Black soldier fly (Hermetia illucens) larvae meal in diets of European seabass: Effects on antioxidative capacity, non-specific immunity, transcriptomic responses, and resistance to the challenge with Vibrio alginolyticus

Highlights

• Experimental diets for European seabass were formulated where dry black solider fly larvae meal (BSFLM) substituted 25, 35, or 50% of dietary FM.

• BSFLM-supplemented diets potentiated the serum antioxidative status of fish.

• Dietary BSFLM strengthens non-specific immunity and upregulated hepatic HSP70, IL-1β, and IL-10 genes.

• Partial replacement of FM up to 50% by BSFLM might enhanced resistance against Vibrio alginolyticus.

Abstract

Black soldier fly larvae meal (BSFLM) has been successfully demonstrated as a promising fish meal (FM) replacer in diets of several fish species including European seabass (Dicentrarchus labrax). However, its impacts on antioxidant capacity, and immune responses of treated fish are still poorly understood. A 60-day feeding trial was carried out to evaluate the effects of partial substitution of FM with different levels of dry BSFLM on the antioxidative status, non-specific immunity, transcriptomic responses, and resistance of European seabass to the challenge with Vibrio alginolyticus. Four isoproteic (45%) and isolipidic diets were formulated by replacing 0.0%, 25%, 35%, and 50% of the dietary FM. Each diet was randomly assigned to four fish groups (in triplicates) (initial mean body weight, 12.1 ± 0.21 g) (20 fish per aquarium) (n = 240). Fish were fed three times daily to the apparent satiation. At the end of the feeding trial, serum antioxidant biomarkers such as malondialdehyde levels, and catalase, superoxide dismutase, and glutathione peroxidase enzyme activities were significantly increased in all BSFLM groups in a dose-dependent manner compared to the control group (P < 0.05). The non-specific immune indices, including phagocytic activity, phagocytic index, serum lysozyme and respiratory burst activities were significantly elevated in BSFLM groups compared to those in the control group (P < 0.05). Significant upregulation of the mRNA expression levels of hepatic heat shock protein 70, interleukin-1beta and interleukin-10 genes were observed in all BSFLM groups compared to the control group (P < 0.05). Additionally, after the challenge with V. alginolyticus, the relative percent of survival was significantly elevated in fish groups fed on diets containing graded levels of BSFLM over the control group (P < 0.05). Conclusively, the present study suggests the potential efficacy of partial replacement of dietary FM protein for up to 50% by BSFLM without negative effects on fish health with possible potentiation of the antioxidative status, and the immune responses of the European seabass.

Introduction

Fishmeal (FM) is considered as a principal protein source used in the formulation of aquafeeds due to its plentiful composition of amino acids, superior digestibility, and palatability. These properities makes it suitable to improve the feed intake, digestion and absorption of nutrients in fish [1]. The decrease in catches of wild fish alongside increased FM requirement in aquafeeds caused a rapid decline in the availability of FM, which will subsequently lead to increase the market price of fish diets [2]. Therefore, for future uses, the FM production will not be enough for the growing aquaculture [3]. This will increase the necessity to find new FM substitutes for the sustainable development of aquafeeds.

Now, research efforts have been focused on the efficacy of replacing FM-based ingredients with plant-based materials. However, plant protein could not replace higher amounts of FM because of the presence of anti-nutritional factors, high content of crude fiber, and imbalance amino acid profile [4]. The protein ingredients of animal origin such as insects may be utilized as potential alternatives for protein sources which could help in the partial or complete FM replacement in fish diets [5]. Insect-based meals are plentiful in several types of essential amino acids, predominantly methionine, lysine, and leucine, with no anti-nutritional factors [6]. Henry et al. [5] and Nogales-Merida et al. [7] reviewed several important types of insect meals that used in fish nutrition and their potential ability to substitute some ingredients in the feeds of several fish species including yellow mealworms (Tenebrio molitor), domesticated silkworms (Bombyx mori), house fly (Musca domestica), mosquitoes (Culex pipiens) and black soldier fly (Hermetia illucens).

Black soldier fly (BSF) (Hermetia illucens) is a unique candidate insect meals with a potential efficacy for FM replacement in practical fish diets [8]. Black soldier fly larvae meal (BSFLM) could replace the FM in diets of several fish species such as Nile tilapia (Oreochromis niloticus) [9], Siberian sturgeon (Acipenser baerii) [10], turbot (Scophthalmus maximus) [11], rainbow trout (Oncorhynchus mykiss) [12], Atlantic salmon (Salmo salar) [13], Jian carp (Cyprinus carpio var. Jian) [14], yellow catfish (Pelreobagrus fulvidraco) [15], African catfish (Clarias gariepinus) [16], and European seabass (Dicentrarchus labrax) [17,18].

Reports showed that BSFLM is characterized by its unique antibacterial activity against several bacterial pathogens [[19], [20], [21], [22]]. Besides its potential immune-stimulating properties in fish such as increasing of the serum lysozyme activity in yellow catfish [15], and upregulation of cytokine genes in the intestinal tissue of marron (Cherax cainii) [23]. Furthermore, BSFLM could boost the antioxidant status of Jian carp through the elevation of catalase enzyme activity [24], and decrease of serum malondialdehyde levels in Japanese seabass (Lateolabrax japonicus) [25]. However, the mechanisms of dietary supplementation with BSFLM in improving the immune responses, antioxidative capacity, and resistance of fish against pathogens are still poorly understood.

European seabass is considered as one of the most economically valuable and widely cultured fish species in Egypt due to its great nutritive value [26]. Our previous study by Abdel-Tawwab et al. [17] reported the potential efficacy of partial replacement of FM protein by BSFLM on the overall performances and nutrient utilization in European seabass. The present study is an experimental trial to evaluate the effects of BSFLM as a partial replacement of dietary FM on antioxidative status, non-specific immunity, transcription of some stress- and immune-related genes, and resistance of European seabass against challenge with Vibrio alginolyticus.