The Open Biology Journal




ISSN: 1874-1967 ― Volume 7, 2019
RESEARCH ARTICLE

Effects of Exercise and Bioprocessed Soybean Meal Diets during Rainbow Trout Rearing



Jill M. Voorhees1, Michael E. Barnes1, *, Steven R. Chipps2, Michael L. Brown3
1 South Dakota Department of Game, Fish and Parks, McNenny State Fish Hatchery, 19619 Trout Loop, Spearfish, SD 57783, USA
2 Department of Natural Resource Management, U.S. Geological Survey, South Dakota Cooperative Fish and Wildlife Research Unit, South Dakota State University, Brookings, SD 57007, USA
3 Department of Natural Resource Management, South Dakota State University, Brookings, SD 57007, USA

Abstract

Background:

Alternative protein sources to fishmeal in fish feeds are needed.

Objectives:

Evaluate rearing performance of adult rainbow trout (Oncorhynchus mykiss) (initial weight 139.0 ±1.5 g, length 232.9 ± 0.8 mm, mean ± SE) fed one of the two isonitrogenous and isocaloric diets (46% protein, 16% lipid) and reared at one of the two levels of exercise (water velocities of either 3.6 cm/s or 33.2 cm/s).

Methods:

Protein in the control diet was based on fishmeal. In the experimental diet, bioprocessed soybean meal replaced approximately 60% of the fishmeal. Fish were fed by hand once-per-day to near satiation, and the food was increased daily. The experiment lasted 90-days.

Results:

There were no significant differences in gain, percent gain, or specific growth rate between the dietary treatments. However, the amount of food fed and feed conversion ratio was significantly lower in the 60% bioprocessed soybean meal diet. Intestinal morphology, relative fin length, splenosomatic index, hepatosomatic index, and viscerosomatic index were not significantly different in the trout fed either diet. Fish reared at 3.6 cm/s had a significantly lower feed conversion ratio (1.02 ± 0.02) than fish reared at 33.2 cm/s (1.13 ± 0.02). However, there were no significant differences in gain, percent gain, specific growth rate, or percentage mortality in fish reared with or without exercise. No significant interactions were observed between diet and exercise (higher water velocity).

Conclusion:

Based on these results, at least 60% of the fishmeal in adult rainbow trout diets can be replaced by bioprocessed soybean meal, even if higher water velocities are used to exercise the fish.

Keywords: Alternative protein, Growth, Oncorhynchus mykiss, Salmonid, Water velocity, Bioprocessed soybean meal.


Article Information


Identifiers and Pagination:

Year: 2019
Volume: 7
First Page: 1
Last Page: 13
Publisher Id: TOBIOJ-7-1
DOI: 10.2174/1874196701907010001

Article History:

Received Date: 07/09/2018
Revision Received Date: 07/03/2019
Acceptance Date: 19/03/2019
Electronic publication date: 16/04/2019
Collection year: 2019

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© 2019 Voorhees 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 South Dakota Department of Game, Fish and Parks, McNenny State Fish Hatchery, 19619 Trout Loop, Spearfish, SD 57783, USA; Tel: 605-645-1262; Fax: 605-645-6921;
E-mail: mike.barnes@state.sd.us





1. INTRODUCTION

The use of soybean (Glycine max) meal in carnivorous fish diets has been subjected to considerable research [1Collins SA, Øverland M, Skrede A, Drew MD. Effect of plant protein sources on growth rate in salmonids: Meta-analysis of dietary inclusion of soybean, pea and canola/rapeseed meals and protein concentrates. Aquaculture 2013; 400-401: 85-100.[http://dx.doi.org/10.1016/j.aquaculture.2013.03.006] , 2Storebakken T, Refstie S, Ruyter B. Soy products as fat and protein sources in fish feed for intensive aquaculture. In: Drackley JK, Ed. Soy in animal nutrition 2000; 127-70.]. However, the inclusion of soybean meal into salmonid diets, such as rainbow trout (Oncorhynchus mykiss), is limited because soybean meal contains numerous antinutritional factors [3Bakke AM. Pathophysiological and immunological characteristics of soybean meal-induced enteropathy in salmon: Contribution of recent molecular investigations. In: Cruz-Suárex LE, Ricque-Marie D, Tapia-Salazar M, Eds. In: Proceedings of International Symposium Aquaculture Nutrition XI. Monterrey: Universidad Autónoma de Nuevo León; 2011; pp. 2011; 345-72.-5Krogdahl Å, Berg-Lea T, Olli JJ. Soybean proteinase inhibitors affect intestinal trypsin activities and amino acid digestibilities in rainbow trout (Oncorhynchus mykiss). CBP: A. Physiology (Bethesda) 1994; 107: 215-9.[http://dx.doi.org/10.1016/0300-9629(94)90296-8] ] which can negatively impact fish health and growth [6Krogdahl Å, Penn M, Thorsen J, Refstie S, Bakke AM. Important antinutrients in plant feedstuffs for aquaculture: An update on recent findings regarding responses in salmonids. Aquacult Res 2010; 41: 333-44.[http://dx.doi.org/10.1111/j.1365-2109.2009.02426.x] -10Sealey WM, Barrows FT, Smith CE, Overturf K, LaPatra SE. Soybean meal level and probiotics in first feeding fry diets alter the ability of rainbow trout Oncorhynchus mykiss to utilize high levels of soybean meal during grow-out. Aquaculture 2009; 293: 195-203.[http://dx.doi.org/10.1016/j.aquaculture.2009.04.013] ]. Soybean meal can be treated with chemicals, pressure, or heat, to reduce or completely eliminate these antinutritional factors [11Barrows FT, Stone DAJ, Hardy RW. The effects of extrusion conditions on the nutritional value of soybean meal for rainbow trout (Oncorhynchus mykiss). Aquaculture 2007; 265: 244-52.[http://dx.doi.org/10.1016/j.aquaculture.2007.01.017] -13Gomes EF, Rema P, Kaushik SJ. Replacement of fish meal by plant proteins in the diet of rainbow trout (Oncorhynchus mykiss): Digestibility and growth performance. Aquaculture 1995; 130: 177-86.[http://dx.doi.org/10.1016/0044-8486(94)00211-6] ]. Bioprocessing, such as fermentation, is another method that can be used to improve the suitability of soybean meal in fish diets, and forms of bioprocessed soybean meal have been investigated as alternative protein sources in rainbow trout diets [14Bruce TJ, Neiger RD, Brown ML. Gut histology, immunology and the intestinal microbiota of rainbow trout, Oncorhynchus mykiss (Walbaum), fed process variants of soybean meal. Aquacult Res 2018; 49: 492-504.[http://dx.doi.org/10.1111/are.13480] -16Yamamoto T, Matsunari H, Sugita T, et al. Optimization of the supplemental essential amino acids to a fish meal-free diet based on fermented soybean meal for rainbow trout Oncorhynchus mykiss. Fish Sci 2012; 78: 359-66.[http://dx.doi.org/10.1007/s12562-011-0456-2] ].

Just as dietary ingredients can impact fish growth, using higher water velocities to exercise fish can also positively impact rearing performance [17Good C, May T, Crouse C, Summerfelt S, Welch TJ. Assessing the impact of swimming exercise and the relative susceptibility of rainbow trout Oncorhynchus mykiss (Walbaum) and Atlantic salmon Salmo salar L. following injection challenge with Weissella ceti. J Fish Dis 2016; 39(11): 1387-91.[http://dx.doi.org/10.1111/jfd.12468] [PMID: 27087506] -20Parker TM, Barnes ME. Effects of different water velocities on hathcery rearing performance and recovery from transportation of rainbow trout fed two different rations. Trans Am Fish Soc 2015; 144: 882-90.[http://dx.doi.org/10.1080/00028487.2015.1047533] ]. Parker and Barnes [20Parker TM, Barnes ME. Effects of different water velocities on hathcery rearing performance and recovery from transportation of rainbow trout fed two different rations. Trans Am Fish Soc 2015; 144: 882-90.[http://dx.doi.org/10.1080/00028487.2015.1047533] ] observed improved growth in rainbow trout fed to satiation and exercised using elevated water velocities in circular tanks. However, growth has been shown to be impaired in exercised fish if the feed amounts were restricted [19Parker TM, Barnes ME. Rearing velocity impacts on landlocked fall Chinook salmon (Oncorhynchus tshawytscha) growth, condition, and survival. Open J Anim Sci 2014; 4: 244-52.[http://dx.doi.org/10.4236/ojas.2014.45031] ].

A few studies evaluating forms of bioprocessed soybean meal (BSM) in rainbow trout diets have been conducted, but novel BSM products continue to be developed. In addition, very little research has been published examining the potential interaction between exercise (increased water velocities) and diet, particularly in relation to non-fishmeal based diets in any fish species. Therefore, the objective of this study was to evaluate the use of a propriety BSM product as the primary dietary protein source, in conjunction with exercise (increased water velocity), during rainbow trout rearing.

2. MATERIALS AND METHODS

This experiment was conducted at Cleghorn Springs State Fish Hatchery, Rapid City, South Dakota, USA. Rearing tanks received flow-through, single-pass, spring water (11° C, total hardness as CaCO3, 360 mg/L; alkalinity as CaCO3, 210 mg/L; pH, 7.6; total dissolved solids, 390 mg/L). The study began on July 7, 2016 and lasted 90 days.

Erwin x Arlee strain rainbow trout (initial weight 139.0 ± 1.5 g, length 232.9 ± 0.8 mm, mean ± SE) were randomly selected and placed into one of the 16, cement-bottom, aluminum-sided, circular tanks (6.1 m diameter, 73.7 cm water depth). Twenty fish were placed into each tank. This experiment used a 2 x 2 design (2 diets, 2 velocities; N = 4). Table 1 shows the study design, with water velocities and diets indicated.

Table 1
The experimental design used for this study, with two diets containing different concentrations of bioprocessed soybean meal (BSM) and two velocities (mean ± SE).


Tank water flows and velocities were constant throughout the experiment, and were measured and maintained using a flowmeter (Flowatch, JDC Electronic SA, Yverdon-les-Bains, Jura-Nord Vaudois, Vaud, Switzerland). Velocity measurements were obtained directly behind the spray bar, 60.0 cm from the side of the tank and mid-depth (36.1 cm from the surface).

The two diets used in this study contained either fishmeal with no BSM, or had BSM replace approximately 60% of the dietary fishmeal (Table 2). A proprietary microbial conversion was used to produce the BSM (South Dakota State University, Brookings, South Dakota, USA). Feeds were prepared using an extruder (ExtruTech model 325, Sabetha, Kansas, USA), and were isocaloric and isonitrogenous. AOAC [21Association of Official Analytical Chemists (AOAC). 2009. [cited: Jan 5 2018] http://www.eoma.aoac.org/] method 2001.11 analysis was used to determine dietary protein, method 2003.5 (modified by substituting petroleum ether for diethyl ether) was used to determine crude lipid, and AACC [22Approved methods of the American association of cereal chemists 10th ed. 10th ed.2000.] method 08-03 was used to determine ash content.

Table 2
Ingredients, formulation, and composition analyses of the diets. Analysis was conducted on pellets after extrusion.


Each fish was individually weighed to the nearest 0.1 g and measured to the nearest 1.0 mm prior to placement into one of the sixteen tanks at the beginning of the experiment. At approximately four week intervals, each individual fish was again weighed and measured. Total tank weight was calculated by adding all of the individual fish weights for each tank. Fish were not fed on the days that they were sampled. The hatchery constant method [23Butterbaugh GL, Willoughby H. A feeding guide for brook, brown and rainbow trout. Prog Fish-Cult 1967; 29: 210-5.[http://dx.doi.org/10.1577/1548-8640(1967)29[210:AFGFBB]2.0.CO;2] ] was used to determine initial feeding amounts, using 1.1 as the anticipated feed conversion ratio and 0.08 cm/day as the projected growth rate, based on the historical maximum growth rate for this strain of rainbow trout at Cleghorn Hatchery. The feed was dispersed by hand once per day, with amounts adjusted daily to ensure feed levels were at or near satiation. Mortality and the food fed amounts were recorded daily.

Prior to data collection on days 1, 31, and 61, the fish were anesthetized using 60 mg/L MS-222 (Tricaine-S, tricaine methanesulfonate, Syndel USA, Ferndale, Washington, USA). At the end of the study, the fish were euthanized using a lethal dose of 250 mg/L MS-222 [24AVMA guidelines for the euthanasia of animals 2013 ed. 2013 ed.2013.]. On the last day of the experiment, individual weights and lengths were recorded from all of the fish in each tank. In addition, fin lengths (to the nearest 1.0 mm) and spleen, liver, and visceral weights (to the nearest 1.0 mg) were also recorded from five randomly selected trout per tank. Fin indices, Specific Growth Rate (SGR), Condition Factor (K), Hepatosomatic Index (HSI) [25Strange RJ. Field examination of fishes.Fisheries techniques 2nd ed. 2nd ed.1996; 433-66.], Splenosomatic Index (SSI) [26Goede RW, Barton BA. Organismic indices and an autopsy-based assessment as indicators of health and condition in fish. In: Biological indicators of stress in fish. Symposium 8 : American Fisheries Society; 1990; pp. 1990; 93-108.], and Viscerosomatic Index (VSI) [26Goede RW, Barton BA. Organismic indices and an autopsy-based assessment as indicators of health and condition in fish. In: Biological indicators of stress in fish. Symposium 8 : American Fisheries Society; 1990; pp. 1990; 93-108.] were calculated.

The equations used in this study included:

At the end of the experiment, possible soy-induced enteritis was assessed by excising a 2-mm wide section of the distal intestine from five randomly-selected fish per tank. After excision, the intestinal tissue was immediately fixed using 10% buffered formalin, and then stained with hematoxylin and eosin [27Bureau DP, Harris AM, Cho CY. The effects of purified alcohol extracts from soy products on feed intake and growth of Chinook salmon (Oncorhynchus tshawytscha) and rainbow trout (Oncorhynchus mykiss). Aquaculture 1998; 72: 27-43.[http://dx.doi.org/10.1016/S0044-8486(97)00254-8] , 28Burrells C, Williams PD, Southgate PJ, Crampton VO. Immunological, physiological and pathological responses of rainbow trout (Oncorhynchus mykiss) to increasing dietary concentrations of soybean proteins. Vet Immunol Immunopathol 1999; 72(3-4): 277-88.[http://dx.doi.org/10.1016/S0165-2427(99)00143-9] [PMID: 10628 672] ]. An ordinal system was then used to score the stained intestinal cross-sections, based on lamina propria thickness and cellularity, submucosal connective tissue width, and leukocyte distribution [29Barnes ME, Brown ML, Bruce T, Sindelar S, Neiger R. Rainbow trout rearing performance, intestinal morphology, and immune response after long-term feeding of high levels of fermented soybean meal. N Am J Aquaculture 2014; 76: 333-45.[http://dx.doi.org/10.1080/15222055.2014.920748] -31Knudsen D, Urán P, Arnous A, Koppe W, Frøkiaer H. Saponin-containing subfractions of soybean molasses induce enteritis in the distal intestine of Atlantic salmon. J Agric Food Chem 2007; 55(6): 2261-7.[http://dx.doi.org/10.1021/jf0626967] [PMID: 17326653] ] (Table 3).

For data analysis, two-way Analysis Of Variance (ANOVA) was performed using the SPSS (9.0) statistical analysis program (SPSS, Chicago, Illinois, USA) was used. If the treatments were significantly different, then Tukey’s HSD post hoc mean separation test was performed. Significance was predetermined at P < 0.05.

This experiment was carried out within the American Fisheries Society “Guidelines for the Use of Fishes in Research” [32Guidelines for the use of fishes in research 2004.] and within the guidelines of the Aquatics Section Research Ethics Committee of the South Dakota Department of Game, Fish and Parks, USA.

Table 3
Histological scoring system used on rainbow trout intestinal cross sections.


3. RESULTS

There were no significant differences in gain, percent gain, SGR, and percent mortality between the tanks of fish receiving the fishmeal reference diet or the 60% BSM diet at the end of the experiment (Table 4). However, food fed and FCR were significantly different between the diets, with the fishmeal reference diet having higher values for both variables. The mean (± SE) FCR for rainbow trout fed the fishmeal diet was 1.10 (± 0.02), which was significantly higher than the 1.04 (± 0.03) value for fish fed 60% BSM.

Table 4
Mean (± SE) gain, percent gain, food fed, Feed Conversion Ratio (FCRa), Specific Growth Rate (SGRb), and mortality of rainbow trout reared at two different velocities and receiving one of two diets with either fishmeal or Bioprocessed Soybean Meal (BSM) as the primary protein source. Overall means with different letters in the same row between the diets or in the same column between the velocities differ significantly (P < 0.05). The absence of letters indicates no significant differences.


Similar to the overall end-of-experiment results, there was no significant difference in gain, percent gain, or SGR in any of the rearing periods between the fish being fed the two different diets. The amount of food fed and FCR were significantly different between the diets in the first two rearing periods and overall, but were not significantly different in the final rearing period.

There were no significant differences in individual fish weight, length, and condition factor between dietary treatments at the end of the experiment (Table 5). There were also no significant differences in fin indices (pelvic, pectoral, dorsal), organosomatic indices (SSI, HSI, VSI), or intestinal histological scores. A representative image of the distal intestines from fish in each treatment group are shown in Figs. (1-4).

The velocity results indicated that the trout in the high velocity tanks had a significantly greater FCR than the fish in the lower velocity tanks in each rearing period and overall. Gain, percent gain, food fed, SGR, and percent mortality were not significantly different between the two velocity treatments at the end of the experiment. However, during the third (final) rearing period gain, percent gain, and SGR were significantly greater in the low velocity treatment, with a mean (± SE) percent gain of 45.9 (± 0.7) %, compared to 41.7 (± 1.6) % for fish in the higher velocity tanks.

Individual fish weight and length were significantly greater at the end of the experiment for fish reared at the low velocity, with the mean (± SE) weights of 527.2 (± 15.2) g and 485.1 (± 9.6) g for the fish at low and high velocities, respectively. There were no significant differences in final fin indices (pectoral, pelvic, dorsal), organosomatic indices (HSI, SSI, VSI), or gut histology scores between the velocity treatments. There were also no significant interactions between diet and velocity in any of the variables measured at the end of the study or during any of the rearing periods.

Table 5
Mean (± SE) condition factor (Ka), fin indicesb, Hepatosomatic Index values (HSIc), Splenosomatic Index (SSId), Viscerosomatic Index (VSIe), and histology scores for lamina propria, connective tissue, and vacuoles of rainbow trout fed one of two diets containing either fishmeal or Bioprocessed Soybean Meal (BSM) as the primary protein source, and reared at two different velocities. There were no significant differences among any of the treatments.


Fig. (1)
Distal intestine of an unexercised rainbow trout fed a fishmeal-based diet.


Fig. (2)
Distal intestine of an exercised rainbow trout fed a fishmeal based diet.


Fig. (3)
Distal intestine of an unexercised rainbow trout fed a bioprocessed soybean meal diet.


Fig. (4)
Distal intestine of an exercised rainbow trout fed a bioprocessed soybean meal diet.


4. DISCUSSION

The results of this experiment indicate that BSM can directly replace at least 60% of the dietary fishmeal in adult rainbow trout diets, even for fish subjected to exercise with higher velocities. Similar results have also been reported for non-exercised rainbow trout fed diets with different forms of BSM than that used in this study [14Bruce TJ, Neiger RD, Brown ML. Gut histology, immunology and the intestinal microbiota of rainbow trout, Oncorhynchus mykiss (Walbaum), fed process variants of soybean meal. Aquacult Res 2018; 49: 492-504.[http://dx.doi.org/10.1111/are.13480] , 33Barnes ME, Brown ML, Rosentrater KA, Sewell JR. An initial investigation replacing fish meal with a commercial fermented soybean meal product in the diets of juvenile rainbow trout. Open J Anim Sci 2012; 2: 234-43.[http://dx.doi.org/10.4236/ojas.2012.24033] -36Bruce TJ, Sindelar SC, Voorhees JM, Brown ML, Barnes ME. Performance and immunological responses of rainbow trout (Oncorhynchus mykiss) fed bioprocessed plant-based proteins. Aquacult Nutr 2017; 23: 1160-8.[http://dx.doi.org/10.1111/anu.12485] ]. Yamamoto et al. [15Yamamoto T, Iwashita Y, Matsunari H, et al. Influence of fermentation conditions for soybean meal in a non-fish meal diet on growth performance and physiological condition of rainbow trout Oncorhynchus mykiss. Aquaculture 2010; 309: 173-80.[http://dx.doi.org/10.1016/j.aquaculture.2010.09.021] , 16Yamamoto T, Matsunari H, Sugita T, et al. Optimization of the supplemental essential amino acids to a fish meal-free diet based on fermented soybean meal for rainbow trout Oncorhynchus mykiss. Fish Sci 2012; 78: 359-66.[http://dx.doi.org/10.1007/s12562-011-0456-2] ] were able to successfully replace all the fishmeal with fermented soybean meal in rainbow trout diets. However, these studies were conducted in much warmer water (16.3 °C), and the diets were supplemented with numerous amino acids. Voorhees et al. [37Voorhees JM, Barnes ME, Chipps SR, Brown ML. Dietary bioprocessed soybean meal does not affect the growth of exercised juvenile rainbow trout (Oncorhynchus mykiss). J Anim Res Nutr; in press] used the same BSM product as the current study and noted that replacing up to 85% of dietary fishmeal was possible without compromising juvenile rainbow trout rearing performance. BSM as a dietary protein source has been evaluated in at least 14 other fish species, including other salmonids [38Refstie S, Landsverk T, Bakke-McKellep AM, et al. Digestive capacity, intestinal morphology, and microflora of 1-year and 2-year old Atlantic cod (Gadus morhua) fed standard or bioprocessed soybean meal. Aquaculture 2006; 261: 269-84.[http://dx.doi.org/10.1016/j.aquaculture.2006.07.011] -55Trushenski JT, Rombenso AN, Page M, Jirsa D, Drawbridge M. Traditional and fermented soybean meal as ingredients in feed for white seabass and yellowtail jack. N Am J Aquaculture 2014; 76: 312-22.[http://dx.doi.org/10.1080/15222055.2014.911227] ].

The duration of this study should have been long enough to provide valid and reliable results. Weathercup and McCraken [56Weathercup RN, McCraken KJ. Changes in rainbow trout, Oncorhynchus mykiss (Walbaum), body composition with weight. Aquaculture 1999; 30: 305-7.[http://dx.doi.org/10.1046/j.1365-2109.1999.00320.x] ] noted that feed trials should last long enough to determine any dietary-induced differences in fish growth and rearing performance. The National Research Council [57Nutrient requirements of fish and shirmp 2011.] recommends minimum study duration of 56-84 days, or longer if needed for large fish to attain 200-300% gain. The 265% gain at the end of this 90-day study met these requirements.

Undesirable effects on the distal intestine of rainbow trout from dietary soybean products are well-documented [4Iwashita Y, Yamamoto T, Furuita H, Sugita T, Suzuki N. Influence of certain soybean antinutritional factors supplemented to a casein-based semipurified diet on intestinal and liver morphology in fingerling rainbow trout Oncorhynchus mykiss. Fish Sci 2008; 74: 1075-82.[http://dx.doi.org/10.1111/j.1444-2906.2008.01627.x] , 8Merrifield DL, Dimitroglou A, Bradley G, Baker RTM, Davies SJ. Soybean meal alters autochthonous microbial populations, microvilli morphology and compromises intestinal enterocyte integrity of rainbow trout, Oncorhynchus mykiss (Walbaum). J Fish Dis 2009; 32(9): 755-66.[http://dx.doi.org/10.1111/j.1365-2761.2009.01052.x] [PMID: 19490 393] -10Sealey WM, Barrows FT, Smith CE, Overturf K, LaPatra SE. Soybean meal level and probiotics in first feeding fry diets alter the ability of rainbow trout Oncorhynchus mykiss to utilize high levels of soybean meal during grow-out. Aquaculture 2009; 293: 195-203.[http://dx.doi.org/10.1016/j.aquaculture.2009.04.013] ]. However, the rainbow trout receiving BSM diet did not show any significant intestinal changes or enteritis. The proprietary process of manufacturing the BSM in this study likely depleted the saponins and other compounds linked to enteritis [7Krogdahl Å, Gajardo K, Kortner TM, et al. Soya saponins induce entritis in Atlantic salmon (Salmo salar L.). J Agric Food Chem 2015; 63(15): 3887-902.[http://dx.doi.org/10.1021/jf506242t] [PMID: 25798699] , 16Yamamoto T, Matsunari H, Sugita T, et al. Optimization of the supplemental essential amino acids to a fish meal-free diet based on fermented soybean meal for rainbow trout Oncorhynchus mykiss. Fish Sci 2012; 78: 359-66.[http://dx.doi.org/10.1007/s12562-011-0456-2] , 33Barnes ME, Brown ML, Rosentrater KA, Sewell JR. An initial investigation replacing fish meal with a commercial fermented soybean meal product in the diets of juvenile rainbow trout. Open J Anim Sci 2012; 2: 234-43.[http://dx.doi.org/10.4236/ojas.2012.24033] , 58Barnes ME, Brown ML, Rosentrater KA, Sewell JR. Preliminary evaluation of rainbow trout diets containing PepSoyGen, a fermented soybean meal product, and additional amino acids. Open Fish Sci J 2013; 6: 19-27.[http://dx.doi.org/10.2174/1874401X01306010019] ].

HSI values are an indicator of the nutritional state of a fish because they indirectly measure glycogen and carbohydrate levels [59Barton BA, Morgan JD, Vijayan MM. Physiological and condition-related indicators of environmental stress in fish.Biological indicators of aquatic ecosystem stress 2002; 111-48.-61Kim JD, Kaushik SJ. Contributions of digestible energy from carbohydrates and estimation of protein/energy requirements for growth of rainbow trout (Oncorhynchus mykiss). Aquaculture 1992; 106: 61-169.[http://dx.doi.org/10.1016/0044-8486(92)90200-5] ]. The similar HSI values in all of the treatments indicate energy partitioning is likely similar among the fish. At approximately 1.5, the HSI values observed in this study were similar to those previously reported in several studies [19Parker TM, Barnes ME. Rearing velocity impacts on landlocked fall Chinook salmon (Oncorhynchus tshawytscha) growth, condition, and survival. Open J Anim Sci 2014; 4: 244-52.[http://dx.doi.org/10.4236/ojas.2014.45031] , 20Parker TM, Barnes ME. Effects of different water velocities on hathcery rearing performance and recovery from transportation of rainbow trout fed two different rations. Trans Am Fish Soc 2015; 144: 882-90.[http://dx.doi.org/10.1080/00028487.2015.1047533] , 29Barnes ME, Brown ML, Bruce T, Sindelar S, Neiger R. Rainbow trout rearing performance, intestinal morphology, and immune response after long-term feeding of high levels of fermented soybean meal. N Am J Aquaculture 2014; 76: 333-45.[http://dx.doi.org/10.1080/15222055.2014.920748] , 34Barnes ME, Brown ML, Bruce TJ, Neiger R, Sindelar S. Effects of fermented soybean meal diet on rainbow trout mortality and immune function during a disease outbreak. J Aquac Feed Sci Nutr 2015; 7: 6-15.[http://dx.doi.org/10.3923/joafsnu.2015.6.15] , 58Barnes ME, Brown ML, Rosentrater KA, Sewell JR. Preliminary evaluation of rainbow trout diets containing PepSoyGen, a fermented soybean meal product, and additional amino acids. Open Fish Sci J 2013; 6: 19-27.[http://dx.doi.org/10.2174/1874401X01306010019] , 62Kientz JL, Barnes ME. Structural complexity improves the rearing performance of rainbow trout in circular tanks. N Am J Aquaculture 2016; 78: 203-7.[http://dx.doi.org/10.1080/15222055.2016.1159629] ], but slightly higher than those reported in four other experiments [15Yamamoto T, Iwashita Y, Matsunari H, et al. Influence of fermentation conditions for soybean meal in a non-fish meal diet on growth performance and physiological condition of rainbow trout Oncorhynchus mykiss. Aquaculture 2010; 309: 173-80.[http://dx.doi.org/10.1016/j.aquaculture.2010.09.021] , 16Yamamoto T, Matsunari H, Sugita T, et al. Optimization of the supplemental essential amino acids to a fish meal-free diet based on fermented soybean meal for rainbow trout Oncorhynchus mykiss. Fish Sci 2012; 78: 359-66.[http://dx.doi.org/10.1007/s12562-011-0456-2] , 34Barnes ME, Brown ML, Bruce TJ, Neiger R, Sindelar S. Effects of fermented soybean meal diet on rainbow trout mortality and immune function during a disease outbreak. J Aquac Feed Sci Nutr 2015; 7: 6-15.[http://dx.doi.org/10.3923/joafsnu.2015.6.15] , 36Bruce TJ, Sindelar SC, Voorhees JM, Brown ML, Barnes ME. Performance and immunological responses of rainbow trout (Oncorhynchus mykiss) fed bioprocessed plant-based proteins. Aquacult Nutr 2017; 23: 1160-8.[http://dx.doi.org/10.1111/anu.12485] ]. These differences could be due to differences in the ages and sizes of the fish examined [59Barton BA, Morgan JD, Vijayan MM. Physiological and condition-related indicators of environmental stress in fish.Biological indicators of aquatic ecosystem stress 2002; 111-48.] and the rainbow trout used in this study were much larger and older than the fish typically used in nutrition experiments.

VSI reflects the use and storage of lipids, and VSI and lipid levels are positively related [63Company R, Calduch-Giner JA, Kaushik S, Perez-Sanchez J. Growth performance and adiposity in gilthead sea bream (Sparus aurata): Risks and benefits of high energy diets. Aquaculture 1999; 171: 279-92.[http://dx.doi.org/10.1016/S0044-8486(98)00495-5] -65Yildiz M, Sener E, Timur M. Effect of seasonal change and different commercial feeds on proximate composition of sea bream (Sparus aurata). Turk J Fish Aquat Sci 2006; 6: 99-104.]. It is likely that the equivalent dietary lipid levels are reflected in the similar VSI values observed in this study. The VSI values of approximately 13.3 in this study are similar to one other study examining adult rainbow trout [29Barnes ME, Brown ML, Bruce T, Sindelar S, Neiger R. Rainbow trout rearing performance, intestinal morphology, and immune response after long-term feeding of high levels of fermented soybean meal. N Am J Aquaculture 2014; 76: 333-45.[http://dx.doi.org/10.1080/15222055.2014.920748] ], but are higher compared to other studies using smaller and younger rainbow trout [19Parker TM, Barnes ME. Rearing velocity impacts on landlocked fall Chinook salmon (Oncorhynchus tshawytscha) growth, condition, and survival. Open J Anim Sci 2014; 4: 244-52.[http://dx.doi.org/10.4236/ojas.2014.45031] , 20Parker TM, Barnes ME. Effects of different water velocities on hathcery rearing performance and recovery from transportation of rainbow trout fed two different rations. Trans Am Fish Soc 2015; 144: 882-90.[http://dx.doi.org/10.1080/00028487.2015.1047533] , 34Barnes ME, Brown ML, Bruce TJ, Neiger R, Sindelar S. Effects of fermented soybean meal diet on rainbow trout mortality and immune function during a disease outbreak. J Aquac Feed Sci Nutr 2015; 7: 6-15.[http://dx.doi.org/10.3923/joafsnu.2015.6.15] -36Bruce TJ, Sindelar SC, Voorhees JM, Brown ML, Barnes ME. Performance and immunological responses of rainbow trout (Oncorhynchus mykiss) fed bioprocessed plant-based proteins. Aquacult Nutr 2017; 23: 1160-8.[http://dx.doi.org/10.1111/anu.12485] , 58Barnes ME, Brown ML, Rosentrater KA, Sewell JR. Preliminary evaluation of rainbow trout diets containing PepSoyGen, a fermented soybean meal product, and additional amino acids. Open Fish Sci J 2013; 6: 19-27.[http://dx.doi.org/10.2174/1874401X01306010019] , 62Kientz JL, Barnes ME. Structural complexity improves the rearing performance of rainbow trout in circular tanks. N Am J Aquaculture 2016; 78: 203-7.[http://dx.doi.org/10.1080/15222055.2016.1159629] ].

SSI is an indication of hematopoietic capacity [59Barton BA, Morgan JD, Vijayan MM. Physiological and condition-related indicators of environmental stress in fish.Biological indicators of aquatic ecosystem stress 2002; 111-48.], as well as antibody production [66Smith LS. Introduction to fish physiology 1991.]. The lack of difference in SSI values likely indicates that neither diet contributed to any changes in fish health during the study. The SSI values observed in this study were within the range reported by several others [20Parker TM, Barnes ME. Effects of different water velocities on hathcery rearing performance and recovery from transportation of rainbow trout fed two different rations. Trans Am Fish Soc 2015; 144: 882-90.[http://dx.doi.org/10.1080/00028487.2015.1047533] , 35Barnes ME, Brown ML, Neiger R. Comparative performance of two rainbow trout strains fed fermented soybean meal. Aquacult Int 2015; 23: 1227-38.[http://dx.doi.org/10.1007/s10499-015-9879-6] , 36Bruce TJ, Sindelar SC, Voorhees JM, Brown ML, Barnes ME. Performance and immunological responses of rainbow trout (Oncorhynchus mykiss) fed bioprocessed plant-based proteins. Aquacult Nutr 2017; 23: 1160-8.[http://dx.doi.org/10.1111/anu.12485] , 57Nutrient requirements of fish and shirmp 2011.].

In addition to diet, increasing water velocities and forcing fish to exercise can also dramatically affect fish rearing performance [17Good C, May T, Crouse C, Summerfelt S, Welch TJ. Assessing the impact of swimming exercise and the relative susceptibility of rainbow trout Oncorhynchus mykiss (Walbaum) and Atlantic salmon Salmo salar L. following injection challenge with Weissella ceti. J Fish Dis 2016; 39(11): 1387-91.[http://dx.doi.org/10.1111/jfd.12468] [PMID: 27087506] -20Parker TM, Barnes ME. Effects of different water velocities on hathcery rearing performance and recovery from transportation of rainbow trout fed two different rations. Trans Am Fish Soc 2015; 144: 882-90.[http://dx.doi.org/10.1080/00028487.2015.1047533] ]. Other studies noted the positive effects of exercise on fish growth have lasted 29 to 70 days, which is a much shorter duration than this study [67Castro V, Grisdale-Helland B, Helland SJ, et al. Aerobic training stimulates growth and promotes disease resistance in Atlantic salmon (Salmo salar). CBP: A. Physiology (Bethesda) 1967; 160: 278-90.[http://dx.doi.org/10.1016/j.cbpa.2011.06.013] -69Young PS, Cech JJ Jr. Improved growth, swimming performance, and muscular development in exercise-conditioned young-of-the-year striped bass (Morone saxatilis). Can J Fish Aquat Sci 1993; 50: 703-7.[http://dx.doi.org/10.1139/f93-080] ]. Only one experiment lasted four months, but it did not report rearing performance [70Gallaugher PE, Thorarensen H, Kiessling A, Farrell AP. Effects of high intensity exercise training on cardiovascular function, oxygen uptake, internal oxygen transport and osmotic balance in chinook salmon (Oncorhynchus tshawytscha) during critical speed swimming. J Exp Biol 2001; 204(Pt 16): 2861-72.[PMID: 11683441] ]. In the current study, exercise improved fish growth, but only for the first two months. What happened after two months of exercise? It is possible the fish became fatigued. Exercise fatigue has also been reported in humans after prolonged and intense exercise periods [71Crewe H, Tucker R, Noakes TD. The rate of increase in rating of perceived exertion predicts the duration of exercise to fatigue at a fixed power output in different environmental conditions. Eur J Appl Physiol 2008; 103(5): 569-77.[http://dx.doi.org/10.1007/s00421-008-0741-7] [PMID: 18461352] -74Noakes TD, St Clair Gibson A, Lambert EV. From catastrophe to complexity: A novel model of integrative central neural regulation of effort and fatigue during exercise in humans: Summary and conclusions. Br J Sports Med 2005; 39(2): 120-4.[http://dx.doi.org/10.1136/bjsm.2003.010330] [PMID: 15665213] ]. Just as was observed in this study with rainbow trout, Voorhees et al. [44Voorhees JM, Barnes ME, Chipps SR, Brown ML. Rearing performance of juvenile brown trout (Salmo trutta) subjected to exercise and dietary bioprocessed soybean meal. Open J Anim Sci 2018; 8: 303-28.[http://dx.doi.org/10.4236/ojas.2018.83023] ] performed a similar experiment using brown trout and found that exercise improved rearing performance, but for only the first two months.

The higher (poorer) FCR in the exercised fish may have been because the fish were underfed. Parker and Barnes [20Parker TM, Barnes ME. Effects of different water velocities on hathcery rearing performance and recovery from transportation of rainbow trout fed two different rations. Trans Am Fish Soc 2015; 144: 882-90.[http://dx.doi.org/10.1080/00028487.2015.1047533] ] reported that exercised rainbow trout fed to satiation had similar FCRs to unexercised trout, but if exercised fish were fed a restricted diet, FCR increased. Although food availability was increased daily in accordance with apparent satiation in this study, it may have been insufficient to compensate for the extra energy demands of exercise at higher velocities.

The relative fin lengths observed in this study were similar between the dietary treatments, indirectly indicating that dietary bioprocessed soybean meal is suitable as a fish meal replacement. It should be noted that relative fish lengths, although influenced by nutrition [75Kindschi GA, Shaw HT, Bruhn DS. Effect of diet on performance, fin quality, and dorsal skin lesions in steelhead. J Appl Aqauac 1991; 1: 113-20.[http://dx.doi.org/10.1300/J028v01n01_10] , 76Lemm CA, Rottiers DV, Dropkin DS, Dennison BA. Growth, composition, and fin quality of Atalantic salmon fed different diets at seasonal temperatures in a laboratory and hatchery. US Fish Wildlife Service Biol Rep 1988; 88: 1-12.], can also be impacted by numerous other factors [75Kindschi GA, Shaw HT, Bruhn DS. Effect of diet on performance, fin quality, and dorsal skin lesions in steelhead. J Appl Aqauac 1991; 1: 113-20.[http://dx.doi.org/10.1300/J028v01n01_10] -84Devesa S, Barja JL, Toranzo AE. Ulcerative skin and fin lesions in reared Turbot, Scopthalmus maximus (L.). J Fish Dis 1989; 12: 323-33.[http://dx.doi.org/10.1111/j.1365-2761.1989.tb00321.x] ]. In addition, the relative fin lengths in this experiment are similar to those reported previously [78Bosakowski T, Wagner EJ. Assessment of fish erosion by comparison of relative fin length in hatchery and wild trout in Utah. Can J Fish Aquat Sci 1994; 51: 636-41.[http://dx.doi.org/10.1139/f94-064] , 85Arndt RE, Routledge MD, Wagner EJ, Mellenthin RF. The use of AquaMats® to enhance growth and improve fin condition among raceway cultured rainbow trout Oncorhynchus mykiss (Walbaum). Aquacult Res 2002; 33: 359-67.[http://dx.doi.org/10.1046/j.1365-2109.2002.00670.x] ].

CONCLUSION

BSM can replace at least 60% of the dietary fishmeal in adult rainbow trout diets with no adverse effects, even if the trout are exercised. However, regardless of diet, fatigue may be occurring in fish subjected to a long period of exercise in continuously-elevated water velocities.

ETHICS APPROVAL AND CONSENT TO PARTICIPATE

The study is approved by Aquatics Section Research Ethics Committee of the South Dakota Department of Game, Fish and Parks, USA.

HUMAN AND ANIMAL RIGHTS

No humans were used for the study. All the reported experiments on animals were in accordance with the American Fisheries Society “Guidelines for the Use of Fishes in Research”.

CONSENT FOR PUBLICATION

Not applicable.

CONFLICT OF INTEREST

The authors declare no conflict of interest, financial or otherwise.

ACKNOWLEDGEMENTS

We thank Cody Treft, Tabor Martin, and Brian Fletcher for assisting in this experiment. Alex Rosburg provided comments on an earlier draft that improved the manuscript. The South Dakota Cooperative Fish and Wildlife Research Unit is jointly sponsored by the U.S. Geological Survey, South Dakota Department of Game, Fish and Parks, South Dakota State University, the Wildlife Management Institute, and the U.S. Fish and Wildlife Service. Any use of trade names is for descriptive purposes only and does not imply endorsement by the U.S. Government.

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