Early mortality syndrome (EMS) is the phrase used to describe an embryonic mortality affecting the offspring of salmonids (coho salmon, chinook salmon, steelhead trout, brown trout, and lake trout) in Lakes Michigan and Ontario and to a lesser extent in Lakes Huron and Erie. At its worst, EMS has the potential to bring affected stocks to extinction. Studies have implicated a lack of thiamine as a cause of EMS. This nutritional deficiency is believed to be the result of consumption of non-native forage fish, including the invasive alewife and rainbow smelt. There are two other examples of similar diseases that exhibit characteristics of EMS: M74 affects salmon in the Baltic Sea, and Cuyaga Syndrome is prevalent in Atlantic salmon in the Finger Lakes of New York. Low egg thiamine levels and improved survival following thiamine treatment of eggs and fry characterize all three diseases (GLFC 1999). In addition to eggs and fry, it has now been reported that adult fish are affected by thiamine deficiency. Furthermore, thiamine deficiency may affect other aquatic top predators, such as walleye and alligator. Given the diversity of ecosystems (Great Lakes, Baltic Sea, state waters (NY, TN, SD), and Florida lakes) and the fact that this problem is impinging on more than one life stage of an affected species, we are placing these syndromes under one umbrella as a thiamine deficiency complex (TDC). The complexity, scope, and seriousness of TDC demand that natural resource agencies work together and devise an approach to move forward aggressively on an integrated research and monitoring program to better understand TDC and to propose and evaluate possible solutions.

Many groups within the Great Lakes scientific community have identified TDC as an important issue. For example, the Strategic Vision for the Great Lakes Fishery Commission (GLFC, 1997) states that research will examine fish diseases such as early mortality syndrome. Several GLFC committees have also highlighted EMS and thiamine deficiency as key problems. Lake committees and their technical committees for both Lake Huron and Lake Michigan have listed EMS as a possible reproductive impediment for predatory species that requires further research. EMS also has implications for aspects of two theme areas of the GLFC Board of Technical Experts (BOTE) committee: a) Reintroduction of Native Fishes to the Great Lakes Proper and b) Exotic Invertebrates and Food-Web Disruption. Reintroduction of self-sustaining populations of native lake trout and Atlantic salmon will depend upon low levels of EMS in offspring and unaffected adult behavior. With respect to the restoration of native species such as Atlantic salmon and lake trout, the binational Lake Ontario Technical Committee met recently, and EMS and food web research were high on the list of priorities (Marion Daniels, OMNR, pers comm). TDC affects efforts to restore and re-introduce native species such as lake trout and Atlantic salmon in the Great Lakes. It may also affect objectives to maintain or enhance wild production of naturalized species such as rainbow trout.

Further, in a recent report on Great Lakes fish health research commissioned by the GLFC, Stephen and Thorburn (2002) identified EMS as an important research priority. These authors noted that the immediate issue concerns impacts on fish reproduction. Stephen and Thorburn also observed that EMS is linked to the issue of exotic species (macro and microorganisms) and their effects on disease ecology and food web dynamics. Discussion at the recent Great Lakes Fish Health Committee February 2003 meeting in South Bend, IN, reaffirmed that understanding the role of thiamine deficiencies, thiaminase and other nutrients in Great Lakes fishes were top research priorities. Finally, the International Joint Commission’s Great Lakes Science Advisory Board identified EMS as an important issue in its 2001-2003 report.

As evident from above, the Great Lakes scientific community recognizes that fish health has implications for the restoration of fish populations. The purpose of this workshop is to develop a plan for advancing a coordinated TDC research and monitoring program, including a funding framework, which addresses high priority needs applicable to the Great Lakes and beyond. Previous workshops, especially those sponsored by the GLFC in 1998, 2000, and 2002, summarized existing EMS research, articulated key research questions, and identified short- and long-term priorities. This workshop will build on and further these valuable efforts. The main purpose of this workshop is to reach consensus on the elements of a proposal to advance a research and monitoring agenda to begin in 2005.

EMS is characterized by loss of equilibrium, hyperexcitability, anorexia, and eventually death in affected salmonid swim-up fry. The non-indigenous species alewife and smelt are major components of salmonid diets in Lakes Michigan and Ontario. These fish contain a thiamine-destroying enzyme, thiaminase. Adult salmonines that were fed alewife have been shown to produce thiamine-deficient fry. EMS was first observed in fish in the late 1960’s and early 1970’s, but it may have been present prior to this time. Anecdotal information from Lake Michigan commercial lake trout fishermen referred to lethargic and dying fish in their gill nets as having “smelt toxicity.” Although EMS probably existed shortly after the arrival of alewife and smelt, recognition of the syndrome was obscured by toxicity of chlorinated organic compounds (dioxin, PCB, DDT, etc.) present in the 1950’s and 1960’s. Supporting documentation reports that sediment levels of these contaminants were sufficient to have caused the death of nearly all salmonid fry during this period based on the toxicity of these compounds described in contemporary research (Phil Cook, EPA, in press). Research has not yet identified a specific causal agent for TDC. However, this may be due to the fact that most studies have been short-term or have not considered interactions among the many variables at work within the ecosystem. A long-term research and monitoring program is needed to identify the potential links between anthropogenetic factors (photosynthetic inhibitors, human pharmaceuticals, flame-retardants), climatic factors, and the increasing number of invasive species entering the Great Lakes. Monitoring is critical in order to identify the key causes of early mortality diseases, to evaluate the outcome of present and future solutions, and to adjust research efforts based on new findings.

Recent increases in EMS in Lake Michigan salmonines (J. Hnath pers. comm., M. Wolmagood, pers. comm., Fitzsimons et al 1999) have occurred at the same time as declines in the important benthic macro-invertebrate Diporeia. These in turn have been linked with the invasion and massive increase in dreissenids although no biological mechanism has yet been found. Nevertheless the possibility exists that dreissenids may be affecting both the decline in Diporeia and the increase in EMS.

The commonality of declines in Diporeia and increases in EMS may relate to the effects of dreissenids on lipid dynamics. Diporeia obtain an important part of their lipid stores in spring from the annual diatom bloom (Gardner et al. 1989, Cavaletto et al. 1996). The invasion of dreissenids has severely reduced and dampened out this important source of nutrition for Diporiea. Although the relationship between lipid levels and mortality in Diporeia is not known, older Diporeia appear to tightly regulate lipid levels suggesting that the lack of Diporeia with intermediate or low lipid levels in some populations may be the result of mortality (Guiguer and Barton 2002). Similarly but somewhat removed from the direct effects on Diporeia are the effects of dreissenids on alewife lipid content and in turn its effect on thiamine nutrition of salmonine predators. Alewives are obligate zooplanktinovores so are strongly dependant on zooplankton that are in turn dependant on phytoplankton (Mills et al. 1992)). In Lake Ontario, large populations of dreissenids that have co-occurred with nutrient reductions have severely reduced phytoplankton biomass (Mills et al. 2003). At the same time, there have been declines in the energy density that is strongly correlated with lipid content, for Lake Ontario alewives (Rand et al. 1994). This may increase the potential for alewives to cause a thiamine deficiency since a negative correlation between lipid content and thiaminase has been observed for Finger Lakes alewives (J. Fitzsimons, unpub. data). Diets comprised largely of alewives that have twice the thiaminase of rainbow smelt (J. Zajicek, unpub. data), have been associated with much greater declines in lake trout egg thiamine than lake trout subsisting on smelt (Fitzsimons et al. 1998). A diet consisting of 35% alewives was associated with a 95% decline in lake trout egg thiamine relative to controls whereas a diet consisting of 100% alewives resulted in a 97% decline (D. Honeyfield, unpub. data)

While contaminants may play a role in thiamine deficiency complex (TDC), several researchers failed to demonstrate their involvement in the thiamine deficiency syndrome that occurs in Atlantic salmon in Cayuga Lake or high, remote Adirondack Mountain lakes (Fisher et al 1996; and Fisher et al 1998; others) or other species in the Great Lakes. History shows that declines in Atlantic salmon occurred in the late 1800's and thereby predate suspect contaminants (Ketola, et al. 2000). That decline was associated with an invasion of alewives. Therefore, TDC may often simply be thiamine deficiency caused by consumption of exotic invaders (such as alewives and smelt) containing the anti-vitamin thiaminase.

Fitzsimons et al (1995) was unable to find a relationship between a range of contaminants (PCBS, pesticides, dioxins, furans, PAHs and trace metals) and EMS in lake trout eggs from Lake Ontario, probably the most contaminated of all of the Great Lakes. Moreover Fitzsimons (1995) concluded that contaminant levels in lake trout eggs throughout the Great Lakes were below those required to alone cause reduced hatching and blue-sac disease. This author, however, could not rule out that contaminant levels may still be sufficient to interact with other factors and cause mortality.

Although no routinely monitored contaminant has been linked to EMS (Honeyfield et al., 1998; other refs.), the effects of several chemicals should be monitored and assessed. Some of these may ultimately lead to death or to reduced fitness of affected fish.

While there may still be some uncertainty as to the full complement of factors causing the TDC, in practically all cases a thiaminase containing prey species is involved. This ranges from alewives in the case of EMS and Cayuga Syndrome, to gizzard shad in the case of alligator reproductive problems, and to herring and sprat in the case of M74. Whatever else is done, at a minimum the situation argues for a change in diet away from thiaminase containing prey and this is likely accomplished by a change in prey. This, however, by no means ensures that the new prey will be eaten as evidenced by Lake Michigan. Despite a relatively high abundance of bloaters in Lake Michigan during the early 1990s, lake trout continued to feed on alewives, according to lake trout egg thiamine concentrations, despite the fact that alewife abundance was relatively low at the time (Fitzsimons et al. 1998, Madenjian et al 2002).

A change in prey for most salmonines and for most of the Great Lakes is at present a moot point. Many of the native prey species on which native species like lake trout relied have been driven to extinction or their abundance otherwise reduced to the extent that they are currently no more than of a mere remnant status. While still open to interpretation many of the declines in native prey fish have been circumstantially linked to the negative effects of alewives and smelt.

As a first step in providing an alternate thiaminase-free prey, a workshop funded under the Fish and Wildlife Restoration Act, has been organized for the summer of 2003 to evaluate prospects for restoration of lake herring in the Great Lakes. This cisco species is currently found throughout the Great Lakes although abundance has been seriously reduced in all of the Great Lakes except Lake Superior.

Positive effects on the thiamine status of a predator like lake trout may occur with only a modest recovery of lake herring because the spread between egg thiamine levels associated with EMS and other effects that result from an alewife diet (eg. <3 nmol/g), and that associated with a lake herring diet (e.g. >20 nmol/g) is so broad. (J. Fitzsimons, unpub. data, Fitzsimons et al. 1998, Brown et al. 1998). These effects may be greatest if lake herring occur in the diet part of the time and in the absence of other thiaminase-containing prey, and at a time when they result in the maximum transfer of thiamine to the developing ovaries. The benefits of a partially restored lake herring population may also be enhanced by the particular strain of lake trout used since lake herring exhibit temperature preferenda that differ from alewives and there is evidence that some strains like the Seneca Lake strain, occur at colder temperatures at greater depths. In Lake Superior, the greater feeding depths occupied by siscowets inferred from stable-isotope analysis, were associated with less smelt in the diet than for lean lake trout (Harvey and Kitchell 2000).

Recent studies of the Cayuga Lake fishes linked thiaminase-induced deficiency to impaired migratory ability in pre-spawning steelhead and reduced male fertility in Atlantic salmon (Ketola and NYS-DEC). While impacts on eggs have been recognized, reduced male fertility presents another obstacle to restoration efforts. Impaired migration limits the availability of spawning habitat and spawning success of anadromous fishes and consequently the distribution of their fry and the habitat they encounter. Therefore, a better understanding of the factors affecting (1) thiaminase activity and abundance of key forage fishes and (2) the magnitude of the impacts of thiaminase in wild predatory fishes is needed.

To reduce losses, an increasing number of hatcheries routinely practice thiamine immersions of affected fry of lake trout, coho salmon and steelhead after they develop thiamine-deficiency signs. It is not known if subtle effects of deficiency persist after affected fry are immersed. Because chronic deficiency of thiamine in other animals can cause lasting neurological injury, it seems likely that there may be yet unrecognized lasting neurological or behavioral impacts on affected fish after stocking. Therefore, studies are needed to better understand any lasting physiological and behavioral impacts of thiamine deficiency in deficient immersed in thiamine in hatcheries.

Landlocked salmon reared in a hatchery on the Saint Marie's River and released in the river grow well and later return to spawn; however, approximately half produce viable eggs containing abundant thiamine and half produce non-viable eggs containing inadequate thiamine (Ketola and coworkers). These fish apparently eat different diets although they have the same general genetic and historical background. Landlocked salmon in Maine coexist in lakes with alewives without apparent impact. Investigation of these observations and other similar ones could provide valuable insights into why some fish which would be expected to be susceptible to thiamine deficiency but do not develop any deficiency.

We propose that studies should include systematic monitoring of the thiaminase status of key forage fishes and the thiamine status of important predators in several Great Lakes as well as key potential indicator inland lakes (i.e., Cayuga Lake) in order to establish the magnitude, trend lines and directions for the EMS syndrome which are essential to demonstrate any effects of future restoration efforts. We also propose that studies to better understand how various important species of fish are affected by thiamine deficiency and how adults, juveniles and embryos are impacted. Impacts evaluated should include but not be limited to--reproduction, physiology, behavior, and ecological impacts. Also, in order to better identify and manage fisheries, studies are needed to determine critical levels of thiamine in eggs and tissues indicative of supporting normal health of the important species of fishes. The New York State-owned fish ladder on Cayuga Inlet has served as an excellent natural laboratory for the study in thiaminase-induced deficiency in Atlantic salmon and steelhead (Fisher et al. 1996; Ketola et al. 2000) and should continue to provide an excellent model for the study of the impacts of thiaminase-induced deficiencies in feral adults, eggs, embryos and juvenile Atlantic salmon and steelhead that exhibit thiaminase-induced deficiency of thiamine.

Eshenroder, RL and CC Krueger. Reintroduction of Native Fishes to the Great Lakes Proper: A Research Theme Area. GLFC-BOTE Theme Area, April 3, 2002, http://www.glfc.org/research/Nativefish.htm

Exotic Invertebrates and Food-Web Disruption, GLFC-BOTE Theme Area, http://www.foodwebdisruption.org

Fisher, J. P., J. D. Fitzsimons, G. F. Combs, Jr., and J. M. Spitsbergen. 1996. Naturally occurring thiamine deficiency causing reproductive failure in Finger Lakes Atlantic salmon and Great Lakes lake trout. Transactions of the American Fisheries Society 125:167-178.

Fisher, J.P., S.B. Brown, G.A. Wooster, and P.R. Bowser. 1998. Maternal blood, egg and larval thiamin levels correlate with larval survival in landlocked Atlantic salmon (Salmo salar). Journal of Nutrition 128:2456-2466.

Great Lakes Fish Health Committee - Research Priorities October 21, 2002, http://www.glfc.org/research/GLFHCResearchpriorities.pdf

Great Lakes Fishery Commission. 1992. Strategic Vision of the Great Lakes Fishery Commission for the Decade of the 1990s. Great Lakes Fishery Commission, Ann Arbor, MI.

Great Lakes Fishery Commission. 1997. A Joint Strategic Plan for Management of Great Lakes Fisheries. Ann Arbor, MI. (Supersedes 1994 version).

Great Lakes Fishery Commission, Board of Technical Experts. 1999. Report on Early Mortality Syndrome Workshop.

Great Lakes Fishery Commission, Board of Technical Experts. 2000. Research Task Report: Report on Early Mortality Syndrome Workshop.

Great Lakes Fishery Commission, Board of Technical Experts. 2002. Research Status Report on Early Mortality Syndrome.

Honeyfield, D. C., J. G. Hnath, J. Copeland, K. Dabrowski, and J. H. Bloom. 1998. Thiamine, ascorbic acid and environmental contaminants in Lake Michigan coho salmon displaying early mortality syndrome. Pages 135-144 in G. McDonald, J. Fitzsimons and D.C. Honeyfield (Eds). Early life stage mortality syndrome in fishes of the Great Lakes and Baltic Sea. Symposium 21, American Fisheries Society, Bethesda, MD 20814.

International Joint Commission, Science Advisory Board Report, 2001-2003.

Ketola, H.G., P.R. Bowser, G.A. Wooster, L.R. Wedge, and S.S. Hurst. 2000. Effects of thiamine on reproduction of Atlantic salmon and a new hypothesis for their extirpation in Lake Ontario. Transactions of the American Fisheries Society 129: 607-612.

McDonald, Gordon, John D. Fitzsimons, and Dale C. Honeyfield, editors. 1998. Early life stage mortality syndrome in fishes of the Great Lakes and Baltic Sea. American Fisheries Society Symposium 21.

Reproductive Disturbances in Baltic Sea Fish: An International Perspective. 1999. Ambio 28(1): 1-109.

Stephen, C and M Thorburn. 2002. Formulating a vision for fish health research in the Great Lakes. Report to the Great Lakes Fishery Commission. June 2002.

Last Modified: October 01, 2004 09:32am
Contact: GS-B-GLSC-WebMaster@usgs.gov
URL: www.glsc.usgs.gov/main.php?content=research_initiatives_thiamine&title;=Initiatives0&menu;=research