Thiamine deficiency impairs common eider (Somateria mollissima) reproduction in the field

Mörner, T.; Hansson, T.; Carlsson, L.; Berg, A.-L.; Ruiz Muñoz, Y.; Gustavsson, H.; Mattsson, R.; Balk, L.
2017 | Sci Rep | 7 (14451) (1-7)

The Baltic Sea population of the common eider (Somateria mollissima) has declined dramatically during the last two decades. Recently, widespread episodic thiamine (vitamin B1) deficiency has been demonstrated in feral birds and suggested to contribute significantly to declining populations. Here we show that the decline of the common eider population in the Baltic Sea is paralleled by high mortality of the pulli a few days after hatch, owing to thiamine deficiency and probably also thereby associated abnormal behaviour resulting in high gull predation. An experiment with artificially incubated common eider eggs collected in the field revealed that thiamine treatment of pulli had a therapeutic effect on the thiamine status of the brain and prevented death. The mortality was 53% in untreated specimens, whereas it was only 7% in thiamine treated specimens. Inability to dive was also linked to brain damage typical for thiamine deficiency. Our results demonstrate how thiamine deficiency causes a range of symptoms in the common eider pulli, as well as massive die-offs a few days after hatch, which probably are the major explanation of the recent dramatic population declines.

Widespread episodic thiamine deficiency in Northern Hemisphere wildlife

Balk, L.; Hägerroth, P.-Å.; Gustavsson, H.; Sigg, L.; Åkerman, G.; Ruiz Muñoz, Y.; Honeyfield, D.C.; Tjärnlund, U.; Oliveira, K.; Ström, K.; McCormick, S.D.; Karlsson, S.; Ström, M.; van Manen, M.; Berg, A.-L.; Halldórsson, H.; Strömquist, J.; Collier, T.K.; Börjeson, H.; Mörner, T.; Hansson, T.
2016 | Sci Rep | 6 (38821) (1-13)

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.

Thiamine deficiency affecting wildlife health in the Baltic Sea area

Mörner, T.; Hägerroth, P.-Å.; Hansson, T.; Tjärnlund, U.; Gustavsson, H.; Åkerman, G.; Balk, L.
2013 | Wildlife Disease Association (WDA)

The 62nd International Conference of the Wildlife Disease Association | July 27, 2013 | Knoxville, Tennessee, USA

Thiamine (vitamin B1) is synthesized in plants, fungi, and bacteria and is essential for all fish and bird species. Thiamine deficiency causes metabolic disorders in several subcellular compartments, such as the cytosol, mitochondria, and peroxisomes. Clinical symptoms include ataxia, convulsions, paralysis, immune suppression, behavioral and memory disorders, reduced feeding, and anorexia. In the Baltic Sea salmon (Salmo salar), thiamine deficiency has been observed since 1974. This disorder has been named the M74 syndrome. It occurs in episodes affecting the reproduction in 10–90% of the females, depending on year and river. The disorder causes neurological disturbances and histopathological changes in the brain, muscles and kidneys, both in the yolk-sac fry and in the adults.

Recently, thiamine deficiency has also been demonstrated in adults, newly hatched young, and eggs of herring gulls (Larus argentatus), and common eider (Somateria mollissima) in connection with extensive paralysis and mortality in bird colonies in the Baltic Sea area. We have observed in these colonies reproductive disorders, with a reduced number of laid eggs, and high mortality (> 90 percent) in eider ducklings during their first week of life. The many observations of advanced thiamine deficiency in adult birds imply that a varying degree of moderate thiamine deficiency occurs among the affected species. This might be an explanation for the observed increased occurrence of incomplete nest building and misplaced eggs in nests of other bird species. The thiamine deficiency may be induced either by a causative agent(s) acting directly on the affected individual, by reduced uptake of thiamine, and/or by insufficient transfer of thiamine between the trophic levels in the food web. Further studies will focus on thiamine levels in the food for these birds, as well as factors involved in the high mortality of juvenile eider ducklings.

Nutrient deficit among Swedish wildlife

Balk, L.; Hägerroth, P.-Å.; Tjärnlund, U.; Åkerman, G.; Gustavsson, H.; Ström, K.; Ström, M.; Ruiz, Y.; Mörner, T.; Sigg, L.; Hansson, T.
2013 | Swedish University of Agricultural Sciences (SLU) (9-9)

Moose Health: Management challenges with growing ungulate populations | October 24, 2013 | Uppsala, Sweden

Thiamine (vitamin B1) is a water-soluble vitamin essential for all living cells. In the cell, thiamine is phosphorylated to thiamine diphosphate, which functions as a cofactor for at least five life sustaining enzymes in the cellular metabolism. Previous studies have shown that sub-lethal thiamine deficiency in vertebrates gives rise to a large number of health effects, such as reduced feeding, memory and learning disturbances, immune suppression, and damage to the blood-brain barrier, as well as altered carbohydrate, protein, and lipid metabolism.

During the last decades, thiamine deficiency has been observed in various animal classes such as fish, birds, and reptiles. Methods to discover and characterize thiamine deficiency among wildlife include analysis of thiamine concentrations and thiamine ratios between various tissues, measurement of thiamine dependent enzyme activities and percentage of apoenzyme, as well as thiamine treatment of thiamine deficient animals (i.e. response to treatment).

Hanöbukten, a bay in southern Sweden, where thiamine (vitamin B1) deficiency cannot be excluded as the primary cause of the ecosystem disturbance

Balk, L.; Hägerroth, P.-Å.; Sigg, L.; Karlsson, S.; Tjärnlund, U.; Åkerman, G.; Gustavsson, H.; Ström, K.; Ruiz, Y.; Ström, M.; Mörner, T.; Hansson, T.
2013 | Ålakademin (35-35)

VATTEN13 : Vad har hänt med vattnet i Hanöbukten? | November 21, 2013 | Åhus, Sweden

Hanöbukten is a large bay at the east coast of the County of Skåne in southern Sweden. It faces the Baltic Sea just south of the waters and archipelago of the County of Blekinge.

During a period of approximately 6–10 years, residents fishing in Hanöbukten have observed an alarming decline in the fish abundance. In fact, the decline is so severe that many local fishermen have given up their profession and sold their boats and equipment, even in cases where their families have been fishing in Hanöbukten for many generations.

These observations have resulted in a public enquiry about the situation in Hanöbukten (Anonymous 2013), executed by the staff at the Swedish Agency for Marine and Water Management (HaV) as a commission from the Swedish government.

The public enquiry of Hanöbukten (Anonymous 2013) indicates that the problems have appeared in recent years, and according to local fishermen, the problems occur in episodes. Hence, it is very interesting that the thiamine deficiency, documented in fish and birds close to Hanöbukten, also occur in episodes and is the only known disorder today with dire consequences for individual specimens as well as entire populations.

The thiamine deficiency may be caused by one, today unknown, substance by a certain biochemical mechanism. Thiamine has a central role in the cellular metabolism of e.g. sugar, lipids, and protein, and thiamine deficiency may compromise several physiological functions, such as the immune defence, vision and hearing, long and short time memory functions, the blood brain barrier, reproduction, temperature regulation, nerve function, reproduction, and survival. Our knowledge so far makes thiamine deficiency a plausible cause for the ongoing disturbance of the ecosystem in Hanöbukten.

On this foundation, we suggest an investigation of thiamine status in some well-characterised vertebrate model-species to elucidate whether biota in Hanöbukten suffer from thiamine deficiency or not.

Reference: Anonymous (2013) Hanöbukten. Regeringsuppdrag. Havs- och vattenmyndighetens rapport 2013-10-31. Havs- och vattenmyndigheten, Göteborg, Sweden, 107 pp.

Lethal thiamine deficiency in several bird species in the Baltic Sea

Balk, L.; Hägerroth, P.-Å.; Hansson, T.; Tjärnlund, U.; Gustavsson, H.; Mörner, T.; Åkerman, G.
2012 | Clin. Chem. Lab. Med. | 50 (A64-A65) | ISBN: ISSN: 1434-6621

Advances and Controversies in B-Vitamins and Choline | September 19, 2019 | Leipzig, Germany

Thiamine deficiency has recently been demonstrated in several species of wild birds, both adults and newly hatched young, in connection with extensive mortality in a paralytic disease in the Baltic Sea. This thiamine deficiency may be the dominating cause of the observed population declines in many bird species during the last three decades. Accordingly, the need for an understanding of this problem is urgent.

Our research team has found reduced thiamine concentrations in the egg-yolk, liver, and brain, as well as reduced activities of the thiamine-dependent enzymes transketolase and alpha-ketoglutarate dehydrogenase in the liver and brain. In these organs, there were also very high proportions of apoenzyme of these enzymes. The thiamine status of females in the field was critical for the degree of breeding failure. The many observations of advanced thiamine deficiency in adult birds strongly suggest that also varying degree of moderate thiamine deficiency occurs among the affected species.

One effect of moderate thiamine deficiency is altered behaviour. We have made plenty of observations of reduced aggressiveness and low noise level in bird colonies, as well as incomplete nest building and egg laying in nests of other species. The observed degree of thiamine deficiency suggests that the birds also suffer from weakening of the blood-brain barrier and immune suppression. This is not only an obvious threat to ecosystem sustainability. For example, infectious diseases may be more easily spread to humans by immunosuppressed birds. The thiamine deficiency may be induced either by a causative agent(s) acting directly on the affected individual, and/or by insufficient transfer of thiamine between the trophic levels in the food web.

Effects of thiamine deficiency on eiders

2011 | Gotland University

International workshop on sea ducks and their food | September 19, 2019 | Visby, Gotland, Sweden

Vilken roll spelar sjukdomen fågeldöden?

2011 | Stiftelsen Sveriges Vildnad

Vad har hänt med våra skärgårdsfåglar? Vart tar ejdern vägen? | May 18, 2011 | Stockholm, Sweden

Thiamine deficiency in the ecosystem

Balk, L.; Hägerroth, P.-Å.; Hansson, T.; Tjärnlund, U.; Gustavsson, H.; Mörner, T.; Åkerman, G.
2011 | Swedish University of Agricultural Sciences (SLU) (43-43) | ISBN: 978-91-576-9057-9 | Report No: CRU Report 26

Reproductive Disorders in Baltic Vertebrate Wildlife (BALTREP 2011) | September 19, 2019 | Uppsala, Sweden

Thiamine, vitamin B1, is a water-soluble vitamin that is essential for vertebrates. Inside the cell, thiamine is phosphorylated to thiamine diphosphate, which functions as a cofactor for at least 5 life sustaining enzymes in the cellular metabolism. Previous studies have shown that sub-lethal thiamine deficiency in vertebrates may give rise to a large number of health effects, such as reduced feeding, memory and learning disturbances, immune suppression, and damage to the blood-brain barrier. Relationships have also been demonstrated between thiamine deficiency and altered lipid metabolism and neurodegenerative diseases.

Thiamine deficiency was recently demonstrated in several species of wild birds that are dying in large numbers from a paralytic disease in the Baltic Sea area. The egg, liver, and brain had reduced thiamine concentrations, and the liver and brain had reduced activities of the thiamine-dependent enzymes. In the liver and brain, there were also elevated proportions of apoenzyme, i.e. enzyme without the thiamine diphosphate cofactor. Moreover, paralyzed individuals were successfully remedied by thiamine treatment. Excess mortality and breeding failure were linked to a thiamine deficiency syndrome, which most probably has contributed significantly to declines in many bird populations during the last decades. Both adults and juveniles are subject to excess mortality, and breeding failure is caused by several factors, such as reduced number of eggs, reduced chick survival, and altered behavior, including rudimentary nest building, reduced aggression rates (attack diving), and low noise level in the colonies.

The thiamine deficiency may be induced either by a causative agent(s) acting directly on the affected individual, and/or by insufficient transfer of thiamine between the trophic levels in the food web. Classical persistent organic pollutants are not primarily suspected, since the affected species occupy a wide range of ecological niches and positions in the food web. The authors stress that they are open to the possibility that other wildlife, beside fish and birds, may suffer from thiamine deficiency as well.

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