Interrelationships between fish nutrition and health

AQUA-631033; No of Pages 7 Aquaculture xxx (2014) xxx–xxx

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Interrelationships between fish nutrition and health Camilo Pohlenz, Delbert M. Gatlin III ⁎ Department of Wildlife and Fisheries Sciences and Intercollegiate Faculty of Nutrition, Texas A&M University, College Station, TX 77840, USA

a r t i c l e

i n f o

Article history: Received 30 January 2014 Received in revised form 7 February 2014 Accepted 10 February 2014 Available online xxxx Keywords: Immunonutrition Fish health Feed additives Immune responses

a b s t r a c t An understanding of how to nurture and/or modulate the different components of the immune system is crucial for the prevention and control of diseases in animal husbandry. It is well established that proper nutrition is essential for maintenance of normal growth and health of all animals including aquatic species. As such, nutritious diets and appropriate feeding regimes play critical roles in intensive aquaculture. In recent years, heightened attention has been given to the development of nutritional strategies that positively influence immunity and disease resistance of cultured organisms to reduce disease-related economic losses. The availability of specific nutrients to immune cells plays a key role on how well those cells perform against a foreign invader. In this sense, research with several fish species has established that not only immunocompetence can be compromised by deficiencies of various nutrients, but that dietary supplementation of some nutrients in excess of minimum requirement levels for optimal growth has been shown to significantly enhance immune responses and disease resistance. For instance, findings from recent studies indicate an important role of key amino acids and their derivatives, like arginine and glutamine, or vitamins, such as vitamin C and E, in modulating immune responses such as increasing phagocytosis and pathogen killing capacity, as well as increasing antibody production and immunological memory. In addition, administration of non-nutritive compounds in the diet has become recognized as a viable means of enhancing immunocompetence of various aquatic species, mainly by the provision of cellular fractions such as β-glucans, complex oligosaccharides (mannanoligosaccharides, fructooligosaccharides or sulfated polysaccharides) or yeast and algae extracts. These compounds may act like Pathogen Associated Molecular Pattern (PAMP) molecules, interacting with the innate immune system through their Pattern Recognition Receptors (PRRs) and increasing their capability for detecting and recognizing potential pathogens and readily triggering immune responses. This article will review the broad range of dietary constituents which have been shown to affect immunocompetence and health of aquatic species and how they may influence components of the immune system. Further advancements in nutritional modulation of the immune response hold promise as an effective and relatively inexpensive alternative in combating diseases in aquaculture. © 2014 Elsevier B.V. All rights reserved.

1. Introduction Aquaculture has become a major source of animal protein for human consumption and trends show it will be of even greater importance for future generations, as fish farming has seen an annual growth higher than other animal-production industries for the last several decades (FAO, 2012). Although diseases are natural events in all animal groups, the intensification of culture technologies has brought about an important increase in the emergence, dispersion and outbreak of infectious diseases, which have placed them as one of the main growthconstricting factors in the industry (Costello, 2009; Pridgeon and Klesius, 2013; Zagmutt et al., 2013). Therefore, the study of the defense mechanisms of cultured animals and the understanding of how to

⁎ Corresponding author at: 216 Heep Laboratory Building, 2258 TAMUS, College Station, TX 77843, USA. Tel.: +1 979 847 9333; fax: +1 979 845 4096. E-mail address: [email protected] (D.M. Gatlin).

nurture and modulate the different components of the immune system are crucial for the prevention, treatment and/or control of fish diseases, hence for guaranteeing the sustainability and future of this important endeavor. Proper nutrition is critical not only to achieve optimal growth rates but also to maintain the health of cultured fish (Sealey and Gatlin, 2001). For a number of years, the fish nutrition field focused mainly on establishing the minimum nutrient requirements for normal growth of different fish species (NRC, 2011). However, nowadays, the role of nutrition on health management through the modulation of immune response and disease resistance has turned into a research area of top priority with aims to lessen the dependence on chemotherapeutics and reduce disease-related economic losses (Kiron, 2012; Oliva-Teles, 2012). This has led to the emergence of the new discipline termed “immunonutrition”, which may be defined as the study of enhancing immunological functions by means of using specific nutrients and/or other dietary compounds — which could be higher than those levels needed for optimal growth.

http://dx.doi.org/10.1016/j.aquaculture.2014.02.008 0044-8486/© 2014 Elsevier B.V. All rights reserved.

Please cite this article as: Pohlenz, C., Gatlin, D.M., Interrelationships between fish nutrition and health, Aquaculture (2014), http://dx.doi.org/ 10.1016/j.aquaculture.2014.02.008

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The aim of the present review is to give a clearer picture of the interrelationships between fish nutrition and health. We do not intend to cite all studies in which additives/supplements have been tested in aquaculture, for this topic there are good broad or specific reviews published that the reader may consult (e.g. Dalmo and Bogwald, 2008; Kiron, 2012; Meena et al., 2012; Oliva-Teles, 2012; Torrecillas et al., in press). Rather, we intend to focus on nutrients or additive groups within the context of the fish's immune response, and their potential to enhance specific functions for better health and protection from disease-causing organisms.

2. Fish immune system Teleost fish possess an immune system very similar to the one found in higher vertebrates, but evolutionarily less developed and even more less understood (Magnadottir, 2006; Sunyer, 2013). The immune system constitutes a highly complex defense mechanism that utilizes a broad range of individual components. It is composed of two major branches, the innate and the adaptive immune systems. During an immune response, both branches orchestrate an extremely close communication, fundamental for successful protection from and eradication of pathogens (Tort et al., 2003). The immune response is a process that involves multiple cellular and humoral components of both immune branches (Table 1), including dendritic cells, neutrophils, macrophages, lymphocytes, cytokines, immunoglobulins, the complement system, among others (Bassity and Clark, 2012; Rauta et al., 2012; Secombes, 2008). However, an important characteristic inherent to fish, is that because of its evolutionary development, the immune system tends to rely more on its innate response for the clearance of an invading microorganism (Magnadottir, 2006), and with this is mind, the macrophage could be considered the most important immune cell, as it not only produces key cytokines, but it is also the chief cell in charge of phagocytosis and destruction of a pathogen after initial recognition in naïve or pre-exposed animals (Bayne and Gerwick, 2001; Shoemaker et al., 2001; Zhu et al., 2013). Although recently, dendritic cells – the most complete antigen presenting cell in higher vertebrates (Banchereau and Steinman, 1998) – has been described in fish. These cells' complete functional characterization during a fish's immune response is yet to be elucidated (Bassity and Clark, 2012). Noteworthy is that due to the great diversity of fish being cultured, substantial differences might be found among some important components of the immune system. For instance, some species will express immunoglobulins (Ig)D, IgM and IgT/Z (Zhang et al., 2011) and others only IgD and IgM (Bengtén et al., 2006); in addition the recombination of these different immunoglobulin isotypes can vary among species (Mashoof et al., 2014). Although these differences could have an impact on specific interventions such as vaccine development, the overall immune response is generally similar among fish species.

3. Immune responses and metabolism There is a constant relation between a pathogen (true or opportunistic) trying to invade and a host limiting the invasion. An imbalance among components of the host–pathogen-environment will create ideal conditions for the onset of a disease (Bowden, 2008), triggering a defense response (Fig. 1). The complexity and specificity of the response means that the limits or boundaries among participants are poorly defined. For this review, the immune response may be divided into three stages: 1) Detection and recognition of the pathogen, 2) Phagocytosis, pathogen killing and antigen presentation, and 3) Immune expansion and creation of immunological memory. The initial acute response against an infection (stages 1 and 2), characterized by a hypermetabolic stage (Lochmiller and Deerenberg, 2000; Wang et al., 2012), is probably the most important for the survival of an animal, because competence of the innate immune system, mainly from phagocytes, is required to detect and activate a generalized response against the invasion of a pathogen (Bayne and Gerwick, 2001; Magnadottir, 2006). The disruption of homeostasis and the establishment of a defense state and/or disease is a costly metabolic process for the host. Infection promotes a complete shift in metabolic priorities towards nutrient needs associated with the immune system (Lochmiller and Deerenberg, 2000). In quiescent immune cells, the utilization of nutrients happens at basal levels, merely for cellular maintenance. However, during an immune challenge, the utilization of key nutrients dramatically increases, especially, there is an important demand for amino acids (Kiron, 2012; Uribe et al., 2011). For instance, in vivo reports suggest important usage of glutamine in ill fish, represented by the rapid decrease in plasma levels of this amino acid (Walker et al., 1996). On the other hand, in vitro studies point out that an activated macrophage consumes energy at a rate comparable to that used by a cardiac muscle cell at maximum capacity (Newsholme and Newsholme, 1989); even more, although the profile of the amino acids used will vary depending on if there is phagocytic or lymphocytic response, arginine and glutamine will play a key role for the overall performance of these cells in fish (Pohlenz et al., 2012a). Besides the possible onset of an anorexic state after an initial infection, a diseased state will activate the mobilization of protein and energy from reserves not only to support the initial acute phase of the immune response, but also to sustain it until the resolution of the problem (Sealey and Gatlin, 2001). Hence, a typical result during this period is a negative nitrogen balance, which could vary depending on the severity of the infection (Lochmiller and Deerenberg, 2000; Lönnström et al., 2001; Midtlyng and Lillehaug, 1998); such condition may be of great importance in fish culture due to their natural history of requiring high dietary levels of protein (NRC, 2011). Under this scenario, the adequate availability of specific nutrients plays a fundamental role in the activation and performance of the immune system against an invading pathogen.

Table 1 Main effector components of fish immune responses. Immune system branch

Cellular components

Humoral components

Specificity

Innate

Physical barriers (mucosae)

Complement system Lysozyme Antimicrobial peptides Pentraxins Antiproteases Natural Igsb Ig M Ig D Ig Z/Tc

Pathogen associated molecular patterns (PAMPs)

Macrophages Neutrophils Dendritic cellsa Adaptative

a b c

B lymphocytes T lymphocytes

Antigen-specific epitopes

Role during an immune response is not totally elucidated in fish. Igs, immunoglobulins. Not found in all fish species.

Please cite this article as: Pohlenz, C., Gatlin, D.M., Interrelationships between fish nutrition and health, Aquaculture (2014), http://dx.doi.org/ 10.1016/j.aquaculture.2014.02.008

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Pathogen detection and recognition Fish:Pathogen encounter PRRs:PAMPs*

Stage 1

Innate Response Phagocytosis Pathogen killing Cytokine secretion

Success

Failure

Limitationof infection and disease

Disease and death

Stage 2

Specific Response Initiation and Instruction Antigen presentation Molecular co-stimulation Cellular expansion

Humoral Response

Cellular Response

B lymphocyte activation Synthesis of specific Igs**

T-helper lymphocytes T-cytotoxic lymphocytes

Stage 3

Adaptive immunity Immunological memory Memory B and T lymphocytes Protection vs. future infections Survival

Fig. 1. General scheme of the three stages of a fish immune response. *PRRs: pathogen recognition receptors; PAMPs: pathogen associated molecular patterns. **Igs: immunoglobulins, secreted by plasma cells, which are derived from activated B-lymphocytes. Modified from Shoemaker et al. (2001).

4. Interrelationships between nutrition and the immune system

4.1. Detection and recognition of the pathogen

Nutrition is a complex and multidimensional factor that will interrelate with the immune system, hence fish health, through a broad array of direct or indirect mechanisms (Kiron, 2012; Oliva-Teles, 2012; Sealey and Gatlin, 2001). Together with the formerly mentioned fact of a vast range of fish species being cultured, the lack of a full understanding of the teleost immune system represents a significant limitation on studying the interrelationships between these two components and therefore on entirely comprehending immunonutrition (Ponton et al., 2013). Studies to date using a given nutrient as an immune system modulator have shown different results among species and even within species (Dalmo and Bogwald, 2008). For instance, contrary to the role of glutamine in mammalian leukocytes, which is consistent across species (Crawford and Cohen, 1985), in fish, the role of glutamine in leukocyte metabolism is complex and appears to be species specific. Conflicting reports document glutamine-dependent and -independent responses of proliferating cultured lymphocytes (Ganassin et al., 1998; McBride and Keast, 1997; Pohlenz et al., 2012a; Rosenberg-Wiser and Avtalion, 1982). Exogenous sources of nutrients should supply minimum levels to meet requirements for normal immune system performance and to protect/restore tissues from collateral damage. However, in certain situations, providing additional nutrients at levels above those required for normal fish maintenance and growth, or even provision of some compounds that are not required at all, may sustain and/or enhance one or more functions of the immune system, hence increasing its efficacy and protection capacity against an invading pathogen (Kiron, 2012; Sealey and Gatlin, 2001). In this sense, there are various nutritional tools that may be implemented to accomplish this objective of enhancing the immune system. Following, we present results obtained with some of the most promising feed additives/supplement groups for functional aquafeeds targeted to the various components of the fish immune system within the context of each response stage.

The immune system recognizes and responds to a broad variety of pathogens, mainly through warning signals named pathogen associated molecular patterns (PAMPs) detected by cellular or humoral pattern recognition receptors/proteins (PRRs) (Abbas et al., 2012; Tort et al., 2003). The encounter with PAMPs will trigger a cascade of cytokine secretion (Roher et al., 2011) with aims to activate a general immune response, including recruiting phagocytes and lymphocytes via chemotaxis, and the activation or secretion of cellular and humoral antimicrobial defense mechanisms, such as the complement system, lysozyme, antimicrobial peptides, etc. (Abbas et al., 2012; Bayne and Gerwick, 2001; Reyes-Cerpa et al., 2012). Providing specific additives to the diet (most of them nondigestible), such as mixed or purified extracts from microbial or vegetable structural components, can take advantage of these warning signals because they may act as PAMPs or PAMP-like molecules and may increase non-specific protection (Fierro-Castro et al., 2012), which has proven to efficiently promote early functions of the immune response of fish (Table 2). Mannanoligosaccharides, β-glucans, sulfated polysaccharides and/or nucleotides are some of the most common additives tested in aquafeeds and various reports indicate they may promote the expression and/or secretion of important pro-inflammatory and chemotactic cytokines, such as Interleukin (IL)-1β, IL-6, IL-8, tumor necrosis factor (TNF)-α and γ-interferon (IFN), along with up-regulation of important PRRs such as toll-like receptor (TLR)3, TLR5 and TLR9 in different fish species.

4.2. Pathogen phagocytosis/killing and antigen presentation Phagocytosis is the internalization of a pathogen with the purpose of its destruction, and afterwards, under the correct conditions, to present its antigens to lymphocytes. This process immediately follows the

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Table 2 Nutrients/additives of proven efficacy for the enhancement of detection and recognition of the pathogen (stage 1). Nutrient/additive

Species

Alginic acid

Common carp, Cyprinus carpio Rainbow trout, Oncorhynchus mykiss Atlantic cod, Gadus morhua Common carp Pacific flounder, Paralichthys olivaceus Rainbow trout

Effect

Reference

Increased leukocyte migratory capacity Up-regulation of IL-1β, IL-8, TNF- α after vaccination β-Glucan Up-regulation of IL-1β after bacterial challenge Up-regulation of IL-1β Increased leukocyte migratory capacity Primed the induction of TNF-α2 expression, Up-regulation of IL-1β, IL-6 and C3 protein Snakehead, Channa striata Increased leukocyte count and total natural antibodies Fructoligosaccharides Caspian roach, Rutilus rutilus Increased total natural antibodies Stellate sturgeon, Acipenser stellatus Increased leukocyte count Triangular bream, Megalobrama terminalis Increased leukocyte count and total natural antibodies Lipopolysaccharide Rainbow trout Up-regulation of IL-1β, IL-8, TNF-α2, TLR-5 and TLR-9 Mannanoligosaccharides Atlantic cod Up-regulation of IL-1β, IL-8 after bacterial challenge Common carp Increased lymphocyte % Giant sturgeon, Huso huso Increased lymphocyte % Labeo rohita Increased leukocyte count Rainbow trout Increased natural antibody titers Snakehead Increased natural plasma antibodies and leukocyte count after challenge with Aeromonas hydrophila Marine algae extract Gilthead seabream, Sparus aurata Up-regulation of IL-1β, IL8 and β-defensin Senegalese sole, Solea senegalensis Increased leukocyte migratory capacity Nucleotides Turbot, Psetta maxima Up-regulation of IL-1β in kidney Rainbow trout Increased plasma natural antibodies Pathogen extract Turbot Increased leukocyte migratory capacity, up-regulation of IL-1β, TNF-α Peptidoglycans Pacific flounder Increased leukocyte migratory capacity Polyinosinic polycytidylic acid Rainbow trout Up-regulation of IL-1β, IL-8, TNF- α1/α2, Mx-1, TLR-3, TLR-5 and TLR-9 Yeast extract Labeo rohita Increased leukocyte count Rainbow trout Increased total leukocyte, neutrophil and monocyte count Snakehead Increased leukocyte count and total natural antibodies

pathogen recognition by a macrophage or neutrophil, and possibly by a dendritic cell (Shoemaker et al., 2001). Phagocytes respond with an important set of killing tools including superoxide anion, hydrogen peroxide, nitric oxide, lysozyme, and other lytic enzymes (Magnadottir, 2006; Secombes and Fletcher, 1992; Tort et al., 2003; Uribe et al., 2011). Supplementing diets with nutrients that could be metabolically used by phagocytes has been an area of interest for enhancing this stage of the immune response (Table 3). For instance, certain amino acids play a crucial role in these immunological processes. Glutamine may provide metabolic fuel to support reaction kinetics (Crawford and Cohen, 1985; Newsholme and Newsholme, 1989). Similarly, arginine is the unique precursor of nitric oxide in activated macrophages (Buentello and Gatlin, 1999; Neumann et al., 1995; Wu and Morris, 1998), and the latter is a potent microbicidal compound and potent modulator of the eukaryotic cytoskeleton (Kasprowicz et al., 2009; Moffat et al., 1996). On the other hand, another possible nutrition tool to enhance functions during this response stage is using nutrients that might modify the physical (fluidity) nature of the plasma membrane and/or alter the expression of receptors involved in these cellular processes, which could enhance the synthesis and secretion of antimicrobial compounds by modulating the protein kinase C pathway (Balfry and Higgs, 2001; Calder, 1998; Calder et al., 1990) or enhancing the synthesis of molecules that could be closely related to antigen processing and presentation such as phospholipase A2 (PA2), prostaglandin E2 (PE2) or myeloid differentiation factor (MyD) 88 (Horsnell et al., 2013; Paduraru et al., 2013; Yen et al., 2011). Supplementing polyunsaturated fatty acids n−3 or n−6, or antioxidant compounds such as vitamin C and E has proven to be effective in this regard (Table 3). It is important to state that even if the phagocytic activity is enhanced by a nutrient/ additive, that does not necessarily correlate to the killing capacity of the cell. Therefore, it is crucial to evaluate both parameters in order to have a better assessment of an immunomodulation effect (Pohlenz et al., 2012a).

Fujiki and Yano (1997) Gioacchini et al. (2008) Lokesh et al. (2012) Selvaraj et al. (2005) Galindo-Villegas et al. (2006) Iliev et al. (2005); Lovoll et al. (2007) Talpur et al. (in press) Soleimani et al. (2012) Akrami et al. (2013) Zhang et al. (2013) Fierro-Castro et al. (2013); Iliev et al. (2005) Lokesh et al. (2012) Akrami et al. (2012) Razeghi et al. (2012) Andrews et al. (2009) Staykov et al. (2007) Talpur et al. (in press) Reyes-Becerril et al. (2013) Diaz-Rosales et al. (2005) Low et al. (2003) Tahmasebi-Kohyani et al. (2011) Leiro et al. (2006) Galindo-Villegas et al. (2006) Fierro-Castro et al. (2013) Andrews et al. (2009) Tukmechi et al. (2011) Talpur et al. (in press)

4.3. Immune expansion and memory creation The ability to develop memory is a fundamental characteristic of the immune system. The successful destruction and processing of an invading pathogen should result in the induction of a strong and lasting response of memory lymphocytes. Because the first contact with an antigen usually induces relatively short-lived effector cells (Van Muiswinkel and Nakao, 2014), the way by which clonal expansion of T lymphocytes is induced and the dimension of the effector cell population generated is key for this process (Secombes, 2008). The capacity to create immunological memory correlates with the expansion of naïve lymphocytes after antigen presentation, cytokine stimulation and molecular co-stimulation at the membrane level (Secombes, 2008; Uribe et al., 2011). Although the synthesis of specific immunoglobulins is an important component of the adaptive immune system, in fish, the correlates of protection are minimal unless there are high circulating titers of these antibodies (Thune et al., 1997). As such, good activation and expansion of B lymphocytes are required. Similar to the previous stage, the supplementation of nutrients that could be used as energy sources, precursors for or used for cellular proliferation or may influence cellular membrane integrity are among the top immunomodulating candidates (Table 4). As this stage requires high proliferation of lymphocytes for appropriate immune expansion, lymphoid tissue may have limited capacity for de novo synthesis of important compounds, such as amino acids, nucleotides and their derivatives, depending to a great extent on exogenous nutrient supply (Navarro et al., 1996). Providing an external source of these nutrients may increase the expression of the recombinant activating gene (RAG)-1 (Low et al., 2003), crucial for lymphocyte maturation (Hansen and Kaattari, 1995), as well as the up-regulation of IgM expression in B lymphocytes residing in the spleen (Low et al., 2003) or kidney (ReyesBecerril et al., 2011) which are essential for antibody secretion and robust development of adaptive immunity.

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Table 3 Nutrients/additives of proven efficacy for the enhancement of pathogen phagocytosis and killing and antigen presentation (stage 2). Nutrient/additive

Species

Effect

Reference

Arachidonic acid

Yellow croaker, Larimichthys polyactis Channel catfish, Ictalurus punctatus

Increased phagocytic activity and production of sPLA2 and PGE2

Li et al. (2012)

Increased phagocytic activity, phagocytic index, macrophage production of nitric oxide, bactericidal capacity Increased macrophage superoxide anion production

Buentello et al. (2007); Buentello and Gatlin (1999); Pohlenz et al. (2012a) Cheng et al. (2012)

Increased phagocytic index, macrophage superoxide anion production Increased neutrophil respiratory burst and macrophage superoxide anion production Increased macrophage superoxide anion and nitric oxide production, upregulation of HIF-I, MIP1-α and HAMP-1 Increased phagocytic index and capacity, macrophage superoxide anion production Increased neutrophil respiratory burst, macrophage bactericidal capacity

Galindo-Villegas et al. (2006) Cheng et al. (2011)

Arginine

Hybrid striped bass, Morone chrysops × M. saxatilis Pacific flounder Red drum, Sciaenops ocellatus Senegalese sole Astaxanthin

Pacific flounder

β-Hydroxy-βmethylbutyrate Glutamine

Rainbow trout Channel catfish Hybrid striped bass Red drum

Linoleic acid n−3 HUFA Polyamines Vitamin C

Vitamin E

Yellow croaker Pacific flounder Gilthead seabream Atlantic salmon, Salmo salar Gilthead seabream Hybrid striped bass Pacific flounder Rainbow trout Turbot Yellow croaker Gilthead seabream Hybrid striped bass Pacific flounder Rainbow trout Yellow croaker

Increased phagocytic index Increased neutrophil respiratory burst and macrophage superoxide anion production Increased neutrophil respiratory burst and macrophage superoxide anion production Increased phagocytic activity, macrophage superoxide anion production Increased macrophage superoxide anion production, complement activity Increased phagocytic activity, up-regulation of MHC-I, CD8, Hep and C3 Increased leukocyte phagocytosis activity Increased phagocytic index and activity, macrophage superoxide anion production, complement activity Increased macrophage superoxide anion production Increased macrophage superoxide anion production Increase natural cytotoxicity and leukocyte phagocytosis activity Increased phagocytic index Increased phagocytosis activity and superoxide anion production Increased phagocytic index and activity, and complement activity Increased macrophage superoxide anion production Increased macrophage superoxide anion production Increased bactericidal activity Increased macrophage superoxide anion production, up-regulation of MyD88

5. Conclusions The aim of the present review was to give insights on how nutrition interrelates with health within the context of the fish's immune responses, and to present a summary of data with promising compounds

Costas et al. (2011) Galindo-Villegas et al. (2006) Siwicki et al. (2003) Pohlenz et al. (2012a) Cheng et al. (2012) Cheng et al. (2011) Zuo et al. (2013) Wang et al. (2006) Reyes-Becerril et al. (2011) Verlhac and Gabaudan (1994) Ortuño et al. (2001); Ortuño et al. (1999) Sealey and Gatlin (2002a) Galindo-Villegas et al. (2006) Verlhac and Gabaudan (1994) Roberts et al. (1995) Ai et al. (2006) Ortuño et al. (2001); Ortuño et al. (2000) Sealey and Gatlin (2002b) Galindo-Villegas et al. (2006); Wang et al. (2006) Kiron et al. (1995) Zuo et al. (2012)

that might be used for making functional aquafeeds to be used under specific situations. Although it is important to state, that even if a specific compound will enhance early stages of the immune response, it does not mean that it may have positive effects on the final outcome of the integrated immune response. Nutritional modulation of the immune

Table 4 Nutrients/additives of proven efficacy for the enhancement of expansion and creation of immunological memory (stage 3). Nutrient/additive

Species

Effect

Reference

Arginine

Channel catfish

β-carotene

Pohlenz et al. (2012b); Pohlenz et al. (2012a) Tachibana et al. (1997)

Increased non-specific proliferation of lymphocytes

Tachibana et al. (1997)

β-Hydroxy-β-methylbutyrate

Japanese parrotfish, Oplegnathus fasciatus Spotted parrotfish, Oplegnathus punctatus Rainbow trout

Increased T and B lymphocyte proliferation, memory lymphocytes and antibody titer against Edwardsiella ictaluri Increased non-specific proliferation of T lymphocytes

Siwicki et al. (2003)

Glutamine

Channel catfish

n−3 HUFA Nucleotides

Rainbow trout Atlantic salmon Channel catfish Hybrid tilapia, Oreochromis niloticus × O. aureus Turbot Gilthead seabream Atlantic salmon Milkfish, Chanos chanos Rainbow trout

Increased non-specific T and B lymphocyte proliferation and total plasma antibody titers Increased non-specific T and B lymphocyte proliferation, tissue-residing B lymphocytes, memory specific lymphocytes and plasma antibody titer against E. ictaluri Increased antibody titers against A. salmonicida Increased plasma antibody titers against A. salmonicida Increased antibody titers against E. ictaluri Increased plasma antibody titers against A. hydrophila, non-specific lymphocyte proliferation Up-regulation of IgM and RAG-1 Up-regulation of IgM Increased proliferation of T lymphocytes, higher plasma antibody titers against Yersinia ruckeri Increased plasma antibody titers against Vibrio vulnificus, enhanced memory factor Increased proliferation of T lymphocytes

Milkfish

Increased plasma antibody titers against Vibrio vulnificus, enhanced memory factor

Polyamines Vitamin C

Vitamin E

Pohlenz et al. (2012b); Pohlenz et al. (2012a) Kiron et al. (1995) Burrells et al. (2001) Welker et al. (2011) Ramadan et al. (1994) Low et al. (2003) Reyes-Becerril et al. (2011) Erdal et al. (1991); Verlhac and Gabaudan (1994) Azad et al. (2007) Verlhac and Gabaudan (1994) Azad et al. (2007)

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system continues to be a potentially powerful tool to improve the health and growth of cultured fish, hence to improve production yield. However, because of the great diversity of fish being cultured along with a lack of full understanding regarding the fish's immune system, immunonutrition is still not fully developed, but warrants a vast future research in this field. In particular, there is an immense need to finetune dosing of various additives, feeding regimes, supplementation times, etc. so that immunonutrition can become more effective and used efficiently to benefit the industry. References Abbas, A.K., Lichtman, A.H., Pillai, S., 2012. Cellular and Molecular Immunology, Seventh ed. Elsevier Saunders, Philadelphia, USA. Ai, Q., Mai, K., Tan, B., Xu, W., Zhang, W., Ma, H., Liufu, Z., 2006. Effects of dietary vitamin C on survival, growth, and immunity of large yellow croaker, Pseudosciaena crocea. Aquaculture 261, 327–336. 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