Intrinsic tracers reveal recent foraging ecology of giant Pacific bluefin tuna at their primary spawning grounds

Marine Ecology Progress Series

Volumn 553, Issue , 2016, Pages 253-266

  Madigan, Daniel J ^a   Chiang, Wei Chuan ^b   Wallsgrove, Natalie J ^c   Popp, Brian N ^c   Kitagawa, Takashi ^d   Anela Choy, C ^e   Tallmon, Jocelyn ^f   Ahmed, Nazmul ^f   Fisher, Nicholas S ^f   Sun, Chi Lu ^g,h  

^a HARVARD UNIVERSITY   (United States)

^b FISHERIES RESEARCH INSTITUTE   (Taiwan)

^c UNIVERSITY OF HAWAII   (United States)

^d UNIVERSITY OF TOKYO   (Japan)

^e MONTEREY BAY AQUARIUM RESEARCH INSTITUTE   (United States)

^f STONY BROOK UNIVERSITY   (United States)

^g NATIONAL TAIWAN OCEAN UNIVERSITY   (Taiwan)

^h NATIONAL TAIWAN UNIVERSITY   (Taiwan)

Author keywords

AA CSIA; Diet; Stable isotopes; Thunnus orientalis; Trophic

Indexed keywords

AMINO ACID; CEPHALOPOD; FORAGING BEHAVIOR; ISOTOPIC ANALYSIS; MIGRATION; PELAGIC FISH; PERCIFORM; PREY AVAILABILITY; SPAWNING GROUND; STABLE ISOTOPE; TRACER; TROPHIC LEVEL;

KUROSHIO REGION; OYASHIO REGION; PACIFIC OCEAN; PACIFIC OCEAN (EAST); PACIFIC OCEAN (WEST); SEA OF JAPAN; TAIWAN;

BRAMIDAE; CEPHALOPODA; ENGRAULIDAE; SCOMBRIDAE; THUNNUS ORIENTALIS;

EID: 84978653512     PISSN: 01718630     EISSN: None     Source Type: Journal    
DOI: 10.3354/meps11782     Document Type: Article

References (79)

1. Bayliff WH (1994) A review of the biology and fisheries for northern bluefin tuna, Thunnus thynnus, in the Pacific Ocean. FAO Fish Tech Pap 336: 244-295
2. Block BA, Jonsen ID, Jorgensen SJ, Winship AJ and others (2011) Tracking apex marine predator movements in a dynamic ocean. Nature 475: 86-90
3. Bond AL, Diamond AW (2011) Recent Bayesian stable-isotope mixing models are highly sensitive to variation in discrimination factors. Ecol Appl 21: 1017-1023
4. Boustany AM, Matteson R, Castleton M, Farwell C, Block BA (2010) Movements of Pacific bluefin tuna (Thunnus orientalis) in the Eastern North Pacific revealed with archival tags. Prog Oceanogr 86: 94-104
5. Bradley CJ, Wallsgrove NJ, Choy CA, Drazen JC, Hetherington ED, Hoen DK, Popp BN (2015) Trophic position estimates of marine teleosts using amino acid compound specific isotopic analysis. Limnol Oceanogr Methods 13: 476-493
6. Butler CM (2007) Atlantic bluefin tuna (Thunnus thynnus) feeding ecology and potential ecosystem effects during winter in North Carolina. MSc thesis, NC State University, Raleigh, NC.
7. Carlisle AB, Kim SL, Semmens BX, Madigan DJ and others (2012) Using stable isotope analysis to understand migration and trophic ecology of northeastern Pacific white sharks (Carcharodon carcharias). PLoS One 7: e30492
8. Carlisle AB, Goldman KJ, Litvin SY, Madigan DJ and others (2015) Stable isotope analysis of vertebrae reveals ontogenetic changes in habitat in an endothermic pelagic shark. Proc R Soc B 282(1799):20141446
9. Caut S, Angulo E, Courchamp F (2009) Variation in discrimination factors (15N and 13C): The effect of diet isotopic values and applications for diet reconstruction. J Appl Ecol 46: 443-453
10. Chase BC (2002) Differences in diet of Atlantic bluefin tuna (Thunnus thynnus) at five seasonal feeding grounds on the New England continental shelf. Fish Bull 100: 168-180
11. Chen KS, Crone P, Hsu CC (2006) Reproductive biology of female Pacific bluefin tuna Thunnus orientalis from south-western North Pacific Ocean. Fish Sci 72: 985-994
12. Chikaraishi Y, Ogawa NO, Ohkouchi N (2010) Further evaluation of the trophic level estimation based on nitrogen isotopic composition of amino acids. In: Ohkouchi N, Tayasu I, Koba K (ed)s) Earth, life, and isotopes. Kyoto University Press, Kyoto, p 37-51
13. Choy CA, Popp BN, Hannides CCS, Drazen JC (2015) Trophic structure and food resources of epipelagic and mesopelagic fishes in the North Pacific Subtropical Gyre ecosystem inferred from nitrogen isotopic compositions. Limnol Oceanogr 60: 1156-1171
14. Colette BB, Nauen CE (1983) FAO species catalogue. Scombrids of the world. An annotated and illustrated catalogue of tunas, mackerels, bonitos and related species known to date. FAO Fish Synop 125(2):137
15. Cury PM, Boyd IL, Bonhommeau S, Anker-Nilssen T and others (2011) Global seabird response to forage fish depletion-one-Third for the birds. Science 334: 1703-1706
16. Dale JJ, Wallsgrove NJ, Popp BN, Holland K (2011) Nursery habitat use and foraging ecology of the brown stingray Dasyatis lata determined from stomach contents, bulk and amino acid stable isotopes. Mar Ecol Prog Ser 433: 221-236
17. Dalton R (2005) Satellite tags give fresh angle on tuna quota. Nature 434: 1056-1057
18. Das K, Lepoint G, Loizeau V, Debacker V, Dauby P, Bouquegneau JM (2000) Tuna and dolphin associations in the north-east Atlantic: evidence of different ecological niches from stable isotope and heavy metal measurements. Mar Pollut Bull 40: 102-109
19. Estrada JA, Lutcavage M, Thorrold SR (2005) Diet and trophic position of Atlantic bluefin tuna (Thunnus thynnus) inferred from stable carbon and nitrogen isotope analysis. Mar Biol 147: 37-45
20. Estrada JA, Rice AN, Natanson LJ, Skomal GB (2006) Use of isotopic analysis of vertebrae in reconstructing ontogenetic feeding ecology in white sharks. Ecology 87: 829-834
21. Fréon P, Cury P, Shannon L, Roy C (2005) Sustainable exploitation of small pelagic fish stocks challenged by environmental and ecosystem changes: A review. Bull Mar Sci 76: 385-462
22. Fujioka K, Masujima M, Boustany AM, Kitagawa T (2015) Horizontal movements of pacific bluefin tuna. In Kitagawa T, Kimura S (ed)s) Biology and ecology of bluefin tuna. CRC Press, Boca Raton, FL, p101-122.
23. Golet WJ, Cooper AB, Campbell R, Lutcavage ME (2007) Decline in condition of northern bluefin tuna (Thunnus thynnus) in the Gulf of Maine. Fish Bull 105: 390-395
24. Golet WJ, Record NR, Lehuta S, Lutcavage M, Galuardi B, Cooper AB, Pershing AJ (2015) The paradox of the pelagics: why bluefin tuna can go hungry in a sea of plenty. Mar Ecol Prog Ser 527: 181-192
25. Gould P, Ostrom P, WalkerW(1997) Trophic relationships of albatrosses associated with squid and large-mesh driftnet fisheries in the North Pacific Ocean. Can J Zool 75: 549-562
26. Graham BS, Grubbs D, Holland K, Popp BN (2007) A rapid ontogenetic shift in the diet of juvenile yellowfin tuna from Hawaii. Mar Biol 150: 647-658
27. Graham BS, Koch PL, Newsome SD, McMahon KW, Aurioles D (2010) Using isoscapes to trace the movements and foraging behavior of top predators in oceanic ecosystems. In: West GJ Bowen, Dawson TE, Tu KP (ed)s) Isoscapes. Springer, Dordrecht, p299-318
28. Hannides CCS, Popp BN, Landry MR, Graham BS (2009) Quantification of zooplankton trophic position in the North Pacific Subtropical Gyre using stable nitrogen isotopes. Limnol Oceanogr 54: 50-61
29. Hussey NE, MacNeil MA, McMeans BC, Olin JA and others (2014) Rescaling the trophic structure of marine food webs. Ecol Lett 17: 239-250
30. ISC (International Scientific Committee for tuna and tuna-like species in the North Pacific Ocean) (2014) Pacific bluefin stock assessment. International Scientific Committee for tuna and tuna-like species in the North Pacific Ocean. La Jolla, CA
31. Ito S (1961) Fishery biology of the sardine, Sardinops melanosticta (T. & S.), in the waters around Japan. Bull Japan Sea Reg Fish Res Lab 9: 1-227
32. Itoh T (2004) Construction of a new schematic illustration of migration for Pacific bluefin tuna. In: Sugimoto T (ed)) Ocean current and biological resources. Seizando, Tokyo, p 254-261
33. Kitagawa T, Nakata H, Kimura S, Itoh T, Tsuji S, Nitta A (2000) Effect of ambient temperature on the vertical distribution and movement of Pacific bluefin tuna Thunnus thynnus orientalis. Mar Ecol Prog Ser 206: 251-260
34. Kitagawa T, Kimura S, Nakata H, Yamada H (2004) Diving behavior of immature, feeding Pacific bluefin tuna (Thunnus thynnus orientalis) in relation to season and area: The East China Sea and the Kuroshio-Oyashio transition region. Fish Oceanogr 13: 161-180
35. Kitagawa T, Kimura S, Nakata H, Yamada H, Nitta A, Sasai Y, Sasaki H (2009) Immature Pacific bluefin tuna, Thunnus orientalis, utilizes cold waters in the Subarctic Frontal Zone for trans-Pacific migration. Environ Biol Fishes 84: 193-196
36. Kitagawa T, Kato Y, Miller MJ, Sasai Y, Sasaki H, Kimura S (2010) The restricted spawning area and season of Pacific bluefin tuna facilitate use of nursery areas: A modeling approach to larval and juvenile dispersal processes. J Exp Mar Biol Ecol 393: 23-31
37. Liu KK, Su MJ, Hsueh CR, Gong GC (1996) The nitrogen isotopic composition of nitrate in the Kuroshio Water northeast of Taiwan: evidence for nitrogen fixation as a source of isotopically light nitrate. Mar Chem 54: 273-292
38. Logan JM, Jardine TD, Miller TJ, Bunn SE, Cunjak RA, Lutcavage ME (2008) Lipid corrections in carbon and nitrogen stable isotope analyses: comparison of chemical extraction and modelling methods. J Anim Ecol 77: 838-846
39. Logan JM, Rodríguez-Marín E, Goñi N, Barreiro S, Arrizabalaga H, Golet W, Lutcavage M (2011) Diet of young Atlantic bluefin tuna (Thunnus thynnus) in eastern and western Atlantic foraging grounds. Mar Biol 158: 73-85
40. Lorrain A, Graham BS, Popp BN, Allain V and others (2015) Nitrogen isotopic baselines and implications for estimating foraging habitat and trophic position of yellowfin tuna in the Indian and Pacific Oceans. Deep-Sea Res II 113: 188-198
41. Madigan DJ (2015) Understanding bluefin migration using intrinsic tracers in tissues. In: Kitagawa T, Kimura S (ed)s) Biology and ecology of bluefin tuna. CRC Press, Boca Raton, FL, p 211-224
42. Madigan DJ, Carlisle AB, Dewar H, Snodgrass OE, Litvin SY, Micheli F, Block BA (2012a) Stable isotope analysis challenges wasp-waist food web assumptions in an upwelling pelagic food web. Sci Rep 2: e654
43. Madigan DJ, Litvin SY, Popp BN, Carlisle AB, Farwell CJ, Block BA (2012b) Tissue turnover rates and isotopic trophic discrimination factors in the endothermic teleost, Pacific bluefin tuna (Thunnus orientalis). PLoS One 7: e49220
44. Madigan DJ, Baumann Z, Carlisle AB, Hoen DK and others (2014) Reconstructing trans-oceanic migration patterns of Pacific bluefin tuna using a chemical tracer toolbox. Ecology 95: 1674-1683
45. Madigan DJ, Brooks EJ, Bond ME, Gelsleichter J and others (2015a) Diet shift and site-fidelity of oceanic whitetip sharks Carcharhinus longimanus along the Great Bahama Bank. Mar Ecol Prog Ser 529: 185-197
46. Madigan DJ, Carlisle AB, Gardner LD, Jayasundara N and others (2015b) Assessing niche width of endothermic fish from genes to ecosystem. Proc Natl Acad Sci USA 112: 8350-8355
47. Matthews FD, Damkaer DM, Knapp LW, Collette BB (1977) Food of western North Atlantic tunas (Thunnus) and lancetfishes (Alepisaurus). US Dept Commerce, National Oceanic and Atmo spheric Administration, National Marine Fisheries Service, Silver Spring, M.D.
48. Moore JW, Semmens BX (2008) Incorporating uncertainty and prior information into stable isotope mixing models. Ecol Lett 11: 470-480
49. Nakada S, Hirose N (2009) Seasonal upwelling underneath the Tsushima Warm Current along the Japanese shelf slope. J Mar Syst 78: 206-213
50. Ohta I, Yamada H (2015) Formation of a pacific bluefin tuna fishing ground on their spawning grounds around the Ryukya Islands. In: Kitagawa T, Kimura S (ed)s) Biology and ecology of bluefin tuna. CRC Press, Boca Raton, FL, p 123-136
51. Okochi Y, Abe O, Tanaka S, Ishihara Y, Shimizu A (2016) Reproductive biology of female Pacific bluefin tuna, Thunnus orientalis, in the Sea of Japan. Fish Res 174: 30-39
52. Phillips DL, Eldridge PM (2006) Estimating the timing of diet shifts using stable isotopes. Oecologia 147: 195-203
53. Phillips DL, Gregg JW (2003) Source partitioning using stable isotopes: coping with too many sources. Oecologia 136: 261-269
54. Pinkas L, Oliphant MS, Iverson ILK (1971) Food habits of albacore, bluefin tuna, and bonito in California waters. Fish Bull Calif Dept Fish Game 152: 1-105
55. Polovina JJ (1996) Decadal variation in the trans-Pacific migration of northern bluefin tuna (Thunnus thynnus) coherent with climate-induced change in prey abundance. Fish Oceanogr 5: 114-119
56. Popp BN, Graham BS, Olson RJ, Hannides CCS and others (2007) Insight into the trophic ecology of yellowfin tuna, Thunnus albacares, from compound-specific nitrogen isotope analysis of proteinaceous amino acids. In: Dawson TE, Siegwolf RTW (ed)s) Terrestrial ecology. Elsevier, Burlington, MA, p 173-190
57. Post DM (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83: 703-718
58. Ramos R, González-Solís J (2012) Trace me if you can: The use of intrinsic biogeochemical markers in marine top predators. Front Ecol Environ 10: 258-266
59. Revill A, Young J, Lansdell M (2009) Stable isotopic evidence for trophic groupings and bio-regionalization of predators and their prey in oceanic waters off eastern Australia. Mar Biol 156: 1241-1253
60. Rooker JR, Secor DH, Zdanowicz VS, Itoh T (2001) Discrimination of northern bluefin tuna from nursery areas in the Pacific Ocean using otolith chemistry. Mar Ecol Prog Ser 218: 275-282
61. Seminoff JA, Benson SR, Arthur KE, Eguchi T, Dutton PH, Tapilatu RF, Popp BN (2012) Stable isotope tracking of endangered sea turtles: validation with satellite telemetry and ä15N analysis of amino acids. PLoS One 7: e37403
62. Sherwood OA, Lehmann MF, Schubert CJ, Scott DB, McCarthy MD (2011) Nutrient regime shift in the western North Atlantic indicated by compound-specific ä15N of deep-sea gorgonian corals. Proc Natl Acad Sci USA 108: 1011-1015
63. Shimose T, Wells RD (2015) Feeding ecology of bluefin tunas. In: Kitagawa T, Kimura S (ed)s) Biology and ecology of bluefin tuna. CRC Press, Boca Raton, FL, p 78-100
64. Shimose T, Tanabe T, Chen KS, Hsu CC (2009) Age determination and growth of Pacific bluefin tuna, Thunnus orientalis, off Japan and Taiwan. Fish Res 100: 134-139
65. Shimose T, Watanabe H, Tanabe T, Kubodera T (2013) Ontogenetic diet shift of age-0 year Pacific bluefin tuna Thunnus orientalis. J Fish Biol 82: 263-276
66. Smith ADM, Brown CJ, Bulman CM, Fulton EA and others (2011) Impacts of fishing low-Trophic level species on marine ecosystems. Science 333: 1147-1150
67. Smith PJ, Griggs L, Chow S (2001) DNA identification of Pacific bluefin tuna (Thunnus orientalis) in the New Zealand fishery. NZ J Mar Freshw Res 35: 843-850
68. Sommer U, Stibor H, Katechakis A, Sommer F, Hansen T (2002) Pelagic food web configurations at different levels of nutrient richness and their implications for the ratio fish production: primary production. In: Vadstein O, Olsen Y (ed)s) Sustainable increase of marine harvesting: fundamental mechanisms and new concepts: Proc 1st Maricult Conf, Trondheim, Norway, 25-28 June 2000. Springer, Dordrecht, p 11-20
69. Tacon AGJ, Metian M (2009) Fishing for feed or fishing for food: increasing global competition for small pelagic forage fish. AMBIO 38: 294-302
70. Takai N, Onaka S, Ikeda Y, Yatsu A, Kidokoro H, Sakamoto W(2000) Geographical variations in carbon and nitrogen stable isotope ratios in squid. J Mar Biol Assoc UK 80: 675-684
71. Tanaka H, Takasuka A, Aoki I, Ohshimo S (2008) Geographical variations in the trophic ecology of Japanese anchovy, Engraulis japonicus, inferred from carbon and nitrogen stable isotope ratios. Mar Biol 154: 557-568
72. Uotani I, Saito T, Hiranuma K, Nishikawa Y (1990) Feeding habit of bluefin tuna Thunnus thynnus larvae in the Western North Pacific Ocean. Bull Jpn Soc Sci Fish 56: 713-717
73. Varela JL, Rodríguez-Marín E, Medina A (2013) Estimating diets of pre-spawning Atlantic bluefin tuna from stomach content and stable isotope analyses. J Sea Res 76: 187-192
74. Whitlock RE, Hazen EL, Walli A, Farwell C and others (2015) Direct quantification of energy intake in an apex marine predator suggests physiology drives seasonal migrations. Sci Adv 1(8):e1400270
75. Wyatt ASJ, Waite AM, Humphries S (2010) Variability in isotope discrimination factors in coral reef fishes: implications for diet and food web reconstruction. PLoS One 5: e13682
76. Yamauchi M (2011) Fishing report of the Pacific bluefin tuna, Thunnus orientalis, caught by a small-scale tuna longline fishing boat and food habits of pelagic fishes around the Ryukyu Archipelago, Japan. University of the Ryukyus, Okinawa
77. Yasue N, Doiuchi R, Takasuka A (2013) Trophodynamic similarities of three sympatric clupeoid species throughout their life histories in the Kii Channel as revealed by stable isotope approach. ICES J Mar Sci 71: 44-55
78. Yokota T, Toriyama M, Kanai F, Nomura S (1961) Studies on the feeding habit of fishes. Rep Nankai Reg Fish Res Lab 14: 1-234
79. Young JW, Lamb TD, Le D, Bradford RW, Whitelaw AW (1997) Feeding ecology and interannual variations in diet of southern bluefin tuna, Thunnus maccoyii, in relation to coastal and oceanic waters off eastern Tasmania, Australia. Environ Biol Fishes 50: 275-291