Lipid and fatty acid dynamics by maternal Pacific bluefin tuna

Autoři: Yuko Hiraoka aff001;  Yumi Okochi aff002;  Seiji Ohshimo aff003;  Tamaki Shimose aff004;  Hiroshi Ashida aff001;  Takuya Sato aff001;  Yasuhiro Ando aff005
Působiště autorů: Bluefin Tuna Resources Department, National Research Institute of Far Seas Fisheries, Japan Fisheries Research and Education Agency, Shizuoka-shi, Shizuoka, Japan aff001;  Environmental Management Unit, JAPAN NUS Co. Ltd, Shinjuku-ku, Tokyo, Japan aff002;  Fisheries Management and Oceanography Department, Seikai National Fisheries Research Institute, Japan Fisheries Research and Education Agency, Nagasaki-shi, Nagasaki, Japan aff003;  Research Center for Subtropical Fisheries, Seikai National Fisheries Research Institute, Japan Fisheries Research and Education Agency, Ishigaki-shi, Okinawa, Japan aff004;  Faculty of Fisheries Sciences, Hokkaido University, Hakodate-shi, Hokkaido, Japan aff005
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
doi: 10.1371/journal.pone.0222824


Lipid and fatty acid composition of female Pacific bluefin tuna (PBF, Thunnus orientalis) reproductive and somatic tissues in southwestern North Pacific and Sea of Japan spawning grounds are compared. Total lipid (TL) levels are higher in liver than white muscle tissues. An increased gonadosomatic index (GSI) during the early spawning season coincided with decreased TL. Levels of triacylglycerols (TAG) in PBF liver tissues from the Nansei Islands and Sea of Japan, and white muscle in fishes from the Sea of Japan, decreased during the spawning season, while TAG in ovary tissues did not. Concurrent reductions in TL and increases in GSI early in the spawning season suggest TAG depletion was caused by allocation from liver and white muscle tissues to oocytes, that the liver is one of the important lipid-storage organs in PBF, and this species mostly reliant on capital deposits as a mixed capital-income breeder. Differences of docosahexaenoic acid (DHA) levels between spawning grounds were lower in ovary than in muscle and liver tissues. However, eicosapentaenoic (EPA) and arachidonic acid (ARA) levels that influence egg development and embryo and larval growth are significantly higher in PBF tissues from the Sea of Japan than Nansei Islands, which coincided with larval quality. These suggest a maternal effect exists, with egg quality influencing offspring survival, and that the reproductive strategy of PBF varies according to local variation at each spawning ground.

Klíčová slova:

Fatty acids – Islands – Larvae – Lipids – Ovaries – Spawning – Oocytes


1. Collette BB, Nauen CE. FAO species catalogue; Volume 2. Scombrids of the world. An annotated and illustrated catalogue of tunas, mackerels, bonitos and related species known to date; 1983.

2. ISC. 2018 Pacific Bluefin Tuna Stock Assessment; Report of the 18th meeting of the International Scientific Committee for Tuna and Tuna-Like Species in the North Pacific Ocean plenary session Annex 14; 2018.

3. Nakatsuka S, Ishida Y, Fukuda H, Akita T. A limit reference point to prevent recruitment overfishing of Pacific bluefin tuna. Mar Policy. 2017; 78: 107–113. doi: 10.1016/j.marpol.2017.01.017

4. Harford WJ, Karnauskas M, Walter JF, Liu H. Non-parametric modeling reveals environmental effects on bluefin tuna recruitment in Atlantic, Pacific, and Southern Oceans. Fish Oceanogr. 2017; 26: 396–412. doi: 10.1111/fog.12205

5. Ishida Y, Fukuda H, Fujioka K, Sakai O, Hiraoka Y, Oshima K, et al. Long-term changes in recruitment of age-0 Pacific bluefin tuna (Thunnus orientalis) and environmental conditions around Japan. Fish. Oceanogr. 2018; 27: 41–48. doi: 10.1111/fog.12232

6. Muhling BA Tommasi D, Ohshimo S, Alxander MA, Dinardo G. Regional-scale surface temperature variability allows prediction of Pacific bluefin tuna recruitment. ICES J Mar Sci. 2018; 75: 1341–1352. doi: 10.1093/icesjms/fsy017

7. Tanaka Y, Satoh K, Iwahashi M, Yamada H. Growth-dependent recruitment of Pacific bluefin tuna Thunnus orientalis in the northwestern Pacific Ocean. Mar Ecol Prog Ser. 2006; 319: 225–235. doi: 10.3354/meps319225

8. Watai M, Hiraoka Y, Ishihara T, Yamasaki I, Ota T, Ohshimo S, et al. Comparative analysis of the early growth history of Pacific bluefin tuna Thunnus orientalis from different spawning grounds. Mar Ecol Prog Ser. 2018; 607: 207–220. doi: 10.3354/meps12807

9. Watai M, Ishihara T, Abe O, Ohshimo S, Strussmann CA. Evaluation of growth-dependent survival during early stage of Pacific bluefin tuna using otolith microstructure analysis. Mar. Freshwat Res. 2017; 68: 2008–2017. doi: 10.1071/MF16337

10. Ohshimo S, Sato T, Okochi Y, Ishihara T, Tawa A, Kawazu M, et al. Long-term change in reproductive condition and evaluation of maternal effects in Pacific bluefin tuna, Thunnus orientalis, in the Sea of Japan. Fish Res. 2018; 204: 390–401. doi: 10.1016/j.fishres.2018.03.017

11. Tocher DR. Metabolism and functions of lipids and fatty acids in teleost fish Rev Fish Sci. 2003; 11: 107–184. doi: 10.1080/713610925

12. Sargent J. Origins and function of eggs lipids: Nutritional implication. In: Bomage NR, Roberts RJ, editors. Broodstock management and egg and larval quality. Oxford: Blackwell; 1995. pp. 353–372.

13. Wiegand MD. Composition, accumulation and utilization of yolk lipids in teleost fish. Rev Fish Biol Fish. 1996; 6: 259–286. doi: 10.1007/BF00122583

14. Fuiman LA, Ojanguren AF. Fatty acid content of eggs determines antipredator performance of fish larvae. J Exp Mar Biol Ecol. 2011; 407: 155–165. doi: 10.1016/j.jembe.2011.06.004

15. Furuita H, Tanaka H, Yamamoto T, Shiraishi M, Takeuchi T. Effects of n−3 HUFA levels in broodstock diet on the reproductive performance and egg and larval quality of the Japanese flounder, Paralichthys olivaceus. Aquaculture. 2000; 187: 387–398. doi: 10.1016/S0044-8486(00)00319-7

16. Hachero-Cruzado I, Olmo P, Sánchez B, Herrera M, Domingues P. Effects of two diets on lipid composition and reproductive performance of brill (Scophthalmus rhombus) eggs. Aquacult. Res. 2012; 43: 1439–1450. doi: 10.1111/j.1365-2109.2011.02946.x

17. Johnston T, Wiegand MD, Leggett WC, Pronyk RJ, Dyal SD, Watchorn KE, et al. 2007 Hatching success of walleye embryos in relation to maternal and ova characteristics. Ecol Freshwat Fish. 2007; 16: 295–306. doi: 10.1111/j.1600-0633.2006.00219.x

18. Perez K, Fuiman L. Maternal diet and larval diet influence survival skills of larval red drum Sciaenops ocellatus. J Fish Biol. 2015; 86: 1286–1304. doi: 10.1111/jfb.12637 25740661

19. Marshall CT, Yaragina NA, Lambert Y, Kjesbu OS. Total lipid energy as a proxy for total egg production by fish stocks. Nature. 1999; 402: 288. doi: 10.1038/46272

20. Wiegand M, Johnston TA, Leggett WC, Watchorn KE, Ballevona AJ, Porteous LR, et al. Contrasting strategies of ova lipid provisioning in relation to maternal characteristics in three walleye (Sander vitreus) populations. Can J Fish Aquat Sci. 2007; 64: 700–712. doi: 10.1139/f07-033

21. Zudaire I, Murua H, Grande M, Pernet F, Bodin N. Accumulation and mobilization of lipids in relation to reproduction of yellowfin tuna (Thunnus albacares) in the western Indian Ocean. Fish res. 2014; 160; 50–59. doi: 10.1016/j.fishres.2013.12.010

22. Fuiman LA, Perez KO. Metabolic programming mediated by an essential fatty acid alters body composition and survival skills of a marine fish. Proc R Soc B. 2015; 282: 20151414. doi: 10.1098/rspb.2015.1414 26582018

23. Rainuzzo JR, Reitan KI, Olsen Y. The significance of lipids at early stages of marine fish: a review. Aquaculture. 1997; 155: 103–115. doi: 10.1016/S0044-8486(97)00121-X

24. Ohshimo S, Tawa T, Ota T, Nishimoto S, Ishihara T, Watai M, et al. Horizontal distribution and habitat of Pacific bluefin tuna, Thunnus orientalis, larvae in the waters around Japan. Bull Mar Sci. 2017; 93: 769–787. doi: 10.5343/bms.2016.1094

25. Shimose T, Farley JH. Age, growth and reporductive biology of bluefin tunas. In: Kitagawa T, Kimura S editors. Biology and Ecology of Bluefin Tuna. London: CRC Press; 2015. pp. 47–77.

26. Ashida H, Suzuki N, Tanabe T, Suzuki N, Aonuma Y. Reproductive condition, batch fecundity, and spawning fraction of large Pacific bluefin tuna Thunnus orientalis landed at Ishigaki Island, Okinawa, Japan. Environ Biol Fishes. 2015; 98: 1173–1183. doi: 10.1007/s10641-014-0350-8

27. Shimose T, Aonuma Y, Suzuki N, Tanabe T. Sexual differences in the occurrence of Pacific bluefin tuna Thunnus orientalis in the spawning ground, Yaeyama Islands. Environ Biol Fishes. 2016; 99; 351–360. doi: 10.1007/s10641-016-0478-9

28. Yabe H, Ueyanagi S, Watanabe H. 1Studies on the early life history of bluefin tuna Thunnus thynnus and on the larva of the southern bluefin tuna T. maccoyii. Rep Nankai Reg Fish Res Lab. 1966; 23: 95–129.

29. Okochi Y, Abe O, Tanaka S, Ishihara Y, Shimizu A. Reproductive biology of female Pacific bluefin tuna, Thunnus orientalis, in the Sea of Japan. Fish Res. 2016; 174: 30–39. doi: 10.1016/j.fishres.2015.08.020

30. Matsumoto Y, Ando Y, Hiraoka Y, Tawa A, Ohshimo S. A simplified gas chromatographic fatty-acid analysis by the direct saponification/methylation procedure and its application on wild tuna larvae. Lipids. 2018; 53: 919–929. doi: 10.1002/lipd.12098 30411800

31. Ishihara T, Watai M, Ohshimo S, Abe O. Differences in larval growth of Pacifc bluefin tuna (Thunnus orientalis) between two spawning areas, and an evaluation of the growth dependent -mortality hypothesis. Environ Biol Fishes. 2019; 102: 581–194. doi: 10.1007/s10641-019-00855-w

32. Chen K-S, Crone P, Hsu C-C. Reproductive biology of female Pacific bluefin tuna Thunnus orientalis from south-western North Pacific Ocean. Fish Sci. 2006; 72: 985–994. doi: 10.1111/j.1444-2906.2006.01247.x

33. Bligh EG, Dyer WJ. A rapid method of total lipid extraction and purification. Can J Biochem Physiol. 1959; 37: 911–917. doi: 10.1139/o59-099 13671378

34. Olsen R, Henderson R. The rapid analysis of neutral and polar marine lipids using double-development HPTLC and scanning densitometry. J Exp Mar Biol Ecol. 1989; 129: 189–197. doi: 10.1016/0022-0981(89)90056-7

35. Baron CB, Coburn RF. Comparison of two copper reagents for detection of saturated and unsaturated neutral lipids by charring densitometry. J Liq Chromatogr. 1984; 7: 2793–2801. doi: 10.1080/01483918408067046

36. Anderson MJ. A new method for non-parametric multivariate analysis of variance. Austral Ecol. 2001; 26: 32–46. doi: 10.1111/j.1442-9993.2001.01070.pp.x

37. McArdle BH, Anderson MJ. Fitting multivariate models to community data: a comment on distance-based redundancy analysis. Ecology. 2001; 82: 290–297. doi: 10.1890/0012-9658(2001)082[0290:FMMTCD]2.0.CO;2

38. Team RC. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. 2016.

39. Johnson RB. Lipid deposition in oocytes of teleost fish during secondary oocyte growth. Rev Fish Sci. 2009; 17: 78–89. doi: 10.1080/10641260802590004

40. Dhurmeea Z, Pethybridge H, Appadoo C, Bodin N. Lipid and fatty acid dynamics in mature female albacore tuna (Thunnus alalunga) in the western Indian Ocean. PloS One. 2018; 13: e0194558. doi: 10.1371/journal.pone.0194558 29608623

41. Grande M, Murua H, Zudaire I, Arsenault-Pernet DJ, Pernet F, Bodin N. Energy allocation strategy of skipjack tuna Katsuwonus pelamis during their reproductive cycle. J Fish Biol. 2016; 89: 2434–2448. doi: 10.1111/jfb.13125 27730635

42. Mourente G, Megina C, Díaz-Salvago E. Lipids in female northern bluefin tuna (Thunnus thynnus thynnus L.) during sexual maturation. Fish Physiol Biochem. 2002; 24: 351–363. doi: 10.1023/A:1015011609017

43. Jusup M, Klanjscek T, Matsuda H, Kooijman S. A full lifecycle bioenergetic model for bluefin tuna. PLoS One. 2011; 6: e21903. doi: 10.1371/journal.pone.0021903 21779352

44. Aranda G, Abascal FJ, Varela JL, Medina A. Spawning behaviour and post-spawning migration patterns of Atlantic bluefin tuna (Thunnus thynnus) ascertained from satellite archival tags. PLoS One. 2013; 8: e76445. doi: 10.1371/journal.pone.0076445 24098502

45. Ohshimo S, Sato T, Okochi Y, Tanaka S, Ishihara T, Ashida H, et al. Evidence of spawning among Pacific bluefin tuna, Thunnus orientalis, in the Kuroshio and Kuroshio–Oyashio transition area. Aquat Living Resour. 2018; 31: 33. doi: 10.1051/alr/2018022

46. Masuma S, Tezuka N, Koiso M, Jinbo T, Takebe T, Yamazaki H, et al. Effects of water temperature on bluefin tuna spawning biology in captivity. Bull Fish Res Agen. 2006; 4 (Suppl): 157–171.

47. McBride RS, Somarakis S, Fitzhugh GR, Albert A, Yaragina NA, Wuenschel MJ, et al. Energy acquisition and allocation to egg production in relation to fish reproductive strategies. Fish Fish. 2015; 16: 23–57. doi: 10.1111/faf.12043

48. Stephens PA, Boyd IL, McNamara JM, Houston AI. Capital breeding and income breeding: their meaning, measurement, and worth. Ecology. 2009; 90: 2057–2067. doi: 10.1890/08-1369.1 19739368

49. Henderson BA, Wong JL, Nepszy SJ. Reproduction of walleye in Lake Erie: allocation of energy. Can J Fish Aquat Sci. 1996; 53: 127–133. doi: 10.1139/f94-099

50. Shimose T, Wells RJD. Feeding ecology of Blue fin Tunas. In: Kitagawa T, Kimura S, editors. Biology and Ecology of Bluefin Tuna. London: CRC Press; 2015. pp. 78–97.

51. Johnston TA, Leggett W. Maternal and environmental gradients in the egg size of an iteroparous fish. Ecology. 2002; 83: 1777–1791. doi: 10.1890/0012-9658(2002)083[1777:MAEGIT]2.0.CO;2

52. Lane RL, Kohler CC. Effects of dietary lipid and fatty acids on white bass reproductive performance, egg hatchability, and overall quality of progeny. N Am J Aquacult. 2006; 68: 141–150. doi: 10.1577/A05-009.1

53. Bell JG, Sargent JR. Arachidonic acid in aquaculture feeds: current status and future opportunities. Aquaculture. 2003; 218: 491–499. doi: 10.1016/S0044-8486(02)00370-8

54. Kitagawa T, Kato Y, Miller MJ, Sasai Y, Sasaki H, Kimura S. 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. 2010; 393: 23–31. doi: 10.1016/j.jembe.2010.06.016

55. Balon EK. Reproductive guilds of fishes: a proposal and definition. J Fish Board Can. 1975; 32: 821–864. doi: 10.1139/f75-110

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