemical proxy; Fishes; Movement; Oceanic; Tracking

Indexed keywords

CARBON; NITROGEN; OXYGEN; SEA WATER;

ANIMAL; ARTICLE; CHEMISTRY; FISH; MUSCLE; PHYSIOLOGY; POPULATION MIGRATION; VESTIBULE;

ANIMAL MIGRATION; ANIMALS; CARBON ISOTOPES; FISHES; MUSCLES; NITROGEN ISOTOPES; OTOLITHIC MEMBRANE; OXYGEN ISOTOPES; SEAWATER;

ANIMALIA; MAMMALIA; PISCES;

EID: 84864009753     PISSN: 00221112     EISSN: 10958649     Source Type: Journal    
DOI: 10.1111/j.1095-8649.2012.03361.x     Document Type: Article

References (96)

1. Abrantes, K. G. & Barnett, A. (2011). Intrapopulation variations in diet and habitat use in a marine apex predator, the broadnose sevengill shark Notorynchus cepedianus. Marine Ecology Progress Series 442, 133-148.
2. Ashford, J. R. & Jones, C. M. (2007). Oxygen and carbon stable isotopes in otoliths record spatial isolation of Patagonian toothfish (Dissostichus eleginoides). Geochimica et Cosmochimica Acta 71, 87-94.
3. Ayvazian, S. G., Bastow, T. P., Edmonds, J. S., How, J. & Nowara, G. B. (2004). Stock structure of Australian herring (Arripis georgiana) in southwestern Australia. Fisheries Research 67, 39-53.
4. 13C of marine animals. Estuarine, Coastal and Shelf Science 81, 368-374.
5. Barnet-Johnson, R., Pearson, T. E., Ramos, F. C., Grimes, C. B. & MacFarlane, R. B. (2008). Tracking natal origins of salmon using isotopes, otoliths, and landscape geology. Limnology and Oceanography 53, 1633-1642.
6. 18O isotopes in otoliths of haddock Melanogrammus aeglefinus from the northwest Atlantic Ocean. Marine Ecology-Progress Series 216, 223-233.
7. Bendry, R., Hayes, T. E. & Palmer, M. R. (2009). Patterns of iron age horse supply: An analysis of strontium isotope ratios in teeth. Archaeometry 51, 140-150.
8. Best, P. B. & Schell, D. M. (1996). Stable isotopes in southern right whale (Eubalaena australis) baleen as indicators of seasonal movements, feeding and growth. Marine Biology 124, 483-494.
9. Bigg, G. R. & Rohling, E. J. (2000). An oxygen isotope dataset for marine water. Journal of Geophysical Research 105, 8527-8535.
10. Block, B. A., Jonsen, I. D., Jorgensen, S. J., Winship, A. J., Shaffer, S. A., Bograd, S. J., Hazen, E. L., Foley, D. G., Breed, G. A., Harrison, A. L., Ganong, J. E., Swithenbank, A., Castleton, M., Dewar, H., Mate, B. R., Shillinger, G. L., Schaefer, K. M., Benson, S. R., Weise, M. J., Henry, R. W. & Costa, D. P. (2011). Tracking apex marine predator movements in a dynamic ocean. Nature 475, 86-90.
11. Boecklen, W. J., Yarnes, C. T., Cook, B. A. & James, A. C. (2011). On the use of stable isotopes in trophic ecology. The Annual Review of Ecology Evolution and Systematics 42, 411-440.
12. Bolle, L. J., Hunter, E., Rijnsdorp, A. D., Pastoors, M. A., Metcalfe, J. D. & Reynolds, J. D. (2005). Do tagging experiments tell the truth? Using electronic tags to evaluate conventional tagging data. ICES Journal of Marine Science 62, 236-246.
13. Borrell, A., Aguilar, A., Gazo, M., Kumarran, R. P. & Cardona, L. (2011). Stable isotope profiles in whale shark (Rhincodon typus) suggest segregation and dissimilarities in the diet depending on sex and size. Environmental Biology of Fishes 92, 559-567.
14. 18O in meteoric precipitation. Geology 30, 315-318.
15. Bowen, G. J., Wassenaar, L. I. & Hobson, K. A. (2005). Global application of stable hydrogen and oxygen isotopes to wildlife forensics. Oecologia 143, 337-348.
16. Carleton, S. A. & Martinez del Rio, C. (2010). Growth and catabolism in isotopic incorporation: a new formulation and experimental data. Functional Ecology 24, 805-812.
17. Cerling, T. E., Ayliffe, L. K., Dearing, M. D., Ehleringer, J. R., Passey, B. H., Podlesak, D. W., Torregrossa, A-M. & West, A. G. (2007). Determining biological tissue turnover using stable isotopes: the reaction progress variable. Oecologia 151, 175-189.
18. Cherel Y. & Hobson K. A. (2007). Geographical variation in carbon stable isotope signatures of marine predators: a tool to investigate their foraging areas in the Southern Ocean. Marine Ecology - Progress Series 329, 281-287.
19. Cherel, Y., Kernaleguen, L., Richard, P. & Guinet, C. (2009). Whisker isotopic signature depicts migration patterns and multi-year intra- and inter-individual foraging strategies in fur seals. Biology Letters 5, 830-832.
20. Clarke, L. M., Munch, S. B., Thorrold, S. R. & Conover, D. O. (2010). High connectivity among locally adapted populations of a marine fish (Menidia menidia). Ecology 91, 3526-3537.
21. Cormie, A. B., Schwarcz, H. P. & Grey, J. (1994). Relationship between the hydrogen and oxygen isotopes of deer bone and their use in the estimation of relative humidity. Geochimica et Cosmochimica Acta 60, 4161-4166.
22. Dempson, J. B., Braithwaite, V. A., Doherty, D. & Power, M. (2010). Stable isotope analysis of marine feeding signatures of Atlantic salmon in the North Atlantic. ICES Journal of Marine Science 67, 52-61.
23. DeNiro, M. J. & Epstein, S. (1978). Influence of diet on distribution of carbon isotopes in animals. Geochimica et Cosmochimica Acta 42, 495-506.
24. DeNiro, M. J. & Epstein, S. (1981). Influence of diet on the distribution of nitrogen isotopes in animals. Geochimica et Cosmochimica Acta 45, 341-351.
25. DeSoto, D. X., Wassenaar, L. I., Hobson, K. A. & Catalan, J. (2011). Effects of size and diet on stable hydrogen isotope values (δD) in fish: implications for tracing origins of individuals and their food sources. Canadian Journal of Fisheries and Aquatic Sciences 68, 2011-2019.
26. Elsdon T. S., Ayvazian S., McMahon K. W. & Thorrold S. R., (2010). Experimental evaluation of stable isotope fractionation in fish muscle and otoliths. Marine Ecology-Progress Series 408, 181-193.
27. Fry, B. (2006). Stable Isotope Ecology. New York, NY: Springer LLC.
28. Fuji, T., Kasai, A., Suzuki, K. W., Ueno, M. & Yamashita, Y. (2011). Migration ecology of juvenile temperate seabass Lateolabrax japonicus: a carbon stable-isotope approach. Journal of Fish Biology 78, 2010-2025.
29. Gao, Y. W. & Beamish, R. J. (2003). Stable isotopic composition of otoliths from tagged Pacific halibut, Hippoglossus stenolepis. Environmental Biology of Fishes 67, 253-261.
30. Graham, B. S., Koch, P. L., Newsome, S. D., McMahon, K. W. & Aurioles, D. (2010). Using isoscapes to trace the movements and foraging behavior of top predators in oceanic ecosystems. In Isoscapes: Understanding Movement, Pattern, and Process on Earth Through Isotope Mapping (West, J. B., Bowen, G. J., Dawson, T. E. & Tu, K. P., eds), pp. 299-318. New York, NY: Springer.
31. 18O values of wild Atlantic salmon (Salmo salar). Rapid Communications in Mass Spectrometry 24, 2491-2498.
32. Hesslein, R. H., Hallard, K. A. & Ramlal, P. (1993). Replacement of sulfur, carbon, and nitrogen in tissue of growing broad whitefish (Coregonus nasus) in response to a change in diet tracked by delta-S-34, delta-C-13 and delta-N-15. Canadian Journal of Fisheries and Aquatic Sciences 50, 2071-2076.
33. Hobson, K. A. (1999). Tracing origins and migration of wildlife using stable isotopes: a review. Oecologia 120, 314-326.
34. Hobson, K. A. & Schell, D. M. (1998). Stable carbon and nitrogen isotope patterns in baleen from eastern Arctic bowhead whales (Balaena mysticetus). Canadian Journal of Fisheries and Aquatic Sciences 55, 2601-2607.
35. Hobson, K. A. & Wassenaar, L. I. (1997). Linking breeding and wintering grounds of neotropical migrant songbirds using stable hydrogen isotopic analyses of feathers. Oecologia 109, 142-148.
36. 13C) are geographic indicators of natal origins of monarch butterflies in eastern North America. Oecologia 120, 397-404.
37. Hobson, K. A., Barnett-Johnson, R. & Cerling, T. (2010). Using isoscapes to track animal migration. In Isoscapes: Understanding Movement, Pattern, and Process on Earth Through Isotope Mapping (West, J. B., Bowen, G. J., Dawson, T. E. & Tu, K. P., eds), pp. 272-298. New York, NY: Springer.
38. Hofmann, M., Wolf-Gladrow, D. A., Takahashi, T., Sutherland, S. C., Six, K. D. & Maier-Reimer, E. (2000). Stable carbon isotope distribution of particulate organic matter in the ocean: a model study. Marine Chemistry 72, 131-150.
39. Høie H., Otterlei E. & Folkvord A. (2004a). Temperature-dependent fractionation of stable oxygen isotopes in otoliths of juvenile cod (Gadus morhua L.). ICES Journal of Marine Science 61, 243-251.
40. Høie H., Andersson C., Folkvord A. & Karlsen O. (2004b). Precision and accuracy of stable isotope signals in otoliths of pen-reared cod (Gadus morhua) when sampled with a high-resolution micromill. Marine Biology 144, 1039-1049.
41. Hussey, N. E., Dudley, S. F. J., McCarthy, I. D., Cliff, G. & Fisk, A. T. (2011). Stable isotope profiles of large marine predators: viable indicators of trophic position, diet, and movement in sharks? Canadian Journal of Fisheries and Aquatic Sciences 68, 2029-2045.
42. Hutchings, J. A. & Reynolds, J. D. (2004). Marine fish population collapses: consequences for recovery and extinction risk. Bioscience 54, 297-309.
43. Hutchinson, J. J. & Trueman, C. N. (2006). Stable isotope analyses of collagen in fish scales: limitations set by scale architecture. Journal of Fish Biology 69, 1874-1880.
44. Jaeger, A., Lecomte, V. J., Weimerskirch, H., Richard, P. & Cherel, Y. (2010). Seabird satellite tracking validates the use of latitudinal isoscapes to depict predators' foraging areas in the Southern Ocean. Rapid Communications in Mass Spectrometry 24, 3456-3460.
45. Jardine, T. D., MacLatchy, D. L., Fairchild, W. L., Cunjack, R. A. & Brown, S. B. (2004). Rapid carbon turnover during growth of Atlantic salmon (Salmo salar) smolts in sea water, and evidence for reduced food consumption by growth-stunts. Hydrobiologica 527, 63-75.
46. Jennings, S., Kaiser, M. J. & Reynolds, J. D. (2001). Marine Fisheries Ecology. Oxford: Blackwell Science.
47. 18O isotopic disequilibria in fish otoliths: metabolic and kinetic effects. Marine Ecology-Progress Series 75, 191-203.
48. 15N in vertebrae of white shark (Carcharodon carcharias) from the eastern North Pacific Ocean. Environmental Biology of Fishes 77, 337-353.
49. Lara, R. J., Alder, V., Franzosi, C. A. & Kattner, G. (2010). Characteristics of suspended particulate organic matter in the southwestern Atlantic: Influence of temperature, nutrient and phytoplankton features on the stable isotope signature. Journal of Marine Systems 79, 199-209.
50. Lee, S. H., Schell, D. M., McDonald, T. L. & Richardson, W. J. (2005). Regional and seasonal feeding by bowhead whales Balaena mysticetus as indicated by stable isotope ratios. Marine Ecology Progress Series 285, 271-287.
51. Longmore, C., Trueman, C. N., Neat, F., O'Gorman, E. J., Milton, J. A. & Mariani, S. (2011). Otolith chemistry indicates life-long spatial population structuring in a deep-sea fish, Coryphaenoides rupestris. Marine Ecology Progress Series 435, 209-224.
52. Lorrain, A., Graham, B., Menard, F., Popp, B., Bouillon, S., van Breugel, P. & Cherel, Y. (2009). Nitrogen and carbon isotope values of individual amino acids: a tool to study foraging ecology of penguins in the Southern Ocean. Marine Ecology-Progress Series 391, 293-306.
53. MacAvoy, S. E., Carney, R. S., Fisher, C. R. & Macko, S. A. (2002). Use of chemosynthetic biomass by large, mobile, benthic predators in the Gulf of Mexico. Marine Ecology Progress Series 225, 65-78.
54. MacKenzie, K. M., Palmer, M. R., Moore, A., Ibbotson, A. T., Beaumont, W. R. C., Poulter, D. J. S. & Trueman, C. N. (2011). Locations of marine animals revealed by carbon isotopes. Scientific Reports 1, 1-6.
55. McClelland, J. W. & Montoya, J. P. (2002). Trophic relationships and the nitrogen isotopic composition of amino acids in plankton. Ecology 83, 2173-2180.
56. McMahon, K. W., Fogel, M. L., Elsdon, T. S. & Thorrold, S. R. (2010). Carbon isotope fractionation of amino acids in fish muscle reflects biosynthesis and isotopic routing from dietary protein. Journal of Animal Ecology 79, 1132-1141.
57. 13C values in otolith amino acids. Canadian Journal of Fisheries and Aquatic Sciences 68, 1330-1340.
58. Menard, F., Lorrain, A., Potier, M. & Marsac, F. (2007). Isotopic evidence of distinct feeding ecologies and movement patterns in two migratory predators (yellowfin tuna and swordfish) of the western Indian Ocean. Marine Biology 153, 141-152.
59. Mendes, S., Newton, J., Reid, R. J., Zuur, A. F. & Pierce, G. J. (2007). Stable carbon and nitrogen isotope ratio profiling of sperm whale teeth reveals ontogenetic movements and trophic ecology. Oecologia 151, 605-615.
60. 15N in adult Pacific herring (Clupea pallasi) following an isotopic shift in diet. Environmental Biology of Fishes 76, 177-189.
61. 15N in marine planktonic ecosystems. In Stable Isotopes in Ecology and Environmental Science, 2nd edn (Michener R. & Lajtha K., eds), pp. 176-201. Malden, MA, Blackwell.
62. Nagelkerken, I., Bothwell, J., Nemeth, R. S., Pitt, J. M. & van der Velde, G. (2008). Interlinkage between Caribbean coral reefs and seagrass beds through feeding migrations by grunts (Haemulidae) depends on habitat accessibility. Marine Ecology Progress Series 368, 155-164.
63. Newsome, S. D., Clementz, M. T., & Koch, P. L. (2010). Using stable isotope biogeochemistry to study marine mammal ecology. Marine Mammal Science 26, 509-572.
64. Ngochera, M. J. & Bootsma, H. A. (2011). Temporal trends of phytoplankton and zooplankton stable isotope composition in tropical Lake Malawi. Journal of Great Lakes Research 37, 45-53.
65. Olson, R. J., Popp, B. N., Graham, B. S., Lopez-Ibarra, G. A., Galvan-Magana, F., Lennert-Cody, C. E., Bocanegra-Castillo, N., Wallsgrove, N. J., Gier, E., Alatorre-Ramirez, V., Ballance, L. T. & Fry, B. (2010). Food-web inferences of stable isotope spatial patterns in copepods and yellowfin tuna in the pelagic eastern Pacific Ocean. Progress in Oceanography 86, 124-138.
66. Papastamatiou, Y. P., Friedlander, A. M., Caselle, J. E. & Lowe, C. G. (2010). Long-term movement patterns and trophic ecology of blacktip reef sharks (Carcharhinus melanopterus) at Palmyra Atoll. Journal of Experimental Marine Biology and Ecology 386, 94-102
67. Patterson, W. P., Smith, G. R. & Lohmann, K. C. (1993). Continental paleothermometry and seasonality using the isotopic composition of aragonitic otoliths of freshwater fishes. American Geophysical Union Monographs 78, 191-215
68. Popp, B. N., Laws, E. A., Bidigare, R. R., Dore, J. E., Hanson, K. L. & Wakeham, S. G. (1998). Effect of phytoplankton cell geometry on carbon isotopic fractionation. Geochimica et Cosmochimica Acta 62, 69-77.
69. Popp B. N., Graham B. S., Olson R. J., Hannides C. C. S., Lott M. J., Lopez-Ibarra G. A., Galvan-Magana F. & Fry B. (2007). Insight into the trophic ecology of yellowfin tuna, Thunnus albacares, from compound-specific nitrogen isotope analysis of proteinaceous amino acids. In Stable Isotopes as Indicators of Ecological Change (Dawson, T. & Siegwolf, R., eds), pp. 173-190. San Diego, CA: Elsevier Academic Press.
70. 15N. Marine Ecology Progress Series 359, 239-248.
71. 15N of size-fractionated plankton at a coastal station in the northern Baltic proper. Marine Ecology Progress Series 203, 47-65.
72. Rooker, J. R., Secor, D. H., DeMetrio, G., Kaufman, A. J., Rios, A. B. & Ticina, V. (2008). Evidence of trans-Atlantic movement and natal homing of bluefin tuna from stable isotopes in otoliths. Marine Ecology Progress Series 368, 231-239.
73. 18O. Canadian Journal of Fisheries and Aquatic Sciences 67, 563-569.
74. Schwarcz, H. P., Gao, Y., Campana, S., Browne, D., Knyf, M. & Brand, U. (1998). Stable carbon isotope variations in otoliths of Atlantic cod (Gadus morhua). Canadian Journal of Fisheries and Aquatic Sciences 55, 1798-1806.
75. Shephard, S., Trueman, C., Rickaby, R. & Rogan, E. (2009). Juvenile life history of NE Atlantic orange roughy from otolith stable isotopes. Deep Sea Research 1 54, 1221-1230.
76. Shiao, J. C., Yui, T. F., Høie, H., Ninnemann, U. & Chang, S. K. (2009). Otolith O and C stable isotope compositions of southern bluefin tuna Thunnus maccoyii (Pisces: Scombridae) as possible environmental and physiological indicators. Zoological Studies 48, 71-82.
77. Solomon, C. T., Weber, P. K., Cech, Jr., J. J., Ingram, B. L., Conrad, M. E., Machavaram, M. V., Pogodina, A. R. & Franklin, R. L. (2005). Experimental determination of the sources of otolith carbon and associated isotopic fractionation. Canadian Journal of Fisheries and Aquatic Sciences 63, 79-89.
78. Stephenson, P. C., Edmonds, J. S., Moran, M. J. & Caputi, N. (2001). Analysis of stable isotope ratios to investigate stock structure of red emperor and Rankin cod in northern Western Australia. Journal of Fish Biology 58, 126-144.
79. Storm-Suke, A., Dempson, J. B., Reist, J. D. & Power, M. (2007). A field-derived oxygen isotope fractionation equation for Salvelinus species. Rapid Communications in Mass Spectrometry 21, 4109-4116.
80. Sturrock, A. M., Trueman, C. N., Darnaude, A. M. & Hunter, E. (2012). Can otolith elemental chemistry retrospectively track migrations in fully marine fishes? Journal of Fish Biology 81, 766-795. doi:10.1111/j.1095-8649.2012.03372.x
81. Tagliabue, A. and Bopp, L. (2008). Towards understanding global variability in ocean carbon-13. Global Biogeochemical Cycles 22, 1025.
82. Tanaka, H., Ohshimo, S., Takagi, N. & Ichimaru, T. (2010). Investigation of the geographical origin and migration of anchovy Engraulis japonicus in Tachibana Bay, Japan: A stable isotope approach. Fisheries Research 102, 217-220.
83. 18O fractionation in aragonitic otoliths of marine fish. Geochimica et Cosmochimica Acta 61, 2909-2919.
84. Trueman, C. N. & Moore, A. (2007). Use of the stable isotope composition of fish -scales for monitoring aquatic ecosystems. In Terrestrial Ecology (Ehleringer, J., ed.), pp. 139-155. Oxford: Elsevier Inc.
85. Trueman, C. N., McGill, R. A. R. & Guyard, P. H. (2005). The effect of growth rate on tissue-diet isotopic spacing in rapidly growing animals. An experimental study with Atlantic salmon (Salmo salar). Rapid Communications in Mass Spectrometry 19, 3239-3247.
86. Verweij, M. C., Nagelkerken, I., Hans, I., Ruseler, S. M. & Mason, P. R. D. (2008). Seagrass nurseries contribute to coral reef fish populations. Limnology and Oceanography 53, 1540-1547.
87. Wada, E., Mizutani, H. & Minagawa, M. (1991). The use of stable isotopes for food web analysis. Critical Reviews in Food Science and Nutrition 30, 361-371.
88. Wada, E., Kabaya, Y. & Kurihara, Y. (1993). Stable isotopic structure of aquatic ecosystems. Journal of Biosciences 18, 483-499.
89. Wainright, S. C., Fogarty, M. J., Greenfield, R. C. & Fry, B. (1993). Long-term changes in the Georges Bank food web-Trends in stable isotopic compositions of fish scales. Marine Biology 115, 481-493.
90. Weidman C. R. & Millner R. (2000). High-resolution stable isotope records from North Atlantic cod. Fisheries Research 46, 327-342.
91. Wells, R. J. D., Rooker, J. R. & Prince, E. D. (2010). Regional variation in the otolith chemistry of blue marlin (Makaira nigricans) and white marlin (Tetrapturus albidus) from the western North Atlantic Ocean. Fisheries Research 106, 430-435.
92. West, J. B., Bowen, G. J., Dawson, T. E. & Tu, K. P. (Eds). (2010). Iscoscapes: Understanding Movement, Pattern and Process on Earth through Isotope Mapping. New York, NY: Springer.
93. Wunder, M. B. (2010). Using isoscapes to model probability surfaces for determining geographic origins. In Isoscapes: Understanding Movement, Pattern, and Process on Earth Through Isotope Mapping (West, J. B., Bowen, G. J., Dawson, T. E. & Tu, K. P., eds), pp. 272-298. New York, NY: Springer.
94. Wurster, C. M., Patterson, W. P., Stewart, D. J., Bowlby, J. N., & Stewart, T. J. (2005). Thermal histories, stress, and metabolic rates of Chinook salmon (Oncorhynchus tshawytscha) in Lake Ontario: evidence from intra-otolith stable isotope analyses. Canadian Journal of Fisheries and Aquatic Sciences 62, 700-713.
95. ICES (2009). Report of the Workshop on Learning from Salmon Tagging Records (WKLUSTRE). Copenhagen: ICES. Available at
96. Schmidt, G. A., Bigg, G. R. & Rohling, E. J. (1999). Global Seawater Oxygen-18 Database-v1.21. Available at