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High Arachidonic Acid Levels in the Tissues of Herbivorous Fish Species (Siganus fuscescens, Calotomus japonicus and Kyphosus bigibbus)

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Lipids

Abstract

The lipid and fatty acid compositions in the various organs (muscle, liver, other viscera) and stomach contents of three common herbivorous fish species in Japan, Siganus fuscescens, Calotomus japonicus and Kyphosus bigibbus, were examined to explore the stable 20:4n-6 (arachidonic acid, ARA) sources. Triacylglycerol (TAG), phosphatidylethanolamine (PtdEtn), and phosphatidylcholine (PtdCho) were the dominant lipid classes, while the major FA contents were 16:0, 18:1n-9, 16:1n-7, 14:0, 18:0, 18:1n-7, and some PUFA, including ARA, 20:5n-3 (eicosapentaenoic acid, EPA), 22:5n-3 (docosapentaenoic acid, DPA), and 22:6n-3 (docosahexaenoic acid, DHA). The amounts of these fatty acids were varied among species and their lipid classes. Phospholipids contained higher levels of PUFA than TAG. However, ARA in both phospholipids and TAG was markedly present in the muscle and viscera of all specimens, particularly in C. japonicus and K. bigibbus. Moreover, their ARA levels were higher than the levels of DHA and EPA. The observed high ARA level is unusual in marine fish and might be characteristic of herbivorous fish. Furthermore, ARA was the dominant PUFA in the stomach contents of the three species, suggesting that the high ARA level originated from their food sources. The above indicates that these three herbivorous fishes are ARA-rich marine foods and have potential utilization as stable ARA resources.

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Abbreviations

ARA:

Arachidonic acid

DAG:

Diacylglycerols

C:

Cholesterols

CE:

Cholesteryl esters

DHA:

Docosahexaenoic acid

DPA:

Docosapentaenoic acid

DMOX:

4, 4-Dimethyloxazoline derivatives

EPA:

Eicosapentaenoic acid

FA:

Fatty acid(s)

FFA:

Free fatty acid(s)

GC/MS:

Gas chromatography/mass spectroscopy

HUFA:

Highly unsaturated fatty acid(s)

MUFA:

Monounsaturated fatty acid(s) (monounsaturates)

NL:

Neutral lipids

OPL:

Other minor phospholipids

PtdCho:

Phosphatidylcholine

PtdEtn:

Phosphatidylethanolamine

PL:

Polar lipid(s)

PUFA:

Polyunsaturated fatty acid

SFA:

Saturated fatty acid(s) (saturates)

TAG:

Triacylglycerol(s)

TFA:

Total fatty acids

TL:

Total lipids

WE:

Wax esters

References

  1. Zyriax B-C, Windler E (2000) Dietary fat in the prevention of cardiovascular disease—a review. Eur J Lipid Sci Technol 102:355–365

    Article  CAS  Google Scholar 

  2. Hooper L, Summerbell CD, Higgins JPT et al (2001) Dietary fat intake and prevention of cardiovascular disease: systematic review. BMJ 322:757–763

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Villa B, Calabresi L, Chiesa G et al (2002) Omega-3 fatty acid ethyl esters increase heart rate variability in patients with coronary disease. Pharmacol Res 45:475–478

    Article  CAS  PubMed  Google Scholar 

  4. Kobatake Y, Kuroda K, Jinnouchi H et al (1984) Differential effects of dietary eicosapentaenoic and docosahexaenoic fatty acids on lowering of triglyceride and cholesterol levels in the serum of rats on hypercholesterolemic diet. J Nutr Sci Vitaminol (Tokyo) 30:357–372

    Article  CAS  Google Scholar 

  5. Jensen CL (2006) Effects of n-3 fatty acids during pregnancy and lactation. Am J Clin Nutr 83:S1452–S1457

    Google Scholar 

  6. Suzuki H, Park SJ, Tamura M, Ando S (1998) Effect of the long-term feeding of dietary lipids on the learning ability, fatty acid composition of brain stem phospholipids and synaptic membrane fluidity in adult mice: a comparison of sardine oil diet with palm oil diet. Mech Ageing Dev 101:119–128

    Article  CAS  PubMed  Google Scholar 

  7. Yonekubo A, Honda S, Okano M et al (1994) Effects of dietary fish oil during the fetal and postnatal periods on the learning ability of postnatal rats. Biosci Biotechnol Biochem 58:799–801

    Article  CAS  Google Scholar 

  8. Birch EE, Hoffman DR, Uauy R et al (1998) Visual acuity and the essentiality of docosahexaenoic acid and arachidonic acid in the diet of term infants. Pediatr Res 44:201–209

    Article  CAS  PubMed  Google Scholar 

  9. Uauy R, Hoffman DR, Mena P et al (2003) Term infant studies of DHA and ARA supplementation on neurodevelopment: results of randomized controlled trials. J Pediatr 143:17–25

    Article  Google Scholar 

  10. Codex Alimentarius Commission (1981) Standard for infant formula and formulas for special medical purposes intended for infants. CODEX STAN 72–1981:revision 2007

  11. Hadley KB, Ryan AS, Forsyth S et al (2016) The essentiality of arachidonic acid in infant development. Nutrients 8:1–47

    Article  Google Scholar 

  12. Katsuki H, Okuda S (1995) Arachidonic acid as a neurotoxic and neurotrophic substance. Prog Neurobiol 46:607–636

    Article  CAS  PubMed  Google Scholar 

  13. Calder PC (2003) n-3 Polyunsaturated fatty acids and inflammation: from molecular biology to the clinic. Lipids 38:343–352

    Article  CAS  PubMed  Google Scholar 

  14. Calder PC (2006) n-3 Polyunsaturated fatty acids, inflammation, and inflammatory diseases. Am J Clin Nutr 83:1505s–1519s

    CAS  PubMed  Google Scholar 

  15. Samuelsson B (1991) Arachidonic acid metabolism: role in inflammation. Z Rheumatol 50(Suppl 1):3–6

    PubMed  Google Scholar 

  16. Koletzko B, Schmidt E, Bremer HJ et al (1989) Effects of dietary long-chain polyunsaturated fatty acids on the essential fatty acid status of premature infants. Eur J Pediatr 148:669–675

    Article  CAS  PubMed  Google Scholar 

  17. Field CJ, Clandinin MT, Van Aerde JE (2001) Polyunsaturated fatty acids and T-cell function: implications for the neonate. Lipids 36:1025–1032

    Article  CAS  PubMed  Google Scholar 

  18. Kolakowska A, Olley J, Dunstan GA (2002) Fish Lipids. In: Sikorski ZE, Kolakowska A (eds) Chem. Funct. Prop. Food Lipids. CRC Press LLC, Boca Raton, pp 221–264

    Google Scholar 

  19. Ephrime Bicoy M, Anna Arlene A-E (2014) Fatty acids in six small pelagic fish species and their crustacean prey from the Mindanao sea, Southern Philippines. Trop life Sci Res 25:105–115

    Google Scholar 

  20. Osman H, Suriah A, Law E (2001) Fatty acid composition and cholesterol content of selected marine fish in Malaysian waters. Food Chem 73:55–60

    Article  CAS  Google Scholar 

  21. Osako K, Saito H, Hossain MA et al (2006) Docosahexaenoic acid levels in the lipids of spotted mackerel Scomber australasicus. Lipids 41:713–720

    Article  CAS  PubMed  Google Scholar 

  22. Saito H, Yamashiro R, Alasalvar C, Konno T (1999) Influence of diet on fatty acids of three subtropical fish, subfamily Caesioninae (Caesio diagramma and C. tile) and Family Siganidae (Siganus canaliculatus). Lipids 34:1073–1082

    Article  CAS  PubMed  Google Scholar 

  23. Saito H, Ishihara K, Murase T (1997) The fatty acid composition in tuna (Bonito, Euthynnus pelamis) caught at three different localities from tropics to temperate. J Sci Food Agric 73:53–59

    Article  CAS  Google Scholar 

  24. Takagi T, Asahi M, Itabashi Y (1985) Fatty acid composition of twelve algae from Japanese waters. Yukagaku 34:1008–1012

    CAS  Google Scholar 

  25. Khotimchenko SV (1991) Fatty acid composition of seven Sargassum species. Phytochemistry 30:2639–2641

    Article  CAS  Google Scholar 

  26. Mateos HT, Lewandowski PA, Su XQ (2010) Seasonal variations of total lipid and fatty acid contents in muscle, gonad and digestive glands of farmed Jade Tiger hybrid abalone in Australia. Food Chem 123:436–441

    Article  CAS  Google Scholar 

  27. Kraffe E, Soudant P, Marty Y (2004) Fatty acids of serine, ethanolamine, and choline plasmalogens in some marine bivalves. Lipids 39:59–66

    Article  CAS  PubMed  Google Scholar 

  28. Oksuz A (2010) Element compositions, fatty acid profiles, and proximate compositions of marbled spinefoot (Siganus rivulatus, Forsskal, 1775) and dusky spinefoot (Siganus luridus, Ruppell, 1878). J Fish 4:177–183

    CAS  Google Scholar 

  29. Fogerty AC, Evans AJ, Ford GL, Kennett BH (1986) Distribution of omega 6 and omega 3 fatty acids in lipid classes in Australian fish. Nutr Rep Int 33:777–786

    CAS  Google Scholar 

  30. Sinclair AJ, Naughton JM, O’Dea K (1983) Elevated levels of arachidonic acid in fish from northern Australia coastal waters. Lipids 18:877–881

    Article  CAS  PubMed  Google Scholar 

  31. Dunstan GA, Sinclair AJ, O’Dea K, Naughton JM (1988) The lipid content and fatty acid composition of various marine species from southern Australian coastal waters. Comp Biochem Physiol Part B Comp Biochem 91:165–169

    Article  Google Scholar 

  32. Saito H (2014) Lipid characteristics of five epinephelinae fishes, Epinephelus fasciatus, Epinephelus retouti, Cephalopholis aurantia, Cephalopholis miniatus, and Variola louti, in the Coral Reef. J Oleo Sci 63:471–484

    Article  CAS  PubMed  Google Scholar 

  33. Fujita D (2010) Current status and problems of isoyake in Japan. Bull Fish Res Agen 32:33–42

    Google Scholar 

  34. Yamaguchi A (2010) Biological aspects of herbivorous fishes in the coastal areas of western Japan. Bull Fish Res Agen 32:89–94

    Google Scholar 

  35. Vergés A, Steinberg PD, Hay ME et al (2014) The tropicalization of temperate marine ecosystems: climate-mediated changes in herbivory and community phase shifts. Proc R Soc B 281:1–10

    Article  Google Scholar 

  36. Kuhawara H, Hashimoto O, Sato A, Fujita D (2010) Introduction of isoyake recovery guideline. Bull Fish Res Agency 32:51–60

    Google Scholar 

  37. Osako K, Saito H, Kuwahara K, Okamoto A (2006) Year-round high arachidonic acid levels in herbivorous rabbit fish Siganus fuscescens tissues. Lipids 41:473–489

    Article  CAS  PubMed  Google Scholar 

  38. Folch J, Less M, Stanley GH (1957) A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226:497–509

    CAS  PubMed  Google Scholar 

  39. Saito H (2004) Lipid and FA composition of the pearl oyster Pinctada fucata martensii: influence of season and maturation. Lipids 39:997–1005

    Article  CAS  PubMed  Google Scholar 

  40. Osako K, Kuwahara K, Saito H et al (2003) Effect of starvation on lipid metabolism and stability of dha content of lipids in horse mackerel (Trachurus japonicus) tissues. Lipids 38:1263–1267

    Article  CAS  PubMed  Google Scholar 

  41. Yu QT, Liu BN, Zhang JY, Huang ZH (1989) Location of double bonds in fatty acids of fish oil and rat testis lipids. Gas chromatography–mass spectrometry of the oxazoline derivatives. Lipids 24:79–83

    Article  CAS  PubMed  Google Scholar 

  42. Ackman RG (1994) Seafoods: chemistry, processing technology and quality. In: Shahidi F, Botta JR (eds) Springer. US, Boston, pp 34–48

    Google Scholar 

  43. Ando S, Mori Y, Nakamura K, Sugawara A (1993) Characteristics of lipid accumulation types in five species of fish. Nippon Suisan Gakkaishi 59:1559–1564

    Article  CAS  Google Scholar 

  44. Takama K, Suzuki T, Yoshida K et al (1994) Lipid content and fatty acid composition of phospholipids in white-flesh fish species. Fish Sci 60:177–184

    CAS  Google Scholar 

  45. Osako K, Saito H, Weng W et al (2009) Lipid characteristics of coastal migratory Sarda orientalis tissues. Fish Sci 75:1055–1066

    Article  CAS  Google Scholar 

  46. Hazel JR, Eugene Williams E (1990) The role of alterations in membrane lipid composition in enabling physiological adaptation of organisms to their physical environment. Prog Lipid Res 29:167–227

    Article  CAS  PubMed  Google Scholar 

  47. Sargent J, McEvoy L, Estevez A et al (1999) Lipid nutrition of marine fish during early development: current status and future directions. Aquaculture 179:217–229

    Article  CAS  Google Scholar 

  48. Kanazawa A, Teshima S, Ono K (1979) Relationship between essential fatty acid requirements of aquatic animals and the capacity for bioconversion of linolenic acid to highly unsaturated fatty acids. Comp Biochem Physiol B 63:295–298

    CAS  PubMed  Google Scholar 

  49. Visentainer JV, Noffs MD, Oliveira Carvalho P et al (2007) Lipid content and fatty acid composition of 15 marine fish species from the Southeast Coast of Brazil. J Am Oil Chem Soc 84:543–547

    Article  CAS  Google Scholar 

  50. Arts MT, Ackman RG, Holub BJ (2001) “Essential fatty acids” in aquatic ecosystems: a crucial link between diet and human health and evolution. Can J Fish Aquat Sci 58:122–137

    Article  CAS  Google Scholar 

  51. Nelson MM, Leighton DL, Phleger CF, Nichols PD (2002) Comparison of growth and lipid composition in the green abalone, Haliotis fulgens, provided specific macroalgal diets. Comp Biochem Physiol Part B Biochem Mol Biol 131:695–712

    Article  Google Scholar 

  52. Saito H, Okabe M (2012) Characteristics of lipid composition differences between cultured and wild ayu (Plecoglossus altivelis). Food Chem 131:1104–1115

    Article  CAS  Google Scholar 

  53. Ogata HY, Emata AC, Garibay ES, Furuita H (2004) Fatty acid composition of five candidate aquaculture species in Central Philippines. Aquaculture 236:361–375

    Article  CAS  Google Scholar 

  54. Suloma A, Ogata HY (2011) Arachidonic acid is a major component in gonadal fatty acids of tropical coral reef fish in the Philippines and Japan. J Aquac Res Dev 2:1–7

    Article  Google Scholar 

  55. Osako K, Yamaguchi A (2003) Seasonal variation in docosahexaenoic acid content in horse mackerel caught in the East China Sea. Fish Sci 69:589–596

    Article  CAS  Google Scholar 

  56. Aidos I, van der Padt A, Luten JB, Boom RM (2002) Seasonal changes in crude and lipid composition of herring fillets, byproducts, and respective produced oils. J Agric Food Chem 50:4589–4599

    Article  CAS  PubMed  Google Scholar 

  57. Akpinar MA, Görgün S, Akpinar AE (2009) A comparative analysis of the fatty acid profiles in the liver and muscles of male and female Salmo trutta macrostigma. Food Chem 112:6–8

    Article  CAS  Google Scholar 

  58. Brett MT, Muller-Navarra DC (1997) The role of highly unsaturated fatty acids in aquatic food web processes. Freshw Biol 38:483–499

    Article  CAS  Google Scholar 

  59. Noda M, Kitayama K, Arai S (2002) Natural food of the Adult-Stage Rabbitfish Siganus fuscescens in autumn and spring at Futoi Island in the sea of Hibiki. Fish Eng 39:5–13

    Google Scholar 

  60. Noda M, Ohara H, Urakawa K et al (2011) Diet and prey availability of Siganus fuscescens occurring in a Sargassum bed at Futaoi Island in the Sea of Hibiki with respect to feeding on large brown macroalgae. Nippon Suisan Gakkaishi 77:1008–1019

    Article  Google Scholar 

  61. Kiriyama T, Fujii A, Fujita Y (2005) Feeding and characteristic bite marks on sargassum fusiforme by several herbivorous fishes. Aquac Sci 53:355–365

    Google Scholar 

  62. Yatsuya K, Kiyomoto S, Yoshimura T (2015) Seasonal changes in dietary composition of the herbivorous fish Kyphosus bigibbus in southwestern Japan. Fish Sci 81:1025–1033

    Article  CAS  Google Scholar 

  63. Horn MH (1989) Biology of marine herbivorous fishes. In: Barnes H (ed) CRC Press, Florida, US, pp 167–272

  64. Kume G, Kubo Y, Yoshimura T et al (2010) Life history characteristics of the protogynous parrotfish Calotomus japonicus from northwest Kyushu, Japan. Ichthyol Res 57:113–120

    Article  Google Scholar 

  65. Bell JG, Tocher DR, Sargent JR (1994) Effect of supplementation with 20:3(n-6), 20:4(n-6) and 20:5(n-3) on the production of prostaglandins E and F of the 1-, 2- and 3-series in turbot (Scophthalmus maximus) brain astroglial cells in primary culture. Biochim Biophys Acta 1211:335–342

    Article  CAS  PubMed  Google Scholar 

  66. Bessonart M, Izquierdo MS, Salhi M et al (1999) Effect of dietary arachidonic acid levels on growth and survival of gilthead sea bream (Sparus aurata L.) larvae. Aquaculture 179:265–275

    Article  CAS  Google Scholar 

  67. Sargent JR, Bell JG, Bell MV, et al. (2013) The metabolism of phospholipids and polyunsaturated fatty acids in fish. In: Lahlou B, Vitiello P (eds) American Geophysical Union, Washington DC, US, pp 103–124

  68. Fernández-Palacios H, Izquierdo MS, Robaina L et al (1995) Effect of n-3 HUFA level in broodstock diets on egg quality of gilthead sea bream (Sparus aurata L.). Aquaculture 132:325–337

    Article  Google Scholar 

  69. Sargent J, Bell G, McEvoy L et al (1999) Recent developments in the essential fatty acid nutrition of fish. Aquaculture 177:191–199

    Article  CAS  Google Scholar 

  70. Koven W, Barr Y, Lutzky S et al (2001) The effect of dietary arachidonic acid (20:4n-6) on growth, survival and resistance to handling stress in gilthead seabream (Sparus aurata) larvae. Aquaculture 193:107–122

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Food Science and Technology, Tokyo University of Marine Science and Technology, 4-5-7, Konan, Minato-ku, Tokyo, 108-8477, Japan

    Asada Jiarpinijnun, Junichiro Shibata, Emiko Okazaki & Kazufumi Osako

  2. Prince of Songkla University, Hat Yai, Songkhla, 90112, Thailand

    Soottawat Benjakul

  3. CPF (Thailand) Public Company Limited, C.P. Tower, 313 Silom Road, Bangrak, Bangkok, 10500, Thailand

    Akasith Pornphatdetaudom

Authors
  1. Asada Jiarpinijnun
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  2. Soottawat Benjakul
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  3. Akasith Pornphatdetaudom
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  4. Junichiro Shibata
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  5. Emiko Okazaki
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  6. Kazufumi Osako
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Correspondence to Kazufumi Osako.

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Jiarpinijnun, A., Benjakul, S., Pornphatdetaudom, A. et al. High Arachidonic Acid Levels in the Tissues of Herbivorous Fish Species (Siganus fuscescens, Calotomus japonicus and Kyphosus bigibbus). Lipids 52, 363–373 (2017). https://doi.org/10.1007/s11745-017-4244-3

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