New FCRR: Marine and Freshwater Miscellanea V

Written by Anna McLaskey and Jacob Lerner

Even though they will never meet, salmon depend on their mothers to give them a good start in life.

Photos of adult Chinook and eggs taken by McLaskey and Lerner during egg sampling at DFO hatcheries.

The energy and nutrients found within their eggs provide juveniles with all they need to develop, grow fast, and move through their early life stages when they are most vulnerable. These nutrients are gathered and stored by their mother during her time foraging in the ocean. They both power her long freshwater migration and are left behind in the eggs she lays, as a legacy to her offspring.

Thiamine, or vitamin B1, is one of the essential nutrients that salmon fry depend on from their eggs. It is required by all animals for metabolic processes and without sufficient quantities, they will suffer a variety of neurological and reproductive effects. For salmon, the effects of low thiamine are most obvious in newly hatched fry. Thiamine-deficient fry exhibit odd behaviors like swimming in corkscrew spirals or laying lethargically; many simply die.

In 2020, these behaviors were observed in California Chinook hatcheries for the first time, and this coincided with mortality rates of up to 90% (Mantua et al. 2021). Although hatchery workers were initially perplexed, the issue was quickly identified as thiamine deficiency complex (TDC). They were able to address the problem by treating eggs with thiamine baths, or injecting adults with thiamine prior to spawning. But for fish spawning in the wild, no such remedy is available.

Since the 1990’s, TDC has been associated with fish and seabird declines in the Great Lakes and the Baltic Sea. In addition to direct mortality, TDC includes sublethal effects across all salmon life stages, including reduced visual acuity and feeding rates, reduced migration performance, and impaired immune response.

In the Pacific, TDC is an emerging phenomenon. It was first observed in 2014 in Chinook from the Yukon River (Larson and Howard 2019) and again in 2020 in the aforementioned California Chinook populations. Despite the occurrence of TDC in Chinook to the north and south of British Columbia, thiamine had only ever been measured in two individual Chinook from the Fraser River (Welch et al. 2018), leaving a large knowledge gap in the risks posed to BC salmon. Now UBC researchers are establishing baseline data on thiamine in BC Chinook and investigating the potential causes of thiamine deficiency.

Photos of adult Chinook and eggs taken by McLaskey and Lerner during egg sampling at DFO hatcheries.

“The data we saw on thiamine deficiency in California Chinook was alarming. When we realized that there were no thiamine data for BC Chinook populations, it was clear that this was a knowledge gap that urgently needed to be filled.” Said Brian Hunt, Associate Professor at UBC’s Institute for the Oceans and Fisheries.

In 2023, the Pelagic Ecosystems Lab at IOF began to address this knowledge gap through a project funded by the BC Salmon Restoration and Innovation Fund (BCSRIF). They are measuring egg thiamine levels of different Chinook populations to assess whether and where TDC is occurring, and investigating the causes of TDC by measuring thiamine levels of migrating adults at river entry and the thiamine content of the prey they eat in the ocean.

Preliminary data on egg thiamine collected from Fisheries and Oceans Canada hatcheries during 2023 from eight populations across BC, show that thiamine deficiency is occurring within BC Chinook, but is not affecting all populations equally. This does not mean all is lost for these salmon, and many hatcheries have implemented treatment programs to augment their thiamine levels. For the UBC researchers though, establishing that TDC may already be affecting Chinook is just the first step.

An ecosystem disruption – causes of TDC

Documenting the occurrence of thiamine deficiency is not the only goal of this project – understanding the causes of TDC is necessary to predict its risks in the future. “It is important to study the food web drivers of thiamine deficiency to understand how we expect this phenomenon to unfold in BC, and how we can best adapt to this challenge,” says research associate Anna McLaskey, who studies nutrition of the lower trophic levels of marine food webs.

The thiamine in salmon eggs is sourced from the same place as the energy it took to get them so far inland: the ocean. And in the ocean lies the answer behind emerging thiamine deficiency. Thiamine is produced at the base of the food web by bacteria and phytoplankton before it is passed up the food chain to fill the needs of all other organisms. Although the exact causes of TDC across all ecosystems is unknown, it results from a disruption to the flow of thiamine up the food chain.

Northern anchovy. Taken by Jacob Lerner.

One hypothesis is that thiamine production at the base of the food web has declined. If less thiamine is produced by phytoplankton and bacteria, there will be less available to the entire food web. In addition, different prey species of Chinook, like forage fish, squid, and krill, contain different thiamine levels so shifts in Chinook diets can influence their thiamine intake.

A second hypothesis centers on an enzyme—thiaminase—which is found in some prey fishes. Thiaminase breaks down thiamine in the stomach, preventing its absorption. Although its evolutionary purpose is unknown, thiaminase can occur at high levels in some salmon prey species. One of these species is the northern anchovy. In the California current, anchovy

populations have recently boomed, rapidly displacing other species to become the primary prey source for Chinook salmon and causing TDC. The Strait of Georgia is currently at the northern range limit of northern anchovy, but their populations have increased in the Salish Sea during recent warm periods (Duguid et al. 2019) and they are particularly prevalent in the southern Strait of Georgia and Howe Sound.

Although thiaminase appears linked to the rise of TDC in California, it is not present at high levels in the Baltic Sea. Instead, scientists there hypothesize that prey with high fat content are to blame. These fats are beneficial because of their high energy content, but the increased metabolic activity requires more thiamine. Fish with high fats, specifically omega-3 fatty acids, are also more prone to peroxidation, which further depletes thiamine through its antioxidant properties. For British Columbia Chinook, it is their large fat deposits that fuel them through their grueling migrations but may also increase their risk of oxidative stress and thiamine deficiency.

British Columbia Chinook

As the focus turns to British Columbia Chinook, their life history may offer some clues as to what to expect. While some populations forage locally in the Strait of Georgia and may be exposed to northern anchovy populations, others migrate west or north to different prey communities. While some spawn in coastal streams, others migrate to the foothills of the Rocky Mountains that require far greater lipid stores to reach.

Jacob Lerner. Taken by Anna McLaskey.

By comparing Chinook with these different traits, we can begin to tease apart the effects of specific prey species, oxidative stress caused by high lipids, or other traits like migration distance or even run timing. Jacob Lerner focused on differences in lipid accumulation and marine ecology among BC Chinook populations for his PhD dissertation. “The diversity across and within Chinook populations is one of the species’ greatest strengths” says Lerner. Now he will link this life history diversity to thiamine levels in different populations of Chinook.

This ongoing project is characterizing the nutritional attributes of local prey species and is sampling egg thiamine levels of Chinook populations again in 2024. This knowledge is required to identify stocks at risk of TDC and to guide mitigation and restoration strategies. Stay tuned to hear more about what we learn as the project progresses.

References

Duguid WDP, Boldt JL, Chalifour L, Greene CM and others (2019) Historical fluctuations and recent observations of Northern Anchovy Engraulis mordax in the Salish Sea. Deep Sea Res II 159: 22−41

Larson, S., & Howard, K. G. (2019). Exploration of AYK Chinook Salmon egg thiamine levels as a potential mechanism contributing to recent low productivity patterns, 2014 and 2015. (Fishery data series no. 19-22; p. 26). Alaska Department of Fish and Game.
Mantua, N., Johnson, R., Field, J., Lindley, S., Williams, T., Todgham, A., Fangue, N., Jeffres, C., Bell, H., Cocherell, D., Rinchard, J., Tillitt, D., Finney, B., Honeyfield, D., Lipscomb, T., Foott, S., Kwak, K., Adkison, M., Kormos, B., … Ruiz-Cooley, I. (2021). Mechanisms, impacts, and mitigation for thiamine deficiency and early life stage mortality in California’s Central Valley Chinook Salmon. North Pacific Anadromous Fish Commission, Technical Report 17, 92– 9.
Welch, D.W.; Futia, M.H.; Rinchard, J.; Teffer, A.K.; Miller, K.M.; Hinch, S.G.; Honeyfield, D.C. Thiamine levels in muscle and eggs of adult Pacific salmon from the Fraser River, British Columbia. J. Aquat. Anim. Health 2018, 30, 191–200.

Tags: Anna McLaskey, Baltic Sea, Brian Hunt, Chinook salmon, Fraser River, Great Lakes, IOF postdoctoral fellows, IOF Research Associates, Jacob Lerner, salmon, thiamine, Yukon River