Marginal efficiencies of long chain-polyunsaturated fatty acid use by barramundi (Lates calcarifer) when fed diets with varying blends of fish oil and poultry fat

doi:10.1016/j.aquaculture.2015.02.027

Aquaculture

Volume 449, 1 December 2015, Pages 48-57

https://doi.org/10.1016/j.aquaculture.2015.02.027 Get rights and content

Highlights

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This study examined the effects of replacing fish oil with poultry fat in barramundi.
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No impact on growth, feed intake or feed conversion was observed.
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By reducing the dietary fish oil it was possible to double the retention of LC-PUFA.
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The oil blends allowed the determination of the marginal efficiencies of fatty acids.
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The marginal efficiencies of LC-PUFA utilisation by barramundi varied substantially.

Abstract

An experiment was conducted with barramundi (Lates calcarifer) juveniles to examine the marginal efficiency of utilisation of long chain-polyunsaturated fatty acids (LC-PUFA). A series of five diets with blends of fish (anchovy) oil and poultry fat (F100:P0, F60:P40, F30:P70, F15:P85, F0:P100) were fed to 208 ± 4.1 g fish over a 12-week period. The replacement of fish oil with poultry fat had no impact on growth performance (average final weight of 548.3 ± 10.2 g) or feed conversion (mean = 1.14 ± 0.02). Analysis of the whole body composition showed that the fatty acid profile reflected that of the fed diet. However it was also shown that there was a disproportional retention of some fatty acids relative to others (notably LOA, 18:2n-6 and LNA, 18:3n-3). By examining the body mass independent retention of different fatty acids with differential levels of intake of each, the marginal efficiencies of the use of these nutrients by this species were able to be determined. The differential retention of fatty acids in the meat was also examined allowing the determination of oil blending strategies to optimise meat n-3 LC-PUFA levels.

Introduction

The replacement of fish oil (FO) with alternative oil sources continues to be a high priority for aquafeed production worldwide. The barramundi (Lates calcarifer), also known as the Asian seabass, is an obligate carnivorous fish central to an expanding aquaculture industry in the Indo-Pacific region with a reported long chain-polyunsaturated fatty acid (LC-PUFA) requirement in juvenile fish of around 1.2% (Williams et al., 2006). However, variable responses of barramundi to FO replacement studies have led to questions being raised about the upper limits of FO substitution in this species (Glencross and Rutherford, 2011, Morton et al., 2014, Raso and Anderson, 2003, Tu et al., 2013). Poultry fat (PF) is produced as a by-product of the chicken processing industry and is characterised by its high 18:1n-9 and 18:2n-6 (oleic acid; OLA and linoleic acid; LOA, respectively) content (Turchini et al., 2009). Poultry fat is commonly used to replace FO in fish diets providing an excellent source of energy, however it is characterised by a lack of n-3 LC-PUFA (Turchini et al., 2009).

Depletion of LC-PUFA in the diet of barramundi can potentially lead to reduced productivity and the onset of essential fatty acid deficiency symptoms (Catacutan and Coloso, 1995, Glencross and Rutherford, 2011, Williams et al., 2006). Moreover, a lack of dietary LC-PUFA will also likely be reflected in the flesh, diminishing the human nutritional value of the product (Turchini et al., 2009). It is well established that the regular consumption of food rich in n-3 LC-PUFA is a fundamental part of a balanced diet and the Food and Agricultural Organisation (FAO) advocates the consumption of 250 to 2000 mg/day (EPA and DHA) for adults (FAO, 2010).

Highly variable or disproportionate retention of lipid or indeed specific fatty acids may indicate metabolic changes as a direct result of the fed diet. Thomassen et al. (2012) found that Atlantic salmon (Salmo salar) consuming a diet containing rapeseed oil with supplemental 20:5n-3 (eicosapentaenoic acid; EPA) oil had significantly higher 22:5n-3 (docosapentaenoic acid; DPA) retention via elongation of C20 to C22. Moreover, these fish selectively retained 22:6n-3 (docosahexaenoic acid; DHA) efficiently and in absolute terms the proportion of DHA was significantly improved when compared to those fish fed only rapeseed oil with no supplemental EPA. Similarly, a dramatic reduction of LC-PUFA retention was demonstrated in both barramundi and Atlantic salmon as dietary LC-PUFA increased (Glencross and Rutherford, 2011, Glencross et al., 2014). In contrast, Atlantic cod retained more LC-PUFA as intake increased (Hansen et al., 2008).

Efficient feed utilisation has a determinant effect on costs and outputs in aquaculture systems. In economics, a future return on an investment is estimated based on financial inputs and is termed the marginal efficiency of capital (Kalecki, 1937). Similarly, this concept can be applied in aquaculture nutrition in order to better understand the relationship between dietary inputs and fish outputs over time. It differs from deposition or retention in that it is not just a mass-balance model but rather is a bioenergetic approach based on the weight independent relationships between the intake and gain of a specific nutrient. The exact fate of ingested nutrients is difficult to measure, however calculation of the marginal (partial) efficiency can provide a clearer understanding of the discrete contributions of a dietary nutrient. The slope coefficient of the linear relationship is termed the efficiency of utilisation for production (k_pf), protein (k_p) and lipid (k_f) and this can be used to estimate the response over a range of nutrient intake levels independent of mass (NRC, 2011). Moreover, the slope of the regression can be further extrapolated until recovered energy for growth is equal to zero thus providing an estimate of nutrient maintenance requirements (NRC, 2011).

A number of studies have used this bioenergetic approach in determining the marginal efficiencies and estimating maintenance requirements of energy, lipid and protein in a variety of fish species. The marginal efficiencies of protein (k_p) and lipid (k_f) of a range of species including Atlantic salmon (Salmo salar), rainbow trout (Oncorhynchus mykiss), European seabass (Dicentrarchus labrax), gilthead sea bream (Sparus aurata), white grouper (Epinephelus aeneus) and yellow-tail kingfish (Seriola lalandi) generally range between k_p 0.53–0.64 and k_f 0.72–0.91 (Booth et al., 2010, Bureau et al., 2006, Helland et al., 2010, Lupatsch et al., 2003). In barramundi, Glencross and Bermudes (2010) showed that over a range of temperatures from 25 to 32 °C the partial efficiency of energy (k_pf) was relatively consistent at 0.56 and protein (k_f) was relatively consistent at 0.51. Despite the apparent importance of essential fatty acids (EFA) the energetic efficiencies and maintenance requirements of these nutrients do not appear to have been investigated in fish using a bioenergetics approach.

It was hypothesised that barramundi would reach a critical limit of FO substitution when absolute levels of dietary LC-PUFA dropped below estimated requirement of around 1.2% (Williams et al., 2006). Therefore a series of diets were developed to examine the effects of diluting fish oil with poultry fat on the growth and feed utilisation performance of juvenile barramundi and to determine the consequences of this on the fillet fatty acid profiles. This study also aimed to develop a strategy for fish oil replacement with defined impacts on meat n-3 LC-PUFA levels.

Section snippets

Ingredient and diet preparation

A single basal diet was formulated to provide protein at 53% and lipid at 16% with an energetic value of 22 MJ/kg. The dry ingredients were passed separately through a hammermill (Mikro Pulverizer, type 1 SH, New Jersey, USA) such that the maximum particle size was less than 750 μm. All ingredients were then thoroughly mixed in using an upright commercial mixer (Bakermix, Model 60 A-G, NSW, Australia). The chemical composition of the main dietary ingredients is presented in Table 1. The single

Growth performance and feed utilisation

During the 82-day growth period, the fish responded to the experimental diets, growing consistent with the predicted model growth (Glencross and Bermudes, 2012). Survival was 100% in all treatments. No significant differences were observed among the treatment diets in terms of growth performance (Table 3). During the growing period, there was greater than 2.5-fold increase in weight among the groups of fish with final fish weights ranging between 545 and 553 g. Similarly, there were no

Discussion

The benefits of regular consumption of seafood rich in n-3 LC-PUFA are well known. These fatty acids are implicated in a range of physiological and metabolic processes and many studies have demonstrated their positive benefit in the prevention and management of cardio-vascular disease and inflammation (Calder, 2012). The FAO's guideline to consume a dose of 250 mg/day EPA and DHA is an achievable yet rarely met target due to the production and subsequent consumption of the predominant vegetable

Conclusion

In conclusion, this study has demonstrated that poultry fat can completely substitute fish oil in growing barramundi. There were no aberrations to fish growth performance or feed utilisation parameters however there were clear differences in the retention and marginal efficiencies of LC-PUFA utilisation. The fish responded to increasing PF by improving the retention of LC-PUFA however the marginal efficiency of LC-PUFA was relatively low, and reasons for this need to be further explored.

Acknowledgments

The authors wish to acknowledge, Nick Polymeris and Dylan Rylatt for their technical support during the trial.

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Poultry by-product meal (PBM) as a replacement for fish meal (FM), an expensive and unsustainable protein aquafeed ingredient, has been tested on different aquaculture fish species. However, the complete replacement of FM with a mixture of PBM and Hermetia illucens (HI) larvae in barramundi culture has not been previously investigated. In this study, results are presented on growth performance, fillet fatty acid composition, serum metabolites, skin mucosal barriers, hepatic steatosis, antioxidant activity, and immunity of juvenile barramundi, Lates calcarifer fed either a FM-based diet (0PBM-0HI) or two test diets in which total FM protein was replaced by a mixture of 70% PBM and 30% full-fat (FHI) and defatted HI larvae (DHI) meal (designated as 70PBM-30FHI and 70PBM-30DHI). After 56 days of feeding, the results showed that the growth was affected when fish were fed 70PBM-30DHI with a higher feed conversion ratio (FCR) with respect to 0PBM-0HI and 70PBM-30FHI diets. There was no variation in growth performance, feed utilization, and FCR between 0PBM-0HI and 70PBM-30FHI. The retention of total saturated and monounsaturated fatty acids increased in the fillet of juveniles fed 70PBM-30FHI and 70PBM-30DHI while total retention of polyunsaturated (PUFA), n-3 PUFA, and n-6 PUFA decreased than the control. Serum alanine transaminase (ALT) increased in fish fed 70PBM-30DHI whereas haptoglobin upsurged in 70PBM-30FHI compared to 0PBM-0HI. There were no significant effects in the serum immune response between dietary treatments whilst serum and liver CAT activity were negatively impacted by 70PBM-30DHI. The 70PBM-30DHI induced hepatic steatosis whilst 0PBM-0HI and 70PBM-30FHI showed no obvious change in the liver. Skin mucosal barriers were impacted by 70PBM-30DHI whilst 70PBM-30FHI fed fish showed a similar response to 0PBM-0HI. The fish fed on 70PBM-30DHI showed a higher proportion of infection rate with Vibrio harveyi than 70PBM-30FHI but showed no variation with the control-fed fish. In summary, FHI larvae meal could be a good complementary protein source, particularly when replacing FM completely with insect-based proteins.
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Different saturated and monounsaturated fatty acids levels in fish oil-free diets to cobia (Rachycentron canadum) juveniles: Effects in growth performance and lipid metabolism
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Citation Excerpt :
The fas expression was up-regulated in liver of fish fed FO-D and MUFA-D, possibly due to the lower SFA levels, especially 12:0, on these diets, while higher levels in SFA-D and MUFA-D. Given the physiological importance of 16:0 in phospholipids composition (Tocher et al., 2008), and the preferential FA oxidation order of SFA (Tocher, 2003), from shorter to longer carbon chains, fas expression was possibly up-regulated to compensate the lower SFA levels in FO-D and MUFA-D. Several studies with different fish species have shown more oxidation of SFA and MUFA when offered in excess, and consequently preserving the LC-PUFA, especially in the muscle (Turchini et al., 2011b; Salini et al., 2015a; Bowzer et al., 2016; Qiu et al., 2017; Rombenso et al., 2017). Also, high dietary PUFA, as usually occurs in FO-based diets, may not be the most efficient practice, as the excess of these FA are commonly oxidized (Torstensen et al., 2000; Salini et al., 2015b). In T. carolinus (Rombenso et al., 2016a), MUFA were accumulated in tissues as the dietary inclusion of this FA increased.
This study aimed to investigate the influences of alternative lipid sources rich in saturated and monounsaturated fatty acids (SFA and MUFA) supplemented with long-chain polyunsaturated fatty acids (LC-PUFA) on production performance and lipid metabolism of Rachycentron canadum (cobia) juveniles. An 8-week feeding trial was carried out using four isoproteic and isolipidic diets as follows: FO-D (fish oil, as control diet), SFA-D (rich in SFA), MIX-D (same levels of SFA and MUFA), and MUFA-D (rich in MUFA). Experimental diets were supplemented with arachidonic acid (ARA), eicosapentaenoic acid (EPA), and docosahexaenoic acid (DHA) (3, 5, and 10 g kg¹, respectively). The growth performance, fatty acid (FA) profile of liver and muscle, hepatocyte morphology, and gene expression related to the FA synthesis and oxidation on the liver were examined. In general, production performance was not impaired in fish-fed FO-free diets, supporting the hypothesis that alternative lipid sources could be used in cobia's aquafeed formulations when the LC-PUFA are adequately supplemented. High dietary SFA levels were disproportionally deposited the liver and muscle. Contrariwise MUFA was mainly deposited in the liver and muscle, reflecting the dietary inclusion levels. The main FA influencing this pattern were 12:0 and 18:1n-9. The expression of fatty acid synthase (fas) was up-regulated in the FO-D group compared to SFA-D and MIX-D groups. There were no differences in the relative expressions of carnitine palmitoyltransferase 1 (cpt-1α) and lipase lipoprotein (lpl). The liver morphology results indicated that fish-fed SFA-D presented a smaller lipid vacuoles area than those fed other experimental diets. This study shows that SFA with shorter carbon chains such as 12:0 can be administered in cobia aquafeeds to stimulate these molecules' catabolism, providing energy for growth, and retaining LC-PUFAs in tissues, especially in the muscle, exhibiting a healthier fillet for consumers.
Hepatic biochemical, morphological and molecular effects of feeding microalgae and poultry oils to gilthead sea bream (Sparus aurata)
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Citation Excerpt :
PO shows a competitive price and availability and has a high potential as energy source given its high saturated (SFA) and monounsaturated fatty acids (MUFA) contents but lacks n-3 LC-PUFA (Rosenlund et al., 2001; Higgs et al., 2006; Hatlen et al., 2015). It has been incorporated as supplemental lipid source or partial replacer of FO in diets for some aquaculture species (Higgs et al., 2006; Hatlen et al., 2015; Turchini et al., 2013; Liland et al., 2015; Salini et al., 2015; Campos et al., 2019). A recent study by our research group found similar growth performance and enhanced fillet DHA deposition in gilthead sea bream fed a blend of microalgae oils and PO when compared to those fed FO (Carvalho et al., 2020).
The present work investigated how the combination of poultry oil with microalgae oils, rich in eicosapentaenoic acid and docosahexaenoic acid (ED diets) or n-6 docosapentaenoic acid and n-3 docosahexaenoic acid (DD diets) modulates hepatic lipid metabolism in gilthead sea bream juveniles. Diets were tested using two different fishmeal contents (15% and 7.5%) and compared against a fish oil-based diet (CTRL) and two negative control diets based on poultry oil as lipid source (PO diets). After 74 days of feeding, sea bream fed 15% FM ED or DD diets showed similar daily growth index to those fed CTRL, while those fed PO diets caused reduced growth. Fish livers reflected the highest contents in n-3 long-chain polyunsaturated fatty acids when fed CTRL, ED or DD diets, which down-regulated fas, scd-1a, fads2, lpl and cpt1, reducing hepatic lipid accumulation and hepatocytes size. In contrast, fish fed PO diets showed the lowest deposition of n-3 long-chain polyunsaturated fatty acids and the highest oleic acid in liver, leading with the highest hepatosomatic index due to increased liver lipids. Therefore, these fish revealed a severe hepatic steatosis associated with an increased expression of lipogenesis-related genes, particularly fas, lpl and sbrep1. Furthermore, PO diets seemed to activate desaturation pathways in fish livers, reflected by the highest accumulation of fatty acids that are products from desaturases and the highest fads2 and scd-1a expressions. The reduction of the dietary fishmeal content to 7.5% lowered fish growth, although hepatic lipid metabolism seemed to be more affected by FO replacement than FM replacement. Combining microalgae with poultry oil could be an alternative lipid and essential fatty acid source to fish oil in marine fish diets.
Effective complete replacement of fish oil by combining poultry and microalgae oils in practical diets for gilthead sea bream (Sparus aurata) fingerlings
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Few ingredients allow the complete replacement of fish meals (FM) and fish oils (FO) in aquaculture feeds without affecting fish performance or fillet nutritive value. This is due to the adequate content of essential nutrients, including the n-3 long-chain polyunsaturated fatty acids (n-3 LC PUFA), and the unique high palatability of FM and fish oil. Some microalgae present abundant amounts of these fatty acids, for instance docosahexaenoic acid (DHA). Therefore, the aim of the present study was to evaluate the effect of two different microalgae products, one providing DHA and eicosapentaenoic acid (EPA, 20:5n-3; ED diet), and the other one DHA and n-6 docosapentaenoic acid (DPA, 22:5n-6; DD diet), in combination with poultry oil and rapeseed oil, as total replacers of fish oil, at two different dietary fish meal contents (15 and 7.5%). The effects of these dietary oil combinations on performance, composition and nutritive quality indexes of gilthead sea bream (Sparus aurata) juveniles were studied and compared against a positive control diet (FO) and two negative control diets (PO diets), one for each dietary fish meal content tested, giving in total 7 experimental diets. Both microalgae products in combination with poultry and rapseed oils were able to completely replace fish oil in practical diets with 15% FM without affecting growth performance, utilization of dietary fatty acids or the nutritional quality of fish fillet for the consumer. On the contrary, PO alone was not able to completely replace fish oil and negatively affected fish performance, in relation to an insufficient dietary n-3 LC-PUFA content. A similar decrease in growth performance was also observed with the reduction of the dietary FM content to 7.5%. In conclusion, both oils from microalgae, providing either DHA and EPA or DHA and n-6 DPA, were effective n-3 LC-PUFA sources for sea bream juveniles and allowed complete replacement of fish oil in combination with more cost-effective lipid sources, such as poultry and rapeseed oils.
Are fish what they eat? A fatty acid's perspective
2020, Progress in Lipid Research
Citation Excerpt :
In most studies, fish oil treatments indeed resulted in lower D values for muscle tissue than alternative lipid sources (seawater studies: [50,77,81–103]; freshwater studies: [46,76,104–133]. However, the opposite was also observed in numerous studies, in which fish oil generally resulted in lower D values compared to alternative lipid sources, particularly in comparison to treatments containing a blend of alternative oils (seawater studies: [30,134–142]; freshwater studies: [143–147]). Where the use of fish oil in the diet resulted in a higher disparity between fish muscle and diet in comparison to other specific oils or oil blends, this suggests that, from a human nutritional viewpoint, dietary fish oil has been underutilised, or potentially “wasted”.
Fish are the main source of long-chain polyunsaturated fatty acids (LC-PUFA, >C₁₈) for human consumption. In general, it has been widely observed that the fatty acid (FA) profiles of farmed fish are reflective of the diet. However, the degree of tissue FA “distortion” based on incorporation of different dietary FA into fish tissues varies greatly depending on FA type, fish species and environmental factors. In terms of fish FA composition, this variation has not been comprehensively reviewed, raising the question: “Are fish what they eat?”. To date, this remains unanswered in detail. To this end, the present review quantitatively summarized the ‘diet-fish’ FA relationship via an analysis of FA composition in diets and fish tissues from 290 articles published between 1998 and 2018. Comparison of this relationship among different fish species, tissue types or individual FA was summarized. Furthermore, the influence of environmental factors such as temperature and salinity, as well as of experimental conditions such as fish size and trophic level, feeding duration, and dietary lipid level on this relationship are discussed herein. Moreover, as a means of restoring LC-PUFA in fish, an emphasis was paid to the fish oil finishing strategy after long-term feeding with alternative lipid sources. It is envisaged that the present review will be beneficial in providing a more comprehensive understanding of the fundamental relationship between the FA composition in diets, and subsequently, in the farmed fish. Such information is integral to maintaining the quality of farmed fish fillets from the perspective of FA composition.

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Marginal efficiencies of long chain-polyunsaturated fatty acid use by barramundi (Lates calcarifer) when fed diets with varying blends of fish oil and poultry fat

Highlights

Abstract

Introduction

Section snippets

Ingredient and diet preparation

Growth performance and feed utilisation

Discussion

Conclusion

Acknowledgments

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