Abstract
Golden pompano Trachinotus ovatus is an economically important warm-water farmed marine fish species. For the past few years, as T. ovatus-intensive aquaculture expanded and culture density raised, diseases have happened more repeatedly, causing many economic losses. In order to improve survival, several chemotherapeutic agents, vaccines, and antibiotics as well as some immunostimulants have been used to prevent bacterial, viral, fungal, and parasitic diseases at many hatcheries and fish farms. Therefore, the optimum type and supplementation level of functional additives are essential to the growth performance of T. ovatus juveniles in aquaculture. In this chapter, we review the functional feed additives (soybean isoflavones and marine red yeast Rhodotorula mucilaginosa) and their effects on the growth performance, nonspecific immune response, and disease resistance of juvenile T. ovatus.
Access provided by Autonomous University of Puebla. Download chapter PDF
Similar content being viewed by others
Keywords
15.1 Introduction
Golden pompano Trachinotus ovatus is an economically important warm-water marine fish species farmed in south coast of China and Southeast Asia (Sun et al. 2014; Zheng et al. 2014). As intensive aquaculture expanded and culture density increased, diseases happened more repeatedly, especially from May to October, causing many economic losses (Xia et al. 2012; Zhang et al. 2014a, b). Fish under intensive culture conditions are more susceptible to pathogen infection than wild fish. The environmental stress caused by discharge of farms into estuaries and bays and the stress caused by high rearing density are factors that make animals more sensitive to pathogens (Bilen et al. 2011). For reduce mortality, several fish farms and hatcheries use many chemotherapeutic agents, vaccines, and antibiotics, as well as some immunostimulants, to prevent bacterial, viral, fungal, and parasitic diseases (Dügenci et al. 2003). However, the drug applications listed above are quite expensive in intensive culture. In addition, they may cause adverse effects like pollution, bioaccumulation, and antibiotic resistance, which can be transferred to wild and human pathogenic microorganisms, thereby posing a threat to human health and sociopolitical and environmental issues (Harikrishnan et al. 2011).
Immunostimulants increase resistance to infectious disease by enhancing nonspecific defense mechanisms. Consequently, the response duration is very short because there is no memory component (Sakai 1999). Since immunostimulants are considered safe and effective against various pathogens, the use of immunostimulants in fish culture to enhance immunity and disease resistance has received considerable attention (Sakai 1999; Harikrishnan et al. 2011). Immunostimulants can be applied via injection, oral administration, or bathing (Sakai 1999; Yin et al. 2006; Jeney and Anderson 1993a, b). Although intraperitoneal injection has been verified to be the most speedy and effective way of administration, incorporation in the diet is considered as most suitable for fish culture, as this method is non-stressful (Siwicki et al. 1994; Esteban et al. 2001). Several immunostimulants, such as levamisole (Siwicki et al. 1990; Jeney and Anderson 1993a, b), chitosan (Siwicki et al. 1994), yeast (Siwicki et al. 1994), glucan (Jorgensen and Robertsen 1995), lipopolysaccharide (Solem et al. 1995), growth hormone (Sakai et al. 1995, 1996), glucan plus vitamin C (Verlhac et al. 1996), yeast RNA (Sakai et al. 2001), and zeranol (Keles et al. 2002), have been administered as feed additives to modulate nonspecific immunity of fish, such as Ictalurus punctatus Rafinesque, Cyprinus carpio L., Salmo salar L., and Oncorhynchus mykiss. In this chapter, we aim to evaluate the role of dietary additives of soybean isoflavones and marine red yeast Rhodotorula mucilaginosa as an immunostimulant to promote growth performance and enhance the nonspecific immune ability and production of golden pompano.
15.2 The Effects of Dietary Soybean Isoflavones (SI) in the Feed of Juvenile Golden Pompano
Isoflavones are a class of molecules called flavonoids, whose basic structural unit is composed of two benzene rings connected by a heterocyclic pyran ring and belongs to a large family of polyphenols (Barnes et al. 2011; Chen et al. 2011). Because isoflavones are structurally similar to natural estrogen, they can exert a variety of estrogen-like biological effects in animals (Ng et al. 2006). In mammals, isoflavones have a wide range of biological activities including antioxidant effects (Jiang et al. 2007), antiestrogenic effects (Cassidy et al. 1995), anticancer effects (Dijsselbloem et al. 2004), anti-inflammatory effects (Verdrengh et al. 2003; Hämäläinen et al. 2007), enzyme-inhibitory effects (Yamashita et al. 1990), cardioprotective effects (Anthony et al. 1996), and antifungal effect (Naim et al. 1974).
15.2.1 Growth
Soybean isoflavones (SI), which are a plant chemical with estrogenic activity, can weakly bind to estrogen receptors, causing competition between natural estrogens and isoflavones (Turan 2006; Kelly et al. 1993). However, Martin et al. (1978) suggested that isoflavones may act as anti-estrogens in the presence of high levels of endogenous estrogens (Martin et al. 1978). Because isoflavones may have hormone-like functions, they may affect animal growth. The effects of soybean isoflavones on growth performance are somewhat variable. For example, supplemental SI can increase the growth rate in barrows (Cook 1998), African catfish Clarias gariepinus (Burchell 1822) (Turan and Akyurt 2005), tilapia Oreochromis aureus (Yu et al. 2006) and tilapia Oreochromis aureus (Turan 2006). Zhou et al. (2015) found that with the increase of dietary SI, the growth performance of T. ovatus was significantly improved when dietary SI level is up to 40 mg kg−1, indicating that dietary SI might promote the growth of fish at a suitable dose.
15.2.2 Nonspecific Immune Response
Proteins are the most important compound in the serum, with albumin and globulin being the major serum proteins (Kumar et al. 2005; Jha et al. 2007). The hemolymph protein content is used as an immune parameter to indicate whether or not a fish is healthy (De Smet and Blust 2001). The complement system is the major humoral component of the innate immune responses and plays an essential role in alerting the host immune system of the presence of potential pathogens as well as their clearance (Muller-Eberhard 1988). The complement system is initiated by one or a combination of three pathways, namely, the classical, lectin, and alternative. All three pathways merge at a common amplification step involving C3 and proceed through a terminal pathway that leads to the formation of a membrane attack complex, which can directly lyse pathogenic cells (Boshra et al. 2006). The results in the previous study on T. ovatus showed that the total plasma protein and C3 content were significantly increased by feeding the dose of SI at 40 mg kg−1 feed (Zhou et al. 2015). However, these immune parameters were not further increased by feeding the fish with the diet supplemented with SI at the level of 60 and 80 mg kg−1 feed, suggesting that high supplementation, especially the dose of 40 mg kg−1 feed is optimal for the increase of plasma total protein and C3 content. To date, there is no exact explanation on how SI works to increase plasma total protein and C3 content in fish. Further studies are necessary to explore the mechanism of the effects of SI on plasma total protein and C3 content of fish.
The innate immune system of fish is considered to be the first line of defense against a broad spectrum of pathogens and is more important for fish as compared with mammals. Lysozyme level or activity is an essential index of innate immunity of fish and is ubiquitous in its distribution among living organisms (Saurabh and Sahoo 2008). The plasma LYZ activity of T. ovatus increased with dietary SI level, increasing from 0 to 40 mg kg−1 SI, with no significant differences among the treatments with over 40 mg kg−1 SI (Zhou et al. 2015). Similarly, a large number of immunostimulants have been reported to increase serum lysozyme levels in fish that may be due to either an increase in the number of phagocytes secreting lysozyme or due to an increase in the amount of lysozyme synthesized per cell (Kumari and Sahoo 2006).
Respiratory bursts are produced by phagocytes in order to attack invasive pathogens during phagocytosis and have been widely used to evaluate the defense ability against pathogens. However, the excessive accumulation of reactive oxygen intermediates (ROIs) is extremely toxic to host cells (Dalmo et al. 1997). It is clear that the SI has an enhancing effect on respiratory burst activity of golden pompano (Zhou et al. 2015). Data from this study showed that compared with the control, the 40 mg kg−1 SO group significantly increased respiratory burst activity, and the other groups supplemented with 20, 60, and 80 mg kg−1 SI had a tendency of an increase in respiratory burst activity. A previous study has demonstrated that dietary administration of immunostimulant (such as emodin) significantly affected respiratory burst activity of Wuchang bream (Zhang et al. 2014a, b). These findings suggest that long-term feeding of the proper immunostimulant (SI) supplementation can maintain the activation of phagocytic cells throughout the experimental period and is fundamental in achieving disease resistance.
15.2.3 Hepatic Antioxidant Status and the Expression of Hepatic Gene HSP70
The nonspecific defense mechanisms of fish include neutrophil activation, production of peroxidase and oxidative free radicals, and initiation of other inflammatory factors (Ainsworth et al. 1991). The stress response might also impact factors such as total antioxidation capacity and levels of glutathione, catalase, SOD, and various peroxidases (Liu et al. 2010; Itou et al. 1996). The SI has exhibited antioxidant effects both in vitro and in vivo (Chen et al. 2011). Isoflavone-supplemented diets can reduce lipid peroxidation and F2-isoprostane levels, a biomarker of lipid peroxidation, in humans (Wiseman et al. 2000). Disilvestro et al. (2005) reported that the SI in capsules could elevate erythrocyte superoxide dismutase in human (Disilvestro et al. 2005). Previous studies showed that SI supplemented at the dose of 20 mg kg−1 feed significantly increased the SOD activity in L. vannamei when compared with other treatments (Chen et al. 2011), and the hepatic antioxidative capacity was strongly increased by dietary SI in tilapia (Oreochromis aureus Steindachner) (Yu et al. 2006). Cai and Wei (1996) suggested that dietary genistein enhances the activities of antioxidant enzymes (SOD, CAT, glutathione reductase, and glutathione peroxidase) in various organs in mice, which may be a mechanism of genistein’s chemopreventive action (Cai and Wei 1996). Consistent with these studies, Zhou et al. observed that compared to the control the treatments supplemented with 40 mg kg−1 SI increased activities of hepatic antioxidant enzymes (SOD, T-AOC, CAT) whereas malondialdehyde content was reduced (Zhou et al. 2015). The present results imply that SI can improve antioxidative status, inhibit free radical formation, and reduce the harm of lipidic superoxide in juvenile golden pompano.
Heat shock proteins (HSPs), also known as stress proteins and extrinsic chaperones, are a suite of highly conserved proteins of varying molecular weight (c. 16–100 kDa) produced in all cellular organisms when they are exposed to stress (Roberts et al. 2010). HSP70 is mainly involved in stress protection, improving cell survival and raising tolerance to environmental stressors or harm (Basu et al. 2002). Thus, HSP70 has been widely used as a bioindicator of stress. HSP70 is induced by heat and chemical shocks in fish, like in mammals (Gornati et al. 2004). A number of studies have shown that Chinese herbs enhance the expression of HSP70 in Wuchang bream (Liu et al. 2012) and white shrimp (Lei and Zeng 2008), and higher dietary carbohydrate increases the expression level of HSP70 (Zhou et al. 2013). Moreover, HSP70 mRNA of broilers was also changed positively by the dietary genistein (Kamboh et al. 2013). Similarly, the relative level of hepatic HSP70 mRNA of T. ovatus increased with increasing dietary SI levels up to 40 mg kg−1 and thereafter levelled off, indicating that dietary SI could enhance the expression of HSP70 (Zhou et al. 2015).
15.2.4 Challenge Test
Currently, because the methodology to comprehensively investigate immunity and disease resistance of fish is still limited, a useful biomarker for disease resistance of fish is difficult to identify. Therefore, bacterial challenge tests have often been used as a final indicator of fish health status after nutrition trials (Lin et al. 2012; Jin et al. 2013). Vibriosis is caused by V. harveyi, a halophilic gram-negative bacterium that is known to cause disease to fish, shrimp, and shellfish either in the culture system or in the wild aquatic environment (Sharma et al. 2012; Austin and Zhang 2006). A previous study showed that dietary SI showed an improved survival rate of L. vannamei against an intramuscular challenge with V. alginolyticus (Chen et al. 2011). This agrees well with the results of other workers (Huang et al. 2005), who found SI-supplemented diets improved survival rate against an intramuscular injecting with V. parahaemolyticus. Zhou et al. (2015) found that dietary SI showed an increased survival rate of T. ovatus against challenge with Vibrio harveyi (Zhou et al. 2015). Therefore, SI showed positive effects on preventing golden pompano against Vibrio harveyi infection.
15.3 Effects of Dietary Additive of Marine Red Yeast Rhodotorula mucilaginosa on Golden Pompano
Yeast can affect nonspecific immunity and protection against furunculosis in rainbow trout (Siwicki et al. 1994). Yeast may improve fish health as antagonists to pathogens and by immunostimulation (Andlid et al. 1995). Rorstad et al. (1993) also reported that yeast glucan showed an adjuvant effect when included in vaccines against furunculosis in Atlantic salmon (Salmo salar L.). Nakano et al. (1999) observed that red yeast had a reducing effect on oxidized oil-induced oxidative stress in rainbow trout (Oncorhynchus mykiss). Xia et al. (2013) observed that marine red yeast Rhodotorula mucilaginosa could promote the growth and immunity of Litopenaeus vannamei.
15.3.1 Growth
The marine red yeast has been widely used for its potential beneficial effect in aquaculture (Yang et al. 2010; Zhang et al. 2013; Sun et al. 2015). Zhou et al. (2016) found that the WG and SGR of T. ovatus fed with 1‰ R. mucilaginosa diet were higher than those of control group. Previous studies also showed that compared to the control group, weight gain (WG) and specific growth rate (SGR) of Litopenaeus vannamei with fed R. paludigenum supplementation increased significantly (Yang et al. 2010; Scholz et al. 1999). Zhang observed that addition of 1 g kg−1 Rhodotorula benthica into brown fish meal can significantly improve feeding rate, protein efficiency rate, and growth performance of turbot, a similar growth level to white fish meal (Zhang et al. 2013). Tovar-Ramı́rez et al. (2004) found that final mean weight of sea bass larvae in the group fed with 1.1% of marine yeast D. hansenii CBS8339 was twice as that of the other groups. These results suggested that the marine red yeast produces many bioactive substances, such as protein, amino acids, fatty acid, polysaccharide, and carotenoids, which could promote the growth of aquatic animals.
15.3.2 Serum Biochemical and Immune Parameters
LYZ is a bactericidal peptide, which is an important component of the immune defense of marine fish species (Liu et al. 2012). It is responsible for breaking down the polysaccharide walls of many kinds of bacteria and thus provides some protection against pathologic infection (Lie et al. 1989; Hauge et al. 2002). The AKP is an important component of lysosomal enzymes that originate from hemocytes to destroy extracellular binvadersQ (Cheng and Rodirick 1975). Therefore, phagocytic competence and AKP activity are related to the quantity and quality of hemocytes. The activities of the immunity active factors (serum LYZ and AKP) in the serum of the lady crab Charybdis japonica have different degrees of the enhancement in 48 h after infection with the polysaccharide of oceanic red yeast (Sun et al. 2015; Wang et al. 2011). Similarly, compared to the control, the R. mucilaginosa diets significantly increased serum LYZ and AKP activities of juvenile T. ovatus (Zhou et al. 2016). Nitric oxide produced by NOS is associated with diverse actions in neurotransmission, vascular systems, and immunity, including antimicrobial and antiviral activities by inhibiting DNA as well as protein and lipid synthesis (Bredt and Snyder 1994; Karupiah et al. 1993; Howe et al. 2002; Lepoivre et al. 1990). Compared to other treatments, the group supplemented with 2‰ R. mucilaginosa significantly increased serum NOS activity (Zhou et al. 2016). This agrees well with the finding of Zhang et al. (2011), who found that the shrimp (Penaeus japonicus) fed the diet with both Bacillus probiotics and IMO (T3) produced significantly higher immune parameters (LYZ activity and NOS activities) than the control group. These results suggested that oceanic red yeast has immune stimulation to some extent.
15.3.3 Hepatic Antioxidative Status
The increase in free radical content may lead to an increase in lipid peroxidation content and lipid peroxidation injury in fish (Liu et al. 2012). The breakdown of hepatic lipid peroxide yields large amounts of aldehydes, alcohols, and hydrocarbons such as MDA, a strongly toxic chemical. The antioxidant enzyme system plays a prominent role in resisting lipid oxide damage (Holmblad and Soderhall 1999; Lopes et al. 2001). Dietary supplementation with marine red yeast can significantly enhance antioxidant activity in aquatic animals (Bon et al. 1997; Li and zhang 2004). A previous study showed the SOD activity of hepatopancreases from L. vannamei in groups fed with the live yeast diet and the dry yeast diet was significantly higher than that in the control group, whereas no statistical difference was found in MDA content of hepatopancreases (Yang et al. 2010). Zhou et al. (2016) found that compared to the control, the groups supplemented with 2–4‰ R. mucilaginosa increased hepatic SOD activity, whereas the 2–5‰ R. mucilaginosa treatment groups decreased hepatic MDA content, especially in the 4‰ R. mucilaginosa group. Taken together, our results suggest that the supplementation with R. mucilaginosa reduces the potential for oxidative damage in T. ovatus.
15.3.4 Effect of R. mucilaginosa on Survival in T. ovatus
Currently, bacterial challenge test has often been used as a final indicator of fish health after nutrition trials (Zhou et al. 2015). Vibriosis is caused by V. harveyi, a halophilic gram-negative bacterium causing disease in fish, shrimp, and shellfish (Sharma et al. 2012; Austin and Zhang 2006). A previous study showed that supplementation of red yeast could make the red yeast colonize in the intestine of fish larvae, which could affect the growth of the larvae and accelerate the maturity of the digestive system to improve survival rates (Gatesoupe 2007). The survival rate of the mice in the group fed with the diet supplemented with the astaxanthin produced by red yeast was higher than that of the control group (Bennedsen et al. 1990). Similarly, dietary R. mucilaginosa showed an increased survival rate of T. ovatus against challenge with V. harveyi (Zhou et al. 2016).
15.3.5 The Effect of R. mucilaginosa on Hemolymph Complement 3 and Complement 4 of T. ovatus After V. harveyi Infection
The complement system is the major humoral component of the innate immune responses and thus plays an essential role in alerting the host immune system of the presence of potential pathogens as well as their clearance, which is initiated by one or a combination of three pathways, namely, the classical, alternative, and lectin (Holland and Lambris 2002; Zhou et al. 2014). The complement C3 is the central component of the complement system, being activated into its respective cleavage products C3a and C3b through one of the three pathways (Boshra et al. 2006). The complement C4 plays an integral role in the activation of the classical and lectin pathways (Boshra et al. 2006). A previous study showed that after challenge by Aeromonas veronii, there was no significant difference in complement 3 among all groups (Yu et al. 2014). However, compared to the control group prior to infection, the serum C3 level significantly increased in the group supplemented with R. mucilaginosa; compared to the control after infection, the 0.1–0.3‰ R. mucilaginosa groups significantly increased serum C4 levels (Zhou et al. 2016).
15.4 Conclusion
In conclusion, dietary soybean isoflavones and R. mucilaginosa supplementation, as an immunostimulant, could promote growth performance and enhance the nonspecific immune ability and production of golden pompano in aquaculture.
References
Ainsworth AJ, Dexiang C, Waterstrat PR (1991) Changes in peripheral blood leukocyte percentages and function of neutrophils in stressed channel catfish. J Aquat Anim Health 3:41–47
Andlid T, Juarez RV, Gustafsson L (1995) Yeast colonizing the intestine of rainbow trout (Salmo gairdneri) and turbot (Scopthalmus maximus). Microb Ecol 30:321–347
Anthony MS, Clarkson TB, Hughes CL, Morgan TM, Burke GL (1996) Soybean isoflavones improve cardiovascular risk factors without affecting the reproductive system of peripubertal rhesus monkeys. J Nutr 126:43–50
Austin B, Zhang XH (2006) Vibrio harveyi: a significant pathogen of marine vertebrates and invertebrates. Lett Appl Microbiol 43:119–124
Barnes S, Prasain J, D’Alessandro T (2011) The metabolism and analysis of isoflavones and other dietary polyphenols in foods and biological systems. Food Funct 2:235–244
Basu N, Todgham AE, Ackerman PA, Bibeau MR, Nakano K, Schulte PM, Iwama GK (2002) Heat shock protein genes and their functional significance in fish. Gene 295:173–183
Bennedsen M, Xin W, Willén R, Wadström T, Andersen LP (1990) Treatment of H. pylori infected mice with antioxidant astaxanthin reduces gastric inflammation, bacterial load and modulates cytokine release by splenocytes. Immunol Lett 70(3):185–189
Bilen S, Bulut M, Bilen AM (2011) Immunostimulant effects of Cotinus coggyria on rainbow trout. Fish Shellfish Immun 30:451–455
Bon JA, Leathers TD, Jayaswal RK (1997) Isolation of astaxanthin-overproducing mutants of phaffia rhodozyma. Biotechnol Lett 19(2):109–112
Boshra H, Li J, Sunyer JO (2006) Recent advances on the complement system of teleost fish. Fish Shellfish Immun 20:239–262
Bredt DS, Snyder SH (1994) Nitric oxide: a physiology messenger molecule. Annu Rev Biochem 63:175–195
Cai Q, Wei H (1996) Effect of dietary genistein on antioxidant enzyme activities in SENCAR mice. Nutr Cancer 25:1–7
Cassidy A, Bingham S, Setchell KDR (1995) Biological effects of isoflavones in young women: importance of the chemical composition of soyabean products. Br J Nutr 74:587–601
Chen XR, Tan BP, Mai KS (2011) Dietary administration of soybean isoflavones enhances the immunity of white shrimp Litopenaeus vannamei and its resistance against Vibrio alginolyticus. Aquac Nutr 17:24–32
Cheng TC, Rodirick GE (1975) Lysosome and other enzymes in the haemolymph of Crassostrea virgiica and Mercenaria mercenaria. Comp Biochem Physiol B 52:443–447
Cook DR (1998) The effect of dietary soybean isoflavones on the rate and efficiency of growth and carcass muscle content in pigs and rats. PhD dissertation, Iowa State University, Ames, IA
Dalmo RA, Ingebrigtsen K, Bøgwald J (1997) Nonspecific defence mechanisms in fish, with particular reference to the reticuloendothelial system (RES). J Fish Dis 20:241–273
De Smet H, Blust R (2001) Stress responses and changes in protein metabolism in carp Cyprinus carpio during cadmium exposure. Ecotox Environ Safe 3:255–262
Dijsselbloem N, Vanden Berghe W, De Naeyer A (2004) Soy isoflavone phyto-pharmaceuticals in interleukin-6 affections: multipurpose nutraceuticals at the crossroad of hormone replacement, anti-cancer and anti-inflammatory therapy. Biochem Pharmacol 68:1171–1185
Disilvestro RA, Goodman J, Dy E, Lavalle G (2005) Soy isoflavone supplementation elevates erythrocyte superoxide dismutase, but not plasma ceruloplasmin in postmenopausal breast cancer survivors. Breast Cancer Res Treat 89:251–255
Dügenci SK, Arda N, Candan A (2003) Some medicinal plants as immunostimulant for fish. J Ethnopharmacol 88:99–106
Esteban MA, Cuesta A, Ortuño J, Meseguer J (2001) Immunomodulatory effects of dietary intake of chitin on gilthead seabream (Sparus aurata L.) innate immune response. Fish Shellfish Immun 11:303–315
Gatesoupe FJ (2007) Live yeasts in the gut: natural occurrence, dietary introduction, and their effects on fish health and development. Aquaculture 267(1/4):20–30
Gornati R, Papis E, Rimoldi S, Terova G, Saroglia M, Bernardini G (2004) Rearing density influences the expression of stress-related genes in sea bass (Dicentrarchus labrax L.). Gene 341:111–118
Hämäläinen M, Nieminen R, Vuorela P, Heinonen M, Moilanen E (2007) Anti-inflammatory effects of flavonoids: genistein, kaempferol, quercetin, and daidzein inhibit STAT-1 and NF-κB activations, whereas flavone, isorhamnetin, naringenin, and pelargonidin inhibit only NF-κB activation along with their inhibitory effect on iNOS expression and NO production in activated macrophages. Mediat Inflamm 2007:45673. https://doi.org/10.1155/2007/45673
Harikrishnan R, Balasundaram C, Heo MS (2011) Impact of plant products on innate and adaptive immune system of cultured finfish and shellfish. Aquaculture 317:1–15
Hauge T, Kjulll AK, Stensvag K (2002) Antibacterial activity in four marine crustacean decapods. Fish Shellfish Immun 12:371–385
Holland MCH, Lambris JD (2002) The complement system in teleosts. Fish Shellfish Immun 12:399–420
Holmblad T, Soderhall K (1999) Cell adhesion molecules and anti-oxidative enzymes in a crustacean; possible role in immunity. Aquaculture 172:111–123
Howe D, Barrows LF, Lindstrom NM, Heinzen RA (2002) Nitric oxide inhibits Coxiella burnetii replication and parasitophorous vacuole maturation. Infect Immun 70:5140–5147
Huang G, Yu D, Guo L, Wang X (2005) Studies on immune effects of soybean isoflavones on fish. South China Fish Sci 1:35–40
Itou T, Lida T, Kawatsu H (1996) Kinetics of oxygen metabolism during respiratory burst in Japanese eel neutrophils. Dev Comp Immunol 20:323–330
Jeney G, Anderson DP (1993a) Enhanced immune response and protection in rainbow trout to Aeromonas salmonicida bacterin following prior immersion in immunostimulants. Fish Shellfish Immun 3:51–58
Jeney G, Anderson DP (1993b) An in vitro technique for surveying immunostimulants in fish. Aquaculture 112:283–287
Jha AK, Pal AK, Sahu NP, Kumar S, Mukherjee SC (2007) Haemato-immunological responses to dietary yeast RNA, ω-3fatty acid and α-carotene in Catla catla juveniles. Fish Shellfish Immun 23:917–927
Jiang Z, Jiang S, Lin Y, Xi P, Wu T (2007) Effects of soybean isoflavone on growth performance, meat quality, and antioxidation in male broilers. Poult Sci 86:1356–1362
Jin Y, Tian L, Zeng S, Xie S, Liu Y (2013) Dietary lipid requirement on nonspecific immune responses in juvenile grass carp (Ctenopharyngodon idella). Fish Shellfish Immun 34:1202–1208
Jorgensen J, Robertsen B (1995) Yeast β-glucan stimulates respiratory burst activity of Atlantic salmon (Salmo salar L.) macrophages. Dev Comp Immunol 19:43–57
Kamboh AA, Hang SQ, Bakhetgul M, Zhu WY (2013) Effects of genistein and hesperidin on biomarkers of heat stress in broilers under persistent summer stress. Poult Sci 92:2411–2418
Karupiah G, Xie QW, Buller RML, Nathan C, Duarte C, MacMicking JD (1993) Inhibition of viral replication by interferon-γ-induced nitric oxide synthase. Science 261:1445–1448
Keles O, Ak S, Bakirel T, Karatas S (2002) The investigation of the anabolic efficiancy and effect on the nonspecific immune system of zeranol in rainbow trout (Oncorhynchus mykiss, Walbaum). Turk J Vet Anim Sci 26:925–931
Kelly GE, Nelson C, Waring MA, Joannou GE, Reeder AY (1993) Metabolites of dietary (soya) isoflavones in human urine. Clin Chim Acta 223:9–22
Kumar S, Sahu NP, Pal AK, Choudhury D, Yengkokpam S, Mukherjee SC (2005) Effect of dietary carbohydrate on haematology, respiratory burst activity and histological changes in L. rohita juveniles. Fish Shellfish Immun 19:331–344
Kumari J, Sahoo PK (2006) Dietary β-1,3 glucan potentiates innate immunity and disease resistance of Asian catfish, Clarias batrachus (L.). J Fish Dis 29:95–101
Lei A, Zeng D (2008) Effects of compound Chinese herbal on the expression of heat stress protein 70 gene in white shrimp (Litopenaeus vannamei). J Guangxi Agric Sci 6:830–833
Lepoivre M, Chenaist B, Yapo A, Lemaire G, Tenu J-P (1990) Alterations of ribonucleotide reductase activity following induction of the nitrite-generating pathway in adenocarcinoma cell. J Biol Chem 265:14143–14149
Li H, Zhang K (2004) The production of β-carotene by fermentation of red yeast. Food Res Dev 25(3):58–60
Lie Ø, Evensen Ø, Sorensen A, Frøysadal E (1989) Study on lysozyme activity in some fish species. Dis Aquat Org 6:1–5
Lin S, Mao S, Yong G, Lin X, Luo L (2012) Dietary administration of chitooligosaccharides to enhance growth, innate immune response and disease resistance of Trachinotus ovatus. Fish Shellfish Immun 32:909–913
Liu B, Xie J, Ge X, Xu P, Wang A, He Y, Zhou Q, Pan L, Chen R (2010) Effects of anthraquinone extract from Rheum officinale bail on the growth performance and physiological responses of Macrobrachium rosenbergii under high temperature stress. Fish Shellfish Immun 29:49–57
Liu B, Ge X, Xie J, Xu P, He Y, Cui Y, Ming J, Zhou Q, Pan L (2012) Effects of anthraquinone extract from Rheum officinale bail on the physiological responses and hsp70 gene expression of Megalobrama amblycephala under Aeromonas hydrophila infection. Fish Shellfish Immun 32(1):1–7
Lopes PA, Pinheiro T, Santos MS, da Luz Mathias M, Collares-Pereira MJ, Viegas-Crespo AM (2001) Response of antioxidant enzymes in freshwater fish populations (Leuciscus alburnoides complex) to inorganic pollutants exposure. Sci Total Environ 280:153–163
Martin PM, Horowitz KB, Ryan DS, McGuire WL (1978) Phytoestrogen interaction with estrogen receptors in human breast cancer cells. J Endocrinol 103:1860–1867
Muller-Eberhard HJ (1988) Molecular organization and function of the complement system. Annu Rev Biochem 57(1):321–347
Naim M, Gestetner B, Zilkah S, Birk Y, Bondi A (1974) Soybean isoflavones, characterization, determination an antifungal activity. J Agric Food Chem 22:806–812
Nakano T, Kanmuri T, Sato M, Takeuchi M (1999) Effect of astaxanthin rich red yeast (Phaffia rhodozyma) on oxidative stress in rainbow trout. Biochim Biophys Acta 1426:119–125
Ng Y, Hanson S, Malison JA, Wentworth B, Barry TP (2006) Genistein and other isoflavones found in soybeans inhibit estrogen metabolism in salmonid fish. Aquaculture 254:658–665
Roberts RJ, Agius C, Saliba C, Bossier P, Sung YY (2010) Heat shock proteins (chaperones) in fish and shellfish and their potential role in relation to fish health: a review. J Fish Dis 33:789–801
Rorstad G, Aasjord PM, Robertsen B (1993) Adjuvant effect of yeast glucan in vaccines against furunculosis in Atlantic salmon, (Salmo salar L.). Fish Shellfish Immun 3:179–190
Sakai M (1999) Current research status of fish immunostimulants. Aquaculture 172:63–92
Sakai M, Kobayashi M, Kawauchi H (1995) Enhancement of chemiluminescent responses of phagocyctic cells from rainbow trout, O. mykiss, by injection of growth hormone. Fish Shellfish Immun 5:375–379
Sakai M, Kobayashi M, Kawauchi H (1996) In vitro activation of fish phagocytic cells by GH, prolactin and somatolactin. J Endocrinol 151:113–118
Sakai M, Taniguchi K, Mamoto K, Ogawa H, Tabata M (2001) Immunostimulant effects of nucleotide isolated from yeast RNA on carp, Cyprinus carpio L. J Fish Dis 24:433–438
Saurabh S, Sahoo PK (2008) Lysozyme: an important defence molecule of fish innate immune system. Aquac Res 39:223–239
Scholz U, Diaz GG, Ricque D, Cruz Suarez LE, Alboreset FV, Latchford J (1999) Enhancement of vibriosis resistance in juvenile Penaeus vannamei by supplementation of diets with different yeast products. Aquaculture 176:271–283
Sharma SRK, Rathore G, Verma DK, Sadhu N, Philipose KK (2012) Vibrio alginolyticus infection in Asian seabass (Lates calcarifer, Bloch) reared in open sea floating cages in India. Aquac Res 44:86–92
Siwicki AK, Anderson DP, Dixon OW (1990) In vitro immunositumulation of rainbow trout (O. mykiss) spleen cells with levamisole. Dev Comp Immunol 14:231–237
Siwicki AK, Anderson DP, Rumsey GL (1994) Dietary intake of immunostimulants by rainbow trout affects nonspecific immunity and protection against furunculosis. Vet Immunol Immunopathol 41:125–139
Solem ST, Jørgensen JB, Robertsen B (1995) Stimulation of respiratory burst and phagocytic activity in Atlantic salmon (Salmo salar L.) macrophages by lipopolysaccharide. Fish Shellfish Immun 5:475–491
Sun L, Guo H, Zhu C, Ma Z, Zhang D (2014) Genetic polymorphism of breeding populations of golden pompano (Trachinotus ovatus). South China Fish Sci 2:67–71
Sun JN, Xie WT, Liu Y, Chun-Hou XU, Guangdong Ocean University (2015) Research advance of the marine red yeast. J Anhui Agric Sci 43(4):84–88
Tovar-Ramı́rez D, Zambonino-Infante J, Cahu C, Gatesoupe FJ, Vázquez-Juárez R (2004) Influence of dietary live yeast on European sea bass (Dicentrarchus labrax) larval development. Aquaculture 234:415–427
Turan F (2006) Improvement of growth performance in tilapia (Orepochrimis aureus Linnaeus) by supplementation of red clover Trifolium pratense in diets. Isr J Aquacult Bamidgeh 58:34–38
Turan F, Akyurt I (2005) Effects of red clover extract on growth performance and body composition of African catfish Clarias gariepinus (Burchell, 1822). Fish Sci 71:618–620
Verdrengh M, Jonsson IM, Holmdahl R, Tarkowski A (2003) Genistein as an anti-inflammatory agent. Inflamm Res 52:341–346
Verlhac V, Gabaudan J, Obach A, Schüep W, Hole R (1996) Influence of dietary glucan and vitamin C on nonspecific and specific immune responses of rainbow trout (Oncorhynchus mykiss). Aquaculture 143:123–133
Wang H, Li S, Yan B, Jiao Y, Wang Y (2011) Extraction of polysaccharide of oceanic red yeast and the study of it’s influence upon immunological activite enzymes of Charybdis japonica (A. Milne-Edwards). Microbiology 38(2):176–180
Wiseman H, O’Reilly JD, Adlercreutz H, Mallet AI, Bowey EA, Rowland IR, Sanders TA (2000) Isoflavone phytoestrogens consumed in soy decreases F(2) isoprostane concentrations and increase resistance of low density lipoproteins to oxidation in humans. Am J Clin Nutr 72:395–400
Xia L, Huang Y, Lu Y (2012) The diseases in Trachinotus ovatus culture and their research progress. Anhui Agric Sci Bull 18:140–150
Xia D, Yang K, Li Z, Yang Y, Wang Y, Wang J, Lin H (2013) Effects of Rhodotorula mucilaginosa on growth performance and immunity of Litopenaeus vannamei. Guangdong Agric Sci 14:133–137
Yamashita Y, Kawada S-Z, Nakano H (1990) Induction of mammalian topoisomerase II dependent DNA cleavage by nonintercalative flavonoids, genistein and orobol. Biochem Pharmacol 39:737–744
Yang S, Wu Z, Jian J, Zhang X (2010) Effect of marine red yeast Rhodosporidium paludigenum on growth and antioxidant competence of Litopenaeus vannamei. Aquaculture 309:62–65
Yin G, Jeney G, Racz T, Xu P, Jun X, Jeney Z (2006) Effect of two Chinese herbs (Astragalus radix and Scutellaria radix) on nonspecific immune response of tilapia, Oreochromis niloticus. Aquaculture 253:39–47
Yu Z, Xia D, Wu T (2006) Effects of daidzein on growth, hormone and physiobiochemical parameters levels in Oreochromis aureus. Chin J Vet Sci 26:183–185
Yu HH, Xue M, Han F, Wang J, Zheng Y, Wu X (2014) A comparative study: effect of several immunomodulators on growth performance, immunity and survival rate after bacterial challenge of Japanese seabass. Chin J Anim Nutr 26(8):1–11
Zhang Q, Tan B, Mai K, Zhang W, Ma H, Ai Q, Wang X, Li F (2011) Dietary administration of bacillus (B. licheniformis and B. subtilis) and isomaltooligosaccharide influences the intestinal microflora, immunological parameters and resistance against Vibrio alginolyticus in shrimp, Penaeus japonicus (decapoda: penaeidae). Aquac Res 42(7):943–952
Zhang R, Niu S, Yang Z, Zhang H (2013) Effects of different amount of Rhodotorula benthica in diet on the feeding and growth of Scophthalmus maximus L. J Heibei Nor Univ (Nat Sci ed) 37(6):618–621
Zhang Q, Yu H, Tong T, Tong W, Dong L, Xu M, Wang A (2014a) Dietary supplementation of Bacillus subtilis and fructooligosaccharide enhance the growth, nonspecific immunity of juvenile ovate pompano, Trachinotus ovatus and its disease resistance against Vibrio vulnificus. Fish Shellfish Immun 38:7–14
Zhang Y, Liu B, Ge X, Liu W, Xie J, Ren M, Cui Y, Xia S, Chen R, Zhou Q, Pan L, Yu Y (2014b) The influence of various feeding patterns of emodin on growth, nonspecific immune responses, and disease resistance to Aeromonas hydrophila in juvenile Wuchang bream (Megalobrama amblycephala). Fish Shellfish Immun 36:187–193
Zheng P, Ma Z, Guo H, Li Y, Jiang S (2014) Ontogenetic development of caudal skeletons in Trachinotus ovatus larvae. South China Fish Sci 5:45–50
Zhou C, Liu B, Ge X, Xie J, Xu P (2013) Effect of dietary carbohydrate on the growth performance, immune response, hepatic antioxidant abilities and heat shock protein 70 expression of Wuchang bream, Megalobrama amblycephala. J Appl Ichthyol 29:1348–1356
Zhou C, Ge X, Lin H, Liu J (2014) Effect of dietary carbohydrate on nonspecific immune response, hepatic antioxidative abilities and disease resistance of juvenile golden pompano (Trachinotus ovatus). Fish Shellfish Immun 41(2):183–190
Zhou C, Lin H, Ge X, Niu J, Wang J, Wang Y, Chen L, Huang Z, Yu W, Tan X (2015) The effects of dietary soybean isoflavones on growth, innate immune responses, hepatic antioxidant abilities and disease resistance of juvenile golden pompano Trachinotus ovatus. Fish Shellfish Immun 43(1):158–166
Zhou C, Lin H, Xia D, Yang K, Yang Y, Zhong H, Yu W (2016) Effect of dietary marine red yeast Rhodotorula mucilaginosa on the growth performance, and also nonspecific immune responses of juvenile golden pompano Trachinotus ovatus when challenged with Vibrio harveyi. Isr J Aquacult Bamidgeh 68:1–9
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2022 China Agriculture Press
About this chapter
Cite this chapter
Zhou, C., Lin, H., Huang, Z., Wang, J., Wang, Y., Yu, W. (2022). Functional Feed Additives to the Diet of Golden Pompano Trachinotus ovatus Juveniles. In: Ma, Z., Yu, G., Qin, J.G. (eds) Ontogenetic development of pompano Trachinotus ovatus. Springer, Singapore. https://doi.org/10.1007/978-981-19-1712-7_15
Download citation
DOI: https://doi.org/10.1007/978-981-19-1712-7_15
Published:
Publisher Name: Springer, Singapore
Print ISBN: 978-981-19-1711-0
Online ISBN: 978-981-19-1712-7
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)