Wild birds of declining European species are dying from a thiamine deficiency syndrome

Abstract

Wild birds of several species are dying in large numbers from an idiopathic paralytic disease in the Baltic Sea area. Here, we demonstrate strong relationships between this disease, breeding failure, and thiamine (vitamin B(1)) deficiency in eggs, pulli, and full-grown individuals. Thiamine is essential for vertebrates, and its diphosphorylated form functions as a cofactor for several life sustaining enzymes, whereas the triphosphorylated form is necessary for the functioning of neuronal membranes. Paralyzed individuals were remedied by thiamine treatment. Moreover, thiamine deficiency and detrimental effects on thiamine-dependent enzymes were demonstrated in the yolk, liver, and brain. We propose that the mortality and breeding failure are part of a thiamine deficiency syndrome, which may have contributed significantly to declines in many bird populations during the last decades.

Fig. 1.

The 10 investigated regions: A, Southwestern Iceland; B, Eastern Iceland; C, County of Västerbotten; D, County of Södra Finland; E, County of Värmland; F, County of Stockholm; G, County of Södermanland; H, County of Kalmar; I, County of Blekinge; and J, County of Skåne.

Fig. 2.

Observations of thiamine deficiency in the herring gull (Larus argentatus). (A) A specimen in the County of Stockholm (region F in Fig. 1) suffering from opisthotonus and difficulty in keeping the wings folded along the side of the body. The specimen is dying while incubating, an abnormal situation. (B) Thiamine treatment of paralyzed full-grown specimens from the Baltic Sea area had a highly significant effect on recovery. (C) Yolk T concentration was 34% lower in the Baltic Sea area (regions D, E, and G–I in Fig. 1) than in Iceland (regions A and B in Fig. 1). (D) Relationship between mean yolk T concentration in the first laid eggs and proportion of nests with 3 eggs in 10 colonies in the Baltic Sea area. Extrapolation to 95% nests with 3 eggs yielded a yolk T concentration of 34 nmol/g wet weight. (E) Liver TK activity in pulli was 12% lower in the Swedish coastal regions together (regions F, G, and I in Fig. 1) than in Iceland (region B in Fig. 1). (F) Liver TK latency (i.e., the proportion of apoenzyme) in pulli was significantly higher in the Swedish coastal regions together (regions F, G, and I in Fig. 1) than in Iceland (region B in Fig. 1). (G) Relationship between liver KGDH activity and latency in pulli. Extrapolation to 4.0% latency, assumed to be normal in healthy individuals, yielded an activity of 36.5 nmol/min per mg protein. (H) Liver thiamine concentrations in pulli. T, TMP, and T+TMP+TDP (SumT) concentrations were 34%, 13%, and 7% lower, respectively, in the Swedish coastal regions together (regions F, G, and I in Fig. 1) than in Iceland (region B in Fig. 1). Error bars (C, E, F, and H) indicate 95% confidence intervals of the mean. P-values are given only when significant. n = number of clutches. Blue, Iceland and red, Baltic Sea area.

Fig. 3.

Observations of thiamine deficiency in the common starling (Sturnus vulgaris). (A) Yolk T concentration, indicating a decreasing gradient from north to south (regions C, G, and I in Fig. 1) in Sweden. (B) Liver KGDH activity in pulli was 24% lower in southern Sweden (regions G and I in Fig. 1) than in Iceland (region A in Fig. 1). Thiamine treatment resulted in 19% higher liver KGDH activity. (C) Liver KGDH latency (i.e., the proportion of apoenzyme) in pulli was 36% higher in southern Sweden (regions G and I in Fig. 1) than in Iceland (region A in Fig. 1). (D) Relationship between liver KGDH activity and latency in pulli. Extrapolation to 4.0% latency, assumed to be normal in healthy individuals, yielded an activity of 30.9 nmol/min per mg protein. (E) Liver thiamine concentrations in pulli. TMP concentration was 20% higher in southern Sweden (regions G and I in Fig. 1) than in Iceland (region A in Fig. 1). (F) Brain TK activity in pulli. Thiamine treatment resulted in 14% higher brain TK activity. (G) Brain TK latency in pulli was significantly higher in southern Sweden (regions G and I in Fig. 1) than in Iceland (region A in Fig. 1). Thiamine treatment resulted in significantly lower brain TK latency. (H) Brain thiamine concentrations in pulli. Error bars (A–C and E–H) indicate 95% confidence intervals of the mean. P-values are given only when significant. n = number of clutches. Blue, Iceland; red, Baltic Sea area; and black, thiamine treatment.

Fig. 4.

Observations of thiamine deficiency in the common eider (Somateria mollissima). (A) Yolk T concentration was 58% lower in the Baltic Sea area (regions D and F–I in Fig. 1) than in Iceland (region A in Fig. 1). (B) Liver TK activity in pulli was 32% lower in the County of Stockholm (region F in Fig. 1) than in Iceland (region A in Fig. 1). (C) Liver TK latency (i.e., the proportion of apoenzyme) in pulli was significantly higher in the County of Stockholm (region F in Fig. 1) than in Iceland (region A in Fig. 1). (D) Relationship between liver KGDH activity and latency in pulli. Extrapolation to 4.0% latency, assumed to be normal in healthy individuals, yielded an activity of 31.9 nmol/min per mg protein. (E) Brain TK activity in pulli was 7% and 26% lower in the County of Stockholm (region F in Fig. 1) and the County of Blekinge (region I in Fig. 1), respectively, than in Iceland (region A in Fig. 1). (F) Brain TK latency in pulli was significantly higher in the County of Blekinge (region I in Fig. 1) than in Iceland (region A in fig. 1). (G) Relationship between brain KGDH activity and latency in pulli. Extrapolation to 3.8% latency, assumed to be normal in healthy individuals, yielded an activity of 11.9 nmol/min per mg protein. (H) Brain thiamine concentrations in pulli. TMP, TDP, and SumT concentrations were 41%, 27%, and 28% lower, respectively, in Sweden (regions F and I in Fig. 1) than in Iceland (region A in Fig. 1). Error bars (A–C, E, F, and H) indicate 95% CI of the mean (A and H) or median (B, C, E, and F). P-values are given only when significant. n = number of clutches. Blue, Iceland and red, Baltic Sea area.