Influence of black soldier fly (Hermetia illucens) larvae oil on growth performance, body composition, tissue fatty acid composition and lipid deposition in juvenile Jian carp (Cyprinus carpio var. Jian)

Highlights

• Black soldier fly larvae oil significantly increased the content of lauric acid fatty acid in hepatopancreas, intraperitoneal fat and muscle.

• Black soldier fly larvae oil reduced the intraperitoneal fat deposition of fish.

• Black soldier fly larvae oil reduced the size of intraperitoneal adipose cells.

• Black soldier fly larvae oil significantly increased the level of PPAR α in intraperitoneal adipose cells.

Abstract

Black soldier fly larvae oil (BSO) is a potential fat source in aquaculture feeds, which is high in lauric acid (21.4%–49.3%). In order to investigate the effects of dietary BSO on growth performance, fatty acid composition and lipid deposition in juvenile Jian carp (Cyprinus carpio var. Jian), five experimental diets were formulated by substitution of 0%, 25%, 50%, 75% and 100% soybean oil (SO) with BSO. Total 300 Jian carp (10.67 ± 0.80 g) were divided randomly into 5 groups (triplicate per group) and was fed with the diets above respectively). After 59 days feeding growth, fatty acid composition and lipid deposition was determined. The results showed that growth, nutritive utilization and serum biochemical parameters of fish in five groups were not different (P > 0.05). Fatty acid composition in the intraperitoneal fat tissue, muscle and hepatopancreas was closely correlated with diets. While, the 22:6n-3 content of treated groups was significantly higher than that of the control group (P < 0.05) in the muscle. Intraperitoneal fat index and the size of adipocyte in intraperitoneal fat decreased in higher BSO intake compared with SO group (P < 0.05). Relative gene expression of PPARα significantly increased (P < 0.05), while PPARγ and FAS was not significantly affected by dietary BSO level (P > 0.05). The Bcl-2/Bax ratios were not different among five groups (P > 0.05). These results suggested that the growth of Jian carp was not affected by dietary BSO, while it decreased lipid deposition in the intraperitoneal fat tissue of Jian carp by higher gene expression of PPARα.

Statement of relevance

Previous studies on nutrition of fish have highlighted the importance of fish oil. However, with the worldwide decreasing supplies as well as the escalating prices of this ingredient, alternative resources were sought and nutritionally evaluated. Plant or vegetable oils are now introduced in fish diets, but these sources have limitations, such as palatability and production issues. In the recent years, insects have received wide attention as a potential source of lipid, especially black soldier fly. Black soldier fly grow and reproduce easily, have high feed conversion efficiency and can be reared on biowastes. Insects often accumulate fat, especially during their immature stages. The lipid content of non-defatted black soldier fly larvae is highly (26%–35%). This study was designed to explore the possibility that black soldier fly larvae oil as a lipid resource in aquafeeds, and to determine its effect on growth performance, feed utilization efficiency, major nutrients composition, fatty acid composition and lipid deposition.

Introduction

As one of the major nutrients, dietary lipids play important roles in fish nutrition. Lipids are important because of its many advantages such as being a potent energy source, a component of cellular membranes, and promoting absorption of lipophilic nutrients (Halver, 2002). Many previous studies of fish have highlighted the importance of fish oil as a major constituent in diets. However, due to increasing costs and limited supplies of global fish oil (Tacon and Metian, 2008), it was currently of great urgency for the aquafeed industry to investigate the possibilities of alternative dietary lipid sources. The black soldier fly (Hermetia illucens) has become a popular bio-recycling organism in the world due to its detritivorous nature (Bondari and Sheppard, 1981, Diener et al., 2009, Sheppard et al., 1994, Stamer et al., 2007, Zheng et al., 2012). It has been reported that black soldier fly larvae contain about 42% protein and 35% fat (Sheppard et al., 1994) and have been demonstrated to be a good alternative feed in fish production (St-Hilaire et al., 2007), with the potential to replace fish meal and fish oil as source of animal feed lipids. Previously, many research of the black soldier fly larvae meal have shown it as an alternative protein source for feed purposes (Newton et al., 2005, Sealey et al., 2011, St-Hilaire et al., 2007, Zhang et al., 2014). Black soldier fly larvae oil (BSO) is a byproduct of black soldier fly larvae meal production. And applied research is now needed to fill the knowledge gaps by utilizing the oil of black soldier fly in fish diets. The fatty acid profiles of black soldier fly larvae show that linoleic acid (LNA, 18:2n-6; concentration (3.6%–4.5%) is much greater than that of α-linolenic acid (ALA, 18:3n-3; 0.08%–0.74%), similar to many plant oils (such as soybean oil and sunflower oil), and rich in medium-chain fatty acids (MCFA) with lauric acid (LA, 12:0) representing 21.4%–49.3% of total fatty acids, which is similar to coconut oil (Tran et al., 2015). There are many studies reported that applying a certain proportional soybean oil (Deng et al., 2014, Emre et al., 2015, Peng et al., 2008), sunflower seed oil (Bell et al., 1996, Bransden et al., 2003, Wijekoon et al., 2014) or coconut oil (Fontagné et al., 2000, Legendre et al., 1995, Luo et al., 2014) to fish feed did not negatively affect growth.

The role of MCFA as energy-yielding substrates has been largely invested in terrestrial animals (Aurousseau et al., 1989, Bozzolo et al., 1993). In mammals, MCFA have been reported to do not need carnitine palmitoyltransferase-1 (CPT-1) mediated transport to enter mitochondria which may accelerate their oxidation. Also in fish, dietary inclusion of MCFA resulted in decreased fat deposition in the muscle, liver and intra-peritoneal fat with similar or improved growth rates (Nakagawa and Kimura, 1993). Negative effects on the efficiency of energy or lipid retention were also seen in Atlantic salmon (Salmo salar) fed purified MCFA (Nordrum et al., 2003) and in polka-dot grouper fed CO, suggesting high levels of C12-β-oxidation (Williams et al., 2006). By comparison, Figueiredo-Silva et al. (2012) revealed high C12 retention from CO, with C12 representing over 20% of total body fatty acids compared to < 1% in trout fed FO. Furthermore, according to a previous study in our lab, the diet with 0.5% ethyl laurate could depress juvenile Pagrus major lipid accumulation (Ji et al., 2005).

Jian carp (Cyprinus carpio var. Jian) is one of the economically important freshwater-cultured fish. In China, the production of Jian carp presents almost 50% of that of common carp every year (Zhou et al., 2008). Since its high meat content, deliciousness, high nutritional value, and cheap price, Jian carp is popular with consumers and the market demand is great.

Therefore, the aim of this study was to estimate the BSO in the diet of Jian carp. We investigated the effects of BSO on growth performance, feed utilization, body fatty acid profiles, serum biochemical parameters, and lipid metabolism in Jian carp, in order to provide reference information for the culture of carp using BSO as lipid source.