The Open Fish Science Journal




(Discontinued)

ISSN: 1874-401X ― Volume 12, 2019
REVIEW ARTICLE

Landlocked Fall Chinook Salmon Maternal Liver and Egg Thiamine Levels in Relation to Reproductive Characteristics



Andrew Doyle1, Michael E. Barnes2, *, Jeremy L. Kientz2, Micheal H. Zehfus3
1 Department Benedictine College Atchison, Kansas, United States
2 McNenny State Fish Hatchery South Dakota Department of Game, Fish and Parks Spearfish, South Dakota, United States
3 Department of Chemistry Black Hills State University, University Spearfish, South Dakota, United States

Abstract

Object:

Landlocked fall Chinook Salmon Oncorhynchus tshawytscha in Lake Oahe, South Dakota, typically experience poor reproductive success.

Introduction:

Salmon diets consist of rainbow smelt Osmerus mordax and other potentially thiaminase-containing fish that could impact reproduction.

Methods:

The thiamine levels of spawning female Salmon, eggs, and reproductive characteristics, were measured in 2000, 2001, 2002, 2003, and 2005.

Results:

Thiamine concentrations varied significantly from year-to-year, with the highest mean values recorded in 2001 at 8.70 nmol/g in maternal livers and 28.80 nmol/g in eggs. Most of the thiamine in the eggs was present as free thiamine, while most of the thiamine in maternal livers was present as thiamine pyrophosphate. The lowest recorded egg total thiamine level was 2.75 nmol/g in 2000. Egg survival to hatch ranged from 20.7% in 2005 to 35.4% in 2002, and was not correlated to egg thiamine levels. Twenty-two spawns experienced total mortality prior to hatch, and had significantly lower egg free thiamine and total thiamine concentrations than eggs from the 77 successful spawns. The eggs from spawns with total mortality were also significantly smaller than those eggs from spawns that did survive, and were produced by females that weighed significantly less. Several small, but significant, correlations were observed between egg size and egg thiamine levels, and female size and liver thiamine.

There was also a significant negative correlation between the number of eggs per spawning female and egg thiamine pyrophosphate, liver thiamine monophosphate, and liver total thiamine levels.

Conclusion:

In general, Lake Oahe Chinook Salmon eggs show little indication of thiamine deficiency in the years sampled, indicating other factors are likely responsible for poor egg survival.

Keywords: Thiamine, Chinook Salmon, Reproduction, Rainbow Smelt, Thiaminase, Lake Oahe.


Article Information


Identifiers and Pagination:

Year: 2017
Volume: 10
First Page: 23
Last Page: 32
Publisher Id: TOFISHSJ-10-23
DOI: 10.2174/1874401X01710010023

Article History:

Received Date: 11/11/2016
Revision Received Date: 04/01/2017
Acceptance Date: 23/01/2017
Electronic publication date: 30/06/2017
Collection year: 2017

© 2017 Doyle et al.

open-access license: This is an open access article distributed under the terms of the Creative Commons Attribution 4.0 International Public License (CC-BY 4.0), a copy of which is available at: (https://creativecommons.org/licenses/by/4.0/legalcode). This license permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.


* Address correspondence to this author at the McNenny State Fish Hatchery South Dakota Department of Game, Fish and Parks Spearfish, South Dakota, United States, Tel: 605-642-6920, Fax: 605-642-6921; E-mail: mike.barnes@state.sd.us




INTRODUCTION

Eggs collected from free-ranging fall Chinook Salmon Oncorhynchus tshawytscha in Lake Oahe, South Dakota (USA) typically experience poor survival during hatchery rearing [1Barnes ME, Hanten RP, Cordes RJ, Sayler WA, Carreiro J. Reproductive performance of inland fall Chinook Salmon. N Am J Aquaculture 2000; 62: 203-11.
[http://dx.doi.org/10.1577/1548-8454(2000)062<0203:RPOIFC>2.3.CO;2]
], with survival less than one-half that observed for Chinook Salmon in their native range [2Johnson HE, Brice RF. Effects of transportation of green eggs, and of water temperature during incubation, on the mortality of Chinook Salmon. Prog Fish-Cult 1953; 15: 104-8.
[http://dx.doi.org/10.1577/1548-8640(1953)15[104:EOTOGE]2.0.CO;2]
, 3Banks JL, Fowler LG. Transportation, storage and handling studies of fall Chinook Salmon gametes and newly fertilized eggs Abernathy Salmon Cultural Development Center, Technology Transfer Series 82-4. US. Fish Wildlife Service 1982.]. The reason for this elevated egg mortality is currently unknown, but may be due to several factors, including elevated water temperatures during oogenesis and spawning [4Marrone GM, Stout DA. Whitlocks Bay Spawning station annual report 97-119. South Dakota Department Game, Fish and Parks. Ann Rep 1997; 1997: 97-119., 5Quinn TP. The behavior and ecology of Pacific Salmon and Trout. Seattle, Washington: University of Washington Press 2005.], parental nutrition [1Barnes ME, Hanten RP, Cordes RJ, Sayler WA, Carreiro J. Reproductive performance of inland fall Chinook Salmon. N Am J Aquaculture 2000; 62: 203-11.
[http://dx.doi.org/10.1577/1548-8454(2000)062<0203:RPOIFC>2.3.CO;2]
, 6Iwamoto RN, Sower S. Salmonid reproduction an international symposium. Seattle, Washington: University of Washington Press 1983; pp. 44-8., 7Poston HA, Ketola HG. Chemical composition of maturing and spawning Atlantic Salmon from different locations. Prog Fish-Cult 1989; 51: 133-9.
[http://dx.doi.org/10.1577/1548-8640(1989)051<0133:CCOMAS>2.3.CO;2]
], and possible inbreeding [1Barnes ME, Hanten RP, Cordes RJ, Sayler WA, Carreiro J. Reproductive performance of inland fall Chinook Salmon. N Am J Aquaculture 2000; 62: 203-11.
[http://dx.doi.org/10.1577/1548-8454(2000)062<0203:RPOIFC>2.3.CO;2]
, 8Gjerde B, Gunnes K, Gjedrem T. Effect of inbreeding on survival and growth in rainbow trout. Aquaculture 1983; 34: 327-32.
[http://dx.doi.org/10.1016/0044-8486(83)90212-0]
, 9Araki H, Berejikian BA, Ford MJ, Blouin MS. Fitness of hatchery-reared Salmonids in the wild. Evol Appl 2008; 1(2): 342-55.
[http://dx.doi.org/10.1111/j.1752-4571.2008.00026.x] [PMID: 25567636]
]. One aspect of parental nutrition that may be influencing reproductive success are thiamine (vitamin B1) levels in the eggs.

In fish, thiamine is found in three different forms or vitamers: thiamin pyrophosphate (TPP), thiamine monophosphate (TMP), and free thiamine. Thiamine pyrophosphate and thiamine monophosphate are the two biologically active forms [10Machlin LJ. Handbook of vitamins. New York: Marcel Dekker, Inc. 1991.]. TPP and TMP are cofactors required for fatty acid and carbohydrate metabolism, specifically the pyruvate decarboxylase complex and enzymes involved in the Krebs cycle [10Machlin LJ. Handbook of vitamins. New York: Marcel Dekker, Inc. 1991.]. Without these enzymes, aerobic respiration will cease. In addition, thiamine deficiencies are also linked with neurological degenerative disorders such as Weirnkie’s syndrome [10Machlin LJ. Handbook of vitamins. New York: Marcel Dekker, Inc. 1991.]. Without thiamine, organisms become lethargic and eventually die because of the decrease in metabolism and neuron degeneration.

Rainbow smelt Osmerus mordax are the primary prey item for Lake Oahe Chinook Salmon when they are abundant [11Hill TD. Life history and bioenergetics of Chinook Salmon in Lake Oahe, South Dakota. Brookings, South PhD Dissertation. Dakota: South Dakota State University 1997.]. Rainbow smelt contain thiaminases, a group of enzymes that break down thiamine [12Gnaedinger RH. Thiaminase activity in fish: An improved assay method. Fish Ind Res 1964; 2: 55-9.-14Fitzsimons JD, Brown SB. Reduced egg thiamine levels in inland and Great Lakes lake Trout and their relationship with diet. In: Fitzsimons JD, Honeyfield DC, Eds. In: Early life stage mortality syndrome in fishes of the Great Lakes and Baltic Sea Am Fish Soc Symp. 1998; 21: pp. 160-71.]. Mortality of Salmonid embryos from thiamine deficiencies resulting from the parental consumption of thiaminase-containing prey has been observed in the Baltic Sea, the Finger Lakes of New York, and the Great Lakes [15Bylund G, Lerche O. Thiamine therapy of M74 affected fry of Atlantic Salmon Salmo salar. Bull Eur Assoc Fish Pathol 1995; 15: 93-7.-19Brown SB, Fitzsimons JD, Honeyfeild DC, Tillitt DE. Implications of thiamine deficiency in Great Lakes Salmonines. J Aquat Anim Health 2005; 17: 113-24.
[http://dx.doi.org/10.1577/H04-015.1]
]. Depending on geography, this mortality was initially called M74, Cayuga syndrome, swim-up syndrome, and Early Mortality Syndrome [20Fisher JP, Brown SB, Wooster GW, Bowser PR. Maternal blood, egg and larval thiamin levels correlate with larval survival in landlocked Atlantic Salmon. J Nutr 1998; 128(12): 2456-66.
[PMID: 9868194]
]. However, all these syndromes have now been grouped together as the thiamine deficiency complex [21Riley SC, Rinchard J, Honeyfield DC, Evans AN, Begnoche L. Increasing thiamine concentrations in lake trout eggs from Lakes Huron and Michigan coincide with low alewife abundance. N Am J Fish Manage 2011; 31: 1052-64.
[http://dx.doi.org/10.1080/02755947.2011.641066]
]. During certain years of hatchery rearing, Lake Oahe Salmon exhibits some of the clinical signs, and mortality patterns, associated with thiamine deficiency complex.

Only one preliminary study has described thiamine levels in Lake Oahe Chinook Salmon and eggs [22Barnes ME, Zehfus MH, Schumacher JA, et al. Maternal liver and egg thiamine concentrations in Chinook Salmon from Lake Oahe, South Dakota. Prairie Nat 2003; 35: 113-7.]. However, this study lasted for only one year, during which rainbow smelt population abundance was low. Smelt and other prey fish populations fluctuate substantially from year-to-year in Lake Oahe, and it is possible that spawning female and egg thiamine levels fluctuate as well. The objective of this study is to document levels of maternal liver and egg thiamine concentrations in conjunction with the reproductive success of Lake Oahe Chinook Salmon over several years.

MATERIALS AND METHODS

Study Area

Lake Oahe is a 150,000 ha mainstem Missouri River reservoir located in North and South Dakota, USA. The South Dakota portion contains approximately 47,755 ha of coldwater habitat (water temperatures ≤ 15° C) at full pool [23Lott J, Marrone G, Stout D. Influence of size-and-date at stocking, imprinting attempts and growth on initial survival, homing ability, maturation patterns and angler harvest of Chinook Salmon in Lake Oahe, South Dakota. Progress Report 97-20. Pierre, South Dakota: South Dakota Department Game, Fish Parks 1997.]. Suitable permanent habitat for Chinook Salmon is typically located directly upstream from Lake Oahe dam, north of Pierre, South Dakota, to Whitlock’s Bay, west of Gettysburg, South Dakota, USA. Female Salmon and eggs used for this study were collected during spawning of feral Chinook Salmon at Whitlocks Spawning Station on Lake Oahe near Gettysburg, South Dakota. Egg incubation occurred at McNenny State Fish Hatchery, rural Spearfish, South Dakota.

Spawning and Egg Incubation

Eggs were pneumatically removed from ripe, free-ranging females that had ascended the fish ladder at Whitlock’s Spawning Station. Prior to gamete collection, male and female Salmon were anesthetized in carbon-dioxide saturated water. Milt was collected from males by hand-stripping, pooled in a container, and kept on ice until it was used to fertilize the eggs. Eggs were removed from ripe females by injecting compressed oxygen at low pressure into their body cavities and the eggs were expressed into a plastic pan. Lake water (11-13° C, total hardness as CaCO3 = 160 mg/L, pH = 8.2, total dissolved solids = 440 mg/L) was added to the pan to activate the milt. After approximately one minute, eggs were washed in lake water to remove excess milt, and then placed in lake water for one-hour to allow for membrane separation (water hardening). After water hardening, the eggs were placed in plastic bags with fresh lake water, and transported approximately 4 hours to McNenny Hatchery. The spawn from each female was maintained discretely during the spawning process, transportation to the hatchery, and during incubation. Based on historical norms and the size of fish at spawning, it was assumed that only age-3 Salmon were used in the study [24Barnes ME, Wipf MM, Domenici NR, Kummer WM, Hanten RP. Decreased hatchery rearing density improves post-stocking harvest and return to spawning of landlocked fall Chinook Salmon. N Am J Aquaculture 2013; 75: 244-50.
[http://dx.doi.org/10.1080/15222055.2013.768573]
].

Upon arrival at McNenny Hatchery, the eggs were disinfected in a 100 mg/L buffered free-iodine solution for 10 min, inventoried by the water displacement method [25Piper RG, McElwain IB, Orme LE, McCraren JP, Fowler LG, Leonard JR. Fish Hatchery Management. Washington, DC: US. Fish and Wildlife Service 1982.], and placed in individual Heath (Flex-a-lite Consolidated, Tacoma, Washington) incubator trays. Well water (11o C, total hardness as CaCO3 - 360 mg/L, alkalinity as CaCO3 - 210 mg/L, pH - 7.6, total dissolved solids - 390 mg/L) at a flow of 12 L/min was used for egg incubation. Formalin treatments using Parasite-S (37% formaldehyde, 6 to 14% methanol, Western Chemical Inc., Ferndale, Washington) at 1,667 mg/L for 15 min were administered daily until retinal pigments were clearly visible (egg eye-up) at incubation d 30, after which dead eggs were removed and percent survival to eye-up calculated. After egg eye-up, additional dead eggs and dead fry were removed by hand until the fry had nearly completed yolk sac absorption and were moved from the incubator. Survival to the eyed stage of development, hatch, and fry swim-up was calculated using the following formulas:

Survival to the eye (%)

= 100 X [1 - (mortality at the eyed stage / initial number of eggs)].

Survival to hatch (%)

= 100 X [1 - (mortality up to hatch / initial number of eggs)].

Survival to swim-up (%)

= 100 X [1 - (total mortality during incubation / initial number of eggs)].

Thiamine Analysis

Immediately after removal from the female, approximately 20 g of eggs were placed into plastic bags, quickly frozen using dry ice, and subsequently stored in a -70° C freezer until analyzed for thiamine content. Immediately after spawning, the liver was removed from each spawning female, quickly frozen using dry ice, and stored at -70° C until thiamine analysis occurred. Thiamine pyrophosphate, thiamine monophosphate, and free thiamine were analyzed using a high pressure liquid chromatography method [26Brown SB, Honeyfield DC, Vandenbyllaardt L, McDonald G, Fitzsimons JD, Honeyfield DC. Thiamine analysis in fish tissues. In: Early life stage mortality syndrome in fishes of the Great Lakes and Baltic Sea. Am Fish Soc Symp 1998; 21: pp. 73-81.]. Total thiamine was calculated by adding the vitamers.

Data Analysis

Data was analyzed using the SPSS (9.0) statistical analysis program (SPSS, Chicago, Illinois, USA). Regression and correlation analysis were used to ascertain any possible relationships among the variables. Yearly data was analyzed using ANOVA and Tukey means comparison procedure. The significance level for all tests was predetermined at P < 0.05.

RESULTS

Egg and maternal liver thiamine concentrations varied significantly from year-to-year (Table 1). Free and total thiamine levels in the eggs were the highest in 2001, followed by 2002, with the lowest levels recorded in 2000, 2003 and 2005. Maternal liver TMP and total thiamine were also significantly greater in 2001 compared to the other years. Egg total thiamine levels ranged from 2.75 to 45.25 nmol/g, and maternal liver total thiamine levels ranged from 1.05 to 16.65 nmol/g. Most of the thiamine in the eggs was present as free thiamine, whereas TPP was the predominant form of thiamine found in maternal livers.

Table 1
Mean (SE) spawning female sizes, reproductive data, and thiamine data from landlocked fall Chinook Salmon from Lake Oahe, South Dakota. Means with different letters across a row are significantly different (P < 0.05).


Overall mean survival to the eyed-egg stage was only 31.9%, with mean survival to fry swim-up at 26.4%. No significant differences in egg or fry survival were observed among any of the years. Survival to the eyed-egg stage and fry swim-up of the spawn containing eggs with 2.75 nmol/g total thiamine was 68% and 62%, respectively.

In comparison to eggs from spawns that failed to hatch, eggs from successful spawns with at least some survival to hatch had a significantly greater concentration of free thiamine (13.75 to 18.40 nmol/g) and total thiamine (14.85 to 19.35 nmol/g) (Table 2). Egg TPP and Egg TMP were not significantly different from the two groups. None of the liver thiamine vitamers were significantly different as well. The eggs that did not hatch were significantly smaller (smaller eggs have a higher number of eggs/ml of water displaced) and came from larger females.

Table 2
Mean (SE) spawning female sizes, reproductive data, and thiamine data from spawns of landlocked fall Chinook Salmon from Lake Oahe, South Dakota that either had some eggs survive to hatch or experienced complete mortality. Means with different letters across a row are significantly different (P < 0.05).


There were no significant correlations observed among survival to the eyed-egg stage, hatch, or fry swim-up and any of the thiamine forms or total thiamine. Egg TPP, TMP, free thiamine, and total thiamine levels were significantly, but weakly, correlated with egg size (Table 3). Small, but significant, correlations were also observed between the number of eggs and liver thiamine levels. Liver free thiamine was significantly correlated with egg free and total thiamine concentrations. There were significant, but weak, correlations between liver total thiamine and spawning female length and weight. Two significant regressions were calculated based on the natural log transformation of egg total thiamine data in relation to the survival from the eyed-egg stage of development to hatch (Fig. 1) and survival from the eyed-egg stage to fry swim-up (Fig. 2).

Female lengths, weights, egg size, and the number of eggs per spawn were significantly different among the years. Fish were the largest in 2002 and 2003. There were significantly fewer eggs per spawn in 2000 and 2001 compared to the other three years and the smallest eggs were observed in 2000, followed by 2005, and then 2001-2003.

Fig. (1)
Survival from the eyed egg stage to hatch of landlocked Chinook Salmon from Lake Oahe, South Dakota in relation to total egg thiamine from 2000 to 2005 (n = 77).


DISCUSSION

At 2.75 nmol/g, the lowest concentration of egg total thiamine in the eggs from one spawning female was above the 1.7 noml/g upper boundary for thiamine deficiency complex identified by [27Fisher JP, Brown SB, Connelly S, Chiottie T, Krueger CC. Interspecies comparisons of blood thiamine in salmonids from the Finger Lakes, and effect of maternal size on blood and egg thiamine in Atlantic Salmon with and without Cayuga syndrome. In: McDonald G, Fitzsimons JD, Honeyfield DC, Eds. Early life stage mortality syndrome in fishes of the Great Lakes and Baltic Sea. Am Fish Soc Symp 1998; 21: pp. 112-23.-30Wolmagood M, Hnath JG, Brown SB, et al. Temporal and spatial variation of early mortality syndrome in Salmonids from Lakes Michigan and Huron. J Aquat Anim Health 2005; 17: 65-76.
[http://dx.doi.org/10.1577/H03-077.1]
]. However, this value (2.75 nmol/g) was slightly less than the 2.99 nmol/g total thiamine value reported to produce 20% mortality in Lake Ontario Chinook Salmon eggs [31Fitzsimons JD, Williston B, Williston G, et al. Egg thiamine status of Lake Ontario Salmonines 1995-2004 with emphasis on lake Trout. J Great Lakes Res 2007; 33: 93-103.
[http://dx.doi.org/10.3394/0380-1330(2007)33[93:ETSOLO]2.0.CO;2]
], but the overall high survival of the fry, and the lack of substantial post-hatch mortality, from this spawn appears to indicate that mortality due to thiamine deficiency did not occur. Of the 99 spawns sampled in this study, only three showed survival of less than 90% between hatch and swim-up, which is the most lethal period for thiamine deficiency complex [28Ketola GH, Bowser PR, Wooster GA, Wedge LR, Hurst SS. Effects of thiamine on reproduction of Atlantic Salmon and a new hypothesis for their extirpation in Lake Ontario. Trans Am Fish Soc 1999; 129: 607-12.
[http://dx.doi.org/10.1577/1548-8659(2000)129<0607:EOTORO>2.0.CO;2]
]. Of these, the lowest concentration of total egg thiamine was 9.25 nmol/g, much greater than the concentration considered the upper end of the thiamine deficiency complex [28Ketola GH, Bowser PR, Wooster GA, Wedge LR, Hurst SS. Effects of thiamine on reproduction of Atlantic Salmon and a new hypothesis for their extirpation in Lake Ontario. Trans Am Fish Soc 1999; 129: 607-12.
[http://dx.doi.org/10.1577/1548-8659(2000)129<0607:EOTORO>2.0.CO;2]
, 31Fitzsimons JD, Williston B, Williston G, et al. Egg thiamine status of Lake Ontario Salmonines 1995-2004 with emphasis on lake Trout. J Great Lakes Res 2007; 33: 93-103.
[http://dx.doi.org/10.3394/0380-1330(2007)33[93:ETSOLO]2.0.CO;2]
], making it unlikely that a lack of thiamine was the cause of fry mortality. The adequacy of thiamine levels in Lake Oahe Salmon observed in this study is further supported by the similar hatch to swim-up survival rates of Lake Oahe Salmon eggs to eggs treated with supplemental thiamine from populations with a history of thiamine deficiency complex [15Bylund G, Lerche O. Thiamine therapy of M74 affected fry of Atlantic Salmon Salmo salar. Bull Eur Assoc Fish Pathol 1995; 15: 93-7., 16Fitzsimons JD. The effect of B-vitamins on a swim-up syndrome in Lake Ontario lake Trout. Great Lakes Res 1995; 21: 286-9.
[http://dx.doi.org/10.1016/S0380-1330(95)71102-9]
, 20Fisher JP, Brown SB, Wooster GW, Bowser PR. Maternal blood, egg and larval thiamin levels correlate with larval survival in landlocked Atlantic Salmon. J Nutr 1998; 128(12): 2456-66.
[PMID: 9868194]
].

Table 3
Significant correlations between the variables (P < 0.05).


The lowest egg total thiamine concentration observed from any spawn during the five years of this study was only slightly lower than the 3.5 nmol/g lowest measurement reported previously for eggs from Lake Oahe Chinook Salmon during a year when smelt were less numerous [22Barnes ME, Zehfus MH, Schumacher JA, et al. Maternal liver and egg thiamine concentrations in Chinook Salmon from Lake Oahe, South Dakota. Prairie Nat 2003; 35: 113-7.]. Eggs from two of the years had similar total thiamine values to the 9.9 nmol/g mean value in 1999 reported [22Barnes ME, Zehfus MH, Schumacher JA, et al. Maternal liver and egg thiamine concentrations in Chinook Salmon from Lake Oahe, South Dakota. Prairie Nat 2003; 35: 113-7.]. However, mean values from the other three years were dramatically larger, approaching nearly 29 nmol/g in 2003. The highest recorded egg total thiamine level was also nearly three times that reported by [22Barnes ME, Zehfus MH, Schumacher JA, et al. Maternal liver and egg thiamine concentrations in Chinook Salmon from Lake Oahe, South Dakota. Prairie Nat 2003; 35: 113-7.].

Fig. (2)
Survival from egg eye-up to fry swim-up of landlocked Chinook Salmon from Lake Oahe, South Dakota in relation to total egg thiamine from 2000 to 2005 (n = 77).


Overall, thiamine levels in Chinook Salmon eggs from Lake Oahe are far greater than levels found in the Great Lakes or the Baltic Sea, where thiamine deficiency complex is frequently observed. The minimum total egg thiamine level observed in this study is typical of Chinook Salmon eggs that did not exhibit thiamine deficiency complex from Lakes Michigan and Huron [30Wolmagood M, Hnath JG, Brown SB, et al. Temporal and spatial variation of early mortality syndrome in Salmonids from Lakes Michigan and Huron. J Aquat Anim Health 2005; 17: 65-76.
[http://dx.doi.org/10.1577/H03-077.1]
]. In Lake Michigan, Lake Huron, and Lake Ontario, mean egg total thiamine levels for Salmonids have been reported as 2.0, 3.1, and 1.3 nmol/g, respectively [32Rolland RM, Gilbertson M, Peterson RE. Chemically induced alterations in functional development and reproduction of fishes: Proceedings from a session at the 1995 Wingspread Conference. Pensacola: Society of Environmental Toxicology and Chemistry (SETAC) 1997; 146-60.]. In the Baltic Sea, egg mean total thiamine levels of 2.7 nmol/g have been reported [33Koski P, Soivio A, Hartikainen K, Hirvi T, Myllyla T. M74 syndrome and thiamine in Salmon broodfish and offspring. Boreal Environ Res 2001; 6: 79-92.]. The mean values from Lake Oahe Chinook Salmon eggs in the current study are as high as ten times greater as these other locations. However, the lowest levels observed in this study are similar to those reported for suspected thiamine-deficient eggs from migratory Chinook Salmon in New York [34Ketola HG, Johnson JH, Rinchard J, et al. Effect of thiamine status on probability of Lake Ontario Chinook Salmon spawning in the upper and lower sections of the Salmon River, New York. N Am J Fish Manage 2009; 29: 895-902.
[http://dx.doi.org/10.1577/M08-021.1]
].

Thiamine deficiency complex may not be a problem for the Salmon in Lake Oahe because the concentration of thiaminase in rainbow smelt may not be sufficient for induction of the complex [16Fitzsimons JD. The effect of B-vitamins on a swim-up syndrome in Lake Ontario lake Trout. Great Lakes Res 1995; 21: 286-9.
[http://dx.doi.org/10.1016/S0380-1330(95)71102-9]
]. The amount of thiaminase in rainbow smelt is up to six times less than the amount in alewife Alosa pseudoharengus [16Fitzsimons JD. The effect of B-vitamins on a swim-up syndrome in Lake Ontario lake Trout. Great Lakes Res 1995; 21: 286-9.
[http://dx.doi.org/10.1016/S0380-1330(95)71102-9]
, 35Tillit DE, Zajicek JE, Brown SB, et al. Thiamine and thiaminase status in forage fish of Salmonines from Lake Michigan. J Aquat Anim Health 2005; 17: 13-25.
[http://dx.doi.org/10.1577/H03-081.1]
]. Thiaminase activity is also four times lower in smelt than in Baltic herring Clupea harengus [36Hirn J, Pekkanen TJ. Quantitative analysis of thiaminase activity in certain fish species. Nord Vet Med 1975; 27(12): 646-8.
[PMID: 1196856]
]. The thiaminase from rainbow smelt may also be diluted by other prey items in the diet of Lake Oahe Chinook Salmon [22Barnes ME, Zehfus MH, Schumacher JA, et al. Maternal liver and egg thiamine concentrations in Chinook Salmon from Lake Oahe, South Dakota. Prairie Nat 2003; 35: 113-7.], making it likely that there may not be enough thiaminase in the Salmon diet to induce thiamine deficiency complex [37Brown SB, Arts MT, Brown LR, et al. Can diet-dependent factors help explain fish-to-fish variation in thiamine-dependent early mortality syndrome? J Aquat Anim Health 2005; 17: 36-47.
[http://dx.doi.org/10.1577/H03-072.1]
].

The reason for the significantly lower levels of thiamine from spawns where none of the eggs survived to hatch versus successful spawns is unknown. Because of the high prevalence of overripe and nonviable spawns in Lake Oahe Salmon [38Barnes ME, Hanten RP, Sayler WA, Cordes RJ. Viability of inland fall Chinook Salmon spawn containing overripe eggs and the reliability of egg viability estimates. N Amer J Aquac 2000; 62: 237-9.
[http://dx.doi.org/10.1577/1548-8454(2000)062<0237:VOIFCS>2.3.CO;2]
], it is possible that thiamine was degraded due to cell death and not because of the action of thiaminase. Twelve of the spawns in the current study had no survival to the eyed-egg stage of development, and were likely nonviable prior to spawning. It is also possible that the thiamine requirements for Oahe Salmon are greater than those in other locations, or there is an interaction between thiamine and other nutritional components, such as fatty acids or bioenergetics [37Brown SB, Arts MT, Brown LR, et al. Can diet-dependent factors help explain fish-to-fish variation in thiamine-dependent early mortality syndrome? J Aquat Anim Health 2005; 17: 36-47.
[http://dx.doi.org/10.1577/H03-072.1]
, 39Ahlgren GL, Nieuwerburgh V, Wänstrand I, Pedersén M, Boberg M, Snoeijs P. Imbalance of fatty acids in the base of the Baltic Sea food web: A mesocosm study. Can J Fish Aquat Sci 2005; 62: 2240-53.
[http://dx.doi.org/10.1139/f05-140]
-42Keinänen M, Uddström A, Mikkonen J, et al. 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 2012; 69: 516-28.
[http://dx.doi.org/10.1093/icesjms/fss041]
].

Lake Oahe Chinook Salmon are considerably smaller than Chinook Salmon in their native range, likely due to nutritional deficiencies resulting from a total freshwater lifecycle in a reservoir with limited coldwater forage [1Barnes ME, Hanten RP, Cordes RJ, Sayler WA, Carreiro J. Reproductive performance of inland fall Chinook Salmon. N Am J Aquaculture 2000; 62: 203-11.
[http://dx.doi.org/10.1577/1548-8454(2000)062<0203:RPOIFC>2.3.CO;2]
]. Lake Oahe Salmon also produce smaller eggs than ocean stocks [1Barnes ME, Hanten RP, Cordes RJ, Sayler WA, Carreiro J. Reproductive performance of inland fall Chinook Salmon. N Am J Aquaculture 2000; 62: 203-11.
[http://dx.doi.org/10.1577/1548-8454(2000)062<0203:RPOIFC>2.3.CO;2]
], and the eggs from spawns with no survival in this study were significantly smaller than eggs from spawns with at least some survival. These very small eggs also contained less thiamine, opening the possibility of an interaction between thiamine and other dietary components consumed by the brood female [37Brown SB, Arts MT, Brown LR, et al. Can diet-dependent factors help explain fish-to-fish variation in thiamine-dependent early mortality syndrome? J Aquat Anim Health 2005; 17: 36-47.
[http://dx.doi.org/10.1577/H03-072.1]
, 39Ahlgren GL, Nieuwerburgh V, Wänstrand I, Pedersén M, Boberg M, Snoeijs P. Imbalance of fatty acids in the base of the Baltic Sea food web: A mesocosm study. Can J Fish Aquat Sci 2005; 62: 2240-53.
[http://dx.doi.org/10.1139/f05-140]
-42Keinänen M, Uddström A, Mikkonen J, et al. 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 2012; 69: 516-28.
[http://dx.doi.org/10.1093/icesjms/fss041]
]. In Lake Oahe Salmon, egg thiamine levels increased with egg size (note that with egg sizes measured as eggs/mL, smaller values represent larger eggs), and egg size increased with maternal length and weight. These larger fish producing larger eggs had a greater ability to acquire more or higher quality food resources [43Johnston TA, Leggett WC. Maternal and environmental gradients in the egg size of an iteroparous fish. Ecol Soc Amer 2002; 83: 1777-91.], which may explain why the eggs from spawns with no survival were smaller and contained less thiamine than eggs that survived.

All of the mean maternal liver total thiamine values were approximately one-third to one-half that reported for Lake Oahe Salmon in 1999 [22Barnes ME, Zehfus MH, Schumacher JA, et al. Maternal liver and egg thiamine concentrations in Chinook Salmon from Lake Oahe, South Dakota. Prairie Nat 2003; 35: 113-7.]. The Lake Oahe rainbow smelt population also increased after 1999, which may explain this decrease in maternal thiamine. Perhaps of more interest, with the exception of 2001, mean maternal liver total thiamine levels were less than the level of total liver thiamine (6.3 nmol/g) in healthy Atlantic Salmon [18Amcoff P, Norrgren L, Borjeson H, Linderberg J. Lowered concentrations of thiamine (vitamin B1) in M74-affected feral Baltic Salmon (Salmon salar). Sweden: Rapport-Naturvaardsverket 1996.], and very similar to Great Lakes Salmonids producing progeny with Thiamine Deficiency Complex [44Brown SB, Honeyfield DC, Hnath JG, et al. Thiamine status in adult Salmonines in the Great Lakes. J Aquat Anim Health 2005; 17: 59-64.
[http://dx.doi.org/10.1577/H04-059.1]
]. These relatively low levels may not be lethal, but lower thiamine levels can impact adult fish neurological function [19Brown SB, Fitzsimons JD, Honeyfeild DC, Tillitt DE. Implications of thiamine deficiency in Great Lakes Salmonines. J Aquat Anim Health 2005; 17: 113-24.
[http://dx.doi.org/10.1577/H04-015.1]
, 45Fitzsimons JD, Williston B, Amcoff P, et al. The effect of thiamine injection on upstream migration, survival and thiamine status of putative thiamine-thiamine deficient coho Salmon. J Aquat Anim Health 2005; 17: 48-58.
[http://dx.doi.org/10.1577/H04-003.1]
], metabolic rates [15Bylund G, Lerche O. Thiamine therapy of M74 affected fry of Atlantic Salmon Salmo salar. Bull Eur Assoc Fish Pathol 1995; 15: 93-7., 28Ketola GH, Bowser PR, Wooster GA, Wedge LR, Hurst SS. Effects of thiamine on reproduction of Atlantic Salmon and a new hypothesis for their extirpation in Lake Ontario. Trans Am Fish Soc 1999; 129: 607-12.
[http://dx.doi.org/10.1577/1548-8659(2000)129<0607:EOTORO>2.0.CO;2]
], and muscle weakness [34Ketola HG, Johnson JH, Rinchard J, et al. Effect of thiamine status on probability of Lake Ontario Chinook Salmon spawning in the upper and lower sections of the Salmon River, New York. N Am J Fish Manage 2009; 29: 895-902.
[http://dx.doi.org/10.1577/M08-021.1]
], thereby potentially decreasing foraging efficiency and subsequently contributing to smaller body sizes [22Barnes ME, Zehfus MH, Schumacher JA, et al. Maternal liver and egg thiamine concentrations in Chinook Salmon from Lake Oahe, South Dakota. Prairie Nat 2003; 35: 113-7., 28Ketola GH, Bowser PR, Wooster GA, Wedge LR, Hurst SS. Effects of thiamine on reproduction of Atlantic Salmon and a new hypothesis for their extirpation in Lake Ontario. Trans Am Fish Soc 1999; 129: 607-12.
[http://dx.doi.org/10.1577/1548-8659(2000)129<0607:EOTORO>2.0.CO;2]
].

Similar to that reported by other authors [14Fitzsimons JD, Brown SB. Reduced egg thiamine levels in inland and Great Lakes lake Trout and their relationship with diet. In: Fitzsimons JD, Honeyfield DC, Eds. In: Early life stage mortality syndrome in fishes of the Great Lakes and Baltic Sea Am Fish Soc Symp. 1998; 21: pp. 160-71., 17Fynn-Aikins K, Bowser PR, Honeyfield DC, Fitzsimons JD, Ketola GH. Effect of dietary amprolium on tissue thiamine and Cayuga syndrome in Atlantic Salmon. Trans Am Fish Soc 1998; 127: 747-57.
[http://dx.doi.org/10.1577/1548-8659(1998)127<0747:EODAOT>2.0.CO;2]
, 30Wolmagood M, Hnath JG, Brown SB, et al. Temporal and spatial variation of early mortality syndrome in Salmonids from Lakes Michigan and Huron. J Aquat Anim Health 2005; 17: 65-76.
[http://dx.doi.org/10.1577/H03-077.1]
, 46Brown SB, Fitzsimons JD, Palace VP, Vandenbyllaardt L. Thiamine and early mortality syndrome in lake trout. In: McDonald G, Fitzsimons JD, Honeyfield DC, Eds. Early life stage mortality syndrome in fishes of the Great Lakes and Baltic Sea. Am Fish Soc Symp 1998; 21: pp. 18-24.], free thiamine was the most prevalent form of thiamine in Lake Oahe Chinook Salmon eggs. Free thiamine likely acts as a storage vitamer and is converted to TPP or TMP later during development [46Brown SB, Fitzsimons JD, Palace VP, Vandenbyllaardt L. Thiamine and early mortality syndrome in lake trout. In: McDonald G, Fitzsimons JD, Honeyfield DC, Eds. Early life stage mortality syndrome in fishes of the Great Lakes and Baltic Sea. Am Fish Soc Symp 1998; 21: pp. 18-24.]. In contrast, TPP was the predominant vitamer in adult tissue. This has also been observed with other adult Salmonids [20Fisher JP, Brown SB, Wooster GW, Bowser PR. Maternal blood, egg and larval thiamin levels correlate with larval survival in landlocked Atlantic Salmon. J Nutr 1998; 128(12): 2456-66.
[PMID: 9868194]
, 47Honeyfield DC, Hinterkopf JP, Fitzsimons JD, Tillitt DE, Zajicek JL, Brown SB. Development of thiamine deficiencies and early mortality syndrome in lake Trout by feeding experimental and feral fish diets containing thiaminase. J Aquat Anim Health 2005; 17: 4-12.
[http://dx.doi.org/10.1577/H03-078.1]
], and is not surprising given that TPP is a biologically-active form of thiamine required for cellular metabolism [10Machlin LJ. Handbook of vitamins. New York: Marcel Dekker, Inc. 1991.].

The relatively weak, but significant, positive correlation between egg size and egg survival observed in this study has been reported for other Salmonids [6Iwamoto RN, Sower S. Salmonid reproduction an international symposium. Seattle, Washington: University of Washington Press 1983; pp. 44-8., 48Gall GA. Influence of size of eggs and age of female on hatchability and growth in rainbow trout. Calif Fish Game 1974; 60: 26-36.]. In contrast, inverse relationships between Chinook Salmon egg size and subsequent survival have been documented, with larger eggs experiencing higher mortality [49Fowler LG. Growth and mortality of fingerling Chinook Salmon as affected by egg size. Prog Fish-Cult 1972; 34: 66-9.
[http://dx.doi.org/10.1577/1548-8640(1972)34[66:GAMOFC]2.0.CO;2]
]. This was also observed during one year with Lake Oahe Chinook Salmon eggs [1Barnes ME, Hanten RP, Cordes RJ, Sayler WA, Carreiro J. Reproductive performance of inland fall Chinook Salmon. N Am J Aquaculture 2000; 62: 203-11.
[http://dx.doi.org/10.1577/1548-8454(2000)062<0203:RPOIFC>2.3.CO;2]
]. However, studies with Chinook Salmon and other Salmonids have found no correlation between the egg size and survival [1Barnes ME, Hanten RP, Cordes RJ, Sayler WA, Carreiro J. Reproductive performance of inland fall Chinook Salmon. N Am J Aquaculture 2000; 62: 203-11.
[http://dx.doi.org/10.1577/1548-8454(2000)062<0203:RPOIFC>2.3.CO;2]
, 50Estay F, Diaz NF, Neira R, Garcia X. Reproductive performance of female coho Salmon in Chile. Prog Fish-Cult 1997; 59: 36-40.
[http://dx.doi.org/10.1577/1548-8640(1997)059<0036:RPOCFC>2.3.CO;2]
, 51Hamoutene D, Lush L, Drover D, Walsh A. Investigation of the temporal effects of spawning season and maternal and paternal differences of egg quality in Atlantic cod Gadus morhua. Broodstock. Aquacult Res 2009; 40: 1668-79.
[http://dx.doi.org/10.1111/j.1365-2109.2009.02271.x]
].

Even though the Chinook Salmon eggs in this study did not appear to be thiamine deficient, survival was still very poor. Survival to the eyed-egg stage of development has been reported from 83% to 98% from Chinook Salmon in their native range [3Banks JL, Fowler LG. Transportation, storage and handling studies of fall Chinook Salmon gametes and newly fertilized eggs Abernathy Salmon Cultural Development Center, Technology Transfer Series 82-4. US. Fish Wildlife Service 1982., 28Ketola GH, Bowser PR, Wooster GA, Wedge LR, Hurst SS. Effects of thiamine on reproduction of Atlantic Salmon and a new hypothesis for their extirpation in Lake Ontario. Trans Am Fish Soc 1999; 129: 607-12.
[http://dx.doi.org/10.1577/1548-8659(2000)129<0607:EOTORO>2.0.CO;2]
, 52Beacham TD, Murray CB. Variation in developmental biology of sockeye Salmon (Oncorhynchus nerka) and Chinook Salmon (O. tshawytscha) in British Columbia. Can J Zool 1989; 67: 2081-9.
[http://dx.doi.org/10.1139/z89-297]
, 53Geist DR, Abernethy CS, Hand KD, Cullinan VI, Chandler JA, Groves PA. Survival, development, and growth of fall Chinook Salmon embryos, alevins, and fry exposed to variable thermal and dissolved oxygen regimes. Trans Am Fish Soc 2006; 135: 1462-77.
[http://dx.doi.org/10.1577/T05-294.1]
]. Egg survival in 2003 and 2005 was also dramatically lower than that previously reported for Lake Oahe Chinook Salmon [1Barnes ME, Hanten RP, Cordes RJ, Sayler WA, Carreiro J. Reproductive performance of inland fall Chinook Salmon. N Am J Aquaculture 2000; 62: 203-11.
[http://dx.doi.org/10.1577/1548-8454(2000)062<0203:RPOIFC>2.3.CO;2]
]. Elevated water temperatures during gamete formation and maturation, energy-related maternal dietary issues, and genetic inbreeding may all contribute to the observed poor reproductive success [1Barnes ME, Hanten RP, Cordes RJ, Sayler WA, Carreiro J. Reproductive performance of inland fall Chinook Salmon. N Am J Aquaculture 2000; 62: 203-11.
[http://dx.doi.org/10.1577/1548-8454(2000)062<0203:RPOIFC>2.3.CO;2]
, 7Poston HA, Ketola HG. Chemical composition of maturing and spawning Atlantic Salmon from different locations. Prog Fish-Cult 1989; 51: 133-9.
[http://dx.doi.org/10.1577/1548-8640(1989)051<0133:CCOMAS>2.3.CO;2]
, 8Gjerde B, Gunnes K, Gjedrem T. Effect of inbreeding on survival and growth in rainbow trout. Aquaculture 1983; 34: 327-32.
[http://dx.doi.org/10.1016/0044-8486(83)90212-0]
, 54Hanten RP. Whitlocks Bay Salmon Spawning Station report 11-02. Pierre, South Dakota: South Dakota Department of Game, Fish and Parks 2011.].

CONCLUSION

Egg and maternal liver thiamine concentrations in landlocked fall Chinook Salmon from Lake Oahe vary dramatically from year-to-year, likely due to the considerable changes in Salmon prey species abundance and availability that frequently occur in Lake Oahe [1Barnes ME, Hanten RP, Cordes RJ, Sayler WA, Carreiro J. Reproductive performance of inland fall Chinook Salmon. N Am J Aquaculture 2000; 62: 203-11.
[http://dx.doi.org/10.1577/1548-8454(2000)062<0203:RPOIFC>2.3.CO;2]
, 55Stone CC, Nealson P. An estimate of abundance and distribution of rainbow smelt in Lake Oahe reservoir using hydroacoustic techniques, 1988-1989. Progress Report 90-8. Pierre, South Dakota: South Dakota Department of Game, Fish and Parks 1990.]. The effects on adult fish physiology of relatively low levels of thiamine in maternal livers are unknown, and further research is needed. Lake Oahe Chinook Salmon eggs show no indication of thiamine deficiency, but survival is still relatively poor. Further research is also needed to ascertain the reason for lower thiamine levels in eggs from spawns that experienced total mortality in comparison to successful spawns.

CONSENT FOR PUBLICATION

Not applicable.

CONFLICT OF INTEREST

The author (editor) declares no conflict of interest, financial or otherwise.

ACKNOWLEDGEMENTS

Funding for this study was partially provided by Federal Aid in Sport Fish Restoration, project F-21-R, study 1587. We thank Jonathan A. Schumacher, Kelly S. Stock, Faraz Farrokhi, Rebecca L. Nutter, Rick Cordes, Will Sayler, Kody Steinbrecher, Fritz Fonck, Dave Stout, Bernie Heath, Brian Smith, John Lott, and Robert P. Hanten for their assistance with egg and tissue collection, thiamine analysis, and egg incubation.

REFERENCES

[1] Barnes ME, Hanten RP, Cordes RJ, Sayler WA, Carreiro J. Reproductive performance of inland fall Chinook Salmon. N Am J Aquaculture 2000; 62: 203-11.
[http://dx.doi.org/10.1577/1548-8454(2000)062<0203:RPOIFC>2.3.CO;2]
[2] Johnson HE, Brice RF. Effects of transportation of green eggs, and of water temperature during incubation, on the mortality of Chinook Salmon. Prog Fish-Cult 1953; 15: 104-8.
[http://dx.doi.org/10.1577/1548-8640(1953)15[104:EOTOGE]2.0.CO;2]
[3] Banks JL, Fowler LG. Transportation, storage and handling studies of fall Chinook Salmon gametes and newly fertilized eggs Abernathy Salmon Cultural Development Center, Technology Transfer Series 82-4. US. Fish Wildlife Service 1982.
[4] Marrone GM, Stout DA. Whitlocks Bay Spawning station annual report 97-119. South Dakota Department Game, Fish and Parks. Ann Rep 1997; 1997: 97-119.
[5] Quinn TP. The behavior and ecology of Pacific Salmon and Trout. Seattle, Washington: University of Washington Press 2005.
[6] Iwamoto RN, Sower S. Salmonid reproduction an international symposium. Seattle, Washington: University of Washington Press 1983; pp. 44-8.
[7] Poston HA, Ketola HG. Chemical composition of maturing and spawning Atlantic Salmon from different locations. Prog Fish-Cult 1989; 51: 133-9.
[http://dx.doi.org/10.1577/1548-8640(1989)051<0133:CCOMAS>2.3.CO;2]
[8] Gjerde B, Gunnes K, Gjedrem T. Effect of inbreeding on survival and growth in rainbow trout. Aquaculture 1983; 34: 327-32.
[http://dx.doi.org/10.1016/0044-8486(83)90212-0]
[9] Araki H, Berejikian BA, Ford MJ, Blouin MS. Fitness of hatchery-reared Salmonids in the wild. Evol Appl 2008; 1(2): 342-55.
[http://dx.doi.org/10.1111/j.1752-4571.2008.00026.x] [PMID: 25567636]
[10] Machlin LJ. Handbook of vitamins. New York: Marcel Dekker, Inc. 1991.
[11] Hill TD. Life history and bioenergetics of Chinook Salmon in Lake Oahe, South Dakota. Brookings, South PhD Dissertation. Dakota: South Dakota State University 1997.
[12] Gnaedinger RH. Thiaminase activity in fish: An improved assay method. Fish Ind Res 1964; 2: 55-9.
[13] Ji YQ, Adelman IR. Thiaminase activity in alewives and smelt in Lakes Huron, Michigan, and Superior. In: McDonald G, Fitzsimons JD, Honeyfield DC, Eds. In: Early life stage mortality syndrome in fishes of the Great Lakes and Baltic Sea Am Fish Soc Symp 1998; 21: pp. 154-9.
[14] Fitzsimons JD, Brown SB. Reduced egg thiamine levels in inland and Great Lakes lake Trout and their relationship with diet. In: Fitzsimons JD, Honeyfield DC, Eds. In: Early life stage mortality syndrome in fishes of the Great Lakes and Baltic Sea Am Fish Soc Symp. 1998; 21: pp. 160-71.
[15] Bylund G, Lerche O. Thiamine therapy of M74 affected fry of Atlantic Salmon Salmo salar. Bull Eur Assoc Fish Pathol 1995; 15: 93-7.
[16] Fitzsimons JD. The effect of B-vitamins on a swim-up syndrome in Lake Ontario lake Trout. Great Lakes Res 1995; 21: 286-9.
[http://dx.doi.org/10.1016/S0380-1330(95)71102-9]
[17] Fynn-Aikins K, Bowser PR, Honeyfield DC, Fitzsimons JD, Ketola GH. Effect of dietary amprolium on tissue thiamine and Cayuga syndrome in Atlantic Salmon. Trans Am Fish Soc 1998; 127: 747-57.
[http://dx.doi.org/10.1577/1548-8659(1998)127<0747:EODAOT>2.0.CO;2]
[18] Amcoff P, Norrgren L, Borjeson H, Linderberg J. Lowered concentrations of thiamine (vitamin B1) in M74-affected feral Baltic Salmon (Salmon salar). Sweden: Rapport-Naturvaardsverket 1996.
[19] Brown SB, Fitzsimons JD, Honeyfeild DC, Tillitt DE. Implications of thiamine deficiency in Great Lakes Salmonines. J Aquat Anim Health 2005; 17: 113-24.
[http://dx.doi.org/10.1577/H04-015.1]
[20] Fisher JP, Brown SB, Wooster GW, Bowser PR. Maternal blood, egg and larval thiamin levels correlate with larval survival in landlocked Atlantic Salmon. J Nutr 1998; 128(12): 2456-66.
[PMID: 9868194]
[21] Riley SC, Rinchard J, Honeyfield DC, Evans AN, Begnoche L. Increasing thiamine concentrations in lake trout eggs from Lakes Huron and Michigan coincide with low alewife abundance. N Am J Fish Manage 2011; 31: 1052-64.
[http://dx.doi.org/10.1080/02755947.2011.641066]
[22] Barnes ME, Zehfus MH, Schumacher JA, et al. Maternal liver and egg thiamine concentrations in Chinook Salmon from Lake Oahe, South Dakota. Prairie Nat 2003; 35: 113-7.
[23] Lott J, Marrone G, Stout D. Influence of size-and-date at stocking, imprinting attempts and growth on initial survival, homing ability, maturation patterns and angler harvest of Chinook Salmon in Lake Oahe, South Dakota. Progress Report 97-20. Pierre, South Dakota: South Dakota Department Game, Fish Parks 1997.
[24] Barnes ME, Wipf MM, Domenici NR, Kummer WM, Hanten RP. Decreased hatchery rearing density improves post-stocking harvest and return to spawning of landlocked fall Chinook Salmon. N Am J Aquaculture 2013; 75: 244-50.
[http://dx.doi.org/10.1080/15222055.2013.768573]
[25] Piper RG, McElwain IB, Orme LE, McCraren JP, Fowler LG, Leonard JR. Fish Hatchery Management. Washington, DC: US. Fish and Wildlife Service 1982.
[26] Brown SB, Honeyfield DC, Vandenbyllaardt L, McDonald G, Fitzsimons JD, Honeyfield DC. Thiamine analysis in fish tissues. In: Early life stage mortality syndrome in fishes of the Great Lakes and Baltic Sea. Am Fish Soc Symp 1998; 21: pp. 73-81.
[27] Fisher JP, Brown SB, Connelly S, Chiottie T, Krueger CC. Interspecies comparisons of blood thiamine in salmonids from the Finger Lakes, and effect of maternal size on blood and egg thiamine in Atlantic Salmon with and without Cayuga syndrome. In: McDonald G, Fitzsimons JD, Honeyfield DC, Eds. Early life stage mortality syndrome in fishes of the Great Lakes and Baltic Sea. Am Fish Soc Symp 1998; 21: pp. 112-23.
[28] Ketola GH, Bowser PR, Wooster GA, Wedge LR, Hurst SS. Effects of thiamine on reproduction of Atlantic Salmon and a new hypothesis for their extirpation in Lake Ontario. Trans Am Fish Soc 1999; 129: 607-12.
[http://dx.doi.org/10.1577/1548-8659(2000)129<0607:EOTORO>2.0.CO;2]
[29] Wooster GA, Bowser PR, Brown SB, Fisher JP. Remediation of Cayuga Syndrome in landlocked Atlantic Salmon Salmo salar using egg and sac-fry bath treatments of thiamine-hydrochloride. J World Aquacult Soc 2000; 31: 149-57.
[http://dx.doi.org/10.1111/j.1749-7345.2000.tb00348.x]
[30] Wolmagood M, Hnath JG, Brown SB, et al. Temporal and spatial variation of early mortality syndrome in Salmonids from Lakes Michigan and Huron. J Aquat Anim Health 2005; 17: 65-76.
[http://dx.doi.org/10.1577/H03-077.1]
[31] Fitzsimons JD, Williston B, Williston G, et al. Egg thiamine status of Lake Ontario Salmonines 1995-2004 with emphasis on lake Trout. J Great Lakes Res 2007; 33: 93-103.
[http://dx.doi.org/10.3394/0380-1330(2007)33[93:ETSOLO]2.0.CO;2]
[32] Rolland RM, Gilbertson M, Peterson RE. Chemically induced alterations in functional development and reproduction of fishes: Proceedings from a session at the 1995 Wingspread Conference. Pensacola: Society of Environmental Toxicology and Chemistry (SETAC) 1997; 146-60.
[33] Koski P, Soivio A, Hartikainen K, Hirvi T, Myllyla T. M74 syndrome and thiamine in Salmon broodfish and offspring. Boreal Environ Res 2001; 6: 79-92.
[34] Ketola HG, Johnson JH, Rinchard J, et al. Effect of thiamine status on probability of Lake Ontario Chinook Salmon spawning in the upper and lower sections of the Salmon River, New York. N Am J Fish Manage 2009; 29: 895-902.
[http://dx.doi.org/10.1577/M08-021.1]
[35] Tillit DE, Zajicek JE, Brown SB, et al. Thiamine and thiaminase status in forage fish of Salmonines from Lake Michigan. J Aquat Anim Health 2005; 17: 13-25.
[http://dx.doi.org/10.1577/H03-081.1]
[36] Hirn J, Pekkanen TJ. Quantitative analysis of thiaminase activity in certain fish species. Nord Vet Med 1975; 27(12): 646-8.
[PMID: 1196856]
[37] Brown SB, Arts MT, Brown LR, et al. Can diet-dependent factors help explain fish-to-fish variation in thiamine-dependent early mortality syndrome? J Aquat Anim Health 2005; 17: 36-47.
[http://dx.doi.org/10.1577/H03-072.1]
[38] Barnes ME, Hanten RP, Sayler WA, Cordes RJ. Viability of inland fall Chinook Salmon spawn containing overripe eggs and the reliability of egg viability estimates. N Amer J Aquac 2000; 62: 237-9.
[http://dx.doi.org/10.1577/1548-8454(2000)062<0237:VOIFCS>2.3.CO;2]
[39] Ahlgren GL, Nieuwerburgh V, Wänstrand I, Pedersén M, Boberg M, Snoeijs P. Imbalance of fatty acids in the base of the Baltic Sea food web: A mesocosm study. Can J Fish Aquat Sci 2005; 62: 2240-53.
[http://dx.doi.org/10.1139/f05-140]
[40] Vuori KA, Nikinmaa M. M74 syndrome in Baltic Salmon and the possible role of oxidative stresses in its development: Present knowledge and perspectives for future studies. Ambio 2007; 36(2-3): 168-72.
[http://dx.doi.org/10.1579/0044-7447(2007)36[168:MSIBSA]2.0.CO;2] [PMID: 17520930]
[41] Czesny S, Dettmers JM, Rinchard J, Dabrowski K. Linking egg thiamine and fatty acid concentrations of Lake Michigan lake Trout with early life stage mortality. J Aquat Anim Health 2009; 21(4): 262-71.
[http://dx.doi.org/10.1577/H07-056.1] [PMID: 20218500]
[42] Keinänen M, Uddström A, Mikkonen J, et al. 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 2012; 69: 516-28.
[http://dx.doi.org/10.1093/icesjms/fss041]
[43] Johnston TA, Leggett WC. Maternal and environmental gradients in the egg size of an iteroparous fish. Ecol Soc Amer 2002; 83: 1777-91.
[44] Brown SB, Honeyfield DC, Hnath JG, et al. Thiamine status in adult Salmonines in the Great Lakes. J Aquat Anim Health 2005; 17: 59-64.
[http://dx.doi.org/10.1577/H04-059.1]
[45] Fitzsimons JD, Williston B, Amcoff P, et al. The effect of thiamine injection on upstream migration, survival and thiamine status of putative thiamine-thiamine deficient coho Salmon. J Aquat Anim Health 2005; 17: 48-58.
[http://dx.doi.org/10.1577/H04-003.1]
[46] Brown SB, Fitzsimons JD, Palace VP, Vandenbyllaardt L. Thiamine and early mortality syndrome in lake trout. In: McDonald G, Fitzsimons JD, Honeyfield DC, Eds. Early life stage mortality syndrome in fishes of the Great Lakes and Baltic Sea. Am Fish Soc Symp 1998; 21: pp. 18-24.
[47] Honeyfield DC, Hinterkopf JP, Fitzsimons JD, Tillitt DE, Zajicek JL, Brown SB. Development of thiamine deficiencies and early mortality syndrome in lake Trout by feeding experimental and feral fish diets containing thiaminase. J Aquat Anim Health 2005; 17: 4-12.
[http://dx.doi.org/10.1577/H03-078.1]
[48] Gall GA. Influence of size of eggs and age of female on hatchability and growth in rainbow trout. Calif Fish Game 1974; 60: 26-36.
[49] Fowler LG. Growth and mortality of fingerling Chinook Salmon as affected by egg size. Prog Fish-Cult 1972; 34: 66-9.
[http://dx.doi.org/10.1577/1548-8640(1972)34[66:GAMOFC]2.0.CO;2]
[50] Estay F, Diaz NF, Neira R, Garcia X. Reproductive performance of female coho Salmon in Chile. Prog Fish-Cult 1997; 59: 36-40.
[http://dx.doi.org/10.1577/1548-8640(1997)059<0036:RPOCFC>2.3.CO;2]
[51] Hamoutene D, Lush L, Drover D, Walsh A. Investigation of the temporal effects of spawning season and maternal and paternal differences of egg quality in Atlantic cod Gadus morhua. Broodstock. Aquacult Res 2009; 40: 1668-79.
[http://dx.doi.org/10.1111/j.1365-2109.2009.02271.x]
[52] Beacham TD, Murray CB. Variation in developmental biology of sockeye Salmon (Oncorhynchus nerka) and Chinook Salmon (O. tshawytscha) in British Columbia. Can J Zool 1989; 67: 2081-9.
[http://dx.doi.org/10.1139/z89-297]
[53] Geist DR, Abernethy CS, Hand KD, Cullinan VI, Chandler JA, Groves PA. Survival, development, and growth of fall Chinook Salmon embryos, alevins, and fry exposed to variable thermal and dissolved oxygen regimes. Trans Am Fish Soc 2006; 135: 1462-77.
[http://dx.doi.org/10.1577/T05-294.1]
[54] Hanten RP. Whitlocks Bay Salmon Spawning Station report 11-02. Pierre, South Dakota: South Dakota Department of Game, Fish and Parks 2011.
[55] Stone CC, Nealson P. An estimate of abundance and distribution of rainbow smelt in Lake Oahe reservoir using hydroacoustic techniques, 1988-1989. Progress Report 90-8. Pierre, South Dakota: South Dakota Department of Game, Fish and Parks 1990.

Endorsements



"Open access will revolutionize 21st century knowledge work and accelerate the diffusion of ideas and evidence that support just in time learning and the evolution of thinking in a number of disciplines."


Daniel Pesut
(Indiana University School of Nursing, USA)

"It is important that students and researchers from all over the world can have easy access to relevant, high-standard and timely scientific information. This is exactly what Open Access Journals provide and this is the reason why I support this endeavor."


Jacques Descotes
(Centre Antipoison-Centre de Pharmacovigilance, France)

"Publishing research articles is the key for future scientific progress. Open Access publishing is therefore of utmost importance for wider dissemination of information, and will help serving the best interest of the scientific community."


Patrice Talaga
(UCB S.A., Belgium)

"Open access journals are a novel concept in the medical literature. They offer accessible information to a wide variety of individuals, including physicians, medical students, clinical investigators, and the general public. They are an outstanding source of medical and scientific information."


Jeffrey M. Weinberg
(St. Luke's-Roosevelt Hospital Center, USA)

"Open access journals are extremely useful for graduate students, investigators and all other interested persons to read important scientific articles and subscribe scientific journals. Indeed, the research articles span a wide range of area and of high quality. This is specially a must for researchers belonging to institutions with limited library facility and funding to subscribe scientific journals."


Debomoy K. Lahiri
(Indiana University School of Medicine, USA)

"Open access journals represent a major break-through in publishing. They provide easy access to the latest research on a wide variety of issues. Relevant and timely articles are made available in a fraction of the time taken by more conventional publishers. Articles are of uniformly high quality and written by the world's leading authorities."


Robert Looney
(Naval Postgraduate School, USA)

"Open access journals have transformed the way scientific data is published and disseminated: particularly, whilst ensuring a high quality standard and transparency in the editorial process, they have increased the access to the scientific literature by those researchers that have limited library support or that are working on small budgets."


Richard Reithinger
(Westat, USA)

"Not only do open access journals greatly improve the access to high quality information for scientists in the developing world, it also provides extra exposure for our papers."


J. Ferwerda
(University of Oxford, UK)

"Open Access 'Chemistry' Journals allow the dissemination of knowledge at your finger tips without paying for the scientific content."


Sean L. Kitson
(Almac Sciences, Northern Ireland)

"In principle, all scientific journals should have open access, as should be science itself. Open access journals are very helpful for students, researchers and the general public including people from institutions which do not have library or cannot afford to subscribe scientific journals. The articles are high standard and cover a wide area."


Hubert Wolterbeek
(Delft University of Technology, The Netherlands)

"The widest possible diffusion of information is critical for the advancement of science. In this perspective, open access journals are instrumental in fostering researches and achievements."


Alessandro Laviano
(Sapienza - University of Rome, Italy)

"Open access journals are very useful for all scientists as they can have quick information in the different fields of science."


Philippe Hernigou
(Paris University, France)

"There are many scientists who can not afford the rather expensive subscriptions to scientific journals. Open access journals offer a good alternative for free access to good quality scientific information."


Fidel Toldrá
(Instituto de Agroquimica y Tecnologia de Alimentos, Spain)

"Open access journals have become a fundamental tool for students, researchers, patients and the general public. Many people from institutions which do not have library or cannot afford to subscribe scientific journals benefit of them on a daily basis. The articles are among the best and cover most scientific areas."


M. Bendandi
(University Clinic of Navarre, Spain)

"These journals provide researchers with a platform for rapid, open access scientific communication. The articles are of high quality and broad scope."


Peter Chiba
(University of Vienna, Austria)

"Open access journals are probably one of the most important contributions to promote and diffuse science worldwide."


Jaime Sampaio
(University of Trás-os-Montes e Alto Douro, Portugal)

"Open access journals make up a new and rather revolutionary way to scientific publication. This option opens several quite interesting possibilities to disseminate openly and freely new knowledge and even to facilitate interpersonal communication among scientists."


Eduardo A. Castro
(INIFTA, Argentina)

"Open access journals are freely available online throughout the world, for you to read, download, copy, distribute, and use. The articles published in the open access journals are high quality and cover a wide range of fields."


Kenji Hashimoto
(Chiba University, Japan)

"Open Access journals offer an innovative and efficient way of publication for academics and professionals in a wide range of disciplines. The papers published are of high quality after rigorous peer review and they are Indexed in: major international databases. I read Open Access journals to keep abreast of the recent development in my field of study."


Daniel Shek
(Chinese University of Hong Kong, Hong Kong)

"It is a modern trend for publishers to establish open access journals. Researchers, faculty members, and students will be greatly benefited by the new journals of Bentham Science Publishers Ltd. in this category."


Jih Ru Hwu
(National Central University, Taiwan)


Browse Contents



Webmaster Contact: info@benthamopen.net
Copyright © 2019 Bentham Open