Total replacement of fish meal with black soldier fly (Hermetia illucens) larvae meal does not compromise the gut health of Atlantic salmon (Salmo salar)
Introduction
Marine ingredients in the Norwegian salmon diet have gradually been replaced by plant sources, decreasing from ~90% in 1990 to ~25% in 2016. Among the plant-based protein sources, soy protein concentrate accounted for 19.2% of the total diet ingredients followed by wheat gluten (9.0%), corn gluten (3.4%), horse beans (2.0%), pea protein concentrate (1.4%), faba beans (1.3%), sunflower meal (1.2%) and other marginally used plant proteins (2.7%) (Aas et al., 2018). While the future availability of plant proteins is guaranteed in the short-term (Shepherd et al., 2017), there is a need for new nutrient sources in Norwegian salmon aquaculture as the production volume is expected to grow. Moreover, as the world population is projected to reach 9.8 billion in 2050 (UN, 2017), global food production must maximize the nutritional output for human consumption and minimize the input of resources, with the lowest possible impact on the environment (Ytrestøyl et al., 2015). Hence, the salmon feed producers need to reduce their dependency on terrestrial plant products that may be used directly for human consumption, and seek new, sustainable feed ingredients for the future salmon aquaculture.
Insects possess an outstanding capacity to upgrade low-quality organic material, require minimal water and cultivable land, and emit little greenhouse gases (van Huis, 2013). At present, exploiting insects as feed ingredients is not in direct competition with food production. Black soldier fly (BSF; Hermetia illucens) is being produced at industrial scale in Europe due to its exceptionally good nutritional value and suitability for massive production. On a dry matter basis, BSF larvae contain about 42% protein and 35% lipid (Newton et al., 1977). In terms of protein quality, BSF larvae contains a favorable essential amino acid profile closer to fishmeal than that of soybean meal (Barroso et al., 2014). Moreover, the fat level and fatty acid profile are diet-dependent, allowing for control using different feed substrates (St-Hilaire et al., 2007a, St-Hilaire et al., 2007b). The potential of BSF larvae as an alternative feed ingredient for fish has been evaluated in several omnivorous and carnivorous species including Atlantic salmon (Belghit et al., 2018; Bondari and Sheppard, 1987; Borgogno et al., 2017; Devic et al., 2017; Hu et al., 2017; Kroeckel et al., 2012; Li et al., 2016; Li et al., 2017; Lock et al., 2016; Magalhaes et al., 2017; Renna et al., 2017; Sealey et al., 2011; St-Hilaire et al., 2007a, St-Hilaire et al., 2007b). The optimal substitution level of fishmeal in the diet by BSF larvae meal varies considerably in different studies ranging from 25% to 100%, possibly due to differences in the larvae meal quality, fish species and diet formulation. While the nutritional value of BSF larvae meal has been extensively studied, its impact on fish health, the gut health in particular, has not been investigated.
The present study was part of a larger investigation consisting of a freshwater and seawater feeding trial that aimed to reveal the nutritional value and possible health effects for Atlantic salmon, of a protein-rich insect meal (IM) produced from BSF larvae. In the 8-week freshwater trial, pre-smolt salmon were fed either a reference diet or a test diet wherein 85% of the dietary protein was supplied by BSF larvae meal. The gut health of fish was evaluated using endpoints including organ and tissue indices, histopathology variables and gene expressions (Li et al., 2019). Results from the freshwater trial showed no indications that dietary inclusion of insect meal may affect the gut health of Atlantic salmon negatively. The insect meal diet seemed to reduce excessive lipid deposition in the pyloric caeca enterocytes and stimulate xenobiotic metabolism (Li et al., 2019). The present study focuses on the gut health in the seawater-phase salmon fed BSF larvae meal for 16 weeks. Post-smolt Atlantic salmon was fed either a reference diet with a combination of fish meal, soy protein concentrate, pea protein concentrate, corn gluten and wheat gluten as protein sources, or a test diet wherein all the fish meal and most of pea protein concentrate were replaced by BSF larvae meal. The gut health of seawater-phase salmon fed a commercially-relevant reference diet and an insect meal test diet was evaluated using the same endpoints measured in the freshwater trial (Li et al., 2019).
Section snippets
Diets and fish husbandry
A feeding trial with seawater-phase Atlantic salmon (initial body weight 1.40 kg, S.D. = 0.043 kg) was conducted at the Gildeskål Research Station (GIFAS), Nordland, Norway, in accordance with laws regulating the experimentation with live animals in Norway. Fish were fed either a commercially-relevant reference diet (REF) with a combination of fish meal, soy protein concentrate, pea protein concentrate, corn gluten and wheat gluten as protein source, or an insect meal diet (IM) wherein all the
Results
To aid readers in interpreting data reported here, results on general fish performance and nutrients utilization, which have been published elsewhere (Belghit et al., 2019), are summarized below.
Both diets were readily accepted by the salmon throughout the whole feeding trial. No differences between the diet groups were recorded for feed intake, feed conversion ratio, body weight gain, protein productive value or whole-body proximate composition. Condition factor, hepatosomatic and
Discussion
In the present study, total replacement of fish meal with BSF larvae meal was associated with a lower degree of steatosis in the proximal intestine and a higher relative weight of distal intestine. Furthermore, replacing fish meal with insect meal in the diet of salmon was associated with increased submucosa cellularity in the proximal intestine.
In our previous experiment, pre-smolt Atlantic salmon were fed a test diet for 8 weeks wherein BSF larvae meal accounted for 60% of the total diet
Data and code availability
The data and code used for the statistical analyses and creation of figures are deposited at the GitHub repository (https://github.com/yanxianl/AquaFly-SeawaterGutHealth-Aquaculture-2019).
Funding
This work is part of the “AquaFly” project (grant number, 238997), funded by the Research Council of Norway, Norway, grant number: 38997. Y.L. is pursuing his Ph.D. degree at NMBU with a scholarship granted by the China Scholarship Council (CSC), a non-profit organization sponsoring Chinese citizens to study abroad. Other costs related to this study were covered by the NMBU. The funding agencies had no role in study design, data collection, and interpretation, decision to publish or preparation
Declaration of Competing Interest
The authors declare no competing financial interest.
Acknowledgements
The authors gratefully acknowledge Ellen K. Hage for organizing the sampling and conducting part of the lab work. Thanks are also due to technicians at the Gildeskål Research Station (GIFAS) for their committed animal care and supports during the sampling.
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