The impact of dietary protein: lipid ratio on growth performance, fatty acid metabolism, product quality and waste output in Atlantic salmon (Salmo salar)
Introduction
The central objective for aquaculture producers is to achieve optimal fish performance whilst minimising production expenses, including the cost of aquafeed. Therefore, aquafeed manufacturers aim to supply products that efficiently utilise dietary nutrients whilst simultaneously reducing the inclusion of increasingly expensive marine-derived ingredients (Hixson, 2014). The resultant dietary formulations inevitably involve a series of ‘trade-offs’ between the cost of added macronutrients, adequate provision of nutrients for both anabolism (growth and tissue synthesis) and catabolism (metabolic energy), nutritional and organoleptic quality of the final product and limiting the negative impacts on the surrounding aquatic environment (Bendiksen et al., 2011; Bureau, 2004; Tocher, 2015; Turchini et al., 2010).
A common strategy for aquafeed manufacturers has been the utilisation of relatively large concentrations of terrestrial animal and plant oil sources to produce diets with a high energy content. Traditionally referred to as ‘protein sparing’, the provision of high fat diets promotes the utilisation of energy from lipid, thus increasing the amount of dietary protein available for tissue synthesis (Einen and Roem, 1997; Francis and Turchini, 2017; Karalazos et al., 2011b; Kaushik and de Oliva Teles, 1985). The protein sparing concept has been particularly popular in salmonid aquaculture, given the innate ability of this species to efficiently use large amounts of dietary lipids as an energy source (Karalazos et al., 2011b; Kaushik and Médale, 1994). Thus, coupled with the historically lower price of dietary lipid in comparison to protein sources, high energy formulations are widely favoured in Atlantic salmon aquafeed (Bendiksen et al., 2011; Einen and Roem, 1997; Pratoomyot et al., 2010; Turchini et al., 2010). However, various lipid sources are now as, if not more, expensive than protein sources, in particular those rich in omega-3 long-chain polyunsaturated fatty acids (n-3 LC PUFA) such as marine based oils. This is a function of stagnant supply of marine derived oils and increasing demand from aquaculture, agriculture and nutraceutical sectors (Francis and Turchini, 2017; Tacon and Metian, 2008; Turchini, 2013; Turchini et al., 2010). At the same time, the well-documented health benefits of n-3 LC PUFA consumption have influenced consumer expectation of farmed fish to provide a dependable source of edible n-3 LC PUFA (Christenson et al., 2017; Tur et al., 2012; Turchini et al., 2011). The Atlantic salmon aquaculture industry sits at the centre of this paradox given their reputation as reliable source of edible n-3 LC PUFA whilst itself consuming a relatively high proportion of globally available fish oil. Given the increased value placed on dietary sources of n-3 LC PUFA, attempts have been made to retro-engineer the protein sparing concept in which high lipid diets are fed to fish in order to conserve protein for growth. Francis and Turchini (2017) on the other-hand proposed the provision of high protein diets in order to conserve n-3 LC PUFA from catabolism in Atlantic salmon… It is known that dietary n-3 LC PUFA, including 20:5n-3 and 22:6n-3 are readily β-oxidised for metabolic energy when in excess of physiological requirements (Codabaccus et al., 2011; Stubhaug et al., 2007). Hence, it has been hypothesised that in contrast to the protein sparing concept, an increase in the protein: lipid ratio would increase the utilisation of dietary protein for catabolic processes and thus favour the retention of dietary fatty acids, in particular, n-3 LC PUFA. However, to date results have been inconclusive and further investigation has been suggested (Francis and Turchini, 2017). Despite this, an increase in the dietary protein: lipid ratio has been shown to improve feed efficiency and growth in farm reared Atlantic salmon (Weihe et al., 2018).
Importantly, however, any variation of the dietary protein: lipid ratio in aquafeed would not only affect the growth and nutritional quality of Atlantic salmon, but a sub-optimal digestible protein: digestible lipid ratio would decrease nitrogen retention efficiency. This would stimulate the catabolism of protein for energy, resulting in an increase of dissolved nitrogenous waste, predominantly, ammonia (Crab et al., 2007; Hardy and Gatlin, 2002; Karalazos et al., 2011a; Kaushik and Cowey, 1991). Poor dietary protein retention causes an increased output of undigested nitrogen entering the surrounding aquatic environment, eliciting potentially deleterious effects on water quality, including eutrophication, particularly in close proximity to the farming operation (Amirkolaie, 2011; Crab et al., 2007; Rabalais, 2002; Wu, 1995). Meanwhile, aquaculture operations are subject to enhanced scrutiny to limit nitrogenous waste effluent, and as a result, effective nutritional strategies are being sought (Australian Government, 2015; Cho and Bureau, 2001; Crab et al., 2007; Hardy and Gatlin, 2002). Various approaches have been implemented by aquaculture operations to address this, including; reducing uneaten feed and tailoring the digestible protein: digestible lipid ratio to limit the amount of protein which is undigested or catabolised for metabolic energy (Bureau, 2004; Cho and Bureau, 1997; Cho et al., 1994; Crab et al., 2007). Specifically, a decrease in the dietary protein: lipid ratio has been shown to significantly reduce nitrogenous waste output in intensive aquaculture systems due to an increase in nitrogen retention efficiency (Crab et al., 2007; Einen and Roem, 1997; Hardy and Gatlin, 2002; Kaushik, 1998; Kaushik and Médale, 1994).
Despite the clear importance of this topic, published information quantifying the effect of an altered dietary protein: lipid ratio in grow-out diets for Atlantic salmon on the nutritional quality of the fish, fatty acid metabolism and protein utilisation, remains sparse, especially in relation to the farming conditions of the southern hemisphere (Francis and Turchini, 2017; Weihe et al., 2018). Furthermore, the extent of possible n-3 LC PUFA sparing remains unclear. Thus, the adoption of modified dietary formulations which limit the negative environmental impact of Atlantic salmon aquaculture may be impeded by a lack of available research data. This is compounded by the lack of data with specific regard to large, seawater reared Atlantic salmon, whose physiological requirements, including protein and lipid utilisation change with life history stage (Handeland et al., 2003; Rosenlund et al., 2016). Therefore, this study aimed to compare two commercial-like, isoenergetic diets, both containing the same raw materials and dietary oil blend (80% poultry by-product oil and 20% fish oil), but with varied protein: lipid ratios; one containing40% protein and 33% lipid (40:33) and the other containing 36% protein and 36% lipid (36:36). These diets were tested on-farm, in a real-word/commercial environment over a five month grow-out period, involving an assessment of industry relevant production performance indicators, such as: nutrient digestibility, fillet fatty acid composition and utilisation, taste evaluation of fillets and an evaluation of undigested protein output. Furthermore, the potential disparity between feed related production costs between the two diets was assessed through a preliminary bio-economic analysis.
Section snippets
Location, animals, experimental design and sampling
The present trial was conducted from May 24 to October 20, 2015 (150 days) on a commercial Atlantic salmon (Salmo salar) farm in Hideaway bay, Dover, Tasmania (Huon Tasmania, Hideaway bay site; 43°15′ 52.2″S 147°04′37.7″E). Immediately preceding the allocation of fish for the trial, an initial sample of 6 fish was randomly selected from the trial cohort, euthanized in excess anaesthetic (AQUI-S, 0.5 mL L−1) and stored at −20 °C until subsequent analysis. One-thousand six hundred and twenty
Feed composition
The feeds were formulated to be isoenergetic and proximate analysis confirmed this (~25.5 KJ g−1) (Table 1). In-line with the feed formulations the protein concentration differed between the two feeds (403.9 and 357.0 mg g−1 diet in 40:33 and 36:36, respectively). The lipid concentration of the feeds also represented the feed formulations (330.5 and 367.7 mg g−1 diet in 40:33 and 36:36, respectively). Accordingly, the protein:lipid ratio of the two experimental feeds were 1.2 and 1.0 in 40:33
Discussion
This study has clearly demonstrated that a variation in the dietary protein: lipid ratio, at the range examined in this study, has no significant effect on growth performance, fatty acid metabolism or final product quality. However, a reduction in the dietary protein: lipid ratio reduced the amount of undigested protein resulting in a reduction in nitrogenous waste. However, the bio-economical analysis revealed that due to small, yet important, differences in growth parameters, an increased
Conclusion
The present study suggests that a reduction in the protein: lipid ratio in aquafeed formulations for market-sized Atlantic salmon elicits minimal effects on lipid and fatty acid utilisation and ultimately found no reduction in fillet nutritional quality including levels of n-3 LC PUFA. Additionally, taste quality was not compromised. Importantly, a significant reduction in undigested nitrogenous waste was observed when the dietary protein: lipid ratio was decreased. However, whereas overall
Conflict of interest
The authors wish to declare funding and donation of materials for the growth trial from Ridley Aquafeed Ltd. (Brisbane, Australia). The authors wish to clarify that the current trial compared different lipid sources in aquafeed and was not directly comparing commercially produced products by Ridley Aquafeed Ltd.
Acknowledgements
The authors gratefully acknowledge the assistance and support from Ridley AquaFeed (Brisbane, Australia) and Huon Aquaculture Ltd. (Dover, Australia). The authors also wish to thank Dr. Karen Hermon for technical assistance and Adrian Steenholdt for management of the feeding trials for their valuable contribution.
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