• aquaculture;
  • fish meal;
  • fish oil;
  • nutrition;
  • sub-optimal temperature


  1. Top of page
  2. Abstract
  3. Introduction
  4. Cold water fish species (≤20°C)
  5. Temperate fish species (20–25°C)
  6. Warm water fish species (≥25°C)
  7. Conclusions
  8. Acknowledgement
  9. References

Temperature is one of the most important physical factors influencing fish growth. Under optimal temperatures, food energy partitioned into fish growth can be maximized. However, when a marine carnivorous species is cultured in an environment where temperature falls outside the optimal range of a fish, growth will be affected. The nutrient–environment interaction is important for optimizing a fish’s nutritional requirements throughout the grow-out period. The most current global issue for the aquaculture industry is the inclusion of alternative ingredients into formulated diets to produce a sustainable seafood product. This requires the substitution of fish meal and fish oil with alternative ingredients from plant and terrestrial animal sources. This review discusses the changes in nutritional requirements (protein, lipid and energy) and physiology of some commonly cultured marine fishes as a consequence of seasonal changes in temperature during the grow-out period. This review also discusses the effects of replacing fish meal and fish oil with alternative protein and lipid sources on the nutritional–environmental interactions of fish performance at different temperatures.


  1. Top of page
  2. Abstract
  3. Introduction
  4. Cold water fish species (≤20°C)
  5. Temperate fish species (20–25°C)
  6. Warm water fish species (≥25°C)
  7. Conclusions
  8. Acknowledgement
  9. References

In 2008, total aquaculture production reached 52.5 million metric tonnes (MMT), which was worth over US$98.4 billion (FAO 2010). From 1970 to 2008 the production from aquaculture increased at an annual average rate of 8.3% to keep up with the demand of the steadily increasing human population and static growth of catches from wild fisheries. By 2012, it is estimated that aquaculture will meet more than 50% of the global food fish consumption (FAO 2010). In 2008, 3.4% of the total aquaculture production (US$6.6 billion) came from marine fish, and although this was much lower than the 41.2% from freshwater fish production (US$40.5 billion), marine fish are higher in value than most freshwater species (FAO 2010). Therefore, the culture of high value marine finfish species is desirable yet often more challenging. Globally, aquaculture is practised mostly in tropical and subtropical regions, particularly in Asia’s inland freshwater regions (FAO 2010). It is possible that due to global warming, temperatures and sea levels may continue to rise over the next few decades (Wigley 2005). This will affect current salinity and pH levels and temperatures that may exceed the threshold limits for some currently farmed finfish species (Brander 2007). This will require the future adaptation of established aquaculture practices and species that are more tolerable to the changing environments.

In the short term, the expansion and diversity of globally cultured fish species continue to rise and require fish to be grown-out in locations with temperature showing distinct seasonal patterns that may not be physiologically suitable for some species currently used in aquaculture. According to the conceptual model on fish biogenetics (Jobling 1994) and other published literature, temperature is the single most important physical factor to influence growth (Jobling 1997), activity and feed intake (Qin et al. 1997; Peres & Oliva-Teles 1999; Ibarz et al. 2007), digestion (Kofuji et al. 2006; Pérez-Casanova et al. 2009; Bermudes et al. 2010), enzyme activity (Miegel et al. 2010) and ultimately metabolism (Katersky and Carter 2007a,b, Table 1). The optimal temperature for growth reflects the temperature at which energy partitioned into growth is maximal (Brett 1979). In the wild, fish species naturally seek out a temperature preferenda close to their optimal temperature for growth (Zinichev & Zotin 1987) or near the optimal temperature for growth efficiency (Larsson 2005). However, cultured fish species are subjected to their imposed surrounding environmental conditions where water temperature can vary considerably over seasons. The effect of temperature fluctuations can influence the level of basal metabolism rather significantly (De Silva & Anderson 1995). Therefore, temperature becomes important to understand the interaction between the nutritional and physiological requirements of individual cultured fish species and their limitations to attain optimal growth and production under these conditions.

Table 1. Selected studies on physiological changes to cold, temperate, and warm water marine species when cultured at sub-optimal temperatures
Fish speciesTemperature (°C)Dietary typeBiological effectsReferences
  1. COM, commercial diet; CP, crude protein; CL, crude lipid; FA, fatty acids; SFA, saturated fatty acids; MUFA, monounsaturated fatty acids; PUFA, polyunsaturated fatty acids; EPA, eicosapentaenoic acid; DHA, docosahexaenoic acid: ADC, apparent digestibility coefficient.

Cold water
 Atlantic salmon (Salmo salar)15 vs. 19COM; values n/aReducing EPA and DHA in tissue at 19°CMiller et al. (2006)
 Atlantic cod (Gadus morhua) and Haddock (Melanogrammus  aeglefinus)2, 6, 1142% CP, 16% CL vs. 55% CP, 11% CLReducing growth and feed intake and increasing gastric empty time as temperature increasesPérez-Casanova et al. (2009)
Temperate water
 Yellowtail kingfish (Seriola lalandi)12 vs. 2063% CP, 16% CLIncreasing protease activity in posterior intestine as temperature increasesMiegel et al. (2010)
 Japanese yellowtail (Seriola quinqueradiata)15–1838% CP, CL n/aSGR, weight gain, FI and protein ADC increased with synthetic stimulant vs. FM control diet at sub-optimal temperaturesKofuji et al. (2006)
 Gilthead seabream (Sparus aurata)8, 12, 14COM 47% CP, 21% CLLiver size increased with pale colour and lowed enzyme activity as temperature decreased. Symptoms improved after 20 days Ibarz et al. (2007)
 8–18COM 47% CP, 21% CLFeeding ceased <13°C; as temperature dropped, muscle PUFA increased, but liver lipids increased; high n-3 FA caused a large, friable, yellowish liver Ibarz et al. (2005)
 8, 12, 14FastedAt 8°C plasma proteins, ions and liver hepatocytes increased compared with higher temperaturesSala-Rabanal et al. (2003)
 European seabass (Dicentrachus labrax)12–15 vs. 17–20COM; values n/aAs temperature dropped, SFA and MUFA dropped, but PUFA increased in liver and muscle tissueDelgado et al. (1994)
 18 vs. 2536, 42, 48, 56% CP, 13% CLAs temperature increased, growth and feed intake dropped. 48% and 56% CP diets increased growth and feed intake regardless of temperaturePeres and Oliva-Teles (1999)
 13, 16, 19, 22, 25, 29COM 44% CP, 22.5% CLGrowth increased up to 25°C; feed intake dropped with temperature; feed efficiency peaked at 24°C Person-Le Ruyet et al. (2004a)
Warm water
 Asian seabass (Lates calcarifer)27, 33, 36, 3950% CP, 18% CLGrowth and feed intake optimal between 27°C and 36°C, but dropped at 39°CKatersky and Carter (2005)
 21, 24, 27, 30, 3350% CP, 19% CLWeight gain at 27, 30 and 33°C. Feed intake at 21°C was 3 times lower than at 33°C; body protein was lower at 24°C than at 33°CKatersky and Carter (2007a,b)
 23, 26, 29, 32, 35, 3853% CP, 18% CLOptimal growth and feed efficiency occurred between 26°C and 35°C. Energy ADC increased with temperatureBermudes et al. (2010)

Metabolism is the basic catabolic and anabolic reactions occurring within an organism resulting in nutrients being used for energy or growth (De Silva & Anderson 1995). The three major nutrients required by fish in aquafeeds are proteins, lipids and carbohydrates. Protein consists of large molecules called amino acids, which are the required metabolic compounds used as either a major energy source or for protein synthesis. Lipids are digested in the gut, releasing their fundamental fatty acids that are absorbed and then resynthesized back into lipid and circulated within the blood stream. When required by the organism the lipid is again catabolized into its constituent fatty acids, which can then be used for the synthesis of membranes or further broken down for energy purposes. Carbohydrates are complex molecules and the most common forms are either starch or cellulose. Starch is catabolized into glucose, which is then further broken down into energy, whereas cellulose cannot be digested by fish (De Silva & Anderson 1995).

Energy requirements for fish are dependent on a range of factors such as fish size, species, feeding preferences and environmental conditions. Fish have a low energy requirement compared with other terrestrial animals for the following reasons: (i) fish do not need to maintain internal body temperature (poikilothermic), (ii) fish live in water and have a swim bladder to adjust body buoyancy so that fish expend less energy to maintain body station in the water column (Goodsell et al. 1996; Trotter et al. 2001), and (iii) fish have a lower energetic expenditure for the detoxification and removal of ammonia (the end product of protein catabolism) prior to excretion (Brett & Groves 1979). In general, marine carnivorous fish species have the ability to utilize the energy from dietary protein and lipid more effectively than dietary carbohydrate (CHO) in comparison with omnivorous species (Shimeno et al. 1996). The reduced ability to utilize CHO has been related to lower amylase activity, CHO metabolism and insulin response in some marine species (Vegara & Jauncey 1993; van Barneveld et al. 1997). However, the inclusion of increasing non-protein energy sources (CHO and lipid) into diets is desirable as they have the ability to spare dietary protein (Shiau & Lan 1996) by reducing the catabolism of protein for energy which improves protein retention and ultimately growth (Lupatsch et al. 2001; Halver & Hardy 2002).

It is important in fish nutrition to have a diet balanced for protein and energy to achieve an appropriate protein: energy ratio (i.e. P:E ratio). The P:E requirement varies among fish species, particularly between cold water and warm water fish. Cold water fish have the ability to utilize higher levels of dietary lipid for energy, thus requiring a lower dietary P:E level than temperate or warm water species. For instance, Atlantic salmon (Salmo salar, Linnaeus 1758) <2.5 kg require a P:E ratio of 19 g crude protein (CP) MJ−1 gross energy (GE), and fish >2.5 kg require 16–17 g CP MJ−1 GE (Storebakken 2002), whereas grow-out size (150–400 g) warm water, humpback grouper (Cromileptes altivelis, Valenciennes, 1828) can require 25–26 g CP MJ−1 GE in the diet (Rachmansyah et al. 2005).

Protein constitutes 65–75% of the dry matter in fish tissues, therefore out of the three major nutrients it is the more essential nutrient in fish nutrition (Wilson 2002). Most cultured fish species require 30–55% crude protein (CP) in the diet, which provides a suite of essential and unessential amino acids required for cell maintenance, growth, development and health of fish (Hepher 1988; NRC 2011). Fish meal (FM) was traditionally the main protein ingredient in fish feeds (NRC 2011). This is due to its excellent palatability, balanced amino acid profile and good digestibility (Alexis & Nengas 2001). Fish meal is usually sourced from small, bony fish species that are not generally used for human consumption, including herring, menhaden, capelin, anchovy, pilchard, sardines and mackerel (Halver & Hardy 2002). Catches of these fish species specifically for reduction into FM and fish oil (FO) have been declining during recent years, but global FM production has remained static since the late 1980s apart from El Niño years (FAO 2010). One of the reasons is due to increased production of offal from the fish processing industry into FM (Jackson 2010). The increase in global aquaculture production has escalated pressures on the demand for FM in aquaculture feeds within the past decade (De Silva & Anderson 1995; Barlow 2000; Watanabe 2002). This demand has increased the price of FM to levels that are too expensive to keep using it as the main protein ingredient in aquaculture feeds as the cost of growing juveniles to market size for many commercial species represents approximately 50% of the operating costs (Kissil et al. 1997). Currently, aquaculture uses around 60–70% of the world’s annual FM supply, which is 5.7 MMT (FAO 2010; Jackson 2010). In 2010, FM was trading at US$1800 per tonne compared with only US$400 per tonne in 2000 (FAO 2010; Jackson 2010).

A major research direction for the past 20 years has focused on how to reduce the reliance on wild fish stocks to feed aquaculture species by replacing FM with more sustainable alternative protein ingredients (De Silva & Anderson 1995; Baeverfjord & Krogdahl 1996; Allan et al. 2000; Hansen et al. 2006; Tacon et al. 2006; Gatlin et al. 2007; Glencross et al. 2007; Tacon & Metian 2008). An alternative protein ingredient should possess adequate nutritional properties, i.e. a high level of protein with a favourable amino acid profile, high nutrient digestibility, acceptable palatability, and be relatively inexpensive compared with FM (Gatlin et al. 2007). However, most suitable alternative ingredients to FM fail to possess at least one or more of the above mentioned desirable requirements.

Plant proteins from protein-rich oilseeds or grain by-product meals are generally less expensive, consistently available, and are a more environmentally sustainable protein ingredient than FM (Hardy 1982; Gatlin et al. 2007). However, the major problem with replacing FM with plant products is their low levels of some essential amino acids, generally methionine and lysine, as well as high levels of indigestible carbohydrate. The presence of anti-nutritional substances such as trypsin inhibitors, antigenic proteins, phytates, soyasaponins and lectins in plant material can also negatively affect palatability, nutrient utilization, feed efficiencies, fish health and ultimately growth (Bureau et al. 1998; Francis et al. 2001; Hansen et al. 2006; Gatlin et al. 2007). For comprehensive reviews on the use of plant proteins and anti-nutritional factors in aquafeeds see Francis et al. (2001) and Gatlin et al. (2007).

Lipids are a source of essential fatty acids, energy, eicosanoids, components of the cell membrane (phospholipids) and assist in the uptake of lipid soluble nutrients (Storebakken 2002). Currently, aquaculture uses around 80–90% of the global FO supply, which is 1.3 MMT (FAO 2010; Jackson 2010). Changes in temperature can lead to many physiological changes in fish. Research has shown that fish can exploit the structural diversity of lipids within their membranes to adapt to changes in ambient temperature (Miller et al. 2006). The omega-3 long chain polyunsaturated fatty acids (n-3 LC-PUFA), eicosapentaenoic acid (EPA; 20:5 n-3) and docosahexaenoic acid (DHA; 22:6 n-3) function as structural and physiological components of the cell membrane in most fish tissues (Sargent et al. 1993). At low temperatures the chemical structure of n-3 LC-PUFA permits a greater degree of unsaturation compared with saturated fatty acids (SFA) (Hazel 1984). This unsaturation is necessary to maintain flexibility and permeability in the phospholipid bi-layer (Lovell 1998). This means that cold and temperate water species require a certain level of n-3 LC-PUFA to maintain cell membrane fluidity and digestion at low temperatures.

Not only is the tissue fatty acid composition highly influenced by water temperature, but it can also change the dietary fatty acid composition (Glencross 2009), digestibility (Torstensen et al. 2000), transport and uptake, elongation and desaturation processes (Bell et al. 2001, 2002), and β-oxidation of fatty acids (Froyland et al. 2000), which can affect the membrane and depositing lipid composition (Torstensen & Tocher 2011). The ability of fish to digest and absorb lipids is based on the fatty acid composition and degree of unsaturation and chain length of the lipid ingredient. These factors are responsible in determining the lipid ingredients melting point, which is a good indicator of lipid digestibility (Turchini et al. 2009). The apparent fatty acid digestibility is highest for long chain polyunsaturated fatty acids (LC-PUFA) > polyunsaturated fatty acids (PUFA) > monounsaturated fatty acids (MUFA) > SFA and short chain > longer chain fatty acids. Animal-based lipid ingredients are richer in SFA and MUFA compared with most plant-based lipid ingredients, which gives these lipids a higher melting point (Bell et al. 1986). Differences in apparent fatty acid digestibility are important to consider when formulating diets for sub-optimal water temperature conditions, particularly when replacing FO with alternative lipid ingredients of plant and animal origin that are higher in SFA and MUFA and lower in n-3 LC-PUFA. For example, the inclusion of palm oil into winter diets for salmonid species is particularly a concern due to the high melting point of palm oils, leading to subsequent reduced fatty acid digestibility and energy availability (Ng et al. 2007).

There is a wide variety of vegetable oil and animal fat ingredients produced globally that are now commonly used in aquaculture feeds (reviewed by Turchini et al. 2009). Vegetable oils and animal fats provide good sources of dietary energy, but with a few exceptions, they are poor sources of n-3 fatty acids (FA), contain no n-3 LC-PUFA, and have high levels of n-6 FA. The n-3 LC-PUFA provides fish with essential polyunsaturated fatty acids (PUFA) for normal growth and the development of cells and tissues (Sargent et al. 1995). The n-3 LC-PUFA also have a vitally important role for human nutrition, particularly in relation to human developmental stages (Sargent et al. 2002). Whereas, high levels of n-6 FA are undesirable in the human diet due to their associated negative health impacts such as an increased risk of cardiovascular disease and autoimmune diseases (Simopoulos 2006). Full replacement of FO with alternative lipid ingredients is limited by the reduced enzymatic ability of most marine fish to convert PUFA, α-linolenic (ALA; 18:3 n-3) and linoleic (LA; 18:2 n-6) acid by chain elongation (Ghioni et al. 1999) and desaturation processes (Tocher & Ghioni 1999) into LC-PUFA; EPA, DHA and arachidonic acid (ARA; 20:4 n-6). Therefore, most practical studies researching the effects of full replacement of FO will formulate diets with enough fish oil to meet the essential n-3 LC-PUFA requirements for the target species, whilst keeping the dietary level of n-6 FA at a minimum (e.g. Bell et al. 2001, 2002).

When a fish species is cultured in an environment where temperature falls outside a fish’s optimal range, at least three fundamental questions are raised regarding aquaculture efficiency. What are the optimal dietary protein and energy requirements needed to maintain optimum performance under sub-optimal temperature conditions? What effect does sub-optimal temperature have on the ability of fish to utilize dietary protein and energy? And finally the most current global issue regarding the production of fish is the sustainable use of marine derived fish meal and fish oil from wild fisheries, but what effect does replacing these ingredients with alternative sources have at sub-optimal temperatures?

In this paper, warm water is referred to species with a temperature optima of ≥25°C, cold water species with temperature optima of ≤20°C, and temperate in between the two extremes (Stickney 1994) as a guideline for discussion, though there may be overlap by some species within the three categories. In this review, we aim to (i) understand the nutritional requirements (protein, lipid and energy) of commonly cultured marine fish species in cold water, temperate and warm water; (ii) discuss the effect of temperature on the nutritional requirements, in particular, feed intake, when fish are cultured in sub-optimal temperatures, and (iii) evaluate the physiological responses of fish to varying protein and energy levels as well as the replacement of dietary FM and FO with alternative protein and lipid ingredients when fish are cultured within and outside of their optimal temperature ranges. The review contributes to the understanding of fish growth performance when fed with alternative protein and lipid ingredients at sub-optimal and optimal temperatures.

Cold water fish species (≤20°C)

  1. Top of page
  2. Abstract
  3. Introduction
  4. Cold water fish species (≤20°C)
  5. Temperate fish species (20–25°C)
  6. Warm water fish species (≥25°C)
  7. Conclusions
  8. Acknowledgement
  9. References

Some commonly cultured cold water marine species include Atlantic salmon (Salmo salar), Atlantic halibut (Hippoglossus hippoglossus, Linnaeus, 1758), Atlantic cod (Gadus morhua, Linnaeus, 1758) and turbot (Scophthalmus maximus, Linnaeus, 1758). These species show optimal growth performances at temperatures of 5–17°C (Elliott 1982; Jobling 1988). Atlantic cod generally reach a market size of 3–4 kg after 34–36 months (Jobling 1988). Similarly, Atlantic halibut take 37–44 months to reach a market weight of 5 kg (Grisdale-Helland & Helland 2002). In Europe, the salmonid industry was formed in the late 18th century and the technique of salmonid farming in net-pens was developed in Norway in the late 1960s. Since then the salmonid industry, mainly in northern Europe, Chile and North America, has become one of the most important cold water, sea-based aquaculture industries world-wide and continues to drive the growth of the marine fish industry (Helland et al. 1991; FAO 2009). In 2008, the annual global production of Atlantic salmon was 1.45 MMT and worth $US7.2 billion (FAO 2009).

Two other popular cold water marine fish species for aquaculture are the Atlantic halibut and Atlantic cod. Due to their consumer popularity, wild stocks have been overfished for many decades, even leading to the collapse of the Atlantic cod fishery throughout eastern Canada in the 1990s (Myers et al. 1997). Atlantic halibut and Atlantic cod are currently listed as endangered and vulnerable in the wild, respectively, on the International Union of Nature Conservation red list of threatened species (IUCN 2010). Overfishing of wild fish stocks and high consumer demand has led to the aquaculture of Atlantic salmon, halibut and cod species in many countries.

Nutritional requirements of cold water fishes

Since the introduction of extruded pellets, diet formulations for cold water species have developed towards lower crude protein (35–42% CP) and higher crude lipid levels (35–40% CL) (Hillestad & Johnsen 1994; Hillestad et al. 1998). If excess energy is included into the diet, then fish cannot utilize this energy and will store the excess as fat, either in the fillet, visceral cavity or in the liver, depending on the species (Watanabe 1982; Stead & Laird 2002; Regost et al. 2006). For instance, the belly flap of Atlantic salmon may contain 70% lipid (Rye et al. 1995). Compared with Atlantic salmon, Atlantic cod have a lower potential to effectively utilize high levels of dietary lipid (>18% CL), and therefore, when fed diets with a low P:E ratio it results in an increased liver size (Lie et al. 1988; Rosenlund et al. 2004). As a result this species has a higher dietary protein requirement (50% CP, Rosenlund et al. 2004). If the energy content of a diet in the form of lipid or CHO is below the required level then fish will utilize dietary protein for energy instead of utilizing the energy for protein synthesis, which reduces growth and also adds to the cost of production (Masumoto 2002).

A compensatory response of increased feed intake of low-energy diets to maintain energy requirements has been shown in fish species cultured at low temperatures. When temperatures decreased from 8°C to 2°C, Atlantic salmon (19 g initial weight) fed a low-lipid energy diet (50% CP, 21% CL and 22.5 MJ kg−1 GE, P:E 22.3 g CP MJ−1 GE) increased their feed consumption and improved feed conversion ratios compared with a high-lipid energy diet (40% CP, 34% CL and 24.8 MJ kg−1 GE, P:E 16.3 g CP MJ−1 GE) (Bendiksen et al. 2002).

Atlantic salmon farmed in Tasmania, Australia can be subjected to ambient temperatures of up to 19°C. This temperature is approaching the upper threshold of survival for this species (Carter et al. 2003). Miller et al. (2006) examined the lipid profile of Atlantic salmon held at 19°C and found that at this temperature the percentage of SFA increased while total PUFA and n-3 LC-PUFA, particularly DHA decreased. These findings imply that there is a major adaptation of the total body lipid to higher temperatures. However, the authors stated that it remained unclear whether n-3 LC-PUFA were directed preferentially towards metabolism for energy production, rather than to storage in muscle tissue in the form of triglycerides.

Not only does changing temperature affect cell membrane structures, but it can also influence digestive processes. Understanding the digestive processes and enzyme activity of fish during seasonal temperature changes is important when formulating diets to optimize growth performance and to reduce feed costs. However, there are few studies published specifically on cold water fish species and the effect of sub-optimal temperatures on the digestibility of nutrients and digestive enzyme activities. Although there have been studies at optimal temperature ranges (Munilla-Morán & Saborido-Rey 1996; Hidalgo et al. 1999; Allan et al. 2000; Vandenberg & De La Noüe 2001). Digestive enzyme activity differs between fish species from cold, temperate and warm water environments (Hidalgo et al. 1999). Munilla-Morán and Saborido-Rey (1996) found that the optimal temperature range for efficient enzymatic protein digestion in the stomach extracts of turbot (Scophthalmus maximus), redfish (Sebastes mentella, Travin, 1951) and a temperate marine species, gilthead seabream (Sparus aurata, Linnaeus, 1758) was 35–40°C, but maximal enzymatic activity for turbot and redfish occurred at 5°C. In comparison with redfish and turbot, gilthead seabream had significantly higher gastric digestion when cultured above 20°C (Munilla-Morán & Saborido-Rey 1996). The biological nature of cold water fish such as redfish and turbot indicates that they have a higher tolerance to wide temperature ranges, but are better adapted to digest protein at cooler temperature, whereas temperate species are more suited to the digestion of protein at warmer temperatures.

Fish meal replacement in cold water fishes

Studies have shown that growth performance, feed efficiency, digestibility and physiology can be altered by interactions of temperature and plant protein inclusion (Table 2). The quality of the diet depends on how well the ingredient is digested and its available amino acid profile (Robaina et al. 1995). In addition, the apparent digestibility can be affected by decreased water temperature, but its effect on the rate of digestion can also be compounded by the composition of the dietary ingredients, such as the amount of digestible and indigestible components of ingredients in the diet, in particular carbohydrates, or the presence of anti-nutritional factors (Bureau et al. 1998). For example, Hansen et al. (2006) studied the digestibility of diets containing solvent extracted soybean meal (SESBM) and soy protein concentrate (SPC) in Atlantic cod (139 g) held at 6.5°C. SESBM inclusion increased from 4% to 16% CP and SPC from 11% to 21% CP. The results indicated that the apparent digestibility coefficients (ADC) were higher in fish fed SPC (85–87%), compared with those fed SESBM (77–83%) and fat ADC were reduced from 95% to 87% as SESBM inclusions increased, but fat ADC remained high ≥94% in fish fed SPC. Therefore, it can be seen that the use of SPC instead of SESBM resulted in the elimination of the negative effects associated with dietary fibre, particularly saponins (Refstie et al. 1998). In conjunction with this study, Hansen et al. (2007) examined the protein utilization of the same diets in fish held at 6.5°C and 11°C. Growth and feed utilization were reduced in fish fed diets containing increasing levels of soybean meal at 11°C, but not at 6.5°C, although reductions in protein retentions were seen at both temperatures with all diets.

Table 2. Selected studies on fish meal diets or the replacement of fish meal with alternative proteins and the biological effects of the inclusion level on cold and temperate water marine fished cultured at sub-optimal temperatures
Fish speciesTemperature (°C)Dietary protein sourceFM replaced (%)Dietary CP (%)Biological effectsReferences
  1. CP, crude protein; FCR, feed conversion rate; FI, feed intake; FM, fish meal; SBM, soybean meal; LM, lupin meal; CGM, corn gluten meal; RM, rapeseed meal; SPC, soy protein concentrate; PR, protein retention.

Cold water
 Atlantic cod (Gadus morhua)7 vs. 11SBM vs. CGM vs. SPC vs. SBM + CGM≤4453–56Growth decreased with plant inclusion at 11°C, but not at 7°C. PR decreased at both temperatures. No intestinal or liver abnormalitiesHansen et al. (2007)
 2, 6, 11FM042 vs. 55No change in growth at low temperature when fed low protein diets Pérez-Casanova et al. (2009)
Temperate water
 Gilthead seabream (Sparus aurata)19SBM vs. LM10, 20, 3055–57Growth similar to control; trypsin activity decreased when fed 30% SBM and lipid deposition in liver when fed >20% SBM and LM Robaina et al. (1995)
 Japanese yellowtail (Seriola quinqueradiata)16, 18, 22, 25FM040, 42, 45Pepsin activity in stomach decreased and trypsin and chymotrypsin activity in intestine increased at 18 and 16°C. Lower digestibility in low protein diets at cool temperatures Kofuji et al. (2005)
 European seabass (Dicentrachus labrax)22SBM, + RM + CGM5–5245–50Growth performance and FI not affected by increased plant protein. Increased fat deposition in plant protein diets Kaushik et al. (2004)
 15 vs. 20FM030, 40, 50, 60FI decreased at 15°C vs. 20°C. 50% protein was optimal for growth and FCR at both temperatures Hidalgo and Alliot (1988)

Fish oil replacement in cold water fishes

There have been a few studies examining the combined effect of temperature and dietary lipid source on fatty acid composition, although the results were not consistent (Grisdale-Helland et al. 2002; Jobling & Bendiksen 2003; Table 3). The lack of consistency between findings can be due to a number of reasons including different species examined, dietary lipid source and inclusion level, as well as different tissues investigated. Generally, dietary lipid affects the non-polar neutral lipids (NL) more so than the polar phospholipids (PL), whereas the effect of temperature is reflected more in the PL than the NL (Jobling & Bendiksen 2003). A study by Jobling and Bendiksen (2003) examined the effect of temperature (2°C and 8°C), lipid source (fish oil or a mixture of rapeseed and linseed oil), and dietary lipid level (21% and 34% CL) on the fatty acid profile of Atlantic salmon parr. Although this study was run in freshwater rather than seawater, the results are still of interest to this review. Higher dietary lipid levels lead to a higher level of lipid deposition than compared with the low lipid feeds. The FO diet had higher concentrations of n-3 LC-PUFA than the vegetable oil in the PL, which was expected. However, the fish fed the vegetable oil had a higher unsaturated fatty acid to saturated fatty acid ratio, indicating that the cell membranes may have a greater fluidity than for the fish fed the FO diets. Other studies have found that replacing 100% fish oil with soybean oil in diets for Atlantic salmon increased hepatic lipid stores at 5°C and not at 12°C (Ruyter et al. 2006). Similarly, Jordal et al. (2007) found that Atlantic salmon fed a vegetable oil blend (rapeseed, palm and linseed oil) over a long time period where the water temperature ranged from 6°C to 17.5°C led to increased hepatic triacylglyceride stores. Increases in liver lipid stores when using alternative lipid ingredients have been associated with a deficiency of essential fatty acids (Turchini et al. 2009) or as a result of reductions in water temperature (Ibarz et al. 2007), or a combination of both (Torstensen & Tocher 2011).

Table 3. Selected studies on fish oil diets and replacement of fish oil with alternative lipids and the effect of their inclusion levels on the growth of cold, temperate and warm water marine species cultured at sub-optimal temperatures
Fish speciesTemperature (°C)Dietary lipid sourceFO replaced (%)Dietary CL (%)Biological effectsReferences
  1. CL, crude lipid; FO, fish oil; SBO, soybean oil; SL, soy lecithin; RO, rapeseed oil; SGR, specific growth rate, FI, feed intake; FE, feed efficiency; FCR, feed efficiency ratio; 18:2n-6, linoleic acid; 18:1n-9, oleic acid; TAG, triacylglyceride; EPA, eicosapentaenoic acid; DHA, docosahexaenoic acid.

Cold water
 Atlantic salmon (Salmo salar)5 vs. 12FO + SBOvs. SBO50 vs. 10030Growth increased at 5 vs. 12°C. No change on growth or FI when fed 100% SBO vs. FO control. SBO caused no change to heart pathology Grisdale-Helland et al. (2002)
 5 vs. 12Same diets as above  At 5 and 12°C 18:2n-6 and 18:1n-9 in TAG fractions of liver and intestine increased and EPA and DHA in fish fed SBO diets decreased Total fat in liver increased at 5°C in SBO fed fish Ruyter et al. (2006)
Temperate water
 Mediterranean yellowtail (Seriola dumerili)18FO 18, 22, 26, 30CL level had no effect on growth, but as inclusion level increased fat deposition increased Talbot et al. (2000)
 Flounder  (Paralichthys olivaceus)12 vs. 17FO vs. FO + SL1 vs. 77 vs. 14Weight gain, FI, and FE decreased at 12 vs. 17°C. At 12°C, 14% CL improved FE and protein efficiency Kim et al. (2006)
 European seabass (Dicentrachus labrax)22 vs. 29RO816Fish fed RO diet at 22°C had lowest SGR, while FCR increased at 29°C Person-Le Ruyet et al. (2004b)
Warm water
 Nassau grouper (Epinephelus striatus)25 vs. 30FO 6, 9, 12, 15Final growth and SGR increased at 30 vs. 25°C, FCR negatively correlated to increasing lipid content Johnson et al. (2002)
 Asian seabass (Lates calcarifer)20 vs. 29FO + SBO 13, 16, 18Increasing CL to 18% at 20°C increased FCR and growth Williams et al. (2006)

The sensitivity of fatty acid digestibility in relation to water temperature has been reported in several studies (Kim et al. 1998; Olsen & Ringø 1998; Torstensen et al. 2000; Caballero et al. 2002; Karalazos et al. 2007; Torstensen & Tocher 2011). Grisdale-Helland et al. (2002) reported that at both 5°C and 12°C the digestibility of SFA were lower than for other fatty acids. These results are similar to a study on rainbow trout (Oncorhynchus mykiss, Walbaum, 1792) where increasing levels of dietary palm oil from 0% to 20%, at the expense of fish oil, led to significant reductions in the digestibility of SFA. Similarly, a drop in water temperature from 15°C to 7°C reduced the digestibility of SFA, regardless of dietary palm oil inclusion (Ng et al. 2003). Bendiksen et al. (2003) investigated the digestibility of the same diets use in a related study by Jobling and Bendiksen (2003) in relation to temperature and oil type. Protein and fat digestibility were lower at 2°C than at 8°C and protein digestibility significantly improved when vegetable oils were included in the diet at 2°C. In contrast, Grisdale-Helland et al. (2002) investigated the total (100%) or partial (50%) replacement of FO with soybean oil (SBO) in high energy diets for Atlantic salmon (108 g) at 5°C and 12°C. In their study, the fish grew faster at 5°C than at 12°C regardless of SBO levels, although feed intake was lower at 5°C than at 12°C. Although Atlantic salmon could be fed 100% SBO in high energy diets without affecting fish health, digestibility was affected by temperature. Protein digestibility was higher at 5°C than at 12°C, but SBO inclusion level had no effect. The digestibility of the FA in the diets was high, but an interaction between diet and temperature was found for most major FA (Grisdale-Helland et al. 2002).

Temperate fish species (20–25°C)

  1. Top of page
  2. Abstract
  3. Introduction
  4. Cold water fish species (≤20°C)
  5. Temperate fish species (20–25°C)
  6. Warm water fish species (≥25°C)
  7. Conclusions
  8. Acknowledgement
  9. References

Some commonly cultured temperate marine fish include the Japanese yellowtail (Seriola quinqueradiata, Temminck & Schlegel, 1845), Mediterranean yellowtail (Seriola  dumerili, Risso, 1810), yellowtail kingfish (Seriola lalandi, Valenciennes, 1833), gilthead seabream (Sparus aurata) and European seabass (Dicentrachus labrax, Linnaeus, 1758, Table 1). Unlike salmonid culture, temperate water fish such as Japanese yellowtail can be cultured in 13–30°C, but optimal temperature ranges for growth are reported to be 20–26°C (Masumoto 2002). When temperatures fall below 17°C, feed consumption and growth are drastically reduced in most temperate species (Masumoto 2002). The Japanese yellowtail is one of the most economically important aquaculture fish species in Japan. In spring time, wild-caught Japanese yellowtail (<10 g per fish) are stocked into sea cages in coastal zones until fish reach 50–100 g (Masumoto 2002). These fish are then sold to growers who raise the fish in sea cages to a market weight of 3 kg in 11 months or 7 kg in 20 months. The average annual seawater temperatures in Japan where Japanese yellowtail are cultured range from 20°C to 24°C in Okinawa and Kagoshima and 17–19°C in Kumamoto and Nagasaki, where fish can reach a market size of 6 kg in 2 years or 3.5–4.5 kg in 3 years, respectively (Nakada 2008). In comparison, yellowtail kingfish grown in south Australian waters are exposed to 11–24°C and reach a market size of 3–4 kg in 12–18 months (Fernandes & Tanner 2008; Miegel et al. 2010).

Gilthead seabream is cultured in the Mediterranean and the Black Sea and is also cultured along the eastern Atlantic Ocean from Senegal to the British Isles (Kissil 1991). Gilthead seabream juveniles (1–3 g per fish) grow in sea cages for 12–14 months at 13–26°C to reach a market size of 400–500 g (Koven et al. 2001). Juvenile sea bass seem to cease growing at 11–15°C and have optimal growth at 22–25°C, with lower and upper lethal temperature limits of 2–3°C and 30–32°C, respectively (Barnabe 1991). European seabass are also commonly cultured in the Mediterranean countries, specifically in Greece, Turkey, Italy and Spain (Kaushik 2002) and are exposed to similar temperatures as gilthead seabream in the grow-out phase.

Nutritional requirements of temperate water fishes

Dietary protein levels of 45–55% and lipid levels of 15–20% are considered ideal for optimal growth in the grow-out phase of sub-adult temperate species such as European seabass, Japanese yellowtail, Mediterranean yellowtail, yellowtail kingfish and gilthead seabream (Alvarez et al. 1998; Peres & Oliva-Teles 1999; Koven 2002; Masumoto 2002). The biological effects of changing temperature and the inclusion level of protein have been studied in some temperate fish species (Table 2). Peres and Oliva-Teles (1999) fed European seabass (5.5 g) diets containing graded levels of FM, 36%, 42%, 48% and 56% CP (12% CL, 19 MJ kg−1 GE) at two temperatures (18 and 25°C). Diets containing 48% crude protein (19.7  MJ  kg−1) satisfied the needs for growth of fish regardless of temperature, but better growth and feed efficiencies occurred at 25°C. A similar study by Hidalgo and Alliot (1988) found that European seabass required 50% protein at 15 or 20°C. However, body protein retention of fish fed a 40% CP and 27% CHO diet at 20°C was higher than at 15°C. This indicates that protein can be spared by CHO inclusion in European seabass more at 20°C than at 15°C. Vidal et al. (2008) found that Mediterranean yellowtail (490 g) performed better when fed a high protein P:E diet (28.9 g CP MJ−1 GE) than a lower P:E diet (24.6 g CP MJ−1 GE) at optimal temperatures (21–26°C). At winter temperatures (19°C) a series of studies by Watanabe et al. (1998, 1999, 2000a,b,c) identified that the P:E requirements for similar sized Japanese yellowtail (400–500 g) were lower (17–20 g CP MJ−1 GE) than that required at optimal temperatures (20–26 g CP MJ−1 GE).

As water temperatures decrease during winter the feeding frequency and feed quantity reduces because fish can regulate the necessary amount of energy they require for maintenance, but for almost no growth. Reductions in water temperature also lead to significant changes to gut transit time and nutrient digestibility as it directly affects feed intake and enzyme activity (Hidalgo et al. 1999; Temming & Herrmann 2001; Kofuji et al. 2005). It has been demonstrated in sub-adult yellowtail kingfish that as the water temperature decreased from 20°C to 12°C feed intake and gut transit time decreased leading to a higher amount of digestion occurring in the anterior section of the gastrointestinal tract (Miegel et al. 2010).

Similarly to cold water species, there is a growing interest to increase the lipid content in diets for temperate water species to improve protein-sparing, reduce dietary feed costs, to improve feed conversion ratios and protein and energy utilization, and ultimately growth performance (Izquierdo et al. 2003). Temperate species have the capacity to utilize high levels of dietary lipid, e.g. gilthead seabream held at 20–24°C and fed a high quality FM diet containing 48% CP and either 22% or 27% CL (24 or 25 MJ kg−1 GE, respectively) had significantly higher growth rates than fish fed 15% CL (22 MJ kg−1 GE) (Caballero et al. 1999). However, unlike cold water salmonoid species, temperate water marine fish species can be less tolerant to diets with high lipid contents when cultured in cold temperatures. This was demonstrated in Mediterranean yellowtail (95 g) fed Atlantic salmon diets (low protein, high lipid) at 18°C (Table 3, Talbot et al. 2000). This study showed that diets high in dietary lipid (30% CL; 18 g CP MJ−1 GE) did not affect growth performance, feed conversion efficiencies or liver size. However, lipid deposition within the muscle tissue and visceral cavity was significantly increased with increasing dietary lipid inclusion, 16% visceral fat (low dietary CL; 18%) to 23.5% visceral fat (high dietary CL; 30%).

European seabass fed a standard diet and held at winter (12–15°C) and spring (17–20°C) exhibited significant changes to the fatty acid profile of the muscle and liver tissue, mostly in the phospholipids fraction (Delgado et al. 1994). The general trend was that at winter temperatures there was an increase in the percentages of LA, ARA, EPA and DHA in the muscle and a subsequent decrease in 18:1n-9 (oleic acid). The liver had increased levels of 18:0 (stearic acid), EPA, DHA, and decreased 16:0 (palmitic acid) and 18:1n-9. These results are in agreement with other studies on species such as the Atlantic salmon where the depositions of unsaturated fatty acids were conversely correlated to temperature (Miller et al. 2006). Person-Le Ruyet et al. (2004b) investigated whether the level of n-3 LC-PUFA in the diet would improve the ability of the European seabass to adapt to high temperatures. Juvenile fish (60 g) were fed a low or high lipid diet containing 0.4% or 2.2% n-3 LC-PUFA (LD, or HD diet, respectively) at 22°C and 29°C. The SGR was higher in fish fed the HD diet than the LD diet at 29°C, and was higher at 29°C than at 22°C. Feed intake was significantly influenced more by temperature, as showed by a higher feed intake at 29°C than at 22°C.

During colder seasons, Japanese yellowtail exhibit low growth due to lower apparent protein digestibility (APD) (Satoh et al. 2004). Researchers have tested diets formulated with different crude lipid levels in an attempt to improve APD. When fish were fed a high protein, low lipid diet (45% CP, 20% CL, 17 MJ kg−1 GE), there were no significant difference in APD at 25, 22, 18 and 16°C. Digestive trypsin activity was higher in fish fed diets with high protein levels, irrespective of temperature, indicating that digestive trypsin activity is strictly regulated by the level of dietary protein in Japanese yellowtail (Kofuji et al. 2005). Diets with lower protein and higher lipid (43–40% CP, 25–29% CL, 18–19 MJ kg−1 GE) had significantly lower APD at 18°C and 16°C than at 25°C and 22°C, indicating that low protein, high lipid diets reduce APD in Japanese yellowtail compared with a higher protein diet in cooler water (Kofuji et al. 2005). In this study, the trypsin and chymotrypsin activities in the intestinal content of Japanese yellowtail were higher in cooler water (16°C and 18°C) than in warmer water (25°C and 22°C). In 2–2.5 kg yellowtail kingfish, higher protease activity was found in the posterior intestine at 12°C than at 20°C (Miegel et al. 2010), suggesting that the increased digestive transit time led to the accumulation of enzymes in the intestinal content, allowing fish to obtain an adequate dietary protein uptake during the winter season. Temperature also influenced the pepsin activity in the stomach content of Japanese yellowtail (Kofuji et al. 2005). Pepsin activity was reduced at 18°C and 16°C (1100–2500 U g wet contents−1), compared with 22°C and 25°C (2400–3100 U g wet contents−1), indicating that pepsin secretion after feeding is reduced in cool temperatures. The authors suggested that increasing the pepsin secretion from the stomach may improve protein digestibility and fish growth during the winter season.

When temperate marine fish are cultured below their optimal thermal range (<17°C), diets are often formulated with high quality protein ingredients as well as being fortified with extra vitamins, minerals and immunostimulants to increase digestibility and to improve immunity to diseases (Tort et al. 2004). In response to the poor APD found in Japanese yellowtail during winter when fed with both high and low protein diets, Kofuji et al. (2006) tested whether adding feeding stimulants would improve APD in this species at low temperatures. Three feeding stimulants were tested: (i) a synthetic feeding stimulant at 1% dietary inclusion (containing l-alanine, l-proline and inosine-5′-monophosphate 2 Na); (ii) natural krill extract at 2% dietary inclusion; and (iii) a natural squid extract at 1% dietary inclusion. The results showed that the inclusion of feeding stimulants increased APD through an increase of pepsin, trypsin and chymotrypsin secretions. Therefore, marine fish held through a winter period may benefit from the inclusion of feeding stimulants into diets to improve digestive functions.

Fish meal replacement in temperate fishes

Partial substitution of alternative ingredients has been successful in diets for temperate species (Table 2). The replacement of fish meal with soybean ingredients has been achieved in juvenile Japanese yellowtail (Shimeno et al. 1992, 1993a,b), Mediterranean yellowtail (Tomas et al. 2005), gilthead seabream (Kissil et al. 2000), black seabream (Peng et al. 2008) and European seabass (Alliot et al. 1979; Dias et al. 1997; Lanari & D’Agaro 2005) although these studies were run at optimal temperatures. Up to 6–16% crude protein from fish meal can be replaced with protein from SESBM in a 40–50% CP diet for Seriola species and European seabass, without significantly reducing the growth, palatability or acceptance of diet. In contrast, at SESBM inclusion levels above 26–36% CP in a 45–50% CP diet, fish growth rates were significantly reduced and feed conversion ratios (FCR) increased compared with the FM control diets (Lee et al. 1991; Shimeno et al. 1992; Lanari & D’Agaro 2005; Tomas et al. 2005). However, Aoki et al. (2000) successfully replaced up to 50% of FM in a 48% CP, 26% CL diet for Japanese yellowtail (144 and 172 g) with a combination of alternative protein ingredients such as SESBM, corn gluten meal and meat meal.

Soy protein concentrate is a more refined soy product than soybean meal, with most anti-nutrients removed. Although SPC has a high protein content (∼66% CP) and is highly digested by most temperate fish species (e.g. 97% in European seabass, 73–87% in Japanese yellowtail), there are problems associated with diet palatability and acceptance by marine fish (Masumoto et al. 1996; Tibaldi & Tulli 1998; Kissil et al. 2000; Peres & Lim 2008). Yellowtail kingfish (700 g) fed diets containing SPC at 40% CP dietary inclusion in a 45% CP, 20% CL diet at sub-optimal temperatures (10–13°C) had significantly reduced growth performances (Bansemer 2011). The reduction of growth performance may have been due to poor palatability and intake of the diet containing the SPC. Contrasting results at optimal temperatures are yet to be reported, although similar palatability issues have been found in gilthead seabream juveniles (12 g) at temperatures of 23–24°C, fed SPC or canola protein concentrate, replacing up to 30%, 60% and 100% of FM in a 50% CP, 15% CL (22 MJ GE kg−1) diet (Kissil et al. 2000). Gilthead seabream could utilize both ingredients well, except for 100% SPC, which was possibly due to a deficiency of methionine. Secondly, these authors reported that as the plant protein inclusion increased, the feed intake decreased because the presence of phytic acid in the plant proteins reduced the palatability of the diet. Results from a study by Robaina et al. (1995) found the presence of phytates in heat treated soybean meal (>20% inclusion) caused slow growth due to a reduction of trypsin activity in gilthead seabream.

The antagonistic combination of reduced water temperature, gut transit time, digestibility and increased levels of indigestible CHO can lead to the possible onset of histological changes to the gastrointestinal tract or pathological diseases. Gilthead seabream and yellowtail kingfish exposed to low temperatures have developed a gut pathology known as ‘winter gut syndrome’ or ‘red intestines’ (Sheppard 2004; Tort et al. 2004). The onset of this disease has been linked to a combination of factors including, (i) cool temperature (i.e. causing a reduction in gut transit times), (ii) high-fat feeds, (iii) the presence of high levels of plant proteins, and (iv) low feed intake and low vitamin/mineral intake, and (v) opportunistic bacteria. These factors have the potential to cause an inflamed and irritated bowl (enteritis), necrosis, ulceration, electrolyte imbalance and ultimately death (Gallardo et al. 2003; Sala-Rabanal et al. 2003; Sheppard 2004). Some of the symptoms of this disease such as an inflamed and irritated bowel appear similar to that of soybean induced enteritis in Atlantic salmon fed diets containing high levels of soybean products (van den Ingh et al. 1991; Krogdahl et al. 2003).

In an effort to minimize the occurrence of winter gut syndrome, production diets have been formulated with high protein inclusion levels (50% CP) containing only high quality FM and FO ingredients as well as increased levels of vitamin C (Tort et al. 2004). However, this syndrome has been difficult to duplicate in laboratory conditions. Therefore, there are no data on the performance of specifically formulated diets to protect against this syndrome in a controlled laboratory system and more research is needed in this area.

Fish oil replacement in temperate fishes

Research on the impact of FO replacement with alternative plant and animal lipid ingredients on growth performance, nutritional requirements, and physiological and histological changes at sub-optimal temperatures is limited in temperate marine fish species (Table 3). Like cold water fish, most research in these areas has focused on the replacement of FO with alternative lipids at optimal temperature (Caballero et al. 2003; Glencross et al. 2003). For instance, gilthead seabream (10 g) can be fed diets replacing up to 60% of dietary lipid in a 46% CP, 25% CL diet with a mixture of SBO, linseed oil and rapeseed oil (Izquierdo et al. 2003; Montero et al. 2003) without compromising growth performance. Similarly, European seabass (5 g) can be fed a diet with plant oils (linseed, palm and rapeseed) replacing 60% of fish oil (16% CL diet) without reducing growth performance or affecting lipid content of muscle tissue or liver (Richard et al. 2006). In this study the authors did not investigate the effect of lipid digestibility, but a study by Francis et al. (2007) found that Murray cod (Maccullochella peelii peelii, Mitchell, 1838) fed blended vegetable oils (olive oil 12%, palm oil 43%, and linseed oil 45%) had a significant negative impact on lipid and individual fatty acid digestibility. These results are in agreement with studies on many fish species from cold and warm water habitats where the combination of chain length, degree of unsaturation and the melting point of individual fatty acids resulted in changes to the digestibility of the lipid ingredient (Francis et al. 2007).

Warm water fish species (≥25°C)

  1. Top of page
  2. Abstract
  3. Introduction
  4. Cold water fish species (≤20°C)
  5. Temperate fish species (20–25°C)
  6. Warm water fish species (≥25°C)
  7. Conclusions
  8. Acknowledgement
  9. References

Most warm water fish species can grow in a wide temperature range 21–39°C, with optimal temperatures at 25°C for maximal growth (Katersky & Carter 2005; Sun et al. 2006; Katersky and Carter 2007a,b). When temperatures drop below 15°C, warm water species, such as Asian seabass (Lates calcarifer, Bloch, 1790) usually stop feeding (Boonyaratpalin 1997). Commonly cultured marine, warm water fish species are Asian seabass, cobia (Rachycentron canadum, Linnaeus, 1766), red drum (Sciaenops ocellatus, Linnaeus, 1766), and many species of groupers including brown-spotted grouper (Epinephelus malabaricus, Bloch & Schneider, 1801), orange-spotted grouper (E. coioides, Hamilton, 1822), polka dot/humpback grouper (Cromileptes altivelis, Valenciennes, 1828) and Nassau grouper (E. striatus, Bloch, 1792).

Asian seabass have been widely cultured in tropical and subtropical estuarine areas of the Indo-Pacific since the early 1980s (Chou & Lee 1997; Katersky & Carter 2007a). Asian seabass species require 5–20 months to reach a market size of 0.5–2 kg, respectively (Boonyaratpalin 1997). Similarly, brown and orange spotted grouper require 12–16 months to reach a market size of 0.6–1 kg. The majority of grouper aquaculture is concentrated in Taiwan where culture temperatures range from 28°C to 32°C in the summer and from 18°C to 23°C in winter (Shiau & Lin 2002). Other tropical fishes including snub-nose pompano (Trachinotus blochii, Lacepede, 1981), three-banded grunt (Plectorhynchus cinctus, Temminck & Schlegel, 1843), lined silver grunter (Pomadasys kaakan, Cuvier, 1830), narrow-banded batfish (Platax orbicularis, Forsskal, 1775), large yellow croaker (Pseudosciaena crocea, Richardson, 1846), brown croaker (Miichthys miiuy, Basilewsky, 1855), tiger grouper (Epinephelus fuscoguttatus, Forsskal, 1775) and potato grouper (E. tukula, Morgans, 1959) have aquaculture potential but need more research and development for their nutritional requirements (Yeh et al. 2012).

Cobia is a relatively new candidate for warm-water aquaculture (Benetti et al. 2007), particularly in Taiwan and other Asia Pacific countries (Liao et al. 2004). In the wild, cobia are found in warm-temperate to tropical waters of the West and East Atlantic, the Caribbean, and in the Indo Pacific off India, Australia and Japan (Briggs 1960). Cobia is a carnivorous fish species that can reach the market size of 4–6 kg in 1 year in offshore net cages (Chou et al. 2004). The culture of cobia has been reported within the temperature range of 16–32°C (Liao et al. 2004). Since commercial culture of this species is relatively new, there is a paucity of research on the specific nutritional requirements for grow-out size fish (Fraser & Davies 2009).

Most groupers are a feasible species for intensive aquaculture due to their fast growth and tolerance to a crowded environment (Shiau & Lin 2002). The majority of grouper species are cultured in Southeast Asia and have been farmed since the 1980s. In Taiwan, five major grouper species are currently cultured, with most of the fish bound for the ‘live fish trade’ (Pierre et al. 2008). Market prices for polka dot grouper can reach up to US$80–95 kg−1 (Williams et al. 2005). Until recently there has been limited information on the nutritional requirements for grouper species. It is important to note that the majority of farmers in Asia (particularly small and medium scale farmers) still use trash fish as the main feed input, instead of the more expensive compound diets (Coloso et al. 1999; Sim et al. 2005). Therefore, efforts to establish grouper aquaculture is being conducted in many research institutions across Asia, including Taiwan, China, Indonesia, Malaysia as well as other Asia Pacific regions to an understanding of their nutritional requirements and to improve grouper hatchery and grow-out technologies (Sim et al. 2005). Research outcomes arising from these projects have provided baseline information on the nutritional requirements for cost-effective grow-out feeds through utilizing sustainable native ingredients. However, follow on research is necessary to continue to reduce the production costs for grouper aquaculture species in these regions (Sim et al. 2005, ACIAR 2009).

Nutritional requirements of warm water fishes

Similarly to temperate water species, warm water species such as Asian seabass, groupers and cobia are carnivorous marine species requiring a high level of protein in their diet (Boonyaratpalin 1997; Chou et al. 2001; Boonyaratpalin & Williams 2002; Table 1). During grow-out, 40–50% CP is the optimal dietary protein level for Asian seabass (Boonyaratpalin & Williams 2002; Katersky and Carter 2007a,b), groupers (Chen & Tsai 1994; Shiau & Lan 1996; Luo et al. 2005; Rachmansyah et al. 2005) and cobia (Chou et al. 2001), while juveniles generally have a higher protein requirement of >50% CP (Boonyaratpalin 1997). The essential amino acid requirements for several warm water species have been conducted (Chen & Tsai 1994; Zhang & Chen 1996; Coloso et al. 1999; Zhou et al. 2006, 2007). These values can be used as a guideline for practical diet formulation for many other warm water species since the amino acid composition, as determined by Wilson’s (1991)‘ideal protein method’ (based on the whole body essential amino acid pattern) does not change significantly among fish species. This method is less time consuming and more economical than conventional methods and can be used until species-specific dietary essential amino acid requirements are empirically established using amino acid test diets (Fagbenro 2000; Luo et al. 2005).

Temperature has been shown to influence the growth of warm water species (Schwarz et al. 2007; Benetti et al. 2010; Bermudes et al. 2010; Table 1). Schwarz et al. (2007) found that weight gain was highest in cobia (330 g per fish) maintained at 29°C compared with 23°C and 18°C, while FCR was not different at 29°C or 23°C, but feed intake was reduced at 23°C. Benetti et al. (2010) studied the performance of cobia fed a commercial diet containing 53% CP and 10% CL and cultured in submersible cages at two separate locations, where temperatures were 25°C and 27°C, respectively. The influence of temperature between the two sites produced vastly different growth rates. Fish at 27°C grew to 6.0 kg in 363 days, whereas at 25°C fish only grew to 3.5 kg. Temperature seemed to be main influence towards the differences in growth, but the authors stated that a high stocking density at the 25°C location may have also been a contributing factor (Benetti et al. (2010).

One of the main differences between cold and temperate species and warm water species such as groupers, cobia, Asian seabass and red drum is the lower tolerance towards high lipid diets (>15% CL) (Craig et al. 1999; Chou et al. 2001; Williams et al. 2004; Rachmansyah et al. 2005; Wang et al. 2005). Lipid levels exceeding 15% CL can lead to suppression of appetite, growth and lipid deposition within the carcass of warm water species such as groupers and cobia (Sargent et al. 2002; Lin & Shiau 2003; Smith et al. 2005; Wang et al. 2005). In comparison with cold and temperate water species, warm water species utilize lipids less efficiently, and as a consequence the P:E requirements for warm water species can be higher, i.e. 25–26 g CP MJ−1 GE for grouper (Rachmansyah et al. 2005) and 28 g CP MJ−1 GE for red drum Sciaenops ocellatus (McGoogan & Gatlin 1998), 25 g CP MJ−1 GE for Asian seabass (Catacutan & Coloso 1995). Warm water species have a greater ability to utilize energy from dietary carbohydrate sources, compared with temperate and coldwater species (NRC 2011). However, warm water fish still have a lower threshold limit for non-protein energy utilization and still prefer dietary protein as the main source of energy, and to a lesser extent dietary CHO and then lipid (Shiau & Lin 2002; Fraser & Davies 2009). Warm water, carnivorous fish have a requirement for dietary n-3 FA, such as 1.0–1.7% n-3 LC-PUFA of the diet for Asian seabass fingerlings (Boonyaratpalin 1997) and 0.8–1.2% n-3 LC-PUFA of the diet for juvenile cobia (Chou et al. 2001). Similarly to cold and temperate species, if insufficient amounts of n-3 LC-PUFA are fed then normal metabolism and growth performance can be suppressed as well as causing liver and cardiac dysfunction (Alexis 1997), developmental abnormalities (Sargent et al. 1999) and reduced immunocompetence (Arts & Kohler 2009).

Increasing the crude dietary starch content from 19.5% to 24.6% and decreasing the protein content from 46% to 42% CP did not influence the growth performance or feed efficiencies for brown-spotted grouper at 29°C (Shiau & Lin 2001). This suggests that protein was spared by energy from carbohydrate when the protein concentration was low. The same authors also tested the ability of brown-spotted groupers to utilize two different sources of carbohydrate (glucose or starch) at a cooler temperature of 23°C. Diets differing only in the CHO source were formulated to contain 47% CP, 9% CL and 14% CHO. Dietary starch was found to be a better source of dietary CHO compared with glucose (Shiau & Lin 2002), due to the slower release of energy into the bloodstream from the more complex carbohydrate (Shiau & Lin 2001). The temperature difference between the two studies suggests that at 23°C a higher dietary protein level (47% CP) was required, whereas at 29°C the lower protein level was better utilized (42% CP).

Growth for warm water species is better at high temperatures (Johnson et al. 2002), but at cooler, sub-optimal water temperatures growth can also be improved through dietary manipulation. Williams et al. (2006) significantly increased the growth and feed conversion efficiency of juvenile Asian seabass at a low temperature (20°C) by increasing the digestible energy content of diets from 15 to 19 MJ kg−1 DE, increasing lipid levels from 2% to 9.5% CL and decreasing CHO levels from 7.1% to 0.3% CHO, while keeping the P:E ratio constant (22.5 g CP MJ−1 GE). In the same study, increasing levels of n-3 LC-PUFA (2.8–11.2% of lipid) and an n-3:n-6 ratio of 0.6–2.2, respectively, slightly improved FCR, but had no effect on feed intake or growth at 20°C, whereas at 29°C, increasing levels of n-3 LC-PUFA resulted in improved growth and FCR (Williams et al. 2006). It was recommended that feeding Asian seabass with high digestible energy feeds in the form of lipid energy during cooler water periods can improve fish productivity, but additional levels of n-3 PUFA was not beneficial.

Fish meal replacement in warm water fishes

Knowledge on fish meal replacement with plant protein for warm water carnivorous fish species is limited and studies on replacing FM have generally been run at optimal temperatures (Laining et al. 2003; Eusebio et al. 2004; Lin et al. 2004). Therefore, there is a paucity of published studies investigating the interactive effects of water temperature and fish meal replacement.

Similarly to cold and temperature water species, gastrointestinal problems have been reported in warm water species fed alternative proteins, especially soybean ingredients. Asian seabass have been successfully fed diets replacing FM with soybean ingredients, but in some instances gastrointestinal problems have been reported. Boonyaratpalin et al. (1998) fed Asian seabass (1.2 g) with four soybean ingredients: SESBM, extruded full-fat, steamed full-fat, and soaked raw full-fat soybean meal. The authors reported that fish growth performance was best on a FM control diet (40% CP, 14% CL diet), and not significantly different to fish fed the SESBM diet (21% dietary inclusion), but the soaked raw full-fat SBM (27.5% dietary inclusion) had the poorest growth performance. Pronounced changes to the gastrointestinal tract occurred to the mucosal epithelium, including poorly developed enterocytes, shortening of the microvilli and hyperplasia of the lamina propria when fish were fed 27.5% soaked raw full-fat soybean meal. Replacing 15% of FM in a 40% CP diet with SESBM seems to be a suitable substitution for Asian seabass, while if palatability for extruded or steamed full fat soybean can be improved, both are also suitable FM alternatives (Boonyaratpalin et al. 1998). These findings are in contrast to Atlantic salmon, where growth performance is usually better in fish fed full-fat soybean meal compared with SESBM (Refstie et al. 2000). This may reflect the ability of Atlantic salmon to utilize higher levels of dietary lipid compared with the warm water Asian seabass species.

In a review on the nutritional requirements of cobia it was pointed out that there were many gaps in the nutritional knowledge of cobia (Fraser & Davies 2009). For example, SESBM was a found to be a suitable partial replacement to fish meal in diets for juvenile cobia, but reductions in growth and feed efficiency still were significantly reduced, which suggests problems in palatability (Romarheim et al. 2008). However, the inclusion of a range of alternative protein ingredients has been found to be well digested in cobia, such as corn gluten meal and poultry meal (Zhou et al. 2004). In diets for Asian seabass, the inclusion of animal protein ingredients into diets results in high apparent digestibility and these ingredients can often be included at higher levels than plant protein sources without negatively affecting growth and feed efficiencies (Laining et al. 2003; Lin et al. 2004).

Research on the replacement of high levels of FM with alternative protein ingredients has identified a requirement for supplementation with taurine, a non-essential amino acid, in cold and temperate water species, particularly in rainbow trout, Japanese yellowtail and red seabream (Gaylord et al. 2006, 2007; Takagi et al. 2006, 2008). Similarly, it has been found that cobia also require dietary taurine supplementation when FM is replaced with alternative protein ingredients. Lunger et al. (2007) supplemented yeast-based protein diets, replacing 50% and 75% of FM in a 41% CP, 13% CL diet, with dietary taurine levels to equal 0.5% diet without taurine supplementation. The fish fed the diet with 50% and 75% yeast-based protein replacement with taurine supplementation had significantly higher specific growth than fish fed without taurine supplementation, while feed efficiencies were significantly higher for fish fed the supplemented diets rather than the control diet. It is recommended that taurine should be considered in diets for warm water species not only at optimal temperatures, but also when replacing FM in diets formulated for sub-optimal water temperatures.

Fish oil replacement in warm water fishes

Similarly to cold and temperate water species, the partial replacement of FO with alternative lipid ingredients has been successful in diets for warm water species such as cobia (Chou et al. 2004; Salze et al. 2010; Trushenski et al. 2010) and grouper (Shapawi et al. 2008) without comprising growth performance. Trushenski et al. (2010) replaced FO with graded inclusion levels of soybean oil (SBO; 0%, 1.2%, 2.4% and 3.6% CL) in diets for juvenile cobia (48% CP, 12% CL). Their study showed that final weight gain was significantly lower at 3.6% CL inclusion level (100% FO replacement) compared with the control diet (100% FO). Similarly, juvenile grouper (13 g) were fed 49% CP, 10% CL diets, of which 100% dietary FO (5.5% CL) was replaced was either SBO, corn oil, sunflower oil or peanut oil at optimal temperatures (28–30.5°C). No significant differences in survival, growth performance, FCR, protein efficiency ratio or hepatosomatic index were found, but the plant oil diets did have an effect on the fatty acid profile of the muscle and liver tissue, such as a significantly decreased level of EPA and DHA + EPA in muscle tissues of all vegetable oil diets, except for peanut oil (Lin et al. 2007). Brown-spotted grouper fed diets replacing FO with corn oil at different inclusions found that the fish fed a fish to corn oil ratio of 3:1 or 1:1 had a similar growth performance to fish fed the FO diet (Lin & Shiau 2007). In addition, the blended FO and corn oil diets enhanced the non-specific immune responses of grouper (i.e. higher plasma leukocyte superoxide anion production, and higher lysozyme and alternative complement activity), compared with fish fed solely the FO diet.

Currently little information exists on the effect of replacing FO with alternative lipid ingredients at sub-optimal temperatures for warm water species (Table 3). However, one study by Craig et al. (1995) investigated how to increase the tolerance of juvenile (2.6 g) red drum (Sciaenops ocellatus) to cold temperatures by examining the influence of dietary lipid content. Fish were fed 7% CL of either menhaden oil, corn oil, coconut oil and hydrogenated menhaden oil (in a 35% CP diet), plus a 14% CL menhaden oil control diet, at 26°C for 6 weeks. The growth performance was poorest in fish fed the coconut oil diet compared with fish fed the FO diet. After the feeding trial, the temperature was reduced by 1°C day−1 from 26°C to 19°C and then a further 0.5°C each day until all the fish died. Fish fed the FO had the lowest median lethal temperature (MLT) of 5.1°C and survived the longest, while fish fed coconut oil had the highest MLT and died first (9.4°C). Fish fed FO had more n-3 LC-PUFA available in the liver (21% total n-3 PUFA) than fish fed the other diets (coconut oil 3% total n-3 PUFA), which enabled fish to retain higher levels of membrane fluidity during extremely low temperatures. These results indicate that the inclusion of high levels of n-3 LC-PUFA are required in the dietary lipid source to regulate lipid metabolism and increase n-3:n-6 ratio, when fish are subjected to cold temperatures (Craig et al. 1995).


  1. Top of page
  2. Abstract
  3. Introduction
  4. Cold water fish species (≤20°C)
  5. Temperate fish species (20–25°C)
  6. Warm water fish species (≥25°C)
  7. Conclusions
  8. Acknowledgement
  9. References

This review has highlighted the effect of changes in water temperature on the nutrient requirements of cold, temperate and warm water fish species and the importance of understanding the interaction between the nutritional and physiological requirements of individual fish species and their limitations to attain optimal growth and production under these changing conditions. Although discrepancies exist between studies, some general conclusions can be drawn to improve the understanding of the nutritional requirements for fish at different temperatures. In addition, based on this review, some future research directions are recommended to improve the understanding of nutritional requirements for fish at different temperatures.

There is a lack of information comparing the nutritional requirements of cold, temperate and warm water species between their respective optimal and sub-optimal temperatures. Many fish species are usually cultured outside their optimum temperature range at some stage during the grow-out period. Therefore, it is important to identify the optimal nutritional requirements when species are held in sub-optimal temperatures and temperature–nutrition effects on growth performances, feed efficiencies and absorptive biochemical and physiological mechanisms. Research should be directed towards filling the gap in knowledge of how fish adapt to sub-optimal temperature ranges and the need to adjust the feed formulation, nutritional requirements and feed management strategies to suit the changing environmental conditions. In addition, emphasis should also be placed on the health of the fish and the potential impacts of temperature and temperature–nutrition interactions.

Most carnivorous marine species require high to moderate levels of dietary protein compared with more omnivorous and freshwater species, irrespective of temperature. The current review shows that the protein level can be reduced in diets for most marine species, but it is the quality and digestibility of nutrients in the diet that is important when fish are cultured at sub-optimal temperatures. At cooler temperatures, fish metabolism is reduced, which in turn lowers the gut-transit time, digestibility, digestive enzyme activity and affects the uptake and absorption of nutrients required for energy and growth. Therefore, high protein and low lipid diets are necessary during cool water periods, as the apparent digestibility of nutrients tends to decrease. In addition, the protein to energy ratio should be scrutinized in feed formulations relative to temperature for cold, temperate and warm water fishes, so that the level of protein can be further reduced by the inclusion of non-fish oil lipids and/or carbohydrate sources.

High replacements of FM with some alternative protein ingredients from plants and animals become problematic in marine fish species. Inclusion of poultry by-product meal into diets at high levels is generally well accepted by several marine carnivorous species as long as the essential amino acids are balanced. On the other hand, plant ingredients contain indigestible carbohydrates that often reduce the digestibility of the diet and lead to histological and functional changes to the gastrointestinal tract. Plant ingredients through various mechanical and chemical processes into more concentrated forms are recommended for inclusion into marine fish diets. However, palatability can become a problem with concentrated ingredients. Therefore, the inclusion of feeding stimulants is necessary to increase feed intake. Feeding stimulants can also be used to improve digestibility by increasing feed intake and utilization of available nutrients in cold water and temperate fish species through increased digestive enzyme activity.

Compared with most cold water fish, temperate species have a lower tolerance to high dietary lipid contents at cooler temperatures. In temperate species, high lipid diets (30% CL inclusion) can increase lipid deposition into the visceral cavity at cooler temperatures, indicating an ineffective use of nutrients. At optimal temperatures, some warm water species do not tolerate diets containing high levels of dietary lipid >15%. Regardless of temperature, all marine species have a dietary requirement for the n-3 LC-PUFA, EPA and DHA. Cold water, temperate and warm water species all require between 1% and 3% of n-3 LC-PUFA in the diet. The actual essential FA requirement for fish is quite low, therefore when FO is replaced by alternative lipid ingredients the main issue is whether the FA composition of the fillet is acceptable from a human dietetic standpoint.

Temperature also affects the ability of fish to utilize alternative lipid ingredients. For example, at colder temperatures alternative lipid ingredients containing more saturated and monounsaturated fatty acids are more difficult to digest and utilize than ingredients containing high levels of PUFA. The requirement for n-3 LC-PUFA in cold and temperate water species, particularly at cooler temperatures is necessary for maintaining membrane flexibility and permeability. Care must be taken to ensure dietary fatty acid requirements for fish species are met when replacing FO with alternative plant and animal lipid ingredients. Since most alternative lipid sources do not contain n-3 LC-PUFA, full replacement with these sources leads to a higher deposition n-6 FA into the flesh and decreased levels of the essential n-3 LC-PUFA, which is undesirable for human nutrition, therefore devaluing the fish quality for human health.


  1. Top of page
  2. Abstract
  3. Introduction
  4. Cold water fish species (≤20°C)
  5. Temperate fish species (20–25°C)
  6. Warm water fish species (≥25°C)
  7. Conclusions
  8. Acknowledgement
  9. References

This review was written as partial fulfilment of the Flinders University PhD programme and whilst holding an Australian Seafood Cooperative Research Council (AS-CRC) scholarship and we would like to acknowledge this support.


  1. Top of page
  2. Abstract
  3. Introduction
  4. Cold water fish species (≤20°C)
  5. Temperate fish species (20–25°C)
  6. Warm water fish species (≥25°C)
  7. Conclusions
  8. Acknowledgement
  9. References
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