Recommended Citation Czesny, Sergiusz; Dettmers, John M.; Rinchard, Jacques; and Dabrowski, Konrad, "Linking Egg Thiamine and Fatty Acid Concentrations of Lake Michigan Lake Trout with Early Life Stage Mortality" (2009). Environmental Science and Biology Faculty Publications. Paper 2. http://digitalcommons.brockport.edu/env_facpub/2
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Journal of Aquatic Animal Health 21:262–271, 2009 Ó Copyright by the American Fisheries Society 2009 DOI: 10.1577/H07-056.1
Linking Egg Thiamine and Fatty Acid Concentrations of Lake Michigan Lake Trout with Early Life Stage Mortality SERGIUSZ CZESNY*
JOHN M. DETTMERS1
University of Illinois, Illinois Natural History Survey, Lake Michigan Biological Station, 400 17th Street, Zion, Illinois 60099, USA
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School of Environment and Natural Resources, The Ohio State University, Columbus, Ohio 43210, USA Abstract.—The natural reproduction of lake trout Salvelinus namaycush in Lake Michigan is thought to be compromised by nutritional deficiency associated with inadequate levels of thiamine (vitamin B1) in their eggs. However, mortality driven by thiamine deficiency (commonly referred to as early mortality syndrome [EMS]) is not the only significant cause of low lake trout survival at early life stages. In this study, we sought to better understand the combined effects of variable levels of thiamine and fatty acids in lake trout eggs on prehatch, posthatch, and swim-up-stage mortality. We sampled the eggs of 29 lake trout females from southwestern Lake Michigan. The concentrations of free thiamine and its vitamers (e.g., thiamine monophosphate [TMP] and thiamine pyrophosphate [TPP]) as well as fatty acid profiles were determined in sampled eggs. Fertilized eggs and embryos were monitored through the advanced swim-up stage (1,000 degree-days). Three distinct periods of mortality were identified: prehatch (0–400 degree-days), immediately posthatch (401–600 degree-days), and swim-up (601–1,000 degree-days). Stepwise multiple regression analysis revealed (1) that cis-7-hexadecenoic acid in both neutral lipids (NL) and phospholipids (PL) correlated with prehatch mortality, (2) that docosapentaenoic acid in PL and docosahexaenoic acid in NL correlated with posthatch mortality, and (3) that total lipids, TPP, and palmitoleic acid in NL, linoleic acid, and palmitic acid in PL correlated with the frequency of EMS. These results indicate the complexity of early life stage mortality in lake trout and suggest that inadequate levels of key fatty acids in eggs, along with variable thiamine content, contribute to the low survival of lake trout progeny in Lake Michigan.
A self-sustaining status for the Lake Michigan populations of lake trout Salvelinus namaycush is a primary but unmet goal of fisheries managers. Historically, the lake trout thrived in its native habitats of Lake Michigan, constituting one of the largest fisheries for this species in the world. By the early 1950s, however, a combination of overfishing, predation by sea lampreys Petromyzon marinus, the invasion of alewives Alosa pseudoharengus, and habitat degradation caused this native predator to become nearly extinct (Hile et al. 1951; Eschmeyer 1957). Since then, large numbers of hatchery-origin lake trout have been stocked every year in an effort to reestablish natural recruitment in Lake Michigan. Although these fish generally survive to adulthood and some are capable of * Corresponding author: [email protected] 1 Present address: Great Lakes Fishery Commission, 2100 Commonwealth Boulevard, Suite 100, Ann Arbor, Michigan 48105, USA. 2 Present address: Department of Environmental Science and Biology, State University of New York, the College at Brockport, 350 New Campus Drive, Brockport, New York 14420, USA. Received December 26, 2007; accepted January 5, 2009 Published online December 14, 2009
producing viable eggs, no significant natural recruitment has been recorded. Bronte et al. (2008) provides an extensive summary of rehabilitation efforts while highlighting impediments to the restoration of lake trout in Lake Michigan. It appears that early mortality syndrome (EMS) and predation on eggs and alevins, along with lakewide population levels that are too low and improper stocking practices are contributing to the lack of natural recruitment of lake trout. Thus far, no single factor has been identified as the prime hindrance to natural recruitment. Nutritional deficiencies associated with inadequate levels of thiamine (vitamin B1) in the eggs have resulted in high mortalities at the swim-up stage of several salmonid species in the Great Lakes (Marcquenski and Brown 1997; Brown et al. 1998a), New York’s Finger Lakes (Fisher et al. 1995), and the Baltic Sea (Amcoff et al. 1998). Mortality caused by thiamine deficiency, commonly referred to as EMS, is a likely effect of the maternal diet’s containing a large proportion of prey fish with high levels of thiaminase, an enzyme that degrades thiamine. High levels of thiaminase are found in forage species such as alewives and rainbow smelt Osmerus mordax (Tillitt et al. 2005). Thus, EMS may be a significant bottleneck to
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EGG THIAMINE AND FATTY ACIDS IN LAKE TROUT
lake trout recruitment (Brown et al. 2005b) because alewives are a major component of their diet in Lake Michigan (Madenjian et al. 1998). Lake trout offspring affected by EMS die at the swim-up stage (anywhere between 600 and 1,000 cumulative degree-days after fertilization). However, significant mortality at earlier life stages (embryonic and immediately after hatch) has also been observed. Blue sac disease, which induces mortality after hatch but before the onset of EMS, has been linked to dioxin exposure. Exposure to dioxins results in oxidative stress associated with the peroxidation of lipid membranes and leads to edema, hemorrhaging, and ultimately mortality (Cantrell et al. 1998). Of all lipids, polyunsaturated fatty acids, which are major components of all biomembranes, are especially susceptible to the oxidative action of free radicals and thus a leading factor in the deterioration of membrane functions. Lipids, particularly polyunsaturated fatty acids (PUFAs), have been recognized to play important roles in regulating and maintaining the overall fitness of fish and population stability (Adams 1998). Fish eggs contain high levels of PUFAs that later, during embryonic development, provide adequate biomembrane fluidity (Hazel 1989). A high level of PUFAs in phospholipids is a critical adaptation in ectotherms because low temperatures could hinder membrane function and cellular metabolism. Several studies have documented that the successful reproductive performance of a fish population is strongly linked to the availability of lipid reserves for gonad development. Lipid energy stored in the livers of mature female Atlantic cod Gadus morhua in the Barents Sea was used as a predictor of their reproductive potential and recruitment (Marshall et al. 1999). It is well established in teleost fish that PUFAs of both the omega-6 (n-6) and omega-3 (n-3) families, that is, arachidonic acid (AA; 20:4[n-6]),3 eicosapentaenoic acid (EPA; 20:5[n3]), and docosahexaenoic acid (DHA; 22:6[n-3]) are required to ensure optimal survival, growth, and development (Watanabe et al. 1982; Sargent et al. 1989; Sargent 1995). Newly hatched fish are especially vulnerable to deficiencies associated with inadequate amounts of PUFAs in their yolk reserves because their rapidly developing tissues, especially the nervous system (including the eyes), requires large quantities of these fatty acids for proper functioning. Thus, any deficien3 In the terms such as 20:4(n-6), the number to the left of the colon is the number of carbon atoms in the compound, the number immediately to the right of the colon is the number of double bonds, and the number after the hyphen indicates the position of the first double bond from the methyl end.
cies, imbalance, or disturbance in the synthesis of fatty acids in the yolk and in the developing embryo may contribute to increased mortality before or shortly after hatch. In rainbow trout Oncorhynchus mykiss broodstock, a diet deficient in n-3 fatty acids decreased the number and size of eggs (Watanabe et al. 1984), increased the incidence of early embryonic mortality, and caused physiological dysfunction of the developing fish (Watanabe et al. 1982). On the contrary, high levels of dietary n-3 PUFAs were also associated with reduced egg production and caused yolk sac hypertrophy and decreased survival in gilthead bream Sparus auratus larvae (Fernandez-Palacios et al. 1995). The negative effects of both high and low levels of n-3 PUFAs indicate that an intermediate level is required to ensure the best reproductive responses. In earlier work, we have demonstrated that proper DHA:EPA and n3:n-6 PUFA ratios are important factors in the survival of larval walleyes Sander vitreus (Czesny et al. 1999). Adequate levels of fatty acids in the cellular membranes of embryos and early life stages of deve...