Citation: Marcquenski, S.V. and S.B. Brown. 1997. Early mortality syndrome (EMS) in salmonid fishes from the Great Lakes. IN Rolland, R.M., Gilbertson, M., Peterson, R.E., eds. "Chemically induced alterations in functional development and reproduction of fishes." SETAC Press. Pensacola, FL.

Executive Summary

From 1968 to the present, early life stage mortality has been documented in salmonids from Lakes Ontario, Michigan, and to a lesser extent, Huron and Erie. Species exhibiting mortality include lake trout (Salvelinus namaycush), chinook salmon (Oncorhynchus tshawytscha), coho salmon (Oncorhynchus kisutch), steelhead (Oncorhynchus mykiss), and brown trout (Salmo trutta). Mortality was first observed by hatchery personnel responsible for rearing progeny from feral broodstocks that mature in these Great Lakes. Hatcheries in the Province of Ontario and in the U.S. states bordering the Great Lakes depend on these feral broodstocks for eggs to sustain a multi-million dollar sport fishery. Although this mortality has only been observed in fish culture situations, it likely contributes to the lack of natural lake trout reproduction in Lake Michigan and Lake Ontario.

Early life stage mortality was variable from 1968 through 1992 and tended not to exceed 20-30% for any species. Hatcheries compensated by simply increasing the number of eggs collected during spawning. However, in January, 1993, coho mortality dramatically increased to 60-90% in Wisconsin, Illinois, Indiana, and Michigan hatcheries. Mortality in other Lake Michigan salmonids also increased, but did not reach these extreme levels. Hatcheries could no longer compensate for these catastrophic losses by collecting more eggs. Eggs from the Pacific Coast could not be imported into the Great Lakes Basin due to concerns about non-indigenous pathogens such as Infectious Hematopoietic Necrosis Virus and Viral Hemorrhagic Septicemia Virus. This prompted the Great Lakes Fishery Commission to sponsor two workshops to facilitate renewed and more extensive investigations into the cause(s) of these early life stage mortalities.

The term Early Mortality Syndrome (EMS) was developed at the first workshop and by definition includes present and historic early life stage mortalities that share common features and affect salmonids in the Great Lakes. As a result of the two workshops, thiamine (Vitamin B1) deficiency was implicated as a possible cause of EMS. Low levels of thiamine have also been associated with two other early life stage mortality syndromes affecting Atlantic salmon (Salmo salar) in New York Finger Lakes (Cayuga Syndrome) and in the Baltic Sea (M74). It is unclear at present why thiamine levels are so low in salmonid eggs in several Great Lakes, New York Finger Lakes, and the Baltic Sea. There is a need for coordinated research at the laboratory and ecosystem level to reveal the underlying mechanisms causing these thiamine responsive syndromes.

Clinical Signs of Early Mortality Syndrome

Clinical signs of EMS are similar among species and over time, but differ from blue sac and dioxin toxicity based on descriptions from earlier published studies (Symula et al. 1990; Walker et al. 1991) and present observations. Signs of EMS include loss of equilibrium, swimming in a spiral or corkscrew pattern, lethargy, dark pigmentation, hyperexcitability when touched, failure to feed, tetany, hemorrhages in various locations, hydrocephalus and death (Johnson and Pecor, 1969; Pecor, 1972; Degurse et al., 1973; Frimeth, 1990; Wisconsin Department of Natural Resources and Michigan Department of Natural Resources, unpublished data; Great Lakes Fishery Commission, 1994; Mac et al., 1985; Mac, 1988; Mac et al., 1993; Fitzsimons et al., 1995; Fitzsimons, 1995; Skea et al., 1995).

Within a species, progeny from different females have variable mortality rates (5-100%), suggesting there is a female-dependent "factor" involved in the syndrome. The intestine of most dead fry is empty, however death due to EMS occurs before death due to starvation (Skea et al., 1985). It appears that fry with EMS do not completely utilize the yolk because they have larger amounts of residual yolk than healthy fry of the same age (Great Lakes Fishery Commission, 1994).

Before January 1993, the onset of EMS in coho and other salmonids from Lake Michigan was predictable and occurred at the swim-up stage, continuing into the feeding fry stage. Death occurred over 10-14 days and mortality rates ranged from 10-20%. However, from January 1993 to 1996, mortality occurred at the sac-fry stage in coho and chinook salmon, brown trout, and steelhead progeny from Lake Michigan broodstocks. Mortality was also observed in coho embryos during the late eyed egg stage. Coho and other salmonid fry mortality occurred over a longer period and the number of fry that died was three times greater than in 1986 and 1987.

Possible Cause(s) of Early Mortality Syndrome The catastrophic increase in coho fry mortality in 1993 prompted the Fish Health Committee and the Board of Technical Experts of the Great Lakes Fishery Commission to sponsor two EMS workshops (July 12-14, 1994 in Ann Arbor, MI and February 2-3, 1995 in Romulus, MI). Hypotheses regarding possible cause(s) of EMS were solicited from experts and presented at the first workshop. Topics included hatchery cultural techniques, broodstock management, genetics (inbreeding), pathogens, nutrition, ecosystem changes, and known contaminants such as PCBs. Invited experts presented evidence that supported or refuted these hypotheses as likely causes of EMS based on epidemiological criteria (Fox, 1991). Full summaries of these presentations can be found in the Proceedings of a Workshop on EMS-Early Mortality Syndrome 1994; copies may be obtained from the Great Lakes Fishery Commission, Ann Arbor, Michigan. The following is a synopsis of the highlights of the workshops.

Fish Culture- Questionnaires were sent to hatcheries that had experienced EMS epizootics. Hatchery personnel responded to questions pertaining to cultural techniques (water temperature, dissolved oxygen, alkalinity, type of incubator, type of feed). Responses indicated that these factors were variable among the hatcheries and thus no cultural factor or set of factors was common to all hatcheries where EMS occurred.

Broodstock Management and Genetics- Feral salmonid broodstocks support state and provincial stocking programs in Lake Michigan and Lake Ontario. Spawning practices have remained basically the same for the past 30 years. There has not been an "infusion" of new genetic material into the Great Lakes since the early 1970's, which may have resulted in a tendency toward inbreeding. However, inbreeding by itself does not appear to cause EMS. There is anecdotal evidence that chinook eggs obtained from Lake Michigan and transferred to Minnesota hatcheries developed EMS as expected. Surviving fish were stocked into Lake Superior. When the fish matured, eggs were collected, reared in hatcheries and EMS did not occur (Darryl Bathel, Minnesota Department of Natural Resources, pers. comm.). Similarly, EMS does not occur in Seeforellen brown trout maintained as a captive broodstock by the state of Michigan, however progeny from Seeforellen brown trout that mature in Lake Michigan do experience EMS (Steve Fajfer, Wisconsin Department of Natural Resources, pers. comm.). It is unlikely that EMS results from inbreeding. EMS is only expressed in progeny from salmonids that mature under environmental conditions present in Lakes Michigan and Ontario, and to a lesser extent, Huron and Erie.

Pathogens- Since 1989, fry with EMS were screened for pathogens using standard cultural techniques, histopathology and electron microscopy. Aside from opportunistic infections of bacterial gill disease, pathogens were not detected in the fry.

Ecosystem Change- Significant changes in the abundance of Lake Michigan forage fish occurred in the mid to late 1980's and concomitant introductions of exotic species such as the spiny water flea (Bythotrephes cedarstroemi) and zebra mussels (Dreissena polymorpha) were also observed. Monitoring the sport harvest in Wisconsin waters has shown that Lake Michigan salmonids have not changed their dietary preference for alewife (Alosa pseudoharengus) (Paul Peeters, Wisconsin Department of Natural Resources, pers. comm.). Primary productivity has decreased in Lake Ontario over the past 15 years (Johengen et al., 1994). The biomass of alewife and rainbow smelt (Osmerus mordax) declined over the same period due to a combination of decreased lake productivity and increased predation pressure by salmonines (Rand et al., 1994). Food web interactions are complex, and further study is needed to clarify the relationship between ecosystem changes and EMS prevalence in Lake Michigan and Lake Ontario.

Contaminants- A direct link between contaminants and EMS has not been established despite many attempts (Pecor, 1972; Degurse et al., 1973; Skea et al., 1985; Mac et al., 1993; Fitzsimons et al., 1995). While recognizing this lack of evidence, workshop participants felt that contaminants might be important in the etiology of EMS because concentrations are highest in the Lakes where EMS mortality is greatest (Lake Michigan and Lake Ontario). Recent work has shown that there may be interactions between thiamine and contaminants such as 2,3,7,8-TCDD. Eggs injected with 2,3,7,8,-TCDD and immersed in thiamine solutions during egg and fry development had higher survival and fewer signs of TCDD toxicity (yolk-sac edema, cranio-facial deformities, etc.) than injected eggs that were incubated without thiamine treatments (Tillitt et al., 1996).

Nutrition- Compelling evidence supporting a nutrition based hypothesis was presented by John Fitzsimons, Department of Fisheries and Oceans, Burlington, Ontario. His initial experiments showed that EMS could be prevented or ameliorated by injecting lake trout fry with thiamine, Vitamin B1 (Fitzsimons, 1995). This surprising observation provided a stepping stone for others working on EMS and similar early life stage mortalities. Those attending the workshop agreed that further work was needed to clarify the relationship between thiamine and EMS, and whether other factors such as contaminants are also important in its etiology.

Most clinical signs of EMS are consistent with signs of thiamine deficiency: loss of equilibrium, hemorrhage, and ataxia (Halver 1989). Fitzsimons (1995) and Hornung et al. (1996) have improved fry survival in "at risk" populations by administering thiamine to freshly fertilized eggs, sac-fry, or combinations of the two. Mortality due to EMS was almost completely prevented by immersing newly fertilized coho eggs in 480 or 960 ppm thiamine HCl during water hardening; untreated controls exhibited 29% mortality (Hornung et al., 1996). Hornung et al. (1996) also showed that water hardening steelhead eggs in 480 ppm thiamine HCl and immersing the resultant fry three weeks after hatch in 480 ppm thiamine HCl decreased EMS mortality from 72% to 27%. Similar treatments are now used on a production scale by hatcheries in Wisconsin, Illinois, Indiana, and Michigan to increase survival of coho, chinook, steelhead and brown trout that develop EMS.

Thiamine is an essential B vitamin and is important as a coenzyme for two reactions that are part of carbohydrate metabolism. A deficiency of thiamine causes beriberi in people and polyneuritis in birds. The neurological signs observed in fry with EMS (loss of equilibrium, corkscrew or spiral swimming) are consistent with signs of thiamine deficiency. Related Syndromes

Researchers investigating early life stage mortalities of Atlantic salmon presented information on "Cayuga Syndrome" and "M74" at the Second EMS Workshop in Romulus, Michigan. In a reciprocal exchange, several North American researchers studying EMS presented their findings at the Second Workshop on Reproduction Disturbances in Fish, held November 20-23, 1995, in Stockholm, Sweden. The American Fisheries Society and the Great Lakes Fishery Commission sponsored a symposium entitled "Early Mortality Syndrome: Reproductive Disruptions in Fish from the Great Lakes, New York Finger Lakes, and the Baltic Region" on August 28, 1996 in Dearborn, Michigan. The extent of current knowledge regarding EMS, M74, and Cayuga Syndrome is due to the great level of cooperation among scientists from North America and Europe. The following are brief synopses of Cayuga Syndrome and M74.

Cayuga Syndrome

Cayuga Syndrome is a sac-fry mortality syndrome affecting progeny of Atlantic salmon that mature in Cayuga Lake, Keuka Lake and Seneca Lake (all New York Finger Lakes). This syndrome was first observed in 1974 at the New York State Department of Environmental Conservation hatchery in Rome, NY (Fisher et al., 1995a). Fisher et al. (1995b) have suggested that Cayuga Syndrome is caused by a naturally occurring thiamine deficiency. Low thiamine levels in eggs may result from broodstocks feeding extensively on alewife which contain thiaminase, an enzyme that destroys thiamine (Greig and Gnaedinger, 1971). Clinical signs of this syndrome include yolk-sac opacities, subcutaneous, pericardial and retrobulbar edemas, vitelline congestion or hemorrhage, branchial congestion, foreshortened maxillae, hydrocephalus, and death. Mortality occurs during the sac-fry stage and affects 100% of the fry from an individual female (Fisher et al., 1995a). The syndrome can be reversed by administering thiamine to affected fry, and concentrations of thiamine in the fry are very low (Fisher et al., 1996). No relation between pathogens and/or contaminants and sac-fry mortality was found (Fisher et al., 1995a).

M74

M74 is a sac-fry mortality syndrome affecting progeny from Atlantic salmon that mature in the Baltic Sea (Norrgren et al., 1993; Bengtsson et al., 1994; Karlsson et al., 1996) and progeny from sea trout (Salmo trutta) in Swedish and Finnish waters of the Baltic Sea (Soivio, 1996). M74 was first described in 1974. >From 1974 to 1991, mortality was generally less than 30%. In 1992 mortality increased, reaching 80-90% in 1993 and declining to about 55% in 1995 (B"rjeson, 1996). As is the case with Cayuga Syndrome, M74 affects 100% of the fry from a specific female, suggesting a female-dependent factor is involved. Clinical signs include initial hyperactivity, lack of coordination, hyper-pigmentation, yolk-sac precipitate, lethargy with sudden outbursts of swimming, and exophthalmia. Fry may show signs of M74 throughout the sac-fry stage, however individuals generally die within 3-5 days after clinical signs appear (Lundstr"m et al., 1996).

Egg color is variable among Atlantic salmon from the Baltic Sea due to the amount of astaxanthin (a carotenoid) in the egg. Lignell (1994) has shown a relationship between the occurrence of M74 and yellow eggs (eggs with low astaxanthin levels). Low levels of antioxidants such as astaxanthin may put the fry at risk for oxidative stresses such as lipid peroxidation (Pettersson and Lignell, 1996).

Based on the therapeutic effect of thiamine to reduce EMS mortality in lake trout (Fitzsimons, 1995), similar treatments were administered to Atlantic salmon exhibiting M74. Survival was higher in treated fry compared to untreated controls (Bylund and Lerche, 1995). Amcoff et al. (1996) measured lower levels of thiamine in newly fertilized Atlantic salmon eggs (0.19 nmol/g) and fry (0.09 nmol/g) that exhibited M74 compared to those that did not: (eggs, 1.70 nmol/g; fry 1.27 nmol/g). These authors also prevented mortality due to M74 by immersing fry in 500 ppm thiamine-enriched water. There may be a thiamine threshold that determines whether or not fry develop M74. Of 44 family groups for which egg concentrations of thiamine were below 0.33 nmol/g, 43 developed M74.

Significant ecosystem changes have occurred in the Baltic Sea over the past 20 years. Infrequent infusions of salt water from the Atlantic Ocean have decreased salinity in the Main Basin. This has decreased the recruitment of Baltic cod which is the primary piscivore in the Baltic Sea. The decline of Baltic cod decreased predation on Baltic herring (Clupea harengus) and sprat (Clupea sprattus), causing a dramatic increase in the biomass of the clupeid populations. Both species contain thiaminase and are also utilized as forage by Atlantic salmon.

Conclusions

At present, the etiologies of EMS, Cayuga Syndrome and M74 are not completely understood. Current information supports the hypothesis that Cayuga Syndrome is the consequence of a thiamine deficiency based on the extensive consumption of forage containing thiaminase. All three syndromes affect top salmonid predators in ecosystems with simple food webs. Several forage species in these food webs contain thiaminase. The Great Lakes and the Baltic Sea ecosystems have undergone dramatic changes over the past 20 years e.g. shifts in forage abundance, introductions of exotic species at multiple trophic levels, and changes in the biomass of top piscivores. These two ecosystems have been exposed to various levels of xenobiotic compounds during the past 50 years which differentiates them from the New York Finger Lakes. EMS, M74 and Cayuga Syndrome can be prevented by exposing eggs and/or fry to thiamine solutions. Thiamine levels in eggs from family groups that go on to develop EMS, Cayuga Syndrome, or M74 are low compared to levels in eggs from reference sites. In the Baltic region, carotenoids like astaxanthin appear important in the etiology of M74, but a similar relationship has yet to be demonstrated for the Great Lakes. The temporal coincidence of dramatic increases in M74 mortality (peaking in 1993) and EMS mortality (peaking in 1993) suggests factors that may act on a global scale. Although there are still many unknowns regarding the etiology of EMS, M74 and Cayuga Syndrome, substantial progress has been made in a relatively short time. This level of achievement is due to interagency partnerships and professional cooperation among scientists studying these syndromes in North America and the Baltic region.

Focus of future EMS research

Although hatchery personnel are able to reduce EMS mortality by administering thiamine to eggs or fry, there is still a need to understand the underlying causes of this syndrome. Other species such as yellow perch (Perca flavescens) and bloater chub (Coregonus hoyi) have demonstrated poor recruitment during the 1990's in Lake Michigan, which overlaps the period of increased EMS mortality observed in salmonids. It is unknown whether this poor recruitment is related to an EMS-like syndrome. There is strong evidence that a deficiency of thiamine predisposes eggs/fry to develop EMS. Future research must discover why thiamine levels are so low in eggs from salmonids that mature in Lake Michigan and Lake Ontario (and to a lesser extent, Lake Huron and Lake Erie) and whether non-salmonids demonstrate similar early life stage mortalities. The following areas for further research were proposed at the conclusion of the EMS Symposium in Dearborn, Michigan:

1. Thiamine concentrations in eggs are regulated by the diet of the female parent. Forage species containing thiaminase may reduce levels of thiamine in the parent available for transport into the egg.

2. There may be interactions between thiamine and contaminants such as dioxin that reduce the amount of thiamine available for normal metabolism.

3. It is possible that thiamine may function in a non-vitamin role similar to the antioxidant properties of Vitamins A, E, and C. Work in the lab could explore functions and interactions among these vitamins, including whether they protect developing eggs and fry from oxidative stresses.

4. There may be a shift in the abundance of thiamine produced at lower trophic levels (yeast, bacteria, algae) due to the presence of new exotic species (zebra mussel, Bythotrephes cedarstroemi).

5. There may be interference in the transport of thiamine from the female parent to the egg.

This is not an all inclusive list, but clearly indicates the need for work at the ecosystem level as well as manipulations in the laboratory to understand the mechanisms that cause EMS.

References

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