Total replacement of fish meal with black soldier fly (Hermetia illucens) larvae meal does not compromise the gut health of Atlantic salmon (Salmo salar)

Highlights

• Replacement of fish meal with insect meal does not compromise gut health of seawater phase Atlantic salmon.

• Reduced enterocyte steatosis in the proximal intestine of fish fed insect meal diet.

• Increased relative weight of distal intestine in fish fed insect meal diet.

Abstract

Limited availability of sustainable feed ingredients is a significant concern in salmon aquaculture. Insects may become an important, sustainable resource for expanding the raw material repertoire. Herein, we present data from a 16-week seawater feeding trial with Atlantic salmon (initial body weight, 1.4 kg) fed either a reference diet with a combination of fish meal, soy protein concentrate, pea protein concentrate, corn gluten and wheat gluten as protein source, or a test diet wherein all the fish meal and most of the pea protein concentrate were replaced by black soldier fly larvae meal. The gut health of fish was evaluated using endpoints including organ and tissue indices, histopathology variables and gene expression indicative of lipid metabolism, immune responses, barrier functions and detoxification/stress responses. A higher relative weight of distal intestine was found in fish fed the insect meal diet. Steatosis of enterocytes was observed in the proximal and mid intestine in both diet groups, albeit, less severe in the proximal intestine of fish fed the insect meal diet. Inflammatory morphological changes, similar to those induced in the distal intestine by standard soybean meal, were present in all the examined intestinal segments, with a higher degree of submucosa cellularity in the proximal intestine of insect meal diet fed fish, the only notable diet effect. Few differentially expressed genes were identified in the proximal or distal intestine. In summary, total replacement of fish meal with black soldier fly larvae meal did not compromise the gut health of Atlantic salmon.

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Marine ingredients in the Norwegian salmon diet have gradually been replaced by plant sources, decreasing from ~90% in 1990 to ~25% in 2016.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).