Severe thiamine deficiency in eastern Baltic cod (Gadus morhua)


Autoři: Josefin Engelhardt aff001;  Oscar Frisell aff001;  Hanna Gustavsson aff001;  Tomas Hansson aff001;  Rajlie Sjöberg aff002;  Tracy K. Collier aff003;  Lennart Balk aff001
Působiště autorů: Department of Environmental Science and Analytical Chemistry, Stockholm University, Stockholm, Sweden aff001;  Institute of Marine Research, Swedish University of Agricultural Sciences, Lysekil, Sweden aff002;  Huxley College of the Environment, Western Washington University, Bellingham, Washington, United States of America aff003
Vyšlo v časopise: PLoS ONE 15(1)
Kategorie: Research Article
doi: 10.1371/journal.pone.0227201

Souhrn

The eastern Baltic cod (Gadus morhua) population has been decreasing in the Baltic Sea for at least 30 years. Condition indices of the Baltic cod have decreased, and previous studies have suggested that this might be due to overfishing, predation, lower dissolved oxygen or changes in salinity. However, numerous studies from the Baltic Sea have demonstrated an ongoing thiamine deficiency in several animal classes, both invertebrates and vertebrates. The thiamine status of the eastern Baltic cod was investigated to determine if thiamine deficiency might be a factor in ongoing population declines. Thiamine concentrations were determined by chemical analyses of thiamine, thiamine monophosphate and thiamine diphosphate (combined SumT) in the liver using high performance liquid chromatography. Biochemical analyses measured the activity of the thiamine diphosphate-dependent enzyme transketolase to determine the proportion of apoenzymes in both liver and brain tissue. These biochemical analyses showed that 77% of the cod were thiamine deficient in the liver, of which 13% had a severe thiamine deficiency (i.e. 25% transketolase enzymes lacked thiamine diphosphate). The brain tissue of 77% of the cod showed thiamine deficiency, of which 64% showed severe thiamine deficiency. The thiamine deficiency biomarkers were investigated to find correlations to different biological parameters, such as length, weight, otolith weight, age (annuli counting) and different organ weights. The results suggested that thiamine deficiency increased with age. The SumT concentration ranged between 2.4–24 nmol/g in the liver, where the specimens with heavier otoliths had lower values of SumT (P = 0.0031). Of the cod sampled, only 2% of the specimens had a Fulton’s condition factor indicating a healthy specimen, and 49% had a condition factor below 0.8, indicating poor health status. These results, showing a severe thiamine deficiency in eastern Baltic cod from the only known area where spawning presently occurs for this species, are of grave concern.

Klíčová slova:

Baltic Sea – Biochemical analysis – Cod – Eels – Gonads – Otolith – Spawning – Thiamine


Zdroje

1. Goyer A. Thiamine in plants: aspects of its metabolism and functions. Phytochemistry. 2010 Oct;71(14–15):1615–24. doi: 10.1016/j.phytochem.2010.06.022 20655074

2. Bellyei S, Szigeti A, Boronkai A, Szabo Z, Bene J, Janaky T, et al. Cloning, sequencing, structural and molecular biological characterization of placental protein 20 (PP20)/human thiamin pyrophosphokinase (hTPK). Placenta. 2005 Jan;26(1):34–46. doi: 10.1016/j.placenta.2004.03.008 15664409

3. Harper AE, Miller R, Block KP. Branched-chain amino acid metabolism. Annu Rev Nutr. 1984 Jul;4(1):409–54.

4. Navarro D, Zwingmann C, Butterworth RF. Impaired oxidation of branched-chain amino acids in the medial thalamus of thiamine-deficient rats. Metab Brain Dis. 2008 Dec;23(4):445–55. doi: 10.1007/s11011-008-9105-6 18773288

5. Foulon V, Antonenkov VD, Croes K, Waelkens E, Mannaerts GP, Van Veldhoven PP, et al. Purification, molecular cloning, and expression of 2-hydroxyphytanoyl-CoA lyase, a peroxisomal thiamine pyrophosphate-dependent enzyme that catalyzes the carbon-carbon bond cleavage during α-oxidation of 3-methyl-branched fatty acids. PNAS. 1999 Aug;96(18):10039–44. doi: 10.1073/pnas.96.18.10039 10468558

6. Sniekers M, Foulon V, Mannaerts GP, Van Maldergem L, Mandel H, Gelb BD, et al. Thiamine pyrophosphate: An essential cofactor for the α-oxidation in mammals—implications for thiamine deficiencies? Cell Mol Life Sci. 2006 Jul;63(13):1553–63. doi: 10.1007/s00018-005-5603-4 16786225

7. Lehninger AL, Nelson DL, Cox MM. Principles of biochemistry. 5th ed. San Francisco: W.H. Freeman; 2005.

8. Nilsson U, Meshalkina L, Lindqvist Y, Schneider G. Examination of substrate binding in thiamin diphosphate-dependent transketolase by protein crystallography and site-directed mutagenesis. J Biol Chem. 1997 Jan;272(3):1864–9. doi: 10.1074/jbc.272.3.1864 8999873

9. Berg JM, Tymoczko JL, Stryer L. Biochemistry. 7th ed. New York: W.H. Freeman; 2012.

10. Wieland OH. The mammalian pyruvate dehydrogenase complex: structure and regulation. Rev Physiol Biochem Pharmacol. 1983; 96:123–70. doi: 10.1007/bfb0031008 6338572

11. Arjunan P, Nemeria N, Brunskill A, Chandrasekhar K, Sax M, Yan Y, et al. Structure of the pyruvate dehydrogenase multienzyme complex E1 component from Escherichia coli at 1.85 Å resolution. Biochemistry. 2002 Apr;41(16):5213–21. doi: 10.1021/bi0118557 11955070

12. Hamada S, Hirashima H, Imaeda M, Okamoto Y, Hamaguchi-Hamada K, Kurumata-Shigeto M. Thiamine deficiency induces massive cell death in the olfactory bulbs of mice. J Neuropathol Exp Neurol. 2013 Dec;72(12):1193–202. doi: 10.1097/NEN.0000000000000017 24226264

13. Butterworth RF, Giguère JF, Besnard AM. Activities of thiamine-dependent enzymes in two experimental models of thiamine-deficiency encephalopathy 2. α-ketoglutarate dehydrogenase. Neurochem Res. 1986 Apr;11(4):567–77. doi: 10.1007/bf00965326 3724963

14. Lai JC, Cooper AJ. Brain α-ketoglutarate dehydrogenase complex: kinetic properties, regional distribution, and effects of inhibitors. J Neurochem. 1986 Nov;47(5):1376–86. doi: 10.1111/j.1471-4159.1986.tb00768.x 3760866

15. Åkerman G, Balk L. Descriptive studies of mortality and morphological disorders in early life stages of cod and salmon originating from the Baltic Sea. Am Fish Soc Symp. 1998;21:41–61.

16. Balk L, Hägerroth P-Å, Åkerman G, Hanson M, Tjärnlund U, Hansson T, et al. Wild birds of declining European species are dying from a thiamine deficiency syndrome. Proc Natl Acad Sci. 2009 Jul;106(29):12001–6. doi: 10.1073/pnas.0902903106 19597145

17. Balaghi M, Pearson WN. Tissue and intracellular distribution of radioactive thiamine in normal and thiamine-deficient rats. J Nutr. 1966 Jun;89(2):127–32. doi: 10.1093/jn/89.2.127 5947519

18. Shangari N, Bruce WR, Poon R, O’brien PJ. Toxicity of glyoxals—role of oxidative stress, metabolic detoxification and thiamine deficiency. Biochem Soc Trans. 2003 Dec;31(6):1390–3.

19. Campbell C. The severe lactic acidosis of thiamine deficiency: acute pernicious or fulminating beriberi. The Lancet. 1984 Aug;324(8400):446–9.

20. Schönfeld P, Struy H. Refsum disease diagnostic marker phytanic acid alters the physical state of membrane proteins of liver mitochondria. FEBS letters. 1999 Aug;457(2):179–83. doi: 10.1016/s0014-5793(99)01009-1 10471774

21. Wanders RJ, Jansen GA, Skjeldal OH. Refsum disease, peroxisomes and phytanic acid oxidation: a review. J Neuropathol Exp Neurol. 2001 Nov;60(11):1021–31. doi: 10.1093/jnen/60.11.1021 11706932

22. Busanello EN, Amaral AU, Tonin AM, ZanattaÂ, Viegas CM, Vargas CR, et al. Disruption of mitochondrial homeostasis by phytanic acid in cerebellum of young rats. The Cerebellum. 2013 Jun;12(3):362–9. doi: 10.1007/s12311-012-0426-y 23081695

23. Singleton CK, Martin PR. Molecular mechanisms of thiamine utilization. Curr Mol Med. 2001 May;1(2):197–207. doi: 10.2174/1566524013363870 11899071

24. Combs GF. The Vitamins. 3rd Edition. Oxford, UK: Elsevier Inc.;2008

25. Manzetti S, Zhang J, van der Spoel D. Thiamin function, metabolism, uptake, and transport. Biochemistry. 2014 Jan;53(5):821–35. doi: 10.1021/bi401618y 24460461

26. Lee BJ, Jaroszewska M, Dabrowski K, Czesny S, Rinchard J. Effects of vitamin B1 (thiamine) deficiency in lake trout alevins and preventive treatments. J Aquat Anim Health. 2009 Dec;21(4):290–301. doi: 10.1577/H07-053.1 20218503

27. Fitzsimons JD, Brown SB, Williston B, Williston G, Brown LR, Moore K, et al. Influence of thiamine deficiency on lake trout larval growth, foraging, and predator avoidance. J Aquat Anim Health. 2009 Dec;21(4):302–14. doi: 10.1577/H08-019.1 20218504

28. Carvalho PS, Tillitt DE, Zajicek JL, Claunch RA, Honeyfield DC, Fitzsimons JD, et al. Thiamine deficiency effects on the vision and foraging ability of lake trout fry. J Aquat Anim Health. 2009 Dec;21(4):315–25. doi: 10.1577/H08-025.1 20218505

29. Fitzsimons JD. The effect of B-vitamins on a swim-up syndrome in Lake Ontario lake trout. J Great Lakes Res. 1995;21(1):286–9.

30. Paton DC, Dorward DF, Fell P. Thiamine deficiency and winter mortality in red wattlebirds, Anthochaera carunculata (aves: meliphagidae) in surburban Melbourne. Aust J Zool. 1983;31(2):147–54.

31. Fitzsimons JD, Brown SB, Brown LR, Verreault G, Tardif R, Drouillard KG, et al. Impacts of diet on thiamine status of Lake Ontario American eels. Trans Am Fish Soc. 2013 Sep;142(5):1358–69.

32. Balk L, Hägerroth PÅ, Gustavsson H, Sigg L, Åkerman G, Muñoz YR, et al. Widespread episodic thiamine deficiency in Northern Hemisphere wildlife. Sci Rep. 2016 Dec;6:38821. doi: 10.1038/srep38821 27958327

33. Amcoff P, Börjeson H, Landergren P, Vallin L, Norrgren L. Thiamine (vitamin B1) concentrations in salmon (Salmo salar), brown trout (Salmo trutta) and cod (Gadus morhua) from the Baltic Sea. Ambio. 1999 Feb;28(1):48–54.

34. Honeyfield DC, Murphy JM, Howard KG, Strasburger WW, Matz AC. An exploratory assessment of thiamine status in western Alaska Chinook salmon (Oncorhynchus tshawytscha). North Pacific Anadromous Fish Commission Bulletin No. 2016 Dec;6:21–31.

35. Brown SB, Honeyfield DC, Hnath JG, Wolgamood M, Marcquenski SV, Fitzsimons JD, et al. Thiamine status in adult salmonines in the Great Lakes. J Aquat Anim Health. 2005 Mar;17(1):59–64.

36. Brown SB, Fitzsimons JD, Palace VP, Vandenbyllaardt L. Thiamine and early mortality syndrome in lake trout. Am Fish Soc Symp. 1998;21:18–25.

37. Fitzsimons JD, Vandenbyllaardt L, Brown SB. The use of thiamine and thiamine antagonists to investigate the etiology of early mortality syndrome in lake trout (Salvelinus namaycush). Aquat Toxicol. 2001 May;52(3–4):229–39. doi: 10.1016/s0166-445x(00)00147-8 11239684

38. Sepúlveda MS, Wiebe JJ, Honeyfield DC, Rauschenberger HR, Hinterkopf JP, Johnson WE, et al. Organochlorine pesticides and thiamine in eggs of largemouth bass and American alligators and their relationship with early life-stage mortality. J Wildl Dis. 2004 Oct;40(4):782–6. doi: 10.7589/0090-3558-40.4.782 15650100

39. Sutherland WJ, Butchart SH, Connor B, Culshaw C, Dicks LV, Dinsdale J, et al. A 2018 horizon scan of emerging issues for global conservation and biological diversity. Trends Ecol Evol. 2018 Jan;33(1):47–58. doi: 10.1016/j.tree.2017.11.006 29217396

40. Bagge O, Thurow F. The Baltic cod stock: fluctuations and possible causes. ICES Marine Science Symposia. 1994;198:254–68.

41. Köster FW, Huwer B, Hinrichsen HH, Neumann V, Makarchouk A, Eero M, et al. Eastern Baltic cod recruitment revisited -dynamics and impacting factors. ICES Journal of Marine Science. 2017 Jan;74(1):3–19.

42. ICES Cod (Gadus morhua) in subdivisions 24–32, eastern Baltic stock (eastern Baltic Sea) ICES Advice on fishing opportunities, catch, and effort. 2018.cod;27.24–32, https://doi.org/10.17895/ices.pub.4378.

43. ICES Cod (Gadus morhua) in subdivisions 24–32, eastern Baltic stock (eastern Baltic Sea) Report of the ICES Advisory Committee, 2019; cod;27.24–32, https://doi.org/10.17895/ices.advice.4747.

44. Fångststatistik yrkesfisket (Catch statistics Commercial fishing) [Internet]. Gothenburg, Sweden: Swedish Agency for Marine and Water Management; 1999-. [cited 2019 Feb 27]. https://www.havochvatten.se/hav/samordning-fakta/data-statistik/fangststatistik-yrkesfisket.html

45. Svedäng H, Hornborg S. Historic changes in length distributions of three Baltic cod (Gadus morhua) stocks: Evidence of growth retardation. Ecology and evolution. 2017 Aug;7(16):6089–102. doi: 10.1002/ece3.3173 28861215

46. Eero M, Hjelm J, Behrens J, Buchmann K, Cardinale M, Casini M, et al. Eastern Baltic cod in distress: biological changes and challenges for stock assessment. ICES Journal of Marine Science. 2015 Jun;72(8):2180–6.

47. Vainikka A, Gårdmark A, Bland B, Hjelm J. Two-and three-dimensional maturation reaction norms for the eastern Baltic cod, Gadus morhua. ICES Journal of Marine Science. 2008 Dec;66(2):248–57.

48. Røjbek MC, Jacobsen C, Tomkiewicz J, Støttrup JG. Linking lipid dynamics with the reproductive cycle in Baltic cod Gadus morhua. Mar Ecol Prog Ser. 2012 Dec;471:215–34.

49. Wieland K, Horbowa K. Recent changes in peak spawning time and location of spawning of cod in the Bornholm Basin, Baltic Sea. ICES CM 1996/J:15.

50. Eero M, Vinther M, Haslob H, Huwer B, Casini M, Storr-Paulsen M, et al. Spatial management of marine resources can enhance the recovery of predators and avoid local depletion of forage fish. Conserv Lett. 2012 Dec;5(6):486–92.

51. Plambech M, Van Deurs M, Steffensen JF, Tirsgård B, Behrens JW. Excess post-hypoxic oxygen consumption in Atlantic cod Gadus morhua. J Fish Biol. 2013 Aug;83(2):396–403. doi: 10.1111/jfb.12171 23902313

52. Teschner EC, Kraus G, Neuenfeldt S, Voss R, Hinrichsen HH, Köster FW. Impact of hypoxia on consumption of Baltic cod in a multispecies stock assessment context. J Appl Ichthyol. 2010 Dec;26(6):836–42.

53. ICES Report of the Study Group on Spatial Analysis for the Baltic Sea (SGSPATIAL), 4–6 November 2014, Gothenburg, Sweden. ICES CM 2014/SSGRSP:08. 49.

54. ICES Report of the Benchmark Workshop on Baltic Cod Stocks (WKBALTCOD), 2–6 March 2015, Rostock, Germany. ICES CM 2015/ACOM:35. 172.

55. Mehrdana F, Bahlool QZ, Skov J, Marana MH, Sindberg D, Mundeling M, et al. Occurrence of zoonotic nematodes Pseudoterranova decipiens, Contracaecum osculatum and Anisakis simplex in cod (Gadus morhua) from the Baltic Sea. Vet Parasitol. 2014 Oct;205(3–4):581–7. doi: 10.1016/j.vetpar.2014.08.027 25224792

56. Svedäng H, Hornborg S. Selective fishing induces density-dependent growth. Nat Commun. 2014 Jun;5:4152. doi: 10.1038/ncomms5152 24920387

57. Andersen KH, Farnsworth KD, Thygesen UH, Beyer JE. The evolutionary pressure from fishing on size at maturation of Baltic cod. Ecol Modell. 2007 Feb;204(1–2):246–52.

58. Bagge O, Thurow F, Steffensen E, Bay J. The Baltic cod. Dana. 1994;10:1–28.

59. Nissling A, Solemdal P, Svensson M, Westin L. Survival, activity and feeding ability of Baltic cod (Gadus morhua) yolk-sac larvae at different salinities. J Fish Biol. 1994 Sep;45(3):435–45.

60. Hinrichsen HH, von Dewitz B, Dierking J, Haslob H, Makarchouk A, Petereit C, et al. Oxygen depletion in coastal seas and the effective spawning stock biomass of an exploited fish species. R Soc Open Sci. 2016 Jan;3(1):150338. doi: 10.1098/rsos.150338 26909164

61. Köster FW, Schnack D. The role of predation on early life stages of cod in the Baltic. Dana. 1994;10:179–201.

62. Åkerman G, Tjärnlund U, Broman D, Näf C, Westin L, Balk L. Comparison of reproductive success of cod, Gadus morhua, from the Barents Sea and Baltic Sea. Mar Environ Res. 1996 Jun 1;42(1–4):139–44.

63. Buchmann K, Kania P. Emerging Pseudoterranova decipiens (Krabbe, 1878) problems in Baltic cod, Gadus morhua L., associated with grey seal colonization of spawning grounds. J Fish Dis. 2012 Nov;35(11):861–6. doi: 10.1111/j.1365-2761.2012.01409.x 22817526

64. Nadolna K, Podolska M. Anisakid larvae in the liver of cod (Gadus morhua) L. from the southern Baltic Sea. J Helminthol. 2014 Jun;88(2):237–46. doi: 10.1017/S0022149X13000096 23452650

65. Zuo S, Kania PW, Mehrdana F, Marana MH, Buchmann K. Contracaecum osculatum and other anisakid nematodes in grey seals and cod in the Baltic Sea: molecular and ecological links. J Helminthol. 2018 Jan;92(1):81–9. doi: 10.1017/S0022149X17000025 28124629

66. Hansson T. Comparison of two measures of missing cofactor in cofactor-dependent enzymes: Proportion versus relative increase. Open Biomarkers Journal. 2012;5:16–21.

67. Torniainen J, Vuorinen PJ, Jones RI, Keinänen M, Palm S, Vuori KA, et al. Migratory connectivity of two Baltic Sea salmon populations: retrospective analysis using stable isotopes of scales. ICES J Mar Sci. 2013 Sep;71(2):336–44.

68. Mahé K, Schwab P, Hiscock C, Cossitt G, Briand D, Goraguer H. Age determination of Atlantic cod (Gadus morhua): 2012 Workshop between Canada and France on cod otoliths [Internet]. Saint Pierre et Miquelon: the French Ministry of the Overseas and the territorial Council; 2012. [cited 2019 April 17]. http://citeseerx.ist.psu.edu/viewdoc/download?doi=10.1.1.1015.3750%20rep=rep1%20type=pdf

69. Tate JR, Nixon PF. Measurement of Michaelis constant for human erythrocyte transketolase and thiamin diphosphate. Anal Biochem. 1987 Jan;160(1):78–87. doi: 10.1016/0003-2697(87)90616-6 3565758

70. Lowry OH, Rosenbrough NJ, Farr AL, Randall RJ. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 May;193(1):265–75. 14907713

71. Brown SB, Honeyfield DC, Vandenbyllaardt L. Thiamine analysis in fish tissues. Am Fish Soc Symp. 1998 Jan;21:73–81.

72. Kankaanpää H, Vuorinen PJ, Sipiä V, Keinänen M. Acute effects and bioaccumulation of nodularin in sea trout (Salmo trutta m. trutta L.) exposed orally to Nodularia spumigena under laboratory conditions. Aquat Toxicol. 2002 Mar;61(3–4):155–68. doi: 10.1016/s0166-445x(02)00054-1 12359387

73. Mörner T, Hansson T, Carlsson L, Berg AL, Muñoz YR, Gustavsson H, et al. Thiamine deficiency impairs common eider (Somateria mollissima) reproduction in the field. Sci Rep. 2017 Oct;7(1):14451. doi: 10.1038/s41598-017-13884-1 29089512

74. Hansson T, Thain JE, Martínez-Gómez C, Hylland K, Gubbins MJ, Balk L. Supporting variables for biological effects measurements in fish and blue mussel. ICES Techniques in Marine Environmental Science. 2017 Aug;60.

75. Kraus G, Müller A, Trella K, Köuster FW. Fecundity of Baltic cod: temporal and spatial variation. J Fish Biol. 2000 Jun;56(6):1327–41.

76. Reeves SA. A simulation study of the implications of age-reading errors for stock assessment and management advice. ICES Journal of Marine Science. 2003 Mar;60(2):314–28.

77. Araya M, Cubillos LA, Guzmán M, Peñailillo J, Sepúlveda A. Evidence of a relationship between age and otolith weight in the Chilean jack mackerel, Trachurus symmetricus murphyi (Nichols). Fish Res. 2001 Apr;51(1):17–26.

78. Fletcher WJ. A test of the relationship between otolith weight and age for the pilchard Sardinops neopilchardus. Can J Fish Aquat Sci. 1991 Jan;48(1):35–8.

79. Lepak JM, Cathcart CN, Hooten MB. Otolith mass as a predictor of age in kokanee salmon (Oncorhynchus nerka) from four Colorado reservoirs. Can J Fish Aquat Sci. 2012 Sep;69(10):1569–75.

80. Lou DC, Mapstone BD, Russ GR, Davies CR, Begg GA. Using otolith weight-age relationships to predict age-based metrics of coral reef fish populations at different spatial scales. Fish Res. 2005 Mar;71(3):279–94.

81. Pilling GM, Grandcourt EM, Kirkwood GP. The utility of otolith weight as a predictor of age in the emperor Lethrinus mahsena and other tropical fish species. Fish Res. 2003 Feb;60(2–3):493–506.

82. Cardinale M, Arrhenius F, Johnsson B. Potential use of otolith weight for the determination of age-structure of Baltic cod (Gadus morhua) and plaice (Pleuronectes platessa). Fish Res. 2000 Apr;45(3):239–52.

83. Xu ZP, Wawrousek EF, Piatigorsky J. Transketolase haploinsufficiency reduces adipose tissue and female fertility in mice. Mol Cell Biol. 2002 Jun;22(17):6142–7. doi: 10.1128/MCB.22.17.6142-6147.2002 12167708

84. Blair PV, Kobayashi R, Edwards HM, Shay NF, Baker DH, Harris RA. Dietary thiamin level influences levels of its diphosphate form and thiamin-dependent enzymic activities of rat liver. J Nutr. 1999 Mar;129(3):641–8. doi: 10.1093/jn/129.3.641 10082768

85. Jeyasingham MD, Pratt OE, Thomson AD, Shaw GK. Reduced stability of rat brain transketolase after conversion to the apo form. J Neurochem. 1986 Jul;47(1):278–81. doi: 10.1111/j.1471-4159.1986.tb02859.x 3711903

86. Trebukhina RV, Ostrovsky YM, Petushok VG, Velichko MG, Tumanov VN. Effect of thiamin deprivation on thiamin metabolism in mice. J Nutr. 1981 Mar;111(3):505–13. doi: 10.1093/jn/111.3.505 6110711

87. Harata N, Iwasaki Y, Ohara Y. Reappraisal of regional thiamine content in the central nervous system of the normal and thiamine-deficient mice. Metab Brain Dis. 1993 Mar;8(1):45–59. doi: 10.1007/bf01000529 8492784

88. Tomiyasu K, Inomata K. Enzyme-cytochemical study of small ganglion cells in experimental thiamine deficiency: Concerning the pain mechanism. Acta Neuropathol. 1991 Mar;81(4):396–400. doi: 10.1007/bf00293460 1851363

89. Rindi G, De Giuseppe L, Ventura U. Distribution and phosphorylation of oxy-thiamine in rat tissues. J Nutr. 1963 Oct;81(2):147–54.

90. Batifoulier F, Verny MA, Besson C, Demigne C, Remesy C. Determination of thiamine and its phosphate esters in rat tissues analyzed as thiochromes on a RP-amide C16 column. J Chromatogr B. 2005 Feb;816(1–2):67–72.

91. Bavington D. Managed annihilation: an unnatural history of the Newfoundland cod collapse. Vancouver: UBC press; 2011.

92. Fisheries and Oceans Canada (DFO). Recovery potential assessment for the Newfoundland and Labrador Designatable Unit (NAFO Divs. 2GHJ, 3KLNO) of Atlantic Cod (Gadus morhua). DFO Can Sci Advis Sec Sci Advis Rep. 2011/037

93. Olsen EM, Heino M, Lilly GR, Morgan MJ, Brattey J, Ernande B, et al. Maturation trends indicative of rapid evolution preceded the collapse of northern cod. Nature. 2004 Apr;428(6986):932. doi: 10.1038/nature02430 15118724

94. Swain DP. Life-history evolution and elevated natural mortality in a population of Atlantic cod (Gadus morhua). Evol Appl. 2011 Jan;4(1):18–29. doi: 10.1111/j.1752-4571.2010.00128.x 25567950

95. Dutil JD, Lambert Y. Natural mortality from poor condition in Atlantic cod (Gadus morhua). Can J Fish Aquat Sci. 2000 Apr;57(4):826–36.

96. Lambert Y, Dutil JD. Condition and energy reserves of Atlantic cod (Gadus morhua) during the collapse of the northern Gulf of St. Lawrence stock. Can J Fish Aquat Sci. 1997 Oct;54(10):2388–400.

97. Rideout RM, Morgan MJ, Lilly GR. Variation in the frequency of skipped spawning in Atlantic cod (Gadus morhua) off Newfoundland and Labrador. ICES Journal of Marine Science. 2006 Jan;63(6):1101–10.

98. Bishop CA, Baird JW. Spatial and temporal variability in condition factors of Divisions 2J and 3KL cod (Gadus morhua). NAFO Sci Coun Stud. 1994;21:105–13.

99. Vallin L, Nissling A, Westin L. Potential factors influencing reproductive success of Baltic cod, Gadus morhua: a review. Ambio. 1999 Feb;28(1):92–9.

100. Fynn-Aikins K, Bowser PR, Honeyfield DC, Fitzsimons JD, Ketola HG. Effect of dietary amprolium on tissue thiamin and Cayuga syndrome in Atlantic salmon. Trans Am Fish Soc. 1998 Sep;127(5):747–57.

101. Prasad R, Rao YVBG, Mehta K, Subrahmanyam D. Effect of thiamine deficiency on the filarial infection of albino rats with Litomosoides carinii. Int J Parasitol. 1980;10(2):93–6. doi: 10.1016/0020-7519(80)90017-x 7372401


Článek vyšel v časopise

PLOS One


2020 Číslo 1