Black soldier fly larvae as a better lipid source than yellow mealworm or silkworm oils for juvenile mirror carp (Cyprinus carpio var. specularis)

Highlights

• BSFO or mixtures of insect oils (MIXO) are a better lipid source than YMO or SWPO diets for juvenile mirror carp.

• Increased growth performance and feed utilization in fish fed BSFO and MIXO than fish of SWPO and YMO groups

• BSFO reduced lipid deposition in the intraperitoneal fat tissue of juvenile mirror carp.

• BSFO or MIXO diets influence the immune system ability of juvenile mirror carp.

Abstract

A feeding trial was conducted to study the effects of different insect oils on growth performance, lipid metabolism, inflammation and related gene expression in juvenile mirror carp (Cyprinus carpio var. Specularis). Triplicate cages of juvenile mirror carp were fed one of four isonitrogenous and isolipidic diets, including black soldier fly oil (BSFO, 25 g kg⁻¹), silkworm pupae oil (SWPO, 25 g kg⁻¹), yellow mealworm oil (YMO, 25 g kg⁻¹), and a mixture of the three insect oils, BSFO, SWPO and YMO (MIXO, 25 g kg⁻¹) (n = 3). After 59 days, the results showed that weight gain and specific growth rate of fish fed with BSFO and MIXO diets were significantly higher than the fish fed the other two insect oil diets, while feed conversion rate in the same dietary groups was significantly lower than fish fed the SWPO and YMO diets. Intra-peritoneal fat index and adipocyte size in intra-peritoneal fat tissue decreased in the fish fed with BSFO and MIXO compared to fish fed the SWPO and YMO diets. Relative gene expression of fatty acid synthase (FAS) significantly decreased, while peroxisome proliferator-activated receptor-α (PPAR-α) significantly increased in intra-peritoneal fat tissue of fish fed with BSFO and MIXO diets compared with mirror carp fed with SWPO and YMO diets. The activity and transcription of total superoxide dismutase (SOD) significantly increased in the liver of fish fed with BSFO and MIXO than fish fed with SWPO and YMO diets. The content of hepatic maleic dialdehyde (MDA) significantly decreased, while serum globulin (GLO) significantly increased in fish fed with BSFO and MIXO than fish fed with SWPO and YMO diets. Moreover, the transcription of anti-inflammatory cytokine (IL-10) was higher in liver of fish fed with BSFO and MIXO diets. Fish fed with SWPO diet significantly up-regulated the hepatic expression of pro-inflammatory cytokine (IL-1β) and tumor necrosis-α (TNF-α) than fish fed with BSFO, YMO or MIXO diets. Overall, compared to others insect oils source (YMO and SWPO), inclusion of BSFO or the combination of the three oils (MIXO) in the diets positively influence growth performance, lipid metabolism of intra-peritoneal fat, liver antioxidant capacity and inflammatory response of juvenile mirror carp.

Introduction

Soybean is one of the most used plant ingredients in aquafeed formulation due to its high protein content and amino acid profile and low prices (Kaushik et al., 2004). However, these ingredients could be used directly in food producing industries and sourcing from agriculture will increase the pressure on arable land. Research on the use of insects as feed ingredients in aquafeeds has developed rapidly in the recent years, leading to an increased number of scientific articles on this topic (Nogales-Mérida et al., 2019; Belghit et al., 2019a; Li et al., 2016; Li et al., 2017; Guerreiro et al., 2020; Dumas et al., 2018). In addition to their nutritive qualities, the production of insect-based feed ingredients is also accompanied by certain environmental benefits, as well as being production animals with exceptionally fast growth, easy reproduction, fast life-cycles and being efficient at converting low-grade organic matter into high-value protein and fat (Liland et al., 2017; Ewald et al., 2020).

The European Union (EU) has recently allowed the use of insect processed animal protein in aquafeeds (EU commission regulation (2017/893–24/05/2017). The insect species allowed for the production of insect are: Black soldier fly (Hermetia illucens, L), Common Housefly (Musca domestica), Yellow Mealworm (Tenebrio molitor), Lesser Mealworm (Alphitobious diaperinus), House cricket (Acheta domesticus), Banded cricket (Gryllodes sigillatus) and Field Cricket (Gryllus assimilis). Among these species, black soldier fly (BSF) and Yellow Mealworm (YM) are considered the two most relevant species for the production of insect ingredients for fish, poultry and pigs (Van Huis, 2013; Nogales-Mérida et al., 2019; Chia et al., 2019; Józefiak et al., 2016). The nutritional composition of different insect species has been widely reviewed (Nogales-Mérida et al., 2019; Sogari et al., 2019). BSF larvae, MW larvae and silkworm pupae (SWP) contain approximatively 42, 56 and 60% of protein/dry weight respectively and typical lipid levels of around 28, 36 and 26%/dry weight respectively (Nogales-Mérida et al., 2019; Karthick Raja et al., 2019). The amount of fatty acids (FA) as well as their profile in insects depend on the species, diets, stage of development and conditions of rearing (Barragan-Fonseca et al., 2017). Compared to others insect (YM, SWP) or plant (soybean, linseed, palm) oils, the BSF larvae show a different FA composition (Ooninx et al., 2015). The largest lipid fraction of this species is the medium-chain FA, mainly lauric acid C12:0 which represents between 21% and 50% of total FA in BSF larvae, making its FA composition similar to coconut oil (Ooninx et al., 2015; Liland et al., 2017). While the FA composition of SWP and YM is dominated by monounsaturated FA (MUFA, oleic acid C18:1n-9) and polyunsaturated FA (PUFA, α-linolenic acid, C18:3n-3 and linoleic acid, C18:2n-6, respectively) (Wang et al., 2020; Wu et al., 2020).

The use of insect as a feed ingredient in aquaculture has gotten increased investments, but most of the attention has been focused on the insect protein and its suitability for use in different fish species and developmental stages (Nogales-Mérida et al., 2019; Belghit et al., 2019a; Karthick Raja et al., 2019; Li et al., 2017; Guerreiro et al., 2020; Belghit et al., 2018; Xu et al., 2018). Although the oil fraction of the insects was initially only a by-product of the production of insect protein meal, the high lipid content and the unique FA compositions of each insect species make the insect oil fraction an interesting and potentially important source of lipids for animal feeds (Luo et al., 2020; Zou et al., 2017; Gasco et al., 2019; Zhang et al., 2011). However, only a few studies have investigated the potential of insect oils in aquafeed (Li et al., 2016; Dumas et al., 2018; Chen et al., 2017; Belghit et al., 2018). Replacement of FO or soybean oil with black soldier fly larvae oil in aquafeeds without negative effects on growth performance or intestinal morphology have been successfully demonstrated in rainbow trout (Oncorhynchus mykiss) and Jian carp (Cyprinus carpio var. Jian), respectively (Dumas et al., 2018; Li et al., 2016). Furthermore, partial replacement of soybean oil with silkworm pupae oil in the diets of juvenile Jian carp, improved growth performance and feed utilization (Chen et al., 2017).

Mirror carp (Cyprinus carpio var. specularis), as a freshwater fish species, has been one of the most widely cultured species all over the world (FAO, 2010). These fish species are omnivorous, and their diets consist of plant food (80%) and animal food (20%), including insect larvae. Mirror carp is a popular farmed fish consumed in China, due to its high nutritional value, delicious taste, high meat content and cheap price (Cheng and Wang, 2005).

Therefore, the objective of this study was to determine the effects of different insect oils extracted from BSF larvae, YM larvae SWP pupae on growth performance, feed efficiency, lipid metabolism, inflammatory response and related gene expression of juvenile mirror carp in order to provide reference information for farmed carp fed different insect oils as lipid source.