Effect of dietary synbiotics on growth, immune response and body composition of Caspian roach ( rutilus)

Item Type article

Authors Chitsaz, H.; Akrami, R.; Arab Arkadeh, M.

Download date 26/09/2021 23:22:49

Link to Item http://hdl.handle.net/1834/37606 Iranian Journal Fisheries Sciences 15(1) 170-182 2016

Effect of dietary synbiotics on growth, immune response and body composition of Caspian roach (Rutilus rutilus)

Chitsaz H.1*; Akrami R.1; Arab Arkadeh M.2

Received: July 2013 Accepted: November 2014

Abstract Effects of dietary synbiotics on growth performance, survival, stress resistance, body composition and immune response in the Caspian roach (Rutilus rutilus) were evaluated. Fish with an initial average weight of 4.14±0.25 g were randomly distributed into tanks (50 fish per tank) and triplicate groups were fed a control diet or diets containing 1 g kg-1 and 2 g kg-1 synbiotics. After an 8-week feeding period, a general enhanced growth performance and feed efficiency were observed in fish fed on the diet containing 2 g kg-1synbiotics (p<0.05). Subsequently, immune responses (Ig levels, lysozyme activity and ACH50) were significantly higher in 2 g kg-1 synbiotics fed fish (p<0.05). Although all levels of dietary synbiotics significantly increased resistance to a salinity stress challenge (p<0.05), the highest survival rate was observed in this group. The intestinal tract of the fish with synbiotic diet supplementation had higher concentrations of lactic acid bacteria (7.13±0.32 log CFU g-1). The protein and lipid contents in the whole body increased in the 2 g kg-1 synbiotics fed group. At the end of experiment the fish fed synbiotics had the highest survival index after 40 hours exposure to salinity stress (13.8 ppt). Results showed that the addition of synbiotics to the diet of Roach (Rutilus rutilus) stimulates the beneficial intestinal microbiota and alters their immune defense system.

Keywords: Synbiotics, Growth, Survival, Body composition, Salinity stress, Immune response, Rutilus rutilus

1-Department of Fisheries, Azadshahr Branch, Islamic Azad University, Azadshahr, Iran. 3-Faculty of Natural Resources and Earth Sciences, Shahr-e kord University. Correspondence author's email: [email protected]

171 Chitsaz et al., Effect of dietary synbiotics on growth, immune response and …

Introduction gastrointestinal tract (Manning and The Caspian roach (Rutilus rutilus) is a Gibson, 2004). Gibson and Roberfroid commercially important in the (1995) have defined the mixture of pre- (Abdoli, 2000) and is also and probiotics as synbiotics that exert a major food source for wild Beluga synergistic effects in promoting sturgeon populations (Keyvanshokooh beneficial bacteria and the health of the and Kalbassi, 2006). Like other Caspian gastrointestinal tract of the host, thus Sea fishes (e.g. sturgeons) the species is their potential applications have spurred considered threatened due to over attention. Although benefits associated fishing, water pollution, and loss of with prebiotics and probiotics are natural habitat and spawning grounds desirable, researchers are concerned (Kiabi et al., 1999). However, the about a conclusive result, depending on Iranian fisheries organization has type and amount of pre- and probiotics developed culture methodologies to rear consumed. Therefore, more studies the Caspian roach up to market size to need to be conducted to provide a better reduce pressure on natural Caspian Sea understanding of their direct effects on populations (Keyvanshokooh et al., health. The use of probiotics and 2009). Global demand for safe food has prebiotics in aquaculture is now widely prompted the search for natural and accepted but limited data is available alternative growth promoters to use in regarding the application of synbiotics fish feeds. A novel approach to these in aquaculture (Li et al., 2009; goals is the application of probiotics Rodriguez-Estrada et al., 2009; Daniels and prebiotics in the fish farming et al., 2010; Zhang et al., 2010; Ai et industry (Irianto and Austin, 2002; al., 2011; Ye et al., 2011; Mehrabi et Wang and Xu, 2006; Wang et al., al., 2012; Nekoubin et al., 2012). The 2008). Probiotics are defined as aim of the present study was to study organisms and substances which the effects of synbiotics (Biomin contribute to intestinal microbial IMBO) on growth performance, balance. In a practical sense, probiotics survival rate, lactic acid bacteria (LAB) are defined as live microorganisms that levels in the intestine, body are used as dietary supplementations in composition and salinity resistance in aquaculture and could enhance the roach (R. rutilus) fry via growth and health of the host supplementation with experimental (Gatesoupe, 1999; Kesarcodi-Watson et roach food. al., 2008). Prebiotics are defined as non-digestible dietary ingredients that Materials and methods beneficially affect the host by Fish culture and feeding trial selectively stimulating the growth of Caspian roach (average weight and/or activating the metabolism of 4.14±0.25 g), obtained from the Sijowal health-promoting bacteria in the Caspian Sea Teleost Fish Propagation Iranian Journal of Fisheries Sciences 15(1) 2016 172 and Cultivation Center (Golestan formulated diets was determined Province, Iran) was randomly stocked according to standard AOAC (AOAC, into 9 tanks (300 L) at a density of 50 1990) methodology. fish per tank (3 tanks per treatment). Water temperature, dissolved oxygen, Growth and feeding performance pH and salinity were monitored daily In order to measure the growth and maintained at 25.2±0.9°C, 5.9±0.6 parameters, weight and length of all mg L_1, 7.53±0.12 and 0.4±0.12 ppt, fish were measured at every 15 day respectively. Continuous aeration was interval. After an 8-week feeding provided to each tank through an air period, Weight Gain (g kg-1), Specific stone connected to a central air Growth Rate (SGR g kg-1 /day), Feed compressor. Conversion Ratio (FCR), Condition Factor (CF g/cm3) and Survival Rate (g Feeding and synbiotic supplement kg-1) were calculated according to the preparation following equations (Bekcan et al., -1 The type of synbiotics applied in this 2006): WG (g kg )=(Wt−W0)× study was Biomin IMBO (Biomin, 100/W0, SGR= (Ln Wt−Ln W0)×100/t , Herzogenburg, Austria) which was FCR=dry feed fed in g/Wet weight gain comprised of probiotic (Entercoccus in g, CF=100× Wt/Lt3, Survival rate = 11 faecium 5×10 CFU/kg) and (Nt/N0) × 100. Here Wt and W0 are Fructooligosaccharide (FOS) as the final and initial body weights (g) prebiotic. A basal diet was formulated respectively, t is duration of for Caspian roach (Table 1); this basal experimental days, N0 is the initial diet served as the control diet and the number of fish and Nt is the final experimental diets were produced by number of fish. supplementation of the basal formulation with varying levels of Chemical analysis of diets and fish synbiotics (1 and 2 g kg-1). The carcasses ingredients were blended thoroughly in The chemical composition of a mixer and pelleted using a meat formulated diets and fish carcasses grinder. The pelleted diets were air- were determined according to standard dried, ground and sieved to produce a AOAC methodology (AOAC, 1990). At suitable crumble (1 mm). Then the feed the end of the experiment, 15 randomly was stored at 4 °C until feeding trials sampled fish from each treatment (5 began. The experimental fish were fish from each tank) were collected for weighted every 15 days in order to carcass analysis. Crude protein content adjust the daily feed rate which was 3–5 was determined by kjeldahl method g kg-1 of the total biomass. The fish using Auto Kjeldahl System, crude lipid were fed twice daily to apparent content by soxhlet extraction method, satiation for 60 days (Akrami et al., ash content in a furnace muffler (550 °C 2010). The chemical composition of for 4 h), moisture content in a dry oven 173 Chitsaz et al., Effect of dietary synbiotics on growth, immune response and …

(105 °C for 24 h) and crude fiber was carried out according to Bergy's content using an automatic analyzer method (Peter and Sneath, 1986(. (Fibertec, Sweden) (AOAC, 1990). Immunological assays Salinity stress challenge Serum total immunoglobulin (Ig) levels At the end of the feeding trial, 10 fish were determined according to the were sampled from each tank and method described by Siwicki and subjected to a salinity stress challenge. Anderson Siwicki and Anderson The fish were exposed to 13.8 g L_1 (1993). Briefly, serum total protein salinity according to Akrami et al. content was measured using a micro (2010). The survival rate of Caspian protein determination method (C-690; roach was calculated at 40 h post Sigma), prior to and after precipitating challenge (Akrami et al., 2010). down the immunoglobulin molecules, using a 12g kg-1 solution of Intestinal microbiota polyethylene glycol (Sigma). The The analysis of intestinal microbiota difference in protein content represents was conducted at the end of the the Ig content. Serum lysozyme activity nutrition trial. Three fish were sampled was determined according to Demers in each treatment and starved for 24 h and Bayne (Demers and Bayne, 1997) prior to microbiological sampling. The and based on lysis of the lysozyme- fish were killed by physical destruction sensitive gram-positive bacterium of the brain and the skin washed in a Micrococcus lysodeikticus (Sigma). solution of 0.1g kg-1 benzalkonium Alternative complement activity was chloride before opening the ventral assayed according to the procedure of surface with sterile scissors. Intestinal Yano (Yano, 1992) by using rabbit red tract of sampled fish were removed, blood cells (RaRBC). The volume of weighed, and suspended in sterile saline serum yielding 50g kg-1 haemolysis was [0.85g kg-1 (w/v) NaCl]. The determined and used to calculate the suspension, serially diluted to 10−6 and complement activity of the sample 0.1 mL of the solution, was spread in (value of ACH50 is in units per triplicate on to nutrient agar (NA). millilitre). DeMan, Rogosa and Sharpe (MRS) was also used to detect Lactic Acid Bacteria Statistical analysis (LAB). All of the plates were incubated Data were analyzed by one-way at room temperature (25°C) and analysis of variance using the statistical examined for 5 days (Rengpipat et al., software SPSS version 18.0. 1998; Mahious and Ollevier, 2005(, Subsequently, significant differences and the number of colonies were between the groups were determined counted. Identification of the samples using Duncan's new multiple range test. Data are presented as treatment Iranian Journal of Fisheries Sciences 15(1) 2016 174 means±standard deviation (SD). The effects of the different dietary Differences were considered significant levels of synbiotics on the immune when p<0.05. responses of roach juveniles are shown in Table 5. All immune responses Results measured (i.e. total Ig, lysozyme The growth performance of roach fed activity and ACH50) were significantly diets supplemented with varying levels higher (p<0.05) in 2.0 g synbiotics kg-1 of dietary synbiotics is presented in diets fed fish compared to the control Table 2. Compared to the control group. Fish fed 2.0 g synbiotics kg-1 treatment, roach fed 2.0 g synbiotics kg-1 diets displayed significantly elevated diet displayed improved (p<0.05) lysozyme activity (51.6±3.8 μg mL-1) growth performance, including weight compared to the control (33.6±3.8 gain (g kg-1), SGR, FCR and CF. μg mL-1). The concentration of total Furthermore, roach fed 1.0 and 2.0 g immunoglobulin (7.2±0.8 mg ml-1) and synbiotics kg-1 diet had significantly ACH50 (54.23±6.92 U mL-1) were higher survival compared to the control significantly higher in fish fed with 2.0 (p<0.05) (Table 2). g synbiotics kg-1 diets compared to the According to the body analysis control group (Table 5). composition data (Table 3) at the end of Results from the salinity challenge the experiment, the percentages of body are presented in Fig. 1. The dietary protein and lipid in fish fed with synbiotics significantly increased the synbiotics was significantly (p<0.05) resistance of roach to the salinity stress higher than that from the control fish challenge (p<0.05). Survival of fish fed whereas the percentage of ash content diets containing 2.0 g synbiotics kg-1 was not (p>0.05). supplementation was significantly Intestinal microbiota analyses are higher than fish fed the basal diet after shown in Table 4. There were the same period (Fig. 1). significant differences in intestinal lactic acid bacteria count in fish fed with 2.0 g synbiotics kg-1 diet (7.13±0.32 CFU g-1) (p<0.05) although the concentration of total heterotrophic bacteria did not differ (p>0.05). 175 Chitsaz et al., Effect of dietary synbiotics on growth, immune response and …

Table 1: Formulation (g kg-1) and proximate composition of diets. Ingredient Diets Control 1 g kg-1 synbiotic 2 g kg-1 synbiotic Fish meal 40 40 40 Wheat flour 25 24 23 Soybean meal 15 15 15 Corn gluten 5 5 5 Soybean oil 6 6 6 Fish oil 6 6 6 Synbiotica 0 1 2 Vitamin/ Mineral premixab 3 3 3 Proximate composition (g kg-1)c Crude protein 35.1 35.3 35.2 Crude lipid 12.1 11.9 12.1 Ash 7.9 8.1 7.8 Moisture 10 9.8 9.7 Crude fiber 5 5.1 4.8 NFEd 19.9 20 20.7 Gross energy (MJ/kg)e 16.51 16.48 16.66 a The type of synbiotics applied in this study was Biomin IMBO (Biomin, Herzogenburg, Austria) which was comprised of probiotic (Entercoccus faecium 5×1011 CFU/kg) and Fructo-oligosaccharide (FOS) as prebiotic. b Vitamin/mineral premix contains (multivitamin and trace minerals per 500 g mixture): vitamin A 1,000 IU, vitamin D3 3,000 IU, vitamin E3 mg, vitamin B1 2 mg, vitamin B2 2 mg, vitamin B6 1 mg, nicotinamid 15 +2 +2 +2 +2 mg, calcium pentotenate 5 mg, vitamin K3 2 mg, Cu 3 mg, Fe 12 mg, Zn 15 mg, Mn 25 mg c Means of the two replicate analyses sample expressed in dry-matter basis d NFE = 100 - (g kg-1 crude protein+g kg-1 crude lipid + g kg-1 ash + g kg-1 fiber + g kg-1 moisture) e Gross energy (GE) (MJ/kg) = (g kg-1 crude protein  23.6+g kg-1 crude lipid  39.5+g kg-1NFE  17)

Table 2: Growth performance of Caspian juvenile fry fed different dietary levels of synbiotics for 8-week. Control 1.0 g synbiotics kg-1 2.0 g synbiotics kg-1 WG (g kg-1) 105.60± 5.9 a 132.73±9.41 b 168.83± 7.75 c SGR (g kg-1/day) 1.72±0.06a 2.14±0.09 b 2.35±0.04 c FCR 4.41±0.18 a 3.45± 0.31 b 2.79±0.17 c CF 0.84±0.04 a 0.96±0.01b 1.1±0.02 c Survival (g kg-1) 74.5±8.66 a 87.3±3.5 b 95.6± 2.9 b

Values in a row with different superscripts denote a significant difference (p<0.05).

Table 3: Whole body composition of Caspian roach juvenile fed diets containing various levels of synbiotics for 8 weeks. Composition Control 1.0 g synbiotics kg-1 2.0 g synbiotics kg-1 (% dry matter) Moisture 78.3 ±0.78 a 77.84 ±0.65 b 71.3 ±0.56 c Protein 14.38 ±0.39 a 15.98 ±0.26 ab 18.16 ±1.13 b Lipid 3.38± 0.39 a 4.18 ±0.26 ab 6.16 ±0.23 b Ash 2.49 ±0.26 a 2.5 ±0.31 a 2.6 ±0.22 a Values in a row with different superscripts denote a significant difference (p<0.05).

Iranian Journal of Fisheries Sciences 15(1) 2016 176

Table 4: Bacteria counts of the intestinal tract of Caspian roach juvenile fed different dietary levels of synbiotics. Bacteria counts Control 1.0 g synbiotics kg-1 2.0 g synbiotics kg- log (CFU g-1) 1 Total bacteria 5.86±1.94 ab 5.88±1.2 ab 6.1±0.79 a Lactic acid 5.42±0.14 b 5.73±0.4 b 7.13±0.32 a Values in a row with different superscripts denote a significant difference (p<0.05).

Table 5: Immune responses of Caspian roach juvenile fed different dietary levels of synbiotics. Control 1.0 g synbiotics kg-1 2.0 g synbiotics kg-1 Lysozym (μg mL-1) 33.6±3.8 a 42.6± 4.35 ab 51.6±3.8 b ACH50 (U mL-1) 48.86 ±2.51 a 49.83±8.13 ab 54.23±6.92 b Total Ig (mg mL-1) 4.9±0.97 a 5.5±0.71 a 7.2±0.8 b Values in a row with different superscripts denote a significant difference (p<0.05).

120 ab Control 110 a a a ab b b b b b 1g/kg Synbiotic 100 a b b b 90 2g/kg Synbiotic 80 a 70 a 60 50 a 40 30 a 20 Cumulative survival rate (%) Cumulative survival rate 10 0 0 8 16 24 32 40 Time (hour)

Figure 1: Percent cumulative survival rate of roach fry after salinity stress test; exposure to 13.8 g L_1 water salinity for 40 h. Values (means±SD) in bars that do not have same letter are significantly different (p<0.05) (by one way ANOVA).

Discussion synbiotics supplement in quail diets There is some information available to improved body weight gain, SGR and date regarding the interaction between reduced FCR (Sahin et al., 2008). In the synbiotics and growth performance in present experiment, the growth (Kumprecht and Zobac 1998; performance, immune response, lactic Shim 2005; Buteikis et al., 2008; Sahin acid bacteria, salinity resistance and et al., 2008). Shim and his co-workers body composition were significantly (2005) reported that a dietary synbiotics (p<0.05) improved by supplementing fed suckling pig, showed positively the basal diet with synbiotics. This is in improved growth performance agreement with results of some studies parameters. A similar finding was also that have revealed the effects of obtained by Buteikis et al. (2008), who synbiotics in increasing growth presented evidence that dietary performance in fish. For instance, synbiotics applied in turkey resulted in Mehrabi et al. (2012), found that in reduced mortality. Addition of rainbow trout (Oncorhynchus mykiss) 177 Chitsaz et al., Effect of dietary synbiotics on growth, immune response and … fingerlings synbiotics (0.5, 1.0 and 1.5 and implantation of the live microbial g kg-1 of diet) significantly increased dietary supplement in the growth performance, survival rate and gastrointestinal tract of the host (Gibson feeding efficiency parameters compared and Robefroid, 1995). With the use of to the control (Mehrabi et al., 2012). synbiotics, it may be possible to Similarly, application of synbiotics was produce greater benefits than the found to enhance growth performance application of individual probionts and survival of Zebrafish (Danio rerio) (Merrifield et al., 2010). According to larvae (Nekoubin et al., 2012) and Soleimani et al. (2012) Dietary Caspian kutum (Rutilus frisii) fry supplementation of FOS improved the (Talibi Haghighi et al., 2010). innate immune response, stress Improved growth performance is likely resistance, digestive enzyme activities to be brought about by elevated and growth performance in Caspian digestive enzyme activities, possible roach (Rutilus rutilus) fry. Stimulation improvements of intestine morphology of the immune response of fish through or via synbiotics fermentation by dietary supplements is of high interest endogenous gut microbes to produce for commercial aquaculture (Staykov short chain fatty acids (SCFAs). et al., 2007). The innate immune Moreover, the synbiotics effect might system is very important in this regard also be potentially influenced by the because aquatic animals are continually type of species and the environment. Ye vulnerable to numerous opportunistic et al. (2011) demonstrated that feeding pathogens and this part of immune FOS, MOS or Bacillus clausii alone, or response provides the first line of in various combinations, improved defense for the host (Magnadóttir, growth performance, feed efficiency 2006). The use of natural and health status of the Japanese immunostimulants is a promising area flounder (Paralichthys olivaceus) in aquaculture because they are which was more pronounced in fish fed biodegradable, biocompatible and safe the synbiotics than those fed pre- and both for the environment and human probiotics alone. Similar synergistic health (Ortuno et al., 2002). It is clear effects were observed in studies with from the present study that dietary MOS+Enterococcus faecalis fed supplementation of synbiotics can rainbow trout (Oncorhynchus mykiss) modulate the innate immune responses (Rodriguez- Estrada et al., 2009). of the Caspian roach. As shown in Synbiotics, the combined application of Table 5, fish fed 2g kg-1 synbiotics had probiotics and prebiotics, is based on significantly greater plasma lysozyme, the principle of providing a probiont total immunoglobulin (Ig) and ACH50 with a competitive advantage over compared to those fed the 1g kg-1 competing endogenous populations; synbiotics and control diet. Similarly, thus, effectively improving the survival Ye et al. (2011) reported that lysozyme Iranian Journal of Fisheries Sciences 15(1) 2016 178 activity was significantly higher in thus positively affect the host’s Japanese flounder (Paralichthys microflora (Ringø et al., 2010). In the olivaceus) fed a synbiotics diet (FOS + present experiment, higher body protein Bacillus clausii, MOS+ Bacillus clausii and lipid content in the fish fed the or FOS + MOS + Bacillus clausii) than synbiotics supplemented diet implies in fish fed the control diet. Similar to this fact that, the ingested food was our results, dietary FOS has been converted more effectively into the reported to stimulate the innate immune structural protein and lipid subsequently responses, such as serum total resulted in more muscle as it is a immunoglobulin and serum lysozyme desirable aspect in fish farming. activity in roach (Soleimani et al., However, application of synbiotics in 2012). The immunostimulatory nature roach diet did not have any significant of synbiotics may be attributed to effect on ash content. Although stimulation of the growth of beneficial supplementation with synbiotics in bacteria such as lactic acid bacteria rainbow trout (Mehrabi et al., 2012) (Zhang et al., 2010). Supplementation and Caspian kutum fry (Talibi Haghighi with synbiotics influenced the immune et al., 2010), specifically increased the system of fish in this study, evidenced carcass protein, there was no significant by the increased total lactic acid difference in lipid and ash content, bacteria in the roach gut. Fish fed a diet among experimental treatments. Ye et containing 2g kg-1 synbiotics showed al. (2011) observed higher value of significant difference in lactic acid body protein deposition in Japanese bacteria in the intestinal tract after 8 flounder (Paralichthys olivaceus) weeks. This finding is concordant with supplemented with FOS+Bacillus several studies on the use of probiotics clausii and FOS+MOS+B.clausii and prebiotics in fish showing that compared to diets with FOS or FOS + bacteria can abound in the intestinal MOS only. The addition of prebiotics to tract of freshwater fish and stimulate a B. clausii supplemented diet did not their immune system (Gatesoupe, further decrease body lipid deposition. 1999). Mourino et al. (2012) observed Salinity stress tests have often been that the administration of synbiotics used as a final indicator of fish quality (inulin and Weissella cibaria) to the after nutrition trials (Taoka et al., diet of hybrid surubium 2006); our results indicated that dietary (Pseudoplatystoma sp.) increased synbiotics significantly increased growth of lactic acid bacteria, which is Caspian roach resistance to salinity in agreement with the observation of stress. Fish fed dietary synbiotics this study. Lactic acid bacteria have showed remarkable survival compared been considered beneficial residents of to the control group. The improved the fish’s intestinal ecosystem by resistance to salinity stress in the producing bacteriocins, which inhibit present study was similar to that growth of certain fish pathogens and reported for cobia (Rachycentron 179 Chitsaz et al., Effect of dietary synbiotics on growth, immune response and … canadum, Salze et al., 2008), white sea survival, body composition and bream larvae (Diplodus sargus, resistance of Caspian Sea white fish Dimitroglou et al., 2010) and Kutum (Rutilus rutilus). Journal of Marine fry (Rutilus frisii ; Akrami et al., 2010). Science and Technology, 21, 8. Soleimani et al. (2012) reported that AOAC, 1990. Official methods of dietary FOS significantly increased analysis. 15th ed. Arlington, VA.: resistance of roach fry to salinity stress Association of Analytical Chemists. challenges. It has been suggested that Bekcan, S., Dogankaya, L. and greater resistance to salinity stress Cakirogullari, G.C., 2006. Growth challenges might be due to improved and body composition of European microvilli alignment, as has been Catfish (Silurus glanis) fed diet reported in MOS fed fish (Dimitroglou containing different percentages of et al., 2010), which may increase the protein. Israeli Journal of protective function of the mucin barrier Aquaculture, 58, 137–142. and affect ion regulation (Salze et al., Buteikis, G., Matusevicius, P., 2008); however, future studies are Januskevicius, A., Jankowski, J., required to test this speculative Mikulski, D., Blok, J. and hypothesis. This study corroborates the Kozłowski, K., 2008. Use of functionality of synbiotics in the diet of synbiotic preparations in turkey diets roach which positively affects growth and their effect on growth performance, immune response, performance. Veterinarija Ir beneficial intestinal microbiota and Zootechnika, 43, 14–19. stress resistance. Daniels, C.L., Merrifield, D.L., Boothroyd, D.P., Davies, S.J., References Factor, J.R. and Arnold, K.E., Abdoli, A, 2000. The inland water 2010. Effect of dietary Bacillus spp. fishes of Iran. Iranian Museum of and mannan oligosaccharides (MOS) Nature and Wildlife. 378P. on European lobster (Homarus Ai, Q., Xu, H., Mai, K., Xu, W., gammarus L.) larvae growth Wang, J. and Zhang, W., 2011. performance, gut morphology and Effects of dietary supplementation of gut microbiota. Aquaculture, 304, Bacillus subtilis and 49–57. fructooligosaccharide on growth Demers, N.E. and Bayne, C.J., 1997. performance, survival, non-specific The immediate effects of stress on immune response and disease hormones and plasma lysozyme in resistance of juvenile large yellow rainbow trout. Developmental and croaker, Larimichthys crocea. Comparative Immunology, 21, 363- Aquaculture, 311, 155-161 73. Akrami, R., 2010. The effects of mannan oligosaccharide on growth, Iranian Journal of Fisheries Sciences 15(1) 2016 180

Gatesoupe, F.J., 1999. Review : The faecium M-74 and mannan- use of probiotics in aquaculture. oligosaccharides in diets for weaning Aquaculture, 180, 147 – 165 piglets. Journal of Science, Gibson, G.R. and Roberfroid, M.B., 43, 477–481. 1995. Dietary modulation of the Li, J.Q., Tan, B.P. and Mai, K.S., human colonic microbiota: 2009. Dietary probiotic Bacillus OJ introducing the concept of and isomal to oligosaccharides prebiotics. Journal of Nutrition, influence the intestine microbial 125(6), 1401–1412. populations, immune responses and Irianto, A. and Austin, B., 2002. resistance to white spot syndrome Probiotics in aquaculture. Journal of virus in shrimp (Litopenaeus Fish Diseases, 25, 633–642 vannamei). Aquaculture, 291, 35–40 Kesarcodi-Watson, A., Kaspar, H., Magnadóttir, B., 2006. Innate Lategan, M.J. and Gibson, L., immunity of fish (overview). Fish 2008. Probiotics in aquaculture: the and Shellfish Immunology, 20, 51- need, principles and mechanisms of 137. action and screening processes. Mahious, A.S. and Ollevier, F., 2005. Aquaculture, 274, 1–14. Probiotics and prebiotics in Keyvanshokooh, S. and Kalbassi, aquaculture: a review. In:Agh N, M.R., 2006. Genetic variation of Sorgeloos P, editors. 1st regional Rutilus rutilus caspicus (Jakowlew workshop on techniques for 1870) populations in Iran based on enrichment of live food for use in random amplified polymorphic DNA larviculture. Urima, Iran; 2005. pp. markers: a preliminary study. 17-26. Aquaculture Research, 1437, 37-40. Manning, T.S. and Gibson, G.R., Keyvanshokooh, S., Vaziri, B. and 2004. Prebiotics. Best Practice and Gharaei, A., 2009. Proteome Research Clinical Gastroenterology, modifications of juvenile beluga 18, 287–298. (Huso huso) brain as an effect of Mehrabi, Z., Firouzbakhsh, F. and dietary methylmercury. Comparative Jafarpour, A., 2012. Effects of Biochemistry and Physiology Part dietary supplementation of synbiotic D: Genomics and Proteomics, 4, on growth performance, serum 243–248. biochemical parameters and carcass Kiabi, B., Abdoli, A. and Naderi, M., composition in rainbow trout 1999. Status of the fish fauna in the (Oncorhynchus mykiss) fingerlings. South Caspian Basin of Iran. Journal of Animal Physiology and Zoology in the Middle East, 18, 57- Animal Nutrition, 96, 474–481. 65. Merrifield, D.L., Dimitroglou, A., Kumprecht, I. and Zobac, P., 1998. Foey, A., Davies, S.J., Baker, Study of the effect of a combined R.T.M. and Bøgwald, J., 2010. The preparation containing Enterococcus current status and future focus of 181 Chitsaz et al., Effect of dietary synbiotics on growth, immune response and …

probiotic and prebiotic applications 2010. Prebiotics in aquaculture: a for salmonids. Aquaculture, 302, 1- review. Aquaculture Nutrition, 16, 18. 117e36. Mourino, J.L., Nascimento, F.D.O., Rodriguez-Estrada, U., Satoh, S., vieria, A.B., Jatoba, B.C., Silva, Haga, Y., Fushimi, H. and D.A., Jesus, G.F.A., Seiffert, W.Q. Sweetman, J., 2009. Effects of and Martins, M.L., 2012. Effect of single and combined dietary supplementation on inulin supplementation of Enterococcus and W.cibaria on haemato- faecalis, mannan oligosaccharide immunological parameters of hybrid and polyhydrobutyric acid on growth surubium (Pseudoplatysoma sp.). performance and immune response Aquaculture Nutrition, 18, 73–80. of rainbow trout Oncorhynchus Nekoubin, H., Gharedashi, E., mykiss. Aquaculture Science, 57, Imanpour, M.R. and 609–617. Asgharimoghadam, A., 2012. The Sahin, T., Kaya, I., Unal, Y. and influence of synbiotic (Biomin Elmali, D.A., 2008. Dietary Imbo) on growth factors and survival Supplementation of probiotic and rate of Zebrafish (Danio rerio) prebiotic combination (combiotics) larvae via supplementation with on performance, carcass quality and biomar. Global Veterinaria, 8(5), blood parameters in growing quails. 503-506. Journal of Animal and Veterinary Ortuno, J., Cuesta, A., Rodriguez, A., Advances, 7, 1370–1373. Esteban, M.A. and Meseguer, J., Salze, G., McLean, E., Schwarz, M.H. 2002. Oral dministration of yeast, and Craig, S.R., 2008. Dietary Saccharomyces cerevisiae, enhances mannan oligosaccharide enhances the cellular innate immune response salinity tolerance and gut of gilthead seabream (Sparus aurata development of larval cobia. L.). Veterinary Immunology and Aquaculture, 274, 148e52. Immunopathology, 85, 41-50. Siwicki, A.K. and Anderson, D.P., Peter, H. and Sneath, A., 1986. 1993. Nonspecific defense Bergeys manual of systematic. mechanisms assay in fish: II. Bacteriology, 2, 1104–1154 potential killing activity of Rengpipat, S., Phianphak, W. and neutrophils and macrophages, Piyatiratitivorakul, S., 1998. lysozyme activity in serum and Effects of a probiotic bacterium on organs and total immunoglobulin black tiger shrimp (Penaeus level in serum. Fish Disease monodon) survival and growth. Diagnosis and Prevention Methods; Aquaculture, 167, 301–313. 1993, 105e12. Olsztyn, Poland. Ringø, E., Olsen, Re., Dalmo, R.A., Soleimani, N., Hoseinifar, S.H., Amlund, H. and Hemre, G.I., Merrifield, D.L., Barati, M. and Iranian Journal of Fisheries Sciences 15(1) 2016 182

HassanAbadi, Z., 2012. Dietary Wang, Y., Wu, Z.X., Pang, S.F., Zhu, supplementation of D.M., Feng, X. and Chen, X.X., fructooligosaccharide (FOS) 2008a. Effects of improves the innate immune fructooligosaccharides on non- response, stress resistance, digestive specific immune function in enzyme activities and growth Carassius auratus. Acta Ecologica performance of Caspian roach Sinica, 32(4), 487–492. (Rutilus rutilus) fry. Fish and Wang, Y.B. and Xu, Z.R., 2006. Shellfish Immunology, 32, 316–321. Effect of probiotics for common carp Staykov, Y., Spring, P., Denev, S. and (Cyprinus carpio) based on growth Sweetman, J., 2007. Effect of performance and digestive enzyme mannan oligosaccharide on the activities. Animal Feed Science and growth performance and immune Technology, 127, 283–292. status of rainbow trout Yano, T., 1992. Assays of hemolytic (Oncorhynchus mykiss). Journal of complement activity. In: Stolen, J.S., Aquaculture International, 15, 153– Fletcher, T.C., Anderson, D.P., 161. Kaattari, S.L., Rowley, A.F. (Eds.), Shim, S.B., 2005. Effects of prebiotics, Techniques in fish immunology.SOS probiotics, and synbiotics in the diet Publications, Fair Haven, NJ, pp. of young pigs. PhD thesis of the 131–141. Wageningen Institute of Animal Ye, J.D., Wang, K., Li, F.D. and Sun Sciences, Wageningen University Y.Z., 2011. Single or combined and Research Centre, Wageningen, effects of fructo- and mannan The Netherlands, pp. 115–128. oligosaccharide supplements and Talibi Haghighi, D., Fallahi, M. and Bacillus clausii on the growth, feed Abdolah Tabar, Y., 2010. Effect of utilization, body composition, different levels of symbiotic digestive enzyme activity, innate (Biomin Imbo) on growth, survival immune response and lipid and body composition of Caspian metabolism of the Japanese flounder kutum (Rutilus frisii kutum) fry, Paralichthys olivaceus. Aquaculture Journal of fisheries, 15, 1-14(In Nutrition, 17, e902-e911 Persian). Zhang, Q., Ma, H.M., Mai, K.S., Taoka, Y., Maeda, H., Jo, J.Y., Jeon, Zhang, W.B., Liufu, Z.Q. and Xu, M.J., Bai, S.C. and Lee, W.J., W., 2010. Interaction of dietary 2006. Growth, stress tolerance and Bacillus subtilis and non-specific immune response of fructooligosaccharide on the growth Japanese flounder Paralichthys performance, non-specific immunity olivaceus to probiotics in a closed of sea cucumber, Apostichopus recirculating system. Fisheries japonicus. Fish and Shellfish Science, 72, 310-21. Immunology, 29, 204–211.