Effect of partial replacement of dietary fish meal and oil by pumpkin kernel cake and rapeseed oil on fatty acid composition and metabolism in Arctic charr (Salvelinus alpinus)
Introduction
The availability, cost and environmental sustainability of feed fish are some of the main bottlenecks preventing the expansion of the aquaculture industry (Tocher et al., 1997, Worm et al., 2006). Farmed carnivorous fish are traditionally fed diets containing large amounts of marine fish meal (FM) and fish oil (FO) (Torstensen et al., 2008). Fish meal is the major protein source in feeds, while FO provides the major source of lipids, including omega-3 long-chain polyunsaturated fatty acids (n − 3 LC-PUFA). Both proteins and lipids derived from FM and FO serve a variety of important biological functions in fish and are important in human nutrition (Drevon, 1992, Nyina-Wamwiza et al., 2010). On the basis of increasing global FM and FO costs, alternative protein and lipid sources are required to ensure the economic and environmental viability of the aquaculture industry (Bendiksen et al., 2011, Tacon and Metian, 2008, Turchini et al., 2009).
Fish oil contains high amounts of n − 3 LC-PUFA, such as eicosapentaenoic acid (EPA; 20:5n − 3) and docosahexaenoic acid (DHA; 22:6n − 3) (Kaushik et al., 1995, Turchini et al., 2009) that are highly retained in farmed fish (Bell et al., 2003, Torstensen et al., 2005). Despite lacking n − 3 LC-PUFA, vegetable oils (VO) have been proposed as sustainable alternatives to dietary FO (Torstensen et al., 2005) with various studies finding no deleterious impact on the health or growth rate of farmed fish when FO was replaced with VO (Bell et al., 2001, Seierstad et al., 2005, Torstensen et al., 2000, Waagbó et al., 1995). However, it is widely accepted that complete or partial replacement of FO with VO reduces particularly the n − 3 LC-PUFA content of fish tissues (Bell et al., 2003, Bell et al., 2004, Mourente and Bell, 2006, Torstensen et al., 2005), which is a concern for the general fish condition and nutritional value to the consumer.
Although tissue fatty acid compositions are closely correlated with those of dietary supply, many fish, including Atlantic salmon (Salmo salar) and brown trout (Salmo trutta) can convert α-linolenic acid (ALA; 18:3n − 3) to EPA and DHA, albeit rather inefficiently (Tocher, 2003). Understanding and utilising this biosynthetic pathway through the provision of VO-derived precursors may enable farmed fish to meet their physiological n − 3 LC-PUFA requirements, even if these n − 3 LC-PUFA are not sufficiently supplied within the diet (Tocher, 2003). Rapeseed oil appears to be a particularly effective alternative due to its lower cost, but higher sustainability and relatively high amounts of the essential n − 3 LC-PUFA precursor ALA (Bell et al., 1997, Bell et al., 2001, Tocher et al., 2001a, Tocher et al., 2001b, Turchini et al., 2009).
Sustainable alternatives to FM include vegetable meals containing 20–50% crude protein, which can approach the levels found in FM typically fed to intensively reared fish (Hertrampf and Piedad-Pascual, 2000, Van Weerd, 1995). Fish meal can be partially or totally replaced with alternative plant protein sources without affecting the survival or growth rate of farmed fish (Fagbenro, 1999, Gomes et al., 1995, Kaushik et al., 1995, Nyina-Wamwiza et al., 2010). However, the use of plant derived protein sources as feed ingredients is limited by the presence of anti-nutritional factors (ANFs) that inhibit specific metabolic pathways, decreasing digestibility and nutrient absorption (Francis et al., 2001).
Methods such as cooking, dehulling, germination, roasting, soaking and extrusion cooking can reduce the presence of ANFs improving plant protein digestibility and utilisation by farmed fish (Nyina-Wamwiza et al., 2010). Many terrestrial meals, such as sunflower oil cake (Nyina-Wamwiza et al., 2010), palm kernel cake (IIuyemi et al., 2010), soybean seed meal (Robaina et al., 1995) and cottonseed meal (Robinson and Li, 1994), and recently pumpkin kernel cake are of particular interest as potential protein sources for farmed fish. Pumpkin seeds contain approximately 32% crude protein and, after oil extraction, up to 70% of dry matter in the kernel cake (Sharma et al., 1986). Furthermore, during a comparative nutritional study, Zdunczyk et al. (1999) reported that pumpkin kernel cake contained a higher crude protein content and fewer ANFs compared to soybean meal.
While many previous investigations identified how FM or FO replacements affected a variety of physical and biochemical variables, less is known about how dual replacement of both marine proteins and lipids with terrestrial alternatives affects the growth rate and fatty acid composition of farmed fish (Torstensen et al., 2008, Turchini et al., 2009). In addition, the use of pumpkin kernel cake as the main source of protein in feed has never been examined in farmed freshwater salmonids, such as Arctic charr (Salvelinus alpinus) that is increasingly farmed (FAO, 2012). Therefore, in the current study we address this question directly by examining the effect of partial replacement of dietary FM and FO with graded amounts of pumpkin kernel cake and rapeseed oil on the growth rate, tissue fatty acid profiles and metabolism in consumer-sized Arctic charr. Our null hypothesis was that there is no difference in the growth rate or tissue fatty acid profiles among the fish feeding on the different diets. Thus, our underlying assumption was that pumpkin kernel cake and rapeseed oil in fish feeds can fully replace commonly used FM and FO resulting in equal fish growth rates. In addition, fish provided with dietary rapeseed oil will endogenously convert dietary ALA to the n − 3 LC-PUFA EPA and DHA and thus prevent any discernable differences in tissue fatty acid profiles compared to fish fed feeds containing typically high contents of FM and FO.
Section snippets
Fish, husbandry and experimental diets
Arctic charr (15–20 g body weight) from the same strain (fish hatchery in Lunz am See, Austria) were held at the aquarium facilities at the WasserCluster Research Centre from August 2012 until October 2013. The experiment was conducted in a flow-through system containing twelve 1000-L rectangular tanks with a continuous supply of gravel filtered spring water (ca. 25 L min− 1). Waste water was drained using a sink hole covered by a 5 mm mesh screen. Fish were subjected to a natural photoperiod
Diet composition
All feeds contained similar contents of total proteins (~ 43–45%), total lipids (~ 23–25%), total ash (~ 8–10%), and moisture (~ 6–9%; Table 2). The contents (mg FA per unit biomass) for total saturated fatty acids (SAFA) decreased 1.4-fold from diets F1 to F4 (Table 3). There was a 1.6-fold decrease in total n–3 PUFA contents between diets F1 and F4, specifically a 4.0 and 4.2-fold decrease in DHA and EPA, respectively (Table 3). Alternatively, total monounsaturated fatty acid (MUFA) contents
Discussion
This study demonstrated that partial replacement of FM and FO with pumpkin kernel cake and rapeseed oil resulted in reduced specific growth rates and a decrease in Arctic charr biomass, particularly with the highest inclusion levels in diet F4, compared to fish fed the F1 diet. These results are in contrast to previous studies that showed no significant impact of individual replacement of either vegetable meals (Gomes et al., 1995, Guillou et al., 1995, Kaushik et al., 1995) or rapeseed oil (
Acknowledgements
This work received financial support from the Austrian Ministry of Life (project Nr. 100837; BMLFUW-LE.1.3.2/0051-II/1/2012) and material support from GARANT Tiernahrung Austria. We are grateful for technical assistance and support from Eduard Schneeberger, and veterinary supervision by Heinz Heistinger. We also thank Katharina Drucker, Katharina Hader, Katharina Winter, and Zahra Changizi for their laboratory assistance.
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