Deficiency syndromes in top predators associated with large-scale changes in the Baltic Sea ecosystem

Autoři: Sanna Majaneva aff001;  Emil Fridolfsson aff001;  Michele Casini aff004;  Catherine Legrand aff001;  Elin Lindehoff aff001;  Piotr Margonski aff005;  Markus Majaneva aff001;  Jonas Nilsson aff001;  Gunta Rubene aff007;  Norbert Wasmund aff008;  Samuel Hylander aff001
Působiště autorů: Department of Biology and Environmental Sciences, Centre for Ecology and Evolution in Microbial model Systems–EEMiS, Linnaeus University, Kalmar, Sweden aff001;  Department of Arctic and Marine Biology, UiT The Arctic University of Norway, Tromsø, Norway aff002;  Department of Biology, Norwegian University of Science and Technology, Trondheim, Norway aff003;  Swedish University of Agricultural Sciences, Department of Aquatic Resources, Institute of Marine Research, Lysekil, Sweden aff004;  National Marine Fisheries Research Institute, Gdynia, Poland aff005;  NTNU University Museum, Norwegian University of Science and Technology, Trondheim, Norway aff006;  Fish Resources Research Department, Institute of Food Safety, Animal Health and Environment BIOR, Riga, Latvia aff007;  Leibniz-Institute for Baltic Sea Research, Warnemünde, Germany aff008
Vyšlo v časopise: PLoS ONE 15(1)
Kategorie: Research Article


Vitamin B1 (thiamin) deficiency is an issue periodically affecting a wide range of taxa worldwide. In aquatic pelagic systems, thiamin is mainly produced by bacteria and phytoplankton and is transferred to fish and birds via zooplankton, but there is no general consensus on when or why this transfer is disrupted. We focus on the occurrence in salmon (Salmo salar) of a thiamin deficiency syndrome (M74), the incidence of which is highly correlated among populations derived from different spawning rivers. Here, we show that M74 in salmon is associated with certain large-scale abiotic changes in the main common feeding area of salmon in the southern Baltic Sea. Years with high M74 incidence were characterized by stagnant periods with relatively low salinity and phosphate and silicate concentrations but high total nitrogen. Consequently, there were major changes in phytoplankton and zooplankton, with, e.g., increased abundances of Cryptophyceae, Dinophyceae, Diatomophyceae and Euglenophyceae and Acartia spp. during high M74 incidence years. The prey fish communities also had increased stocks of both herring and sprat in these years. Overall, this suggests important changes in the entire food web structure and nutritional pathways in the common feeding period during high M74 incidence years. Previous research has emphasized the importance of the abundance of planktivorous fish for the occurrence of M74. By using this 27-year time series, we expand this analysis to the entire ecosystem and discuss potential mechanisms inducing thiamin deficiency in salmon.

Klíčová slova:

Baltic Sea – Biomass – Ecosystems – Food web structure – Phytoplankton – Rivers – Salmon – Zooplankton


1. Bengtsson B-E, Hill C, Bergman Å, Brandt I, Johansson N, Magnhagen C, et al. (1999). Reproductive Disturbances in Baltic Fish: A Synopsis of the FiRe Project. AMBIO. 28(1):2–8.

2. Fitzsimons JD, Brown SB, Honeyfield DC, Hnath JG. (1999). A Review of Early Mortality Syndrome (EMS) in Great Lakes Salmonids: Relationship with Thiamine Deficiency. AMBIO. 28(1):9–15.

3. Balk L, Hägerroth PÅ, Åkerman G, Hanson M, Tjärnlund U, Hansson T, et al. (2009). Wild birds of declining European species are dying from a thiamine deficiency syndrome. PNAS. 106(29):12001–6. doi: 10.1073/pnas.0902903106 19597145

4. Balk L, Hägerroth PÅ, Gustavsson H, Sigg L, Åkerman G, Ruiz Munoz Y, et al. (2016). Widespread episodic thiamine deficiency in Northern Hemisphere wildlife. Sci Rep. 6:38821. doi: 10.1038/srep38821 27958327

5. Brown SB, Fitzsimons JD, Honeyfield DC, Tillitt DE. (2005). Implications of Thiamine Deficiency in Great Lakes Salmonines. J Aquat Anim Health. 17(1):113–24. doi: 10.1577/h04-015.1

6. Keinänen M, Uddström A, Mikkonen J, Casini M, Pönni J, Myllylä T, et al. (2012). The thiamine deficiency syndrome M74, a reproductive disorder of Atlantic salmon (Salmo salar) feeding in the Baltic Sea, is related to the fat and thiamine content of prey fish. ICES J Mar Sci. 69(4):516–28. doi: 10.1093/icesjms/fss041

7. Mikkonen J, Keinänen M, Casini M, Ponni J, Vuorinen PJ. (2011). Relationships between fish stock changes in the Baltic Sea and the M74 syndrome, a reproductive disorder of Atlantic salmon (Salmo salar). ICES J Mar Sci. 68(10):2134–44. doi: 10.1093/icesjms/fsr156

8. Sutherland WJ, Butchart SHM, Connor B, Culshaw C, Dicks LV, Dinsdale J, et al. (2018). A 2018 Horizon Scan of Emerging Issues for Global Conservation and Biological Diversity. Trends Ecol Evol. 33(1):47–58. doi: 10.1016/j.tree.2017.11.006 29217396

9. Keinänen M, Käkelä R, Ritvanen T, Myllylä T, Pönni J, Vuorinen PJ. (2017). Fatty acid composition of sprat (Sprattus sprattus) and herring (Clupea harengus) in the Baltic Sea as potential prey for salmon (Salmo salar). Helgol Mar Res. 71(1). doi: 10.1186/s10152-017-0484-0

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

11. Kraft CE, Angert ER. (2017). Competition for vitamin B1 (thiamin) structures numerous ecological interactions. Q Rev Biol. 92(2):151–68. doi: 10.1086/692168 29562121

12. Börjesson H. (2016). Redovisning av M74-förekomsten i svenska kompensationsodlade laxstammar från Östersjön för 2016.1–5.

13. ICES. (2014). Report of the Baltic Salmon and Trout Assessment Working Group (WGBAST). ICES CM. ACOM:08:1–347.

14. Norrgren L, Andersson T, Bergqvist P-A, Björklund I. (1993). Chemical, physiological and morphological studies of feral baltic salmon (Salmo salar) suffering from abnormal fry mortality. Environ Toxicol Chem. 12(11):2065–75. doi: 10.1897/1552-8618(1993)12[2065:Cpamso]2.0.Co;2

15. Börjeson H, Amcoff P, Ragnarsson B, Norrgren L. (1999). Reconditioning of sea-run Baltic salmon (Salmo salar) that have produced progeny with the M74 syndrome. AMBIO. 28(1):30–6.

16. Cooray R, Holmberg M, Hellström A, Härdig J, Mattson R, Gunnarsson A, et al. (1999). Screening for Microorganisms Associated with M74 Disease Syndrome in Sea-Run Baltic Salmon (Salmo salar). AMBIO. 28(1):77–81.

17. Vuorinen PJ, Parmanne R, Vartiainen T, Keinänen M, Kiviranta H, Kotovuori O, et al. (2002). PCDD, PCDF, PCB and thiamine in Baltic herring (Clupea harengus L.) and sprat (Sprattus sprattus (L.)) as a background to the M74 syndrome of Baltic salmon (Salmo salar L.). ICES J Mar Sci. 59(3):480–96. doi: 10.1006/jmsc.2002.1200

18. Hasselquist Langefors Å. (2005). Adaptive and Neutral Genetic Variation and Colonization History of Atlantic Salmon, Salmo salar. Environ Biol Fish. 74(3–4):297–308. doi: 10.1007/s10641-005-0501-z

19. Karlsson L, Karlström Ö. (1994). The Baltic salmon (Salmo salar L.): its history, present situation and future. Dana. 10:61–85.

20. Torniainen J, Vuorinen PJ, Jones RI, Keinänen M, Palm S, Vuori KAM, et al. (2013). Migratory connectivity of two Baltic Sea salmon populations: retrospective analysis using stable isotopes of scales. ICES J Mar Sci. 71(2):336–44. doi: 10.1093/icesjms/fst153

21. McKinnel S, Lundqvist H. (1998). The effect of sexual maturation on the spatial distribution of Baltic salmon. J Fish Biol. 52:1175–85.

22. Kallio-Nyberg I, Ikonen E. (1992). Migration pattern of two salmon stocks in the Baltic Sea. ICES J Mar Sci. 49:191–8.

23. Jutila E, Jokikokko E, Kallio-Nyberg I, Saloniemi I, Pasanen P. (2003). Differences in sea migration between wild and reared Atlantic salmon (Salmo salar L.) in the Baltic Sea. Fish Res. 60:333–43.

24. Kallio-Nyberg I, Romakkaniemi A, Jokikokko E, Saloniemi I, Jutila E. (2015). Differences between wild and reared Salmo salar stocks of two northern Baltic Sea rivers. Fish Res. 165:85–95. doi: 10.1016/j.fishres.2014.12.022

25. Hansson S, Karlsson L, Ikonen E, Christensen O, Mitans A, Uzars D, et al. (2001). Stomach analyses of Baltic salmon from 1959–1962 and 1994–1997: possible relations between diet and yolk-sac-fry mortality (M74). J Fish Biol. 58(6):1730–45. doi: 10.1006/jfbi.2001.1585

26. Karlsson L, Ikonen E, Mitans A, Hansson S. (1999). The Diet of Salmon (Salmo salar) in the Baltic Sea and Connections with the M74 Syndrome. AMBIO. 28(1):37–42.

27. Keinänen M, Käkelä R, Ritvanen T, Pönni J, Harjunpää H, Myllylä T, et al. (2018). Fatty acid signatures connect thiamine deficiency with the diet of the Atlantic salmon (Salmo salar) feeding in the Baltic Sea. Mar Biol. 165(10). doi: 10.1007/s00227-018-3418-8 30369636

28. Honeyfield DC, Hinterkopf JP, Fitzsimons JD, Tillitt DE, Zajicek JL, Brown SB. (2005). Development of Thiamine Deficiencies and Early Mortality Syndrome in Lake Trout by Feeding Experimental and Feral Fish Diets Containing Thiaminase. J Aquat Anim Health. 17(1):4–12. doi: 10.1577/h03-078.1

29. Combs GF. (2012). The Vitamins. 4 ed. San Diego, California, USA: Academic Press. 599 p.

30. Wistbacka S, Bylund G. (2008). Thiaminase activity of Baltic salmon prey species: a comparision of net- and predator-caught samples. J Fish Biol. 72(4):787–802. doi: 10.1111/j.1095-8649.2007.01722.x

31. Wistbacka S, Heinonen A, Bylund G. (2002). Thiaminase activity of gastrointestinal contents of salmon and herring from the Baltic Sea. J Fish Biol. 60(4):1031–42. doi: 10.1006/jfbi.2002.1912

32. Croft MT, Warren MJ, Smith AG. (2006). Algae need their vitamins. Eukaryot Cell. 5(8):1175–83. doi: 10.1128/EC.00097-06 16896203

33. Tang YZ, Koch F, Gobler CJ. (2010). Most harmful algal bloom species are vitamin B1 and B12 auxotrophs. PNAS. 107(48):20756–61. doi: 10.1073/pnas.1009566107 21068377

34. Sañudo-Wilhelmy SA, Gómez-Consarnau L, Suffridge C, Webb EA. (2014). The role of B vitamins in marine biogeochemistry. Annu Rev Mar Sci. 6:339–67. doi: 10.1146/annurev-marine-120710-100912 24050603

35. McRose D, Guo J, Monier A, Sudek S, Wilken S, Yan S, et al. (2014). Alternatives to vitamin B1 uptake revealed with discovery of riboswitches in multiple marine eukaryotic lineages. ISME J. 8(12):2517–29. doi: 10.1038/ismej.2014.146 25171333

36. Paerl RW, Bouget FY, Lozano JC, Verge V, Schatt P, Allen EE, et al. (2017). Use of plankton-derived vitamin B1 precursors, especially thiazole-related precursor, by key marine picoeukaryotic phytoplankton. ISME J. 11(3):753–65. doi: 10.1038/ismej.2016.145 27935586

37. Paerl RW, Sundh J, Tan D, Svenningsen SL, Hylander S, Andersson AF, et al. (2018). Prevalent reliance of bacterioplankton on exogenous vitamin B1 and precursor availability. PNAS. 115(44):E10447–E56. doi: 10.1073/pnas.1806425115 30322929

38. Paerl RW, Bertrand EM, Rowland E, Schatt P, Mehiri M, Niehaus TD, et al. (2018). Carboxythiazole is a key microbial nutrient currency and critical component of thiamin biosynthesis. Sci Rep. 8(1):5940. doi: 10.1038/s41598-018-24321-2 29654239

39. Casini M, Lövgren J, Hjelm J, Cardinale M, Molinero JC, Kornilovs G. (2008). Multi-level trophic cascades in a heavily exploited open marine ecosystem. Proc R Soc B. 275(1644):1793–801. doi: 10.1098/rspb.2007.1752 18460432

40. Möllmann C, Diekmann R. (2012). Marine ecosystem regime shifts induced by climate and overfishing: a review for the northern hemisphere. In: Woodward G, Ute J, O´Gorman EJ, editors. Global Change in Multispecies Systems: Part II. Advances in Ecological Research. 47: Academic Press. p. 303–47.

41. Alheit J, Möllmann C, Dutz J, Kornilovs G, Loewe P, Mohrholz V, et al. (2005). Synchronous ecological regime shifts in the central Baltic and the North Sea in the late 1980s. ICES J Mar Sci. 62(7):1205–15. doi: 10.1016/j.icesjms.2005.04.024

42. Möllmann C, Müller-Karulis B, Kornilovs G, St. John MA. (2008). Effects of climate and overfishing on zooplankton dynamics and ecosystem structure: regime shifts, trophic cascade, and feedback loops in a simple ecosystem. ICES J Mar Sci. 65:302–10. doi: 10.1093/icesjms/fsm197

43. Möllmann C, Diekmann R, Müller-Karulis B, Kornilovs G, Plikshs M, Axe P. (2009). Reorganization of a large marine ecosystem due to atmospheric and anthropogenic pressure: a discontinuous regime shift in the Central Baltic Sea. Glob Chang Biol. 15(6):1377–93. doi: 10.1111/j.1365-2486.2008.01814.x

44. Casini M, Hjelm J, Molinero J-C, Lövgren J, Cardinale M, Bartolino V, et al. (2009). Trophic cascades promote threshold-like shifts in pelagic marine ecosystems. Proc Nat Acad Sci USA. 106(1):197–202. doi: 10.1073/pnas.0806649105 19109431

45. Wasmund N, Tuimala J, Suikkanen S, Vandepitte L, Kraberg A. (2011). Long-term trends in phytoplankton composition in the western and central Baltic Sea. J Mar Syst. 87(2):145–59. doi: 10.1016/j.jmarsys.2011.03.010

46. Ahlgren G, Van Nieuwerburgh L, Wänstrand I, Pedersén M, Boberg M, Snoeijs P. (2005). Imbalance of fatty acids in the base of the Baltic Sea food web—a mesocosm study. Can J Fish Aquat Sci. 62(10):2240–53. doi: 10.1139/f05-140

47. Ejsmond MJ, Blackburn N, Fridolfsson E, Haecky P, Andersson A, Casini M, et al. (2019). Modeling vitamin B1 transfer to consumers in the aquatic food web. Sci Rep. 9(1):10045. doi: 10.1038/s41598-019-46422-2 31296876

48. HELCOM. (1988). Guidelines for the Baltic Monitoring Programme for the Third Stage. Part D. Biological determinands. Baltic Sea Environ Proc. 27 D.

49. Kornilovs G, Möllmann C, Sidrevics L, Berzinsh V. (2004). Fish predation modified climate-induced long-term trends of mesozooplankton in a semi-enclosed coastal gulf. ICES CM. L:13:1–26.

50. Otto SA, Kornilovs G, Llope M, Möllmann C. (2014). Interactions among density, climate, and food web effects determine long-term life cycle dynamics of a key copepod. Mar Ecol Prog Ser. 498:73–84.

51. Köster FW, Möllmann C, Neuenfeldt S, Vinther M, St. John MA, Tomkiewicz J, et al. (2003). Fish stock development in the Central Baltic Sea (1974–1999) in relation to variability in the environment. ICES J Mar Sci Symp. 219:294–306.

52. Clarke Gorley. (2015). PRIMER v7: User Manual/Tutorial. Plymouth: PRIMER-E.

53. Anderson MJ, Robinson J. (2003). Generalized discriminant analysis based on distances. Aust N Z J Stat. 45(3):301–17.

54. Anderson MJ, Willis TJ. (2003). Canonical analysis of principal coordinates: A useful method of constrained ordination for ecology. Ecology. 84(2):511–25.

55. Dancey C, Reidy J. (2011). Statistics Without Maths for Psychology. Using SPSS for Windows. 3 ed. Essex: Pearson Education Limited.

56. Amcoff P, Börjeson H, Landergren P, Vallin L, Norrgren L. (1999). Thiamine (Vitamin B₁) Concentrations in Salmon (Salmo salar), Brown Trout (Salmo trutta) and Cod (Gadus morhua) from the Baltic Sea. AMBIO. 28(1):48–54.

57. Woodward B. (1994). Dietary vitamin requirements of cultured young fish, with emphasis on quantitative estimates for salmonids. Aquaculture. 124:133–68.

58. Mohrholz V, Naumann M, Nausch G, Krüger S, Gräwe U. (2015). Fresh oxygen for the Baltic Sea—An exceptional saline inflow after a decade of stagnation. J Mar Syst. 148:152–66. doi: 10.1016/j.jmarsys.2015.03.005

59. Ianora A, Miralto A, Poulet SA, Carotenuto Y, Buttino I, Romano G, et al. (2004). Aldehyde suppression of copepod recruitment in blooms of a ubiquitous planktonic diatom. Nature. 429(6990):403–7. doi: 10.1038/nature02526 15164060

60. Vargas CA, Escribano R, Poulet S. (2006). Phytoplankton food quality determines time windows for successful zooplankton reproductive pulses. Ecology. 87(12):2992–9. doi: 10.1890/0012-9658(2006)87[2992:pfqdtw];2 17249223

61. Sañudo-Wilhelmy SA, Cutter LS, Durazo R, Smail EA, Gómez-Consarnau L, Webb EA, et al. (2012). Multiple B-vitamin depletion in large areas of the coastal ocean. PNAS. 109(35):14041–5. doi: 10.1073/pnas.1208755109 22826241

62. Wasmund N. (2017). The Diatom/Dinoflagellate Index as an Indicator of Ecosystem Changes in the Baltic Sea. 2. Historical Data for Use in Determination of Good Environmental Status. Front Mar Sci. 4(153). doi: 10.3389/fmars.2017.00153

63. Klais R, Tamminen T, Kremp A, Spilling K, Olli K. (2011). Decadal-scale changes of dinoflagellates and diatoms in the anomalous Baltic Sea spring bloom. PloS one. 6(6):e21567. doi: 10.1371/journal.pone.0021567 21747911

64. Wasmund N, Nausch G, Feistel R. (2013). Silicate consumption: an indicator for long-term trends in spring diatom development in the Baltic Sea. J Plankton Res. 35(2):393–406. doi: 10.1093/plankt/fbs101

65. Heal KR, Carlson LT, Devol AH, Armbrust EV, Moffett JW, Stahl DA, et al. (2014). Determination of four forms of vitamin B12 and other B vitamins in seawater by liquid chromatography/tandem mass spectrometry. Rapid Commun Mass Spectrom. 28(22):2398–404. doi: 10.1002/rcm.7040 25303468

66. Gómez-Consarnau L, Sachdeva R, Gifford SM, Cutter LS, Fuhrman JA, Sañudo-Wilhelmy SA, et al. (2018). Mosaic patterns of B-vitamin synthesis and utilization in a natural marine microbial community. Environ Microbiol. 20(8):2809–23. doi: 10.1111/1462-2920.14133 29659156

67. Suffridge C, Cutter L, Sañudo-Wilhelmy SA. (2017). A New Analytical Method for Direct Measurement of Particulate and Dissolved B-vitamins and Their Congeners in Seawater. Front Mar Sci. 4. doi: 10.3389/fmars.2017.00011

68. Carini P, Campbell EO, Morre J, Sanudo-Wilhelmy SA, Thrash JC, Bennett SE, et al. (2014). Discovery of a SAR11 growth requirement for thiamin's pyrimidine precursor and its distribution in the Sargasso Sea. ISME J. 8(8):1727–38. doi: 10.1038/ismej.2014.61 24781899

69. Gutowska MA, Shome B, Sudek S, McRose DL, Hamilton M, Giovannoni SJ, et al. (2017). Globally Important Haptophyte Algae Use Exogenous Pyrimidine Compounds More Efficiently than Thiamin. mBio. 8(5). doi: 10.1128/mBio.01459-17 29018119

70. Sylvander P, Häubner N, Snoeijs P. (2013). The thiamine content of phytoplankton cells is affected by abiotic stress and growth rate. Microb Ecol. 65(3):566–77. doi: 10.1007/s00248-012-0156-1 23263236

71. Fridolfsson E, Lindehoff E, Legrand C, Hylander S. (2018). Thiamin (vitamin B1) content in phytoplankton and zooplankton in the presence of filamentous cyanobacteria. Limnol Oceanogr. 63(6):2423–35. doi: 10.1002/lno.10949

72. Fridolfsson E, Bunse C, Legrand C, Lindehoff E, Majaneva S, Hylander S. (2019). Seasonal variation and species-specific concentrations of the essential vitamin B1 (thiamin) in zooplankton and seston. 166(6):70. doi: 10.1007/s00227-019-3520-6

73. Huntley M, -G. BK, Star JL. (1983). Particle rejection by Calanus pacificus: discrimination between similarly sized particles. Mar Biol. 74:151–60.

74. Hong J, Talapatra S, Katz J, Tester PA, Waggett RJ, Place AR. (2012). Algal toxins alter copepod feeding behavior. PloS one. 7(5):e36845. doi: 10.1371/journal.pone.0036845 22629336

75. Casini M, Cardinale M, Arrhenius F. (2004). Feeding preferences of herring (Clupea harengus) and sprat (Sprattus sprattus) in the southern Baltic Sea. ICES J Mar Sci. 61(8):1267–77. doi: 10.1016/j.icesjms.2003.12.011

76. Fitzsimons JD, Williston B, Zajicek JL, Tillitt DE, Brown SB, Brown LR, et al. (2005). Thiamine Content and Thiaminase Activity of Ten Freshwater Stocks and One Marine Stock of Alewives. J Aquat Anim Health. 17(1):26–35. doi: 10.1577/h04-002.1

77. Tillitt DE, Zajicek JL, Brown SB, Brown LR, Fitzsimons JD, Honeyfield DC, et al. (2005). Thiamine and Thiaminase Status in Forage Fish of Salmonines from Lake Michigan. J Aquat Anim Health. 17(1):13–25. doi: 10.1577/h03-081.1

78. Arrhenius F, Hansson S. (1996). Growth and seasonal changes in energy content of young Baltic Sea herring (Clupea harengus L). Ices J Mar Sci. 53(5):792–801.

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