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Dietary supplementation of multi-strain probiotic in male rainbow trout (Oncorhynchus mykiss) broodstock: Effects on feed efficiency, hemato-biochemical parameters, immune response, and semen quality

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Abstract

The present study aimed to determine the effects of dietary probiotic supplementation on feed efficiency, physiological parameters, and semen quality of male rainbow trout (Oncorhynchus mykiss) broodstock. For this purpose, a total of 48 breeders with an average initial weight of 1366.1 ± 33.8 g were divided into 4 groups and 3 replicates. Fish were fed with diets containing 0 (control), 1 × 109 (P1), 2 × 109 (P2), and 4 × 109 (P3) CFU multi-strain probiotic kg−1 diet for 8 weeks. According to the results, P2 treatment significantly enhanced body weight increase, specific growth rate, and protein efficiency ratio and decreased feed conversion ratio. Moreover, the highest values of red blood cells count, hemoglobin, and hematocrit values were observed in P2 treatment (P < 0.05). The lowest levels of glucose, cholesterol, and triglyceride were found in P1, P2, and P3 treatments, respectively. Also, the highest levels of total protein and albumin were obtained in P2 and P1 treatments (P < 0.05). Based on the results, plasma enzymes contents were significantly decreased in P2 and P3 treatments. In terms of immune parameters, the complement component 3, complement component 4, and immunoglobulin M levels were increased in all probiotic-fed treatments (P < 0.05). For spermatological features, the highest spermatocrit value, sperm concentration, and motility time were observed in the P2 treatment (P < 0.05). Consequently, we conclude that multi-strain probiotics can be used as functional feed additives in male rainbow trout broodstock to enhance semen quality, improve physiological responses, and better feed efficiency.

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The data and materials that support the findings of this study are available from the corresponding author upon reasonable request.

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References

  • Abasali H, Mohamad S (2011) Effect of dietary probiotic level on the reproductive performance of female platy Xiphophorus maculatus. Agric J 6:119–123

    Article  CAS  Google Scholar 

  • Adeshina I, Abubakar MIO, Ajala BE (2020) Dietary supplementation with Lactobacillus acidophilus enhanced the growth, gut morphometry, antioxidant capacity, and the immune response in juveniles of the common carp, Cyprinus carpio. Fish Physiol Biochem 46:1375–1385

    Article  CAS  PubMed  Google Scholar 

  • Ahmadifard N, Aminlooi VR, Tukmechi A, Agh N (2019) Evaluation of the impacts of long-term enriched Artemia with Bacillus subtilis on growth performance, reproduction, intestinal microflora, and resistance to Aeromonas hydrophila of ornamental fish Poecilia latipinna. Probiotics Antimicrob 11:957–965

    Article  CAS  Google Scholar 

  • Akbari Nargesi E, Falahatkar B, Sajjadi MM (2020) Dietary supplementation of probiotics and influence on feed efficiency, growth parameters and reproductive performance in female rainbow trout (Oncorhynchus mykiss) broodstock. Aquac Nutr 26:98–108

    Article  CAS  Google Scholar 

  • Alavi SMH, Cosson J, Kazemi R (2006) Semen characteristics in Acipenser persicus in relation to sequential stripping. J Appl Ichthyol 22:400–405

    Article  Google Scholar 

  • Alavi SMH, Rodina M, Policar T, Kozak P, Psenicka M, Linhart O (2007) Semen of Perca fluviatilis L.: Sperm volume and density, seminal plasma indices and effects of dilution ratio, ions and osmolality on sperm motility. Theriogenology 68:276–283

    Article  CAS  PubMed  Google Scholar 

  • Alavi SMH, Rodina M, Policar T, Linhart O (2009) Relationship between semen characteristics and body size in Barbus barbus L. (Teleostei: Cyprinidae) and effects of ions and osmolality on sperm motility. Comp Biochem Physiol 153A:430–437

    Article  CAS  Google Scholar 

  • Al-Dohail MA, Hashim R, Aliyu-Paiko M (2009) Effects of the probiotic, Lactobacillus acidophilus, on the growth performance, haematology parameters and immunoglobulin concentration in African Catfish (Clarias gariepinus, Burchell 1822) fingerling. Aquac Res 40:1642–1652

    Article  Google Scholar 

  • Amin A, El Asely A, Abd El-Naby AS, Samir F, El-Ashram A, Sudhakaran R, Dawood MA (2019) Growth performance, intestinal histomorphology and growth-related gene expression in response to dietary Ziziphus mauritiana in Nile tilapia (Oreochromis niloticus). Aquaculture 512:734301

    Article  CAS  Google Scholar 

  • Anee IJ, Alam S, Begum RA, Shahjahan RM, Khandaker AM (2021) The role of probiotics on animal health and nutrition. J Basic Appl Zool 82:1–16

    Article  Google Scholar 

  • Assan D, Kuebutornye FKA, Hlordzi V, Chen H, Mraz J, Mustapha UF, Abarike ED (2022) Effects of probiotics on digestive enzymes of fish (finfish and shellfish); status and prospects: a mini review. Comp Biochem Physiol 257B:110653

    Article  Google Scholar 

  • Balcázar JL, De Blas I, Ruiz-Zarzuela I, Cunningham D, Vendrell D, Múzquiz JL (2006) The role of probiotics in aquaculture. Vet Microbiol 114:173–186

    Article  PubMed  Google Scholar 

  • Balcázar JL, De Blas I, Ruiz-Zarzuela I, Vendrell D, Calvo AC, Márquez I, Gironés O, Muzquiz JL (2007) Changes in intestinal microbiota and humoral immune response following probiotic administration in brown trout (Salmo trutta). Br J Nutr 97:522–527

    Article  PubMed  Google Scholar 

  • Baquero F, Martínez JL, Cantón R (2008) Antibiotics and antibiotic resistance in water environments. Curr Opin Biotech 19:260–265

    Article  CAS  PubMed  Google Scholar 

  • Blaxhall P, Daisley K (1973) Routine haematological methods for use with fish blood. J Fish Biol 5:771–781

    Article  Google Scholar 

  • Bobe J, Labbé C (2010) Egg and sperm quality in fish. Gen Comp Endocrinol 165:535–548

    Article  CAS  PubMed  Google Scholar 

  • Brown M (2011) Modes of action of probiotics: recent developments. J Anim Vet Adv 10:1895–1900

    Article  CAS  Google Scholar 

  • Cabrita E, Martínez-Páramo S, Gavaia PJ, Riesco MF, Valcarce DG, Sarasquete C, Herráez MP, Robles V (2014) Factors enhancing fish sperm quality and emerging tools for sperm analysis. Aquaculture 432:389–401

    Article  CAS  Google Scholar 

  • Cámara-Ruiz M, Balebona MC, Moriñigo MÁ, Esteban MÁ (2020) Probiotic Shewanella putrefaciens (SpPdp11) as a fish health modulator: a review. Microorganisms 8:1990

    Article  PubMed  PubMed Central  Google Scholar 

  • Canyurt MA, Akhan S (2008a) Effect of ascorbic acid supplementation on sperm quality of rainbow trout (Oncorhynchus mykiss). Turkish J Fish Aquat Sci 8:171–175

    Google Scholar 

  • Canyurt MA, Akhan S (2008b) Effect of dietary vitamin E on the sperm quality of rainbow trout (Oncorhynchus mykiss). Aquac Res 39:1014–1018

    Article  CAS  Google Scholar 

  • Carnevali O, Avella MA, Gioacchini G (2013) Effects of probiotic administration on zebrafish development and reproduction. Gen Comp Endocrinol 188:297–302

    Article  CAS  PubMed  Google Scholar 

  • Carnevali O, Maradonna F, Gioacchini G (2017) Integrated control of fish metabolism, wellbeing and reproduction: the role of probiotic. Aquaculture 472:144–155

    Article  CAS  Google Scholar 

  • Cejko BI, Kucharczyk D (2015) Application of dopaminergic antagonist: metoclopramide, in reproduction of crucian carp Carassius carassius (L.) under controlled conditions. Anim Reprod Sci 160:74–81

    Article  CAS  PubMed  Google Scholar 

  • Chen X, Zhang Z, Fernandes JM, Gao Y, Yin P, Liu Y, Tian L, Xie S, Niu J (2020) Beneficial effects on growth, haematic indicators, immune status, antioxidant function and gut health in Juvenile Nile tilapia (Oreochromis niloticus) by dietary administration of a multi-strain probiotic. Aquac Nutr 26:1369–1382

    Article  CAS  Google Scholar 

  • Cheng Y, Franěk R, Rodina M, Xin M, Cosson J, Zhang S, Linhart O (2021) Optimization of Sperm Management and Fertilization in Zebrafish (Danio rerio (Hamilton)). Animals 11:1558

    Article  PubMed  PubMed Central  Google Scholar 

  • Costa LB, Tse MLP, Miyada VS (2007) Herbal extracts as alternatives to antimicrobial growth promoters for weanling pigs. Rev Bras De Zootec 36:589–595

    Article  Google Scholar 

  • Dacie J, Lewis S (1995) Practical haematology, 8th edn. Churchill Livingstone, Edinburgh

    Google Scholar 

  • Dash P, Tandel RS, Bhat RAH, Mallik S, Pandey NN, Singh AK, Sarma D (2018) The addition of probiotic bacteria to microbial floc: Water quality, growth, non-specific immune response and disease resistance of Cyprinus carpio in mid-Himalayan altitude. Aquaculture 495:961–969

    Article  Google Scholar 

  • Dawood MA, Koshio S, Ishikawa M, Yokoyama S (2016) Effects of dietary inactivated Pediococcus pentosaceus on growth performance, feed utilization and blood characteristics of red sea bream, Pagrus major juvenile. Aquac Nutr 22:923–932

    Article  CAS  Google Scholar 

  • Dawood MA, Koshio S, Ishikawa M, El-Sabagh M, Yokoyama S, Wang WL, Yukun Z, Olivier A (2017) Physiological response, blood chemistry profile and mucus secretion of red sea bream (Pagrus major) fed diets supplemented with Lactobacillus rhamnosus under low salinity stress. Fish Physiol Biochem 43:179–192

    Article  CAS  PubMed  Google Scholar 

  • Dawood MA, Koshio S, Abdel-Daim MM, Van Doan H (2019) Probiotic application for sustainable aquaculture. Rev Aquac 11:907–924

    Article  Google Scholar 

  • De BC, Meena DK, Behera BK, Das P, Mohapatra PD, Sharma AP (2014) Probiotics in fish and shellfish culture: immunomodulatory and ecophysiological responses. Fish Physiol Biochem 40:921–971

    CAS  Google Scholar 

  • Dias DC, Leonardo AFG, Tachibana L, Correa CF, Bordon ICAC, Romagosa E, Ranzani-Paiva MJT (2012) Effect of incorporating probiotics into the diet of matrinxã (Brycon amazonicus) breeders. J Appl Ichthyol 28:40–45

    Article  CAS  Google Scholar 

  • Dias DC, Furlaneto FDPB, Sussel FR, Tachibana L, Gonçalves GS, Ishikawa CM, Natori MM, Ranzani-Paiva MJT (2020) Economic feasibility of probiotic use in the diet of Nile tilapia, Oreochromis niloticus, during the reproductive period. Acta Sci Anim Sci 42:47960

    Article  Google Scholar 

  • Doumas BT, Watson WA, Biggs HG (1971) Albumin standards and the measurement of serum albumin with bromcresol green. Clin Chim Acta 31:87–96

    Article  CAS  PubMed  Google Scholar 

  • Du RY, Zhang HQ, Chen JX, Zhu J, He JY, Luo L, Lin SM, Chen YJ (2021) Effects of dietary Bacillus subtilis DSM 32315 supplementation on the growth, immunity and intestinal morphology, microbiota and inflammatory response of juvenile largemouth bass Micropterus salmoides. Aquac Nutr 27:2119–2131

    Article  CAS  Google Scholar 

  • El-Haroun ER, Goda AS, Kabir Chowdhury MA (2006) Effect of dietary probiotic Biogen® supplementation as a growth promoter on growth performance and feed utilization of Nile tilapia Oreochromis niloticus (L.). Aquac Res 37:1473–1480

    Article  CAS  Google Scholar 

  • El-Kady AA, Magouz FI, Mahmoud SA, Abdel-Rahim MM (2022) The effects of some commercial probiotics as water additive on water quality, fish performance, blood biochemical parameters, expression of growth and immune-related genes, and histology of Nile tilapia (Oreochromis niloticus). Aquaculture 546:737249

    Article  CAS  Google Scholar 

  • El-Rhman AM, Khattab YA, Shalaby AM (2009) Micrococcus luteus and Pseudomonas species as probiotics for promoting the growth performance and health of Nile tilapia, Oreochromis niloticus. Fish Shellfish Immunol 27:175–180

    Article  Google Scholar 

  • El-Saadony MT, Alagawany M, Patra AK, Kar I, Tiwari R, Dawood MA, Dhama K, Abdel-Latif HM (2021) The functionality of probiotics in aquaculture: an overview. Fish Shellfish Immunol 117:36–52

    Article  PubMed  Google Scholar 

  • Fan Y, Wang X, Wang Y, Liu H, Yu X, Li L, Ye H, Wang S, Gai C, Xu L, Diao J (2021) Potential effects of dietary probiotics with Chinese herb polysaccharides on the growth performance, immunity, disease resistance, and intestinal microbiota of rainbow trout (Oncorhynchus mykiss). J World Aquac Soc 52:1194–1208

    Article  CAS  Google Scholar 

  • Feng T, Wang J (2020) Oxidative stress tolerance and antioxidant capacity of lactic acid bacteria as probiotic: A systematic review. Gut Microbes 12:1801944

    Article  PubMed  PubMed Central  Google Scholar 

  • Fuller R (1989) A review: probiotics in man and animals. J Appl Bacteriol 66:365–378

    Article  CAS  PubMed  Google Scholar 

  • Geraylou Z, Souffreau C, Rurangwa E, De Meester L, Courtin CM, Delcour JA, Buyse J, Ollevier F (2013) Effects of dietary arabinoxylan-oligosaccharides (AXOS) and endogenous probiotics on the growth performance, non-specific immunity and gut microbiota of juvenile Siberian sturgeon (Acipenser baerii). Fish Shellfish Immunol 35:766–775

    Article  CAS  PubMed  Google Scholar 

  • Ghaedi G, Falahatkar B, Yavari V, Sheibani MT, Broujeni GN (2015) The onset of stress response in rainbow trout Oncorhynchus mykiss embryos subjected to density and handling. Fish Physiol Biochem 41:485–493

    Article  CAS  PubMed  Google Scholar 

  • Ghodrati M, Hosseini Shekarabi SP, Rajabi Islami H, Shenavar Masouleh A, Shamsaie Mehrgan M (2021) Singular or combined dietary administration of multi-strain probiotics and multi-enzyme influences growth, body composition, digestive enzyme activity, and intestinal morphology in Siberian sturgeon (Acipenser baerii). Aquac Nutr 27:966–976

    Article  CAS  Google Scholar 

  • Ghosh S, Sinha A, Sahu C (2007) Effect of probiotic on reproductive performance in female livebearing ornamental fish. Aquac Res 38:518–526

    Article  Google Scholar 

  • Gioacchini G, Maradonna F, Lombardo F, Bizzaro D, Olivotto I, Carnevali O (2010) Increase of fecundity by probiotic administration in zebrafish (Danio rerio). Reproduction 140:953–959

    Article  CAS  PubMed  Google Scholar 

  • Giorgini E, Conti C, Ferraris P, Sabbatini S, Tosi G, Rubini C, Vaccari L, Gioacchini G, Carnevali O (2010) Effects of Lactobacillus rhamnosus on zebrafish oocyte maturation: an FTIR imaging and biochemical analysis. Anal Bioanal Chem 398:3063–3072

    Article  CAS  PubMed  Google Scholar 

  • Gómez GD, Balcázar JL (2008) A review on the interactions between gut microbiota and innate immunity of fish. FEMS Microbiol Immunol 52:145–154

    Article  Google Scholar 

  • Gonçalves AT, Gallardo-Escárate C (2017) Microbiome dynamic modulation through functional diets based on pre-and probiotics (mannan-oligosaccharides and Saccharomyces cerevisiae) in juvenile rainbow trout (Oncorhynchus mykiss). J Appl Microbiol 122:1333–1347

    Article  PubMed  Google Scholar 

  • Gupta A, Gupta P, Dhawan A (2014) Dietary supplementation of probiotics affects growth, immune response and disease resistance of Cyprinus carpio fry. Fish Shellfish Immunol 41:113–119

    Article  CAS  PubMed  Google Scholar 

  • Han B, Long WQ, He JY, Liu YJ, Si YQ, Tian LX (2015) Effects of dietary Bacillus licheniformis on growth performance, immunological parameters, intestinal morphology and resistance of juvenile Nile tilapia (Oreochromis niloticus) to challenge infections. Fish Shellfish Immunol 46:225–231

    Article  CAS  PubMed  Google Scholar 

  • Hayatgheib N, Moreau E, Calvez S, Lepelletier D, Pouliquen H (2020) A review of functional feeds and the control of Aeromonas infections in freshwater fish. Aquac Int 28:1083–1123

    Article  Google Scholar 

  • Heo MS, Subramanian D, Kim DH (2017) Dietary effect of probiotic bacteria, Bacillus amyloliquefaciens-JFP2 on growth and innate immune response in rock bream Oplegnathus fasciatus, challenged with Streptococcus iniae. Isr J Aquac 69:20893

    Google Scholar 

  • Hernandez de-Dios MA, Tovar-Ramírez D, Maldonado García D, Galaviz-Espinoza MA, Spanopoulos Zarco M, Maldonado-García MC (2022) Functional additives as a boost to reproductive performance in marine fish: a review. Fishes 7:7050262

    Article  Google Scholar 

  • Hoseinifar SH, Sun YZ, Wang A, Zhou Z (2018) Probiotics as means of diseases control in aquaculture, a review of current knowledge and future perspectives. Front Microbiol 9:2429

    Article  PubMed  PubMed Central  Google Scholar 

  • Hoseinifar SH, Yousefi S, Van Doan H, Ashouri G, Gioacchini G, Maradonna F, Carnevali O (2020) Oxidative stress and antioxidant defense in fish: The implications of probiotic, prebiotic, and synbiotics. Rev Fish Sci Aquac 29:198–217

    Article  Google Scholar 

  • Izquierdo MS, Fernandez-Palacios H, Tacon AGJ (2001) Effect of broodstock nutrition on reproductive performance of fish. Aquaculture 197:25–42

    Article  Google Scholar 

  • Izquierdo MS, Turkmen S, Montero D, Zamorano MJ, Afonso JM, Karalazos V, Fernández-Palacios H (2015) Nutritional programming through broodstock diets to improve utilization of very low fishmeal and fish oil diets in gilthead sea bream. Aquaculture 449:18–26

    Article  CAS  Google Scholar 

  • Kong Y, Li M, Li R, Shan X, Wang G (2020) Evaluation of cholesterol lowering property and antibacterial activity of two potential lactic acid bacteria isolated from the intestine of snakehead fish (Channa argus). Aquac Rep 17:100342

    Article  Google Scholar 

  • Köprücü K, Yonar ME, Özcan S (2015) Effect of dietary n-3 polyunsaturated fatty acids on antioxidant defense and sperm quality in rainbow trout (Oncorhynchus mykiss) under regular stripping conditions. Anim Reprod Sci 163:135–143

    Article  PubMed  Google Scholar 

  • Kowalski RK, Cejko BI (2019) Sperm quality in fish: determinants and affecting factors. Theriogenology 135:94–108

    Article  PubMed  Google Scholar 

  • Lara-Flores M (2011) The use of probiotic in aquaculture: an overview. Int Res J Microbiol 2:471–478

    Google Scholar 

  • Lazado CC, Caipang CMA, Brinchmann MF, Kiron V (2011) In vitro adherence of two candidate probiotics from Atlantic cod and their interference with the adhesion of two pathogenic bacteria. Vet Microbiol 148:252–259

    Article  PubMed  Google Scholar 

  • Lazado CC, Caipang CMA, Estante EG (2015) Prospects of host-associated microorganisms in fish and penaeids as probiotics with immunomodulatory functions. Fish Shellfish Immunol 45:2–12

    Article  CAS  PubMed  Google Scholar 

  • Lefèvre PL, Palin MF, Murphy BD (2011) Polyamines on the reproductive landscape. Endocr Rev 32:694–712

    Article  PubMed  Google Scholar 

  • Li X, Ringø E, Hoseinifar SH, Lauzon HL, Birkbeck H, Yang D (2019) The adherence and colonization of microorganisms in fish gastrointestinal tract. Rev Aquac 11:603–618

    Article  CAS  Google Scholar 

  • Lieke T, Meinelt T, Hoseinifar SH, Pan B, Straus DL, Steinberg CE (2020) Sustainable aquaculture requires environmental-friendly treatment strategies for fish diseases. Rev Aquac 12:943–965

    Article  Google Scholar 

  • Lombardo F, Gioacchini G, Carnevali O (2011) Probiotic-based nutritional effects on killifish reproduction. Fish Aquacult J 33:1–11

    Google Scholar 

  • Luquet P, Watanabe T (1986) Interaction “nutrition-reproduction” in fish. Fish Physiol Biochem 2:121–129

    Article  CAS  PubMed  Google Scholar 

  • Maas RM, Verdegem MC, Debnath S, Marchal L, Schrama JW (2021) Effect of enzymes (phytase and xylanase), probiotics (B. amyloliquefaciens) and their combination on growth performance and nutrient utilisation in Nile tilapia. Aquaculture 533:736226

    Article  CAS  Google Scholar 

  • Mamun MAA, Nasren S, Rathore SS, Sidiq MJ, Dharmakar P, Anjusha KV (2019) Assessment of probiotic in aquaculture: functional changes and impact on fish gut. Microbiol Res Int 29:1–10

    Google Scholar 

  • Medellin-Peña MJ, Wang H, Johnson R, Anand S, Griffiths MW (2007) Probiotics affect virulence-related gene expression in Escherichia coli O157: H7. Appl Environ Microbiol 73:4259–4267

    Article  PubMed  PubMed Central  Google Scholar 

  • Mehdinejad N, Imanpour MR, Jafari V (2019) Combined or individual effects of dietary probiotic, pediococcus acidilactici and nucleotide on reproductive performance in goldfish (Carassius auratus). Probiotics Antimicrob 11:233–238

    Article  CAS  Google Scholar 

  • Mehrim AI, Khalil FF, Hassan ME (2015) Hydroyeast Aquaculture® as a reproductive enhancer agent for the adult Nile tilapia (Oreochromis niloticus Linnaeus, 1758). Fish Physiol Biochem 41:371–381

    Article  CAS  PubMed  Google Scholar 

  • Melo-Bolívar JF, Ruiz Pardo RY, Hume ME, Villamil Díaz LM (2021) Multistrain probiotics use in main commercially cultured freshwater fish: a systematic review of evidence. Rev Aquac 13:1758–1780

    Article  Google Scholar 

  • Merrifield DL, Bradley G, Baker RTM, Davies SJ (2010) Probiotic applications for rainbow trout (Oncorhynchus mykiss Walbaum) II. Effects on growth performance, feed utilization, intestinal microbiota and related health criteria postantibiotic treatment. Aquac Nutr 16:496–503

    Article  CAS  Google Scholar 

  • Migaud H, Bell G, Cabrita E, McAndrew B, Davie A, Bobe J, Herraez MP, Carrillo M (2013) Gamete quality and broodstock management in temperate fish. Rev Aquac 5:194–223

    Article  Google Scholar 

  • Miller MB, Bassler BL (2001) Quorum sensing in bacteria. Annu Rev Microbiol 55:165–199

    Article  CAS  PubMed  Google Scholar 

  • Mishra V, Shah C, Mokashe N, Chavan R, Yadav H, Prajapati J (2015) Probiotics as potential antioxidants: a systematic review. J Agric Food Chem 63:3615–3626

    Article  CAS  PubMed  Google Scholar 

  • Mohapatra S, Chakraborty T, Kumar V, DeBoeck G, Mohanta KN (2013) Aquaculture and stress management: a review of probiotic intervention. J Anim Physiol Anim Nutr 97:405–430

    Article  CAS  Google Scholar 

  • Nandi A, Banerjee G, Dan SK, Ghosh K, Ray AK (2017) Probiotic efficiency of Bacillus sp. in Labeo rohita challenged by Aeromonas hydrophila: assessment of stress profile, haemato-biochemical parameters and immune responses. Aquac Res 48:4334–4345

    Article  CAS  Google Scholar 

  • National Research Council (2011) Guide for the care and use of laboratory animals, 8th edn. The National Academies Press, Washington

    Google Scholar 

  • Nayak SK (2010) Probiotics and immunity: a fish perspective. Fish Shellfish Immunol 29:2–14

    Article  CAS  PubMed  Google Scholar 

  • Nayak SK (2021) Multifaceted applications of probiotic Bacillus species in aquaculture with special reference to Bacillus subtilis. Rev Aquac 13:862–906

    Article  Google Scholar 

  • Pan X, Wu T, Song Z, Tang H, Zhao Z (2008) Immune responses and enhanced disease resistance in Chinese drum, Miichthys miiuy (Basilewsky), after oral administration of live or dead cells of Clostridium butyrium CB2. J Fish Dis 31:679–686

    Article  CAS  PubMed  Google Scholar 

  • Panigrahi A, Azad IS (2007) Microbial intervention for better fish health in aquaculture: the Indian scenario. Fish Physiol Biochem 33:429–440

    Article  CAS  Google Scholar 

  • Pourhosein Sarameh S, Bahri AH, Falahatkar B, Yarmohammadi M, Salarzadeh A (2019) The effect of fish and rapeseed oils on growth performance, egg fatty acid composition and offspring quality of sterlet sturgeon (Acipenser ruthenus). Aquac Nutr 25:543–554

    Article  CAS  Google Scholar 

  • Qin C, Xu L, Yang Y, He S, Dai Y, Zhao H, Zhou Z (2014) Comparison of fecundity and offspring immunity in zebrafish fed Lactobacillus rhamnosus CICC 6141 and Lactobacillus casei BL23. Reproduction 147:53–64

    Article  CAS  PubMed  Google Scholar 

  • Ramesh D, Souissi S (2018) Effects of potential probiotic Bacillus subtilis KADR1 and its subcellular components on immune responses and disease resistance in Labeo rohita. Aquac Res 49:367–377

    Article  CAS  Google Scholar 

  • Refaey MM, Li D, Tian X, Zhang Z, Zhang X, Li L, Tang R (2018) High stocking density alters growth performance, blood biochemistry, intestinal histology, and muscle quality of channel catfish Ictalurus punctatus. Aquaculture 492:73–81

    Article  CAS  Google Scholar 

  • Ridha MT, Azad IS (2012) Preliminary evaluation of growth performance and immune response of Nile tilapia Oreochromis niloticus supplemented with two putative probiotic bacteria. Aquac Res 43:843–852

    Article  CAS  Google Scholar 

  • Ringø E, Van Doan H, Lee SH, Soltani M, Hoseinifar SH, Harikrishnan R, Song SK (2020) Probiotics, lactic acid bacteria and bacilli: interesting supplementation for aquaculture. J Appl Microbiol 129:116–136

    Article  PubMed  Google Scholar 

  • Rodrigues LM, Damasceno DZ, Marques Gomes RL, Sosa BDS, Moro EB, Sanches EA, Bittencourt F, Signor A (2021) Reproductive physiology of Rhamdia quelen is improved by dietary inclusion of probiotics. Aquac Res 52:1677–1687

    Article  Google Scholar 

  • Salinas I, Abelli L, Bertoni F, Picchietti S, Roque A, Furones D, Cuesta A, Meseguer J, Esteban MÁ (2008) Monospecies and multispecies probiotic formulations produce different systemic and local immunostimulatory effects in the gilthead seabream (Sparus aurata L.). Fish Shellfish Immunol 25:114–123

    Article  CAS  PubMed  Google Scholar 

  • Schiavone R, Zilli L, Vilella S, Fauvel C (2006) Human chorionic gonadotropin induces spermatogenesis and spermiation in 1-year-old European sea bass (Dicentrarchus labrax): Assessment of sperm quality. Aquaculture 255:522–531

    Article  CAS  Google Scholar 

  • Servin AL (2004) Antagonistic activities of lactobacilli and bifidobacteria against microbial pathogens. FEMS Microbiol Rev 28:405–440

    Article  CAS  PubMed  Google Scholar 

  • Sharifuzzaman SM, Austin B (2017) Probiotics for disease control in aquaculture. In: Austin B, Newaj-Fyzul A (eds) A diagnosis and control of diseases of fish and shellfish. Wiley, New York, pp 189–222

    Chapter  Google Scholar 

  • Sheikhzadeh N, Reza A, Allah JJR, Hossein TN (2010) Effect of Ergosan on semen quality of male rainbow trout (Oncorhynchus mykiss) broodstock. Anim Reprod Sci 122:183–188

    Article  CAS  PubMed  Google Scholar 

  • Sun YZ, Yang HL, Ma RL, Lin WY (2010) Probiotic applications of two dominant gut Bacillus strains with antagonistic activity improved the growth performance and immune responses of grouper Epinephelus coioides. Fish Shellfish Immunol 29:803–809

    Article  PubMed  Google Scholar 

  • Sutthi N, Thaimuangphol W, Rodmongkoldee M, Leelapatra W, Panase P (2018) Growth performances, survival rate, and biochemical parameters of Nile tilapia (Oreochromis niloticus) reared in water treated with probiotic. Comp Clin Pathol 27:597–603

    Article  CAS  Google Scholar 

  • Thurlow CM, Williams MA, Carrias A, Ran C, Newman M, Tweedie J, Allison E, Jescovitch LN, Wilson AE, Terhune JS, Liles MR (2019) Bacillus velezensis AP193 exerts probiotic effects in channel catfish (Ictalurus punctatus) and reduces aquaculture pond eutrophication. Aquaculture 503:347–356

    Article  Google Scholar 

  • Tinh NTN, Dierckens K, Sorgeloos P, Bossier P (2008) A review of the functionality of probiotics in the larviculture food chain. Mar Biotech 10:1–12

    Article  CAS  Google Scholar 

  • Tofalo R, Cocchi S, Suzzi G (2019) Polyamines and gut microbiota. Front Nutr 6:16

    Article  PubMed  PubMed Central  Google Scholar 

  • Tremellen K, Pearce K (2017) Probiotics to improve testicular function-a comment on mechanism of action and therapeutic potential of probiotics beyond reproduction. Andrology 5:1052–1053

    Article  CAS  PubMed  Google Scholar 

  • Trinder P (1969) Determination of glucose in blood using glucose oxidase with an alternative oxygen acceptor. Ann Clin Biochem 6:24–27

    Article  CAS  Google Scholar 

  • Valcarce DG, Pardo MÁ, Riesco MF, Cruz Z, Robles V (2015) Effect of diet supplementation with a commercial probiotic containing Pediococcus acidilactici (Lindner, 1887) on the expression of five quality markers in zebrafish (Danio rerio (Hamilton, 1822)) testis. J Appl Ichthyol 31:18–21

    Article  CAS  Google Scholar 

  • Valcarce DG, Riesco MF, Martínez-Vázquez JM, Robles V (2019a) Diet supplemented with antioxidant and anti-inflammatory probiotics improves sperm quality after only one spermatogenic cycle in zebrafish model. Nutrients 11:843

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Valcarce DG, Riesco MF, Martínez-Vázquez JM, Robles V (2019b) Long exposure to a diet supplemented with antioxidant and anti-inflammatory probiotics improves sperm quality and progeny survival in the zebrafish model. Biomolecules 9:338

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Valdebenito II, Gallegos PC, Effer BR (2015) Gamete quality in fish: evaluation parameters and determining factors. Zygote 23:177–197

    Article  PubMed  Google Scholar 

  • Vázquez GR, Guerrero G (2007) Characterization of blood cells and hematological parameters in Cichlasoma dimerus (Teleostei, Perciformes). Tissue Cell 39:151–160

    Article  Google Scholar 

  • Verschuere L, Rombaut G, Sorgeloos P, Verstraete W (2000) Probiotic bacteria as biological control agents in aquaculture. Microbiol Mol Biol Rev 64:655–671

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vílchez MC, Santangeli S, Maradonna F, Gioacchini G, Verdenelli C, Gallego V, Peñaranda DS, Tveiten H, Pérez L, Carnevali O, Asturiano JF (2015) Effect of the probiotic Lactobacillus rhamnosus on the expression of genes involved in European eel spermatogenesis. Theriogenology 84:1321–1331

    Article  PubMed  Google Scholar 

  • Wang Y, Xu NV, Xi A, Ahmed Z, Zhang B, Bai X (2009) Effects of Lactobacillus plantarum MA2 isolated from Tibet kefir on lipid metabolism and intestinal microflora of rats fed on high-cholesterol diet. Appl Microbiol Biotechnol 84:341–347

    Article  CAS  PubMed  Google Scholar 

  • Wang AR, Ran C, Ringø E, Zhou ZG (2018) Progress in fish gastrointestinal microbiota research. Rev Aquac 10:626–640

    Article  Google Scholar 

  • Wu A (2006) Tietz clinical guide to laboratory tests, 4th edn. Elsevier Publishing, New York

    Google Scholar 

  • Yanbo W, Zirong X (2006) Effect of probiotics for common carp (Cyprinus carpio) based on growth performance and digestive enzyme activities. Anim Feed Sci Technol 127:283–292

    Article  Google Scholar 

  • Yang G, Cao H, Jiang W, Hu B, Jian S, Wen C, Kajbaf K, Kumar V, Tao Z, Peng M (2019) Dietary supplementation of Bacillus cereus as probiotics in Pengze crucian carp (Carassius auratus var. Pengze): Effects on growth performance, fillet quality, serum biochemical parameters and intestinal histology. Aquac Res 50:2207–2217

    Article  CAS  Google Scholar 

  • Yilmaz S, Yilmaz E, Dawood MA, Ringø E, Ahmadifar E, Abdel-Latif HM (2022) Probiotics, prebiotics, and synbiotics used to control vibriosis in fish: A review. Aquaculture 547:737514

    Article  CAS  Google Scholar 

  • Yousuf S, Tyagi A, Singh R (2022) Probiotic supplementation as an emerging alternative to chemical therapeutics in finfish aquaculture: a review. Probiotics Antimicrob: 1–18. https://doi.org/10.1007/s12602-022-09971-z

  • Yuan XY, Liu WB, Liang C, Sun CX, Xue YF, Wan ZD, Jiang GZ (2017) Effects of partial replacement of fish meal by yeast hydrolysate on complement system and stress resistance in juvenile Jian carp (Cyprinus carpio var. Jian). Fish Shellfish Immunol 67:312–321

  • Zhang CN, Li XF, Xu WN, Jiang GZ, Lu KL, Wang LN, Liu WB (2013) Combined effects of dietary fructooligosaccharide and Bacillus licheniformis on innate immunity, antioxidant capability and disease resistance of triangular bream (Megalobrama terminalis). Fish Shellfish Immunol. 35:1380–1386

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Acknowledgements

The researchers would like to thank T. Shamsipour for providing broodstock and ponds for this project. We would also like to express our thanks to M. Mohammadi and other friends who contributed to advance this experiment.

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Erfan Akbari Nargesi: conceptualization, methodology, acquisition of data, software analysis, interpretation of data, writing-original draft preparation, reviewing, and editing; Bahram Falahatkar: conceptualization, supervision, methodology, reviewing, and editing.

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Correspondence to Bahram Falahatkar.

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All experiments were conducted in accordance with the National Institutes of Health guide for the care and use of laboratory animals (National Research Council 2011). The study was approved by the Research Ethics Committee of the University of Guilan.

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Akbari Nargesi, E., Falahatkar, B. Dietary supplementation of multi-strain probiotic in male rainbow trout (Oncorhynchus mykiss) broodstock: Effects on feed efficiency, hemato-biochemical parameters, immune response, and semen quality. Fish Physiol Biochem 49, 371–384 (2023). https://doi.org/10.1007/s10695-023-01181-w

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