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Fatty Acid Composition of Tropical Fish Depends on Reservoir Trophic Status and Fish Feeding Habit

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Lipids

Abstract

Eutrophication results in a deficiency of n-3 LC-PUFA (long-chain polyunsaturated fatty acids) in aquatic food chains, affecting fish nutrition and physiology. The trophic transfer of FA (fatty acids) to fish species of different feeding habits was investigated in two reservoirs in southeast Brazil—the mesotrophic Ponte Nova Reservoir (PN) and the hypereutrophic Billings Reservoir (Bil). Total FA profile of stomach contents and adipose tissue, triacylglycerols (TAG), and phospholipids (PL) from liver and muscle of the omnivorous Astyanax fasciatus and the carnivorous Hoplias malabaricus were analyzed by gas chromatography. A prevalence of n-6PUFA, as 18:2n-6 (linoleic acid) and 20:4n-6 (arachidonic acid, ARA) was observed in the stomach contents and in the tissues of A. fasciatus from the PN reservoir. In contrast, n-3 LC-PUFA, as 20:5n-3 (eicosapentaenoic acid, EPA) was accumulated in fish tissues from Bil, resulting in higher n3/n6 and EPA/ARA ratios, compared to fish from PN. This differential FA accumulation was also observed for H. malabaricus, but differences were slightly minor, and no changes were observed in the EPA/ARA ratios between fish from both reservoirs. Regardless reservoir, FA profiles of TAG resembled that of their diet, whereas FA profiles of PL were more conservative and mainly comprised by LC-PUFA. We conclude that reservoir trophic status affected the FA composition of food resources available to these fish species, resulting in differential allocation of n-3 and n-6 FA. As expected, FA profile of the investigated fish species also reflected their feeding habit and physiological demands.

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Abbreviations

18-PUFA:

Polyunsaturated fatty acid with 18 carbons

LC-PUFA:

Long-chain polyunsaturated fatty acid (with 20-22 carbons)

Af:

Astyanax fasciatus

ARA (20:4n-6):

Arachidonic acid

AT:

Adipose tissue

BFA:

Branched chain fatty acids

Bil:

Billings (hypereutrophic reservoir)

DHA (22:6n-3):

Docosahexaenoic acid

EPA (20:5n-3):

Eicosapentaenoic acid

FA:

Fatty acids

FAME:

Fatty acid metil-esters

Hm:

Hoplias malabaricus

HPL:

Hepatic phospholipids

HTAG:

Hepatic triacylglycerols

MPL:

Muscle phospholipids

MTAG:

Muscle triacylglycerols

MUFA:

Monounsaturated fatty acids

n-3:

Omega 3

n-6:

Omega 6

OFA:

Odd chain fatty acids

PL:

Phospholipids

PN:

Ponte Nova (mesotrophic reservoir)

PUFA:

Polyunsaturated fatty acids

SC:

Stomach content

SDA:

Stepwise discriminant analyses

SFA:

Saturated fatty acids

TAG:

Triacylglycerol

TSI:

Trophic state index

References

  1. 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 

  2. Müller-Navarra DC (2008) Food web paradigms: the biochemical view on trophic interactions. Int Rev Hydrobiol 93:489–505

    Article  Google Scholar 

  3. Bell MV, Tocher DR (2009) In: Arts MT, Brett MT, Kainz ME (eds) Lipids in aquatic ecosystems. Springer, New York

    Google Scholar 

  4. Vagner M, Santigosa E (2011) Characterization and modulation of gene expression and enzymatic activity of delta-6 desaturase in teleosts: a review. Aquaculture 315:131–143

    Article  CAS  Google Scholar 

  5. Parrish CC (2009) In: Arts MT, Brett MT, Kainz ME (eds) Lipids in aquatic ecosystems. Springer, New York

    Google Scholar 

  6. Ahlgren G, Gustafsson IB, Boberg M (1992) Fatty acid content and chemical composition of freshwater microalgae. J Phycol 28:37–50

    Article  CAS  Google Scholar 

  7. Brett MT, Müller-Navarra DC, Person J (2009) In: Arts MT, Brett MT, Kainz ME (eds) Lipids in Aquatic ecosystems. Springer, New York

    Google Scholar 

  8. Perhar G, Arhonditsis GB, Brett MT (2012) Modelling the role of highly unsaturated fatty acids in planktonic food web processes: a mechanistic approach. Environ Rev 20:155–172

    Article  Google Scholar 

  9. Arts MT, Brett MT, Kainz MJ (2009) Lipids in aquatic ecosystems. Springer, New York

    Google Scholar 

  10. Sargent JR, Tocher DR, Bell JG (2002) In: Halver JE, Hardy RW (eds) Fish nutrition, 3rd edn. Academic Press, London

  11. Tocher DR (2003) Metabolism and functions of lipids and fatty acids in teleost fish. Rev Fish Sci 11(2):107–184

    Article  CAS  Google Scholar 

  12. Wathes DC, Abayasekara RE, Aitken RJ (2007) Polyunsaturated fatty acids in male and female reproduction. Biol Reprod 77:190–201

    Article  CAS  PubMed  Google Scholar 

  13. Arts MT, Kohler CC (2009) In: Arts MT, Brett MT, Kainz ME (eds) Lipids in aquatic ecosystems. Springer, New York

    Google Scholar 

  14. Hurtado MA, Reza M, Ibarra AM, Wille M, Sorgeloos P, Soudant P, Palacios E (2009) Arachidonic acid (20:4n-6) effect on reproduction, immunology, and prostaglandin E2 levels in Crassostrea corteziensis (Hertlein, 1951). Aquaculture 294:300–305

    Article  CAS  Google Scholar 

  15. Stoknes IS, Økland HMW, Falch E, Synnes M (2004) Fatty acid and lipid class composition in eyes and brain from teleosts and elasmobranchs. Comp Biochem Physiol (B) 138:183–191

    Article  Google Scholar 

  16. Crockett EL, Londraville RL (2006) In: Evan DH, Claiborne JB (eds) The physiology of fish, 3rd edn. CRC Press, Florida

    Google Scholar 

  17. Kraffe E, Marty Y, Guderley H (2007) Changes in mitochondrial oxidative capacities during thermal acclimation of rainbow trout Oncorhynchus mykiss: roles of membrane proteins, phospholipids and their fatty acids composition. J Exp Biol 210:149–165

    Article  CAS  PubMed  Google Scholar 

  18. Ribeiro CS (2010) A influência térmica na regulação da expressão gênica e sua ação na dinâmica de membranas celulares. Rev Biol 4:6–9

    Google Scholar 

  19. Lister AL, Van Der Kraak GJ (2009) Regulation of prostaglandin synthesis in ovaries of sexually-mature zebrafish (Danio rerio). Mol Reprod Dev 76:1064–1075

    Article  CAS  PubMed  Google Scholar 

  20. Norambuena F, Mackenzie S, Bell JG, Callol A, Estévez A, Duncan N (2012) Prostaglandin (F and E, 2- and 3-series) production and cyclooxygenase (COX-2) gene expression of wild and cultured broodstock of senegalese sole (Solea senegalensis). Gen Comp Endocrinol 177:256–262

    Article  CAS  PubMed  Google Scholar 

  21. Knight OM, Van Der Kraak G (2015) The role of eicosanoids in 17α,20β-dihydroxy-4-pregnen-3-one induced ovulation and spawning in Danio rerio. Gen Comp Endocrinol 213:50–58

    Article  CAS  PubMed  Google Scholar 

  22. Koussoroplis AM, Bec A, Perga M, Koutrakis GB, Desvilettes C (2011) Fatty acids transfer in the food web of a coastal Mediterranean lagoon: evidence for high-arachidonic acid retention in fish. Estuar Coast Shelf Sci 91:450–461

    Article  CAS  Google Scholar 

  23. Nalepa TF, Fanslow DL, Foley AJ, Lang GA, Eadie BJ, Quigley MA (2006) Continued disappearance of the benthic amphipod Diporeia spp. in Lake Michigan: is there evidence for food limitation? Can J Fish Aqua Sci 63:872–890

    Article  CAS  Google Scholar 

  24. Müller-Navarra DC, Brett MT, Park S, Chandra S, Ballantyne AP, Zorita E, Goldman CR (2004) Unsaturated fatty acid content in seston and tropho-dynamic coupling in lakes. Nature 427:69–71

    Article  PubMed  Google Scholar 

  25. Persson J, Vrede T (2006) Polyunsaturated fatty acids in zooplankton: variation due to taxonomy and trophic position. Freshw Biol 51:887–900

    Article  CAS  Google Scholar 

  26. Ravet JL, Brett MT, Arhonditsis GB (2010) The effects of seston lipids on zooplankton fatty acids composition in lake Washington. Ecology 91:180–190

    Article  PubMed  Google Scholar 

  27. Burns CW, Brett MT, Schallenberg M (2011) A comparison of the trophic transfer of fatty acids in freshwater plankton by cladocerans and calanoid copepods. Freshw Biol 56:889–903

    Article  Google Scholar 

  28. Kainz M, Arts MT, Mazumder A (2004) Essential fatty acids in the planktonic food webs and their ecological role for higher trophic levels. Limnol Oceanogr 49(5):1784–1793

    Article  CAS  Google Scholar 

  29. Lau DC, Vrede T, Pickova J, Goedkoop W (2012) Fatty acid composition of consumers in boreal lakes—variation across species, space and time. Freshw Biol 57:24–28

    Article  CAS  Google Scholar 

  30. Razavi NR, Arts MT, Qu M, Jin B, Ren W, Wang Y, Campbell LM (2014) Effect of eutrophication on mercury, selenium and essential fatty acids in Bighead Carp (Hypophthalmichtys nobilis) from reservoirs of eastern China. Sci Total Environ 499:36–46

    Article  CAS  PubMed  Google Scholar 

  31. Strandberg U, Hiltunen M, Jelkanen E, Taipale SJ, Kainz MJ, Brett MT, Kakaala P (2015) Selective transfer of polyunsaturated fatty acids from phytoplankton to planktivorous fish in large boreal lakes. Sci Total Environ 536:858–865

    Article  CAS  PubMed  Google Scholar 

  32. Carvalho MC (2003) Comunidade fitoplanctônica como instrumento de biomonitoramento de reservatórios do Estado de São Paulo. PhD thesis. São Paulo University

  33. Monteiro-Júnior AJ (2006) Caracterização limnológica e compartimentalização do reservatório de Ponte Nova, Alto Tietê, SP—uma contribuição ao seu manejo. PhD Thesis. São Paulo University

  34. Sant’Anna C, Melcher SS, Carvalho MC, Gemelgo MP, Azevedo MTP (2007) Planktonic cyanobacteria from upper Tietê basin reservoirs, SP, Brazil. Rev Bras Bot 30(1):1–17

  35. Gomes AD, Tolussi CE, Ribeiro CS, Honji RM, Moreira RG (2014) The role of ovarian steroids in reproductive plasticity in Hoplias malabaricus (Teleostei: Characiformes: Erythrinidae) in tropical reservoirs with different degrees of pollution. Gen Comp Endocrinol 222:1–10

    Article  PubMed  Google Scholar 

  36. Moschini-Carlos VM, Freitas LG, Pompêo M (2010) Limnological evaluation of water in the Rio Grande and Taquacetuba branches of the Billings Complex (São Paulo, Brazil) and the management implications. Ambi-água 5(3):47–59

    Article  Google Scholar 

  37. Cortez TM (2013) Aspectos ecológicos e sua relação com o polimorfismo genético e a taxonomia convencional de cianobactérias da represa Billings. MSc Thesis, São Paulo University

  38. Marceniuk AP, Hilsdorf AWS (2010) Peixes das cabeceiras do Rio Tietê e Parque das Neblinas. Ócsso Design, São Paulo

    Google Scholar 

  39. Mariani CF, Pompêo MLM (2008) Potentially bioavailable metals in sediment from a tropical polymictic environment Rio Grande Reservoir, Brazil. J Soils Sediment 8:248–288

    Article  Google Scholar 

  40. Vilella FS, Becker FG, Hartz SM (2002) Diet of Astyanax species (Teleostei, Characidae) in an Atlantic Forest River in Southern Brazil. Braz Arch Biol Technol 42(2):223–232

    Article  Google Scholar 

  41. Gurgel HCB (2004) Estrutura populacional e época de reprodução de Astyanax fasciatus (Curvier) (Characidae, Tetragonopterinae) do Rio Ceará Mirim, Poço Branco, Rio Grande do Norte, Brasil. Rev Bras Zool 21(1):131–135

    Article  Google Scholar 

  42. Fowler HW (1950) Os peixes de água doce do Brasil. Arq Zool Estado de São Paulo 6:362–364

    Google Scholar 

  43. Godoy MP (1959) Age, growth, sexual maturity, behavior, migration, tagging and transplantation of curimbatá (Prochilodus scrofa Steindachner, 1881) of Mogi Guassú river, São Paulo State, Brazil. An Acad Bras Ciên 31:447–477

    Google Scholar 

  44. Oyakawa OT (2003) In: Reis RE, Kullander SO, Ferraris CJ, Jr (eds) Check list of the freshwater fishes of South and Central America, EDIPUCRS, Porto Alegre

  45. Folch J, Less M, Stanley GH (1957) A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226:497–503

    CAS  PubMed  Google Scholar 

  46. Parrish CC (1999) In: Arts MT, Wainman BC (eds) Lipids in freshwater ecosystems. Springer, New York

    Google Scholar 

  47. Yang Z (1995) Development of a gas chromatographic method for profiling neutral lipids in marine samples. MSc Thesis, Memorial University of Newfoundland

  48. Christie WW (2003) Lipids analysis. The Oily Press, Bridgwater

    Google Scholar 

  49. Budge SM, Iverson SJ, Koopman HN (2006) Studying trophic ecology in marine ecosystems using fatty acids: a primer on analysis and interpretation. Mar Mammal Sci 22:759–801

    Article  Google Scholar 

  50. CETESB (2008) Relatório da qualidade das águas interiores do Estado de São Paulo—2007. Companhia Ambiental do Estado de São Paulo. Secretaria do Meio Ambiente do Estado de São Paulo, São Paulo

  51. Matsumura-Tundisi T, Tundisi JG, Luzia AP, Degani RM (2010) Occurrence of Ceratium furcoides (Lenvander) Langhans 1925 bloom at the billings reservoir, São Paulo State, Brazil. Braz J Biol 70(3):825–829

    Article  CAS  PubMed  Google Scholar 

  52. Napolitano GE (1999) In: Arts MT, Wainman BC (eds) Lipids in freshwater ecosystems. Springer, New York

    Google Scholar 

  53. Boëchat IG, Adrian R (2005) Biochemical composition of algivorous freshwater ciliates: you are not what you eat. FEMS Microbiol Ecol 53:393–400

    Article  PubMed  Google Scholar 

  54. Sendacz S, Caleffi S, Santos-Soares J (2006) Zooplankton biomass of reservoir in diferente trophic conditions in the state of São Paulo, Brazil. Braz J Biol 66(1B):337–350

    Article  CAS  PubMed  Google Scholar 

  55. Parrish CC, Abrajano TA, Budge SM, Helleur RJ, Hudson ED, Pulchan K, Ramos C (2000) In: Wangersky PJ (ed) Marine chemistry. Springer-Verlag, New York

  56. Gladyshev MI, Arts MT, Sushchik NN (2009) In: Arts MT, Brett MT, Kainz M (eds) Lipids in aquatic ecosystems. Springer, New York

    Google Scholar 

  57. Henderson RJ, Tocher DR (1987) The lipid composition and biochemistry of freshwater fish. Prog Lipid Res 26:281–347

    Article  CAS  PubMed  Google Scholar 

  58. Ackman RG (1999) In: Arts MT, Wainman BC (eds) Lipids in freshwater ecosystem. Springer, New York

    Google Scholar 

  59. Hessen DO, Leu E (2006) Trophic transfer and trophic modification of fatty acids in high Arctic lakes. Freshw Biol 51:1987–1998

    Article  CAS  Google Scholar 

  60. Sargent JR (1995) In: Bromage NR, Robert RJ (eds) Broodstock managements and egg and larval quality. Blackweel Sci, Cambridge

    Google Scholar 

  61. Turchini GM, Torstensen BE, Ng W (2009) Fish oil replacement in finfish nutrition. Rev Aquacult 1:10–57

    Article  Google Scholar 

  62. Khozin-Goldberg I, Cohen Z, Pimenta-Leibowitz M, Nechev J, Zilberg D (2006) Feeding with arachidonic acid-rich triacylglycerol from the microalgae Parietochloris incisa improved recovery of guppies from infection with Tetrahymena sp. Aquaculture 255:142–150

    Article  CAS  Google Scholar 

  63. Xu H, Ai Q, Mai K, Xu W, Wang J, Ma H, Zhang W, Wang X, Liufu Z (2010) Effects of dietary arachidonic acid on growth performance, survival, immune response and tissue fatty acid composition of juvenile Japanese seabass, Lateolabrax japonicas. Aquaculture 307:75–82

    Article  CAS  Google Scholar 

  64. Henrotte E, Milla S, Mandiki SNM, Kestemont P (2011) Arachidonic acid induces production of 17α, 20β-dihydroxy-4-pregnen-3-one (DHP) via a putative PGE2 receptor in fish follicles from the Eurasian perch. Lipids 46:179–187

    Article  CAS  PubMed  Google Scholar 

  65. Lall SP (2000) In: Cruz-Suárez, Ricque-Marie D, Tapia-Salazar M, Olvera-Novoa MA, Civera-Cerecedo R (eds) Advances en Nutrición Acuícola, Memorias del V Simposium Internacional de Nutrición Acuícola, Mérida, Yucatán, Mexico

  66. Alhgren G, Sonesten L, Boberg M, Gustafon IB (1996) Fatty acid content of some freshwater fish in lakes of different trophic levels—a bottom-up effect? Ecol Freshw Fish 5:15–27

    Article  Google Scholar 

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Acknowledgments

The present study was funded by the Fundação de Incentivo à Pesquisa do Estado de São Paulo (FAPESP) (Research Grant: 2012/50371-2; Ph.D. scholarship: 2010/50555-0) and by the Comissão de Aperfeiçoamento de Pessoal do Nível Superior (CAPES). The authors would like to thank the fishermen Evaldo Bizarrias and Milton Nunes de Santana and the LAMEROA team, for their help in fish collection, and IB/USP for providing logistics and facilities for collection.

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Authors and Affiliations

  1. Departamento de Fisiologia do Instituto de Biociências, Universidade de São Paulo, Rua do Matão, Trav. 14, 321, São Paulo, SP, 05508-090, Brazil

    Aline D. Gomes, Carlos E. Tolussi, Renato M. Honji & Renata G. Moreira

  2. Departamento de Geociências, Universidade Federal de São João Del Rei, São João Del Rei, MG, Brazil

    Iola G. Boëchat

  3. Departamento de Ecologia do Instituto de Biociências, Universidade de São Paulo, São Paulo, SP, Brazil

    Marcelo L. M. Pompêo & Maíra P. T. Cortez

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  1. Aline D. Gomes
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  2. Carlos E. Tolussi
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  3. Iola G. Boëchat
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  4. Marcelo L. M. Pompêo
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  5. Maíra P. T. Cortez
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  6. Renato M. Honji
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  7. Renata G. Moreira
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Correspondence to Aline D. Gomes.

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Gomes, A.D., Tolussi, C.E., Boëchat, I.G. et al. Fatty Acid Composition of Tropical Fish Depends on Reservoir Trophic Status and Fish Feeding Habit. Lipids 51, 1193–1206 (2016). https://doi.org/10.1007/s11745-016-4196-z

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