Widespread episodic thiamine deficiency in Northern Hemisphere wildlife

Abstract

Many wildlife populations are declining at rates higher than can be explained by known threats to biodiversity. Recently, thiamine (vitamin B₁) deficiency has emerged as a possible contributing cause. Here, thiamine status was systematically investigated in three animal classes: bivalves, ray-finned fishes, and birds. Thiamine diphosphate is required as a cofactor in at least five life-sustaining enzymes that are required for basic cellular metabolism. Analysis of different phosphorylated forms of thiamine, as well as of activities and amount of holoenzyme and apoenzyme forms of thiamine-dependent enzymes, revealed episodically occurring thiamine deficiency in all three animal classes. These biochemical effects were also linked to secondary effects on growth, condition, liver size, blood chemistry and composition, histopathology, swimming behaviour and endurance, parasite infestation, and reproduction. It is unlikely that the thiamine deficiency is caused by impaired phosphorylation within the cells. Rather, the results point towards insufficient amounts of thiamine in the food. By investigating a large geographic area, by extending the focus from lethal to sublethal thiamine deficiency, and by linking biochemical alterations to secondary effects, we demonstrate that the problem of thiamine deficiency is considerably more widespread and severe than previously reported.

Figure 1. The 15 investigated regions in the Northern Hemisphere.

(A) South-western Iceland. (B) Northern Iceland. (C) North-eastern Iceland. (D) Eastern Iceland. (E) County of Uppsala. (F) County of Stockholm. (G) County of Södermanland. (H) County of Östergötland. (I) County of Blekinge. (J) County of Skåne. (K) County of Halland. (L) Gloucestershire. (M) Maryland. (N) Massachusetts. (O) Quebec. • The European eel (Anguilla anguilla) and the American eel (A. rostrata) reproduce in the Sargasso Sea. The maps were modified with GIMP 2.8.16 (http://www.gimp.org/downloads/) from Free World Maps (http://www.freeworldmaps.net/printable/).

Figure 2. Blue mussel (Mytilus sp.).

(a) Soft body SumT at G1 in the County of Södermanland (red or orange) and at A4 in Iceland (blue). (b) Soft body SumT in Iceland (blue) and the Baltic Sea area (red). ANOVA-type regression model. (c) Concentration and proportion soft body T, TDP, and TMP in Icelandic (blue) specimens with high SumT and Baltic Sea (red) specimens with low SumT. (d) Digestive gland TK latency and soft body (except digestive gland) SumT in the Baltic Sea. (e) Digestive gland TK activity and latency at G1 during four seasons. (f) Soft body SumT at G1 (red) and chlorophyll a in the water at G2 (green) in the County of Södermanland. Dashed line: five weeks delayed chlorophyll a curve. (g,h) Dry body weight in specimens of different lengths at G1 2011 (red/black, this investigation) and Vrångskär in the County of Södermanland 1973 (green, adapted from Kautsky16). (g) The shaded area indicates the reproductive period (March 1–June 10) defined by Kautsky. (h) Week 17–19. Dashed lines: 95% CI. • Bars: arithmetic means. Whiskers: 95% CI. C: control. Group comparisons are indicated by brackets.

Figure 3. Common eider (Somateria mollissima) and domestic chicken (Gallus gallus).

(a–f) Domestic chicken thiamine “complete” group (green, 17.5 nmol T per g dry fodder) and thiamine “deficient” group (orange, 1.2 nmol T per g dry fodder), common eider females at D3 in eastern Iceland (blue) and at I10–14 in the County of Blekinge (red). Student’s t-test. (a) Liver SumT. (b) Brain SumT. (c) Liver KGDH activity. (d) Liver KGDH latency. (e) Brain KGDH activity. (f) Brain KGDH latency. (g) Box plot of common eider egg yolk T in Iceland. Data from 2005 were adapted from Balk et al.. Wilcoxon-Mann-Whitney test. (h) A 100 year survey of more than 20,000 common eider nests on 28 islands in the archipelago at F9 in the County of Stockholm. • Bars: arithmetic means. Whiskers: 95% CI (except in the box plot). C: control. Group comparisons are indicated by brackets.

Figure 4. European eel (Anguilla anguilla) and American eel (A. rostrata).

(a–e) Untreated (blue) and T-treated (green) elvers from L1 in the UK. The T-treated specimens were bathed twice in a 100 mg/L T solution for 48 h each time. (a) Concentration and proportion muscle T, TDP, and TMP. (b–e) Student’s t-test. (b) Muscle TDP. (c) Muscle TMP. (d) Liver TK activity. (e) Liver TK latency. (f–h) Female European silver eels in Sweden. (f) Liver TK latency and SumT. (g) SG and liver SumT. (h) Brain TK activity and BCI. (i) White muscle SumT in female European silver eels in Sweden (red) and two groups of American silver eels in St. Lawrence River, Canada (pink/black), adapted from Fitzsimons et al.. The range is indicated to the right of each coloured bar. (j) Critical swim speed and white muscle SumT in experimental American yellow eels from M1 in Maryland, USA. (k) Number of the swim bladder parasite Anguillicola crassus and proportion liver TDP in female European silver eels in Sweden. • Bars: arithmetic means. Whiskers: 95% CI. OLS: ordinary least squares regression. GM: geometric mean regression.

Figure 5. Salmonines (Salmoninae).

(a–g) Atlantic salmon (Salmo salar). (a) Liver TK activity and latency in both sexes. (b) Brain KGDH activity and latency in both sexes. (c) Proportion TDP and T concentration in the brain and liver in both sexes. (d) Liver TK latency and white muscle SumT in both sexes. (e) Egg SumT and liver TK latency in females. (f) Mean egg SumT and mean muscle SumT in females from the field (red, this investigation) and experimental females (green, adapted from Fynn-Aikins et al.20). (g) The white muscle T concentration was low up to a white muscle SumT threshold of ca 17–19 nmol/g, where it started to increase. (h) Original data (plain bars) and literature data (striped bars, selection from Tables S5c,d) on egg SumT concentrations in mature female salmonines in the Northern Hemisphere. I9′, K1, River Teno, and experimental control: Atlantic salmon. I9″: sea trout (S. trutta). Lake Michigan’^,”, Lake Huron’^,”: lake trout (Salvelinus namaycush). Pacific coast’: Chinook salmon (Oncorhynchus tshawytscha). Pacific coast”: coho salmon (O. kisutch). (A) 3.9 nmol/g, threshold for mortality in the offspring; (B) 8.3 nmol/g, threshold for 20% reduced growth in the offspring; (C) 12 nmol/g, threshold for liver TK latency in the parental females; and (D) 17–19 nmol/g, suggested threshold range for sublethal thiamine deficiency in the parental females and their offspring. • Bars: arithmetic means. Whiskers: 95% CI. OLS: ordinary least squares regression. GM: geometric mean regression.