Skip to main content
Log in

Reduced thiamine utilization by Seneca Lake lake trout embryos and potential implications to restoration of lake trout in the Great Lakes

  • Published:
Environmental Biology of Fishes Aims and scope Submit manuscript

Abstract

Lake trout stocks in the Great Lakes basin show variability in the relationship between a thiamine-dependent early mortality syndrome (EMS) and egg thiamine (B1) concentration but the reasons are unclear. EMS has been linked to a diet of alewives and their high thiaminase activity. We examined the relationship among four alewife-dependent B1-deficient lake trout stocks, and determined B1 utilization rates for three of these stocks, and a non-alewife-dependent B1-replete stock. Although the EMS-B1 relationship was similar between an inland lake stock and Lake Ontario, there was almost no EMS in lake trout from two Finger Lakes: Cayuga (CL) and Seneca (SL) Lakes. B1 utilization rate for the SL stock was lower than for all other stocks. Similarity in the EMS-B1 relationship (CL, SL) and reduced thiamine utilization in the SL stock suggests that Finger Lakes lake trout are better able to cope with the low egg thiamine concentration resulting from an alewife diet. Reduced thiamine utilization during the embryonic stage, possibly as a result of adaptive genetic variation, may result in a greater contribution by Seneca Lake strain lake trout to wild lake trout populations in the Great Lakes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Data availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

  • Balk L, Hagerroth PA, Gustavsson H, Sigg L, Akerman G, Ruiz Munoz Y, Honeyfield DC, Tjarnlund U, Oliveira K, Ström K, McCormick SD, Karlsson S, Ström M, van Manen M, Berg AL, Halldorsson HP, Strömquist J, Collier TK, Börjeson H, Mörner T, Hansson T (2016) Widespread episodic thiamine deficiency in Northern Hemisphere wildlife. Scien Rep 6:38821

    Article  CAS  Google Scholar 

  • Bean TH (1884) On the occurrence of the branch alewife in certain lakes of New York. Section 1. In: Goode GB (ed) The fisheries, and fishery industries of the United States. U.S. Government Printing Office, Washington, D.C, pp 588–593

    Google Scholar 

  • Bettendorff L (2013) Thiamine. In: Zempleni J, Suttie JW, Gregory JF, Stover PJ (eds) Handbook of vitamins, 5th edn. CRC Press, Boca Raton, pp 267–324

    Google Scholar 

  • Brandt SB (1986) Food of trout and salmon in Lake Ontario. J Great Lakes Res 12:200–205

    Article  Google Scholar 

  • Bronte CR, Holey ME, Madenjian CP, Jonas JL, Claramunt RM, McKee PC, Toneys ML, Ebener MP, Breidert B, Fleischer GW, Hess R, Martell AW, Olsen EJ (2007) Relative abundance, site fidelity, and survival of adult lake trout in Lake Michigan from 1999 to 2001: implications for future restoration strategies. N Am J Fish Manage 27:137–155

    Article  Google Scholar 

  • Bronte CR, Ebener MP, Schreiner DR, DeVault DS, Petzold MM, Jensen DA, Richards C, Lozano SJ (2003) Fish community change in Lake Superior, 1970–2000. Can J Fish Aquat Sci 60:1552–1574

    Article  Google Scholar 

  • Brown SB, Honeyfield DC, Vandenbyllaardt L (1998b) Thiamine analysis in fish tissues. In: McDonald G, Fitzsimons JD, Honeyfield DC (eds) Early life stage mortality syndrome in fishes of the Great Lakes and Baltic Sea. American Fisheries Society, Symposium 21, Bethesda, Maryland pp 73–81

  • Brown S B, Fitzsimons JD, Palace VP, Vandenbyllaardt L (1998a). Thiamine and early mortality syndrome in lake trout (Salvelinus namaycush). In: McDonald G, Fitzsimons JD, Honeyfield DC (eds) Early life stage mortality syndrome in fishes of the Great Lakes and Baltic Sea. American Fisheries Society, Symposium 21, Bethesda, Maryland pp 18–25

  • Carlson SM, Cunningham CJ, Westley PAH (2014) Evolutionary rescue in a changing world. Trend Ecol Evol 29:521–530

    Article  Google Scholar 

  • Carvalho PSM, Tillitt DE, Zajicek JL, Claunch RA, Honeyfield DC, Fitzsimons JD, Brown SB (2009) Thiamine deficiency effects on the vision and foraging ability of lake trout fry. J Aquat Anim Health 21:315–325

    Article  PubMed  Google Scholar 

  • Christie MR, Sepúlveda MS, Dunlop ES (2019) Rapid resistance to pesticide control is predicted to evolve in an invasive fish. Sci Rep 9:1–13

    Article  CAS  Google Scholar 

  • Czesny S, Dettmers JM, Rinchard J, Dabrowski K (2009) Linking egg thiamine and fatty acid concentrations of Lake Michigan lake trout with early life stage mortality. J Aquat Anim Health 21:262–271

    Article  PubMed  Google Scholar 

  • Czesny S, Rinchard J, Lee BJ, Dabrowski K, Dettmers JM, Cao Y (2012) Does spatial variation in egg thiamine and fatty-acid concentration of Lake Michigan lake trout Salvelinus namaycush lead to differential early mortality syndrome and yolk oedema mortality in offspring? J Fish Biol 80:2475–2493

    Article  CAS  PubMed  Google Scholar 

  • Daniels RA (2001) Untested assumptions: the role of the canals in the dispersal of sea lamprey, alewife, and other fishes in the eastern United States. Environ Biol Fishes 60:309–329

    Article  Google Scholar 

  • DeKoning J, Noakes M, Keatley K, Phillips R, Janssen J (2006) Genetic analysis of wild lake trout embryos recovered from Lake Michigan. Trans Am Fish Soc 135:399–407

    Article  CAS  Google Scholar 

  • Depeint F, Bruce WR, Shangari N, Mehta R, O’Brien PJ (2006) Mitochondrial function and toxicity: role of the B vitamin family on mitochondrial energy metabolism. Chem Biol Interact 163:94–112

    Article  CAS  PubMed  Google Scholar 

  • De Vault D, Dunn W, Bergqvist P-A, Wiberg K, Rappe C (1989) Polychlorinated dibenzofurans and polychlorinated dibenzo-p-dioxins in Great Lakes fish: a baseline and interlake comparison. Environ Toxicol Chem 8:1013–1022

    Article  CAS  Google Scholar 

  • Diana JS (1990) Food habits of angler-caught salmonines in western Lake Huron. J Great Lakes Res 16:271–278

    Article  Google Scholar 

  • Dunlop ES, Milne SW, Ridgway MS (2010) Temporal trends in the numbers and characteristics of Lake Huron fish schools between 2000 and 2004. J Great Lakes Res 36:74–85

    Article  Google Scholar 

  • Ellrott BE, Marsden JE (2004) Lake trout reproduction in Lake Champlain. Trans Am Fish Soc 133:252–264

    Article  Google Scholar 

  • Elrod JH, O’Gorman R, Schneider CP, Eckert TH, Schaner T, Bowlby JN, Schleen LP (1995) Lake trout rehabilitation in Lake Ontario. J Great Lakes Res 21(Suppl. 1):83–107

    Article  Google Scholar 

  • Evans DO, Willox CC (1991) Loss of exploited, indigenous populations of lake trout, Salvelinus namaycush, by stocking of non-native stocks. Can J Fish Aquat Sci 48(Suppl. 1):134–147

    Article  Google Scholar 

  • Favé M-J, Turgeon J (2008) Patterns of genetic diversity in Great Lakes bloaters (Coregonus hoyi) with a view to future reintroduction in Lake Ontario. Conserv Genet 9:281–293

    Article  Google Scholar 

  • Fisher JP, Brown SB, Wooster GA, Bowser PR (1998) Maternal blood, egg, and larval thiamin levels correlate with larval survival in landlocked Atlantic salmon (Salmo salar). J Nutr 128:2456–2466

    CAS  PubMed  Google Scholar 

  • Fisher JP, Fitzsimons JD, Combs GF, Spitsbergen JM (1996) Naturally occurring thiamine deficiency causing reproductive failure in Finger Lakes Atlantic salmon and Great Lakes trout. Trans Am Fish Soc 125:167–178

    Article  CAS  Google Scholar 

  • Fitzsimons JD (1995a) The effect of B-vitamins on a swim-up syndrome in Lake Ontario lake trout. J Great Lake Res 21(Suppl 1):286–289

    Article  CAS  Google Scholar 

  • Fitzsimons JD (1995b) A critical review of effects of contaminants on early life stage (ELS) mortality of lake trout in the Great Lakes. J Great Lakes Res 21(Suppl. 1):267–276

    Article  CAS  Google Scholar 

  • Fitzsimons JD, Brown SB (1998) Reduced egg thiamine levels in inland and Great Lakes lake trout and their relationship to diet. In: McDonald, G, Fitzsimons JD, Honeyfield DC (eds) Early life stage mortality syndrome in fishes of the Great Lakes and the Baltic Sea. American Fisheries Society, Symposium 21, Bethesda, Maryland pp 160–171

  • Fitzsimons JD, Brown SB, Honeyfield DC, Hnath JG (1999) A review of early mortality syndrome (EMS) in Great Lakes salmonids: relationship with thiamine deficiency. Ambio 28:9–15

    Google Scholar 

  • Fitzsimons JD, Brown SB, Williston B, Williston G, Brown LS, Moore K, Honeyfield DC, Tillitt DE (2009) Influence of thiamine deficiency on lake trout larval growth, foraging, and predator avoidance. J Aquat Anim Health 21:302–314

    Article  PubMed  Google Scholar 

  • Fitzsimons JD, Fodor G, Williston B, Don H, Gray B, Benner M, Breedon T, Gilroy D (2005) Deepwater spawning by lake trout (Salvelinus namaycush) in Keuka Lake, New York. J Great Lakes Res 31:1–10

    Article  Google Scholar 

  • Fitzsimons JD, Huestis S, Williston B (1995) Occurrence of a swim-up syndrome in Lake Ontario lake trout in relation to contaminants and cultural practices. J Great Lakes Res 21(Suppl 1):277–285

    Article  CAS  Google Scholar 

  • Fitzsimons JD, Vandenbyllaardt L, Brown SB (2001) The use of thiamine and thiamine antagonists to investigate the etiology of early mortality syndrome in lake trout (Salvelinus namaycush). Aquat Toxicol 52:229–239

    Article  CAS  PubMed  Google Scholar 

  • Fitzsimons JD, Williston B, Vandenbyllaardt L, El-Shaarawi A, Brown SB (2012) Use of a thiamine antagonist to evaluate the effects of thiamine deficiency on lake trout embryonic development. J Great Lakes Res 38:236–242

    Article  CAS  Google Scholar 

  • Fitzsimons JD, Williston B, Williston G, Brown L, El- Shaarawi A, Vandenbyllaardt L, Honeyfield D, Tillitt D, Wolgamood M, Brown SB (2007) Egg thiamine status of Lake Ontario salmonines 1995–2004 with emphasis on lake trout. J Great Lakes Res 33:93–103

    Article  CAS  Google Scholar 

  • Foster NR, O’Connor DV, Schreck CB (1993) Gamete ripening and hormonal correlates in three strains of lake trout. Trans Am Fish Soc 122:252–326

    Article  CAS  Google Scholar 

  • Futia MH, Connerton MJ, Weidel BC, Rinchard J (2019) Diet predictions of Lake Ontario salmonines based on fatty acids and correlations between their fat content and thiamine concentrations. J Great Lakes Res 45:934–948

    Article  CAS  Google Scholar 

  • George EM, Stott W, Young BP, Karboski CT, Crabtree DL, Roseman EF, Rudstam LG (2017) Confirmation of cisco spawning in Chaumont Bay, Lake Ontario using an egg pumping device. J Great Lakes Res 43:204–208

    Article  Google Scholar 

  • Gibson GE, Zhang H (2002) Interactions of oxidative stress with thiamine homeostasis promote neurodegeneration. Neuroch Int 40:493–504

    Article  CAS  Google Scholar 

  • Hansen MJ (1999) Lake trout in the Great Lakes: basinwide stock collapse and binational restoration. In: Taylor WW, Ferreri CP (eds) Great lakes fishery policy and management: a binational perspective. Michigan State University Press, East Lansing (MI), pp 417–453

    Google Scholar 

  • Harder AM, Ardren WR, Evans AN, Futia MH, Kraft CE, Marsden JE, Richter CA, Rinchard J, Tillitt DE, Christie MR (2018) Thiamine deficiency in fishes: causes, consequences, and potential solutions. Rev Fish Biol Fish 28:865–886

    Article  Google Scholar 

  • Harder AM, Willoughby JR, Arden WR, Christie MR (2019) Among-family variation in survival and gene expression uncovers adaptive genetic variation in a threatened fish. Mol Ecol 29:1035–1049

    Article  PubMed  CAS  Google Scholar 

  • Honeyfield DC, Daniels ME, Brown LR, Arts MT, Walsh MG, Brown SB (2012) Survey of four essential nutrients and thiaminase activity in five Lake Ontario prey fish species. J Great Lakes Res 38:11–17

    Article  CAS  Google Scholar 

  • Honeyfield DC, Hinterkopf JP, Fitzsimons JD, Tillitt DE, Zajicek JL, Brown SB (2005) Development of thiamine deficiencies and early mortality syndrome in lake trout by feeding experimental and feral fish diets containing thiaminase. J Aquat Anim Health 17:4–12

    Article  Google Scholar 

  • Honeyfield D, Murphy J, Howard K, Strasburger WW, Matz A (2016) An exploratory assessment of thiamine status in western Alaska Chinook salmon (Oncorhynchus tshawytscha). North Pac Anad Fish Comm Bull 6:21–31

    Google Scholar 

  • Houde ALS, Saez PJ, Wilson CC, Bureau DP, Neff BD (2015) Effects of feeding high dietary thiaminase to sub-adult Atlantic salmon from three populations. J Great Lakes Res 41:898–906

    Article  CAS  Google Scholar 

  • Huestis SY, Servos MR, Whittle DM, van den Heuvel M, Dixon DG (1997) Evaluation of temporal and age-related trends of chemically and biologically generated 2,3,7,8-tetrachlorodibenzo-p-dioxin equivalents in Lake Ontario lake trout, 1977–1993. Environ Toxicol Chem 16:154–164

    Article  CAS  Google Scholar 

  • Ivan L, Schmitt BR, Rose KA, Riley SC, Rose JB, Murphy CA (2018) Evaluation of the thiamine dose-response relationship for lake trout (Salvelinus namaycush) fry using an individual based model. J Gt Lakes Res 44:1393–1404

    Article  Google Scholar 

  • Jude DJ, Tesar FJ, Deboe SF, Miller TJ (1987) Diet and selection of major prey species by Lake Michigan salmonines, 1973–1982. Trans Am Fish Soc 116:677–691

    Article  Google Scholar 

  • Jurgenson CT, Begley TP, Ealick SE (2009) The structural and biochemical foundations of thiamin biosynthesis. Annu Rev Biochem 78:569–603

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Keinänen M, Uddström A, Mikkonen J, Casini M, Pönni J, Myllylä T, Aro E, Vuorinen P (2012) The thiamine deficiency syndrome M74, a reproductive disorder of Atlantic salmon (Salmo salar) feeding in the Baltic Sea, is related to the fat and thiamine content of prey fish. ICES J Mar Sci 69:516–528

    Article  Google Scholar 

  • Ketola HG, Bowser PR, Wooster GA, Wedge LR, Hurst SS (2000) Effects of thiamine on reproduction of Atlantic salmon and a new hypothesis for their extirpation in Lake Ontario. Trans Am Fish Soc 129:607–612

    Article  CAS  Google Scholar 

  • Kraft CE, Angert ER (2017) Competition for vitamin B1 (thiamin) structures numerous ecological interactions. Q Rev Biol 92:151–168

    Article  PubMed  Google Scholar 

  • Krueger CC, Ihssen PE (1995) Review of genetics of lake trout in the Great Lakes: history, molecular genetics, physiology, strain comparisons and restoration management. J Gt Lakes Res 21(Suppl 1):348–363

    Article  Google Scholar 

  • Krueger CC, Perkins DL, Mills EL, Marsden JE (1995) Predation by alewives on lake trout fry in Lake Ontario: role of an exotic species in preventing restoration of a native species. J Gt Lakes Res 21(Suppl 1):458–469

    Article  Google Scholar 

  • Ladago BJ, Marsden JE, Evans AN (2016) Early feeding by lake trout fry. Trans Am Fish Soc 145:1–6

    Article  Google Scholar 

  • Lantry JR (2001) Spatial and temporal dynamics of predation by Lake Ontario trout and salmon. M.S. thesis, College of Environmental Science and Forestry, State University of New York, Syracuse.

  • Larson WA, Kornis MS, Turnquist KN, Bronte CR, Holey ME, Hanson SD, Treska, TJ, Stott W, Sloss BL (2020) The genetic composition of wild recruits in a recovering lake trout population in Lake Michigan is influenced by capture location and stocking history. Can J Fish Aquat Sci In press

  • Madenjian CP, DeSorcie TJ, Stedman RM (1998) Ontogenic and spatial patterns in diet and growth of lake trout in Lake Michigan. Trans Am Fish Soc 127:236–252

    Article  Google Scholar 

  • Madenjian CP, Elliot RF, DeSorcie TJ, Stedman RM, O’Connor DV, Rottiers DV (2000) Lipid concentrations in Lake Michigan fishes: seasonal, spatial, ontogenetic, and long-term trends. J Great Lake Res 26:427–444

    Article  CAS  Google Scholar 

  • Madenjian CP, Fahnenstiel GL, Johengen TH, Nalepa TF, Vanderploeg HA, Fleischer GW, Schneeberger PJ, Benjamin DM, Smith EB, Bence JR, Rutherford ES, Lavis DS, Robertson DM, Jude DJ, Ebener MP (2002) Dynamics of the Lake Michigan food web, 1970–2000. Can J Fish Aquat Sci 59:736–753

    Article  Google Scholar 

  • Madenjian CP, O’Gorman R, Bunnell DB, Argyle RL, Roseman EF, Warner DM, Stockwell JD, Stapanian MA (2008) Adverse effects of alewives on Laurentian Great Lakes fish communities. NA J Fish Manage 28:263–282

    Article  Google Scholar 

  • Marsden JE, Kozel CL, Chipman BD (2018) Recruitment of lake trout in Lake Champlain. J Gt Lakes Res 44:166–173

    Article  Google Scholar 

  • Marcquenski SV, Brown SB (1997) Early mortality syndrome ( EMS) in salmonid fishes from Great Lakes. In: Chemically induced alteration in functional development and reproduction of fishes. Rolland, R.M., Gilbertson, M. Peterson, R.E. (eds). SETAC Press, Pensacola, FL.

  • Mills EL, Casselman JM, Dermott R, Fitzsimons JD, Gal G, Holeck KT, Hoyle JA, Johannsson OE, Lantry BF, Makarewicz JC, Millard ES, Munawar IF, Munawar M, O’Gorman R, Owens RW, Rudstam LG, Schaner T, Stewart TJ (2003) Lake Ontario: food web dynamics in a changing ecosystem (1970–2000). Can J Fish Aquat Sci 60:471–490

    Article  Google Scholar 

  • Miller MA, Holey ME (1992) Diets of lake trout inhabiting nearshore and offshore Lake Michigan environments. J Great Lakes Res 18:51–60

    Article  Google Scholar 

  • Muir AM, Krueger CC, Hansen MJ (2012) Re-establishing lake trout in the Laurentian Great Lakes: past, present, and future. In: Taylor WW, Lynch AJ, Leonard NJ (eds) Great Lakes fisheries policy and management: a binational perspective, 2nd edn. Michigan State University Press, East Lansing, pp 533–588

    Google Scholar 

  • Nicholson AJ (1933) The balance of animal populations. J Anim Ecol 2:131–178

    Article  Google Scholar 

  • Nishimura H, Kawasaki Y, Nosaka K, Kaneko Y, Iwashima A (1991) A constitutive thiamine metabolism mutation, thi80, causing reduced thiamine pyrophosphokinase activity in Saccharomyces cerevisiae. J Bacteriol 173:2716–2719

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Page KS, Scribner KT, Bennett KR, Garzel LM, Burnham-Curtis MK (2003) Molecular genetic assessment of stocking success and sources of natural lake trout recruitment in the Great Lakes. Trans Amer Fish Soc 132:877–894

    Article  Google Scholar 

  • Palace VP, Brown SB, Baron CL, Fitzsimons J, Woodin B, Stegeman JJ, Klaverkamp JF (1998) An evaluation of the relationships among oxidative stress, antioxidant vitamins and early mortality syndrome (EMS) of lake trout (Salvelinus namaycush) from Lake Ontario. Aquat Toxicol 43:195–208

    Article  CAS  Google Scholar 

  • Park LCH, Zhang H, Sheu KR, Calingasan NY, Kristal BS, Lindsay G, Gibson GE (1999) Metabolic impairment induces oxidative stress, compromises inflammatory responses, and inactivates a key mitochondrial enzyme in microglia. J Neurochem 72:1948–1958

    Article  CAS  PubMed  Google Scholar 

  • Perkins DL, Fitzsimons JD, Marsden JE, Krueger CC, May B (1995) Differences in reproduction among hatchery strains of lake trout at eight spawning areas in Lake Ontario: genetic evidence from mixed-stock analysis. J Great Lakes Res 21(Suppl 1):364–374

    Article  Google Scholar 

  • Rasmussen JB, Rowan DJ, Lean DRS, Carey JH (1990) Food chain structure in Ontario lakes determines PCB levels in lake trout (Salvelinus namaycush) and other pelagic fish. Can J Fish Aquat Sci 47:2030–2038

    Article  Google Scholar 

  • R Core Team. 2014. R: a language and environment for statistical computing [online]. Foundation for Statistical Computing, Vienna, Austria. ISBN 3–900051–07–0. Available from http://www.R-project.org/

  • Riley SC, Evans AN (2008) Phylogenetic and ecological characteristics associated with thiaminase activity in Great Lakes fishes. Trans Am Fish Soc 137:147–157

    Article  Google Scholar 

  • Riley SC, He J, Johnson JE, O’Brien TP, Schaeffer JS (2007) Evidence of widespread natural reproduction by lake trout Salvelinus namaycush in the Michigan waters of Lake Huron. J Great Lakes Res 33:917–921

    Article  Google Scholar 

  • Riley SC, Rinchard J, Honeyfield DC, Evans AN, Begnoche L (2011) Increasing thiamine concentrations in lake trout eggs from Lakes Huron and Michigan coincide with low alewife abundance. NA J Fish Manage 31:1052–1064

    Article  Google Scholar 

  • Riley SC, Roseman EF, Nichols SJ, O’Brien TP, Kiley CS, Schaeffer JS (2008) Deepwater demersal fish community collapse in Lake Huron. Trans Am Fish Soc 137:1879–1890

    Article  Google Scholar 

  • Roseman EF, Schaeffer JS, Bright E, Fielder DG (2014) Angler-caught piscivore diets 544 reflect fish community changes in Lake Huron. Trans Am Fish Soc 143:1419–1433

    Article  CAS  Google Scholar 

  • Roseman EF, Stott WS, O’Brien TP, Riley SC, Schaeffer JS (2009) Heritage strain and diet of wild young of year and yearling lake trout in the main basin of Lake Huron. J Great Lakes Res 35:620–626

    Article  Google Scholar 

  • Royce WE (1951) Breeding habits of lake trout in New York. Fish Bull 52:59–76

    Google Scholar 

  • Schneider CP, Owens RW, Bergstedt RA, O’Gorman R (1996) Predation by sea lamprey (Petromyzon marinus) on lake trout (Salvelinus namaycush) in southern Lake Ontario, 1982–1992. Can J Fish Aquat Sci 53:1921–1931

    Article  Google Scholar 

  • Scribner K, Tsehaye I, Brenden T, Stott W, Kanefsky J, Bence J (2018) Hatchery strain contributions to emerging wild lake trout populations in Lake Huron. J Hered 109:675–688

    Article  PubMed  Google Scholar 

  • Selgeby J, Bronte CR, Brown EH Jr, Hansen MJ, Holey ME, VanAmberg JP, Muth KM, Makauskas DB, McKee P, Anderson DM, Ferreri CP, Schram ST (1995) Lake trout restoration in the Great Lakes: stock-size criteria for natural reproduction. J Great Lakes Res 21(Suppl. 1):498–504

    Article  Google Scholar 

  • Simonin PW, Rudstam LG, Parrish DL, Pientka B, Sullivan PJ (2018) Piscivore diet shifts and trophic level change after alewife establishment in Lake Champlain. Trans Am Fish Soc 147:939–947

    Article  CAS  Google Scholar 

  • Smith HM (1892) Report on an investigation of the fisheries in Lake Ontario. House of Representatives, Miscellaneous Document 341, and Bulletin of the U.S. Fish Commission 10:177–215

    Google Scholar 

  • Stockwell JD, Ebener MP, Black JA, Gorman OT, Halpern T, Hrabik TR, Kinnunen RE, Mattes WP, Oyadomari J, Schram ST, Schreiner DR, Seider MJ, Scribner K, Sitar SP, Yule DL (2009) A synthesis of cisco recovery in Lake Superior: implications for native fish rehabilitation in the Laurentian Great Lakes. NA Fish Manage 29:626–652

    Article  Google Scholar 

  • Stohs SJ (1990) Oxidative stress induced by 2, 3, 7, 8-tetrachlorodibenzo-p-dioxin (TCDD). Free Radic Biol Med 9:79–90

    Article  CAS  PubMed  Google Scholar 

  • Sutherland WJ, Butchart SHM, Connor B, Culshaw C, Dicks LV, Dinsdale J, Gleave RA (2018) A 2018 horizon scan of emerging issues for global conservation and biological diversity. Trends Ecol Evol 33:47–58

    Article  PubMed  Google Scholar 

  • Tanner HA, Tody WH (2002) History of the Great Lakes salmon fishery: a Michigan perspective. In: Lynch KD, Jones ML, Taylor WW (eds) Sustaining North American salmon: perspectives across regions and disciplines. American Fisheries Society, Bethesda, Maryland, pp 139–154

    Google Scholar 

  • Tillitt DE, Zajicek JL, Brown SB, Fitzsimons JD, Honeyfield DC, Holey ME, Wright GM (2005) Thiamine and thiaminase status in forage fish of salmonines from Lake Michigan. J Aquat Anim Health 17:13–25

    Article  Google Scholar 

  • Vuorinen PJ, Rokka M, Ritvanen T, Käkelä R, Nikonen S, Pakarinen T, Keinänen M (2020) Changes in thiamine concentrations, fatty acid composition, and some other lipid-related biochemical indices in Baltic Sea Atlantic salmon (Salmo salar) during the spawning run and pre-spawning fasting. Helgoland Mar Res 74:10

    Article  Google Scholar 

  • Werner RM, Rook B, Greil R (2006) Egg thiamine status and occurrence of early mortality syndrome (EMS) in Atlantic salmon from the St. Marys River. Michigan J Great Lakes Res 32:293–305

    Article  CAS  Google Scholar 

  • Wigley RL (1959) Life history of the sea lamprey of Cayuga Lake, New York. U.S. Fish Wildlife Serv Fish Bul 154:561–617

    Google Scholar 

  • Wirgin I, Waldman JR (2004) Resistance to contaminants in North American fish populations. Mol Mech Mutagen 552:73–100

    CAS  Google Scholar 

  • Wolf LE (1942) Fish-diet disease of trout: a vitamin deficiency produced by diets containing raw fish. N.Y. State Conservation Department, Fish Res Bull No. 2:16 pp

  • Youngs WD, Oglesby RT (1972) Cayuga Lake: effects of exploitation and introductions on the salmonid community. J Fish Res Bd Can 29:787–794

    Article  Google Scholar 

Download references

Acknowledgements

We would like to thank Lenore Vandenbyllaardt for thiamine analysis, Bill Williston for assistance in egg collection and rearing eggs, Ken Osika for supplying eggs from Cayuga and Seneca lakes, and Paul Methner for supplying eggs from Lake Manitou.

Author information

Authors and Affiliations

Author notes

  1. Scott B. Brown is deceased. This paper is dedicated to his memory.

    • John D. Fitzsimons
Authors

Contributions

The authors agree that each individual listed in the author list (1) made substantial contributions to the conception or design of the work and the acquisition, analysis, or interpretation of data; (2) drafted the work or revised it critically for important intellectual content; (3) approved the version to be published, and (4) agree to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. Environ Biol Fish (2020) 103:1565–1581 1577. As a result of his death, Scott Brown did not participate in the drafting or approval of this work nor can he be held accountable for the work. The corresponding author (JDF) has the implied permission from Environment Canada where Dr. Brown was employed.

Corresponding author

Correspondence to John D. Fitzsimons.

Ethics declarations

Ethics approval

All procedures performed in the study involving animals were conducted under animal use and care procedures of Canadian Council on Animal Care.

Consent to participate

Not applicable as this research did not involve human participants.

Consent for publication

The authors J.D. Fitzsimons and A. El-Shaarawi agree with the content of the manuscript, give explicit consent to submit for publication, and have permission from responsible authorities at Fisheries and Oceans Canada and Environment Canada.

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Fitzsimons, J.D., Brown, S.B. & El-Shaarawi, A.H. Reduced thiamine utilization by Seneca Lake lake trout embryos and potential implications to restoration of lake trout in the Great Lakes. Environ Biol Fish 104, 751–766 (2021). https://doi.org/10.1007/s10641-021-01109-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10641-021-01109-4

Keywords

Navigation