1. Introduction
The United Nations (UN) has projected a rise in world population to almost 10 billion people by 2050 [
1]. Such population growth in combination with climate change effects, wealth distribution inequalities, the state of natural resources, peace and sustainability, among other factors [
2], may undermine the achievement of the Sustainable Development Goals (SDGs) linked to food production, hunger, poverty and health. The UN’s SDG goal 2 is facing serious setbacks due to the population increase [
3]. Moreover, recent devastating natural disasters and the disease pandemic, as well as religious and political crises, have also negatively impacted food systems.
In some areas climate change is hampering crop and animal production [
4], thus affecting the aquaculture sector and its potential to support food production, as aquafeed production relies on crop and animal products. The fisheries sector has recorded declines in fish catch that affect the production of fish meal for aquafeed [
5,
6]. The shrinking availability of fish for the aquaculture industry has led to an increase in the market price of fish meal [
7], undermining the affordable protein supply.
Thorarinsdottir et al. [
8] posited that having access to feed stuffs that are safe and economical has become essential to strengthen the aquaculture industry and the development of more sustainable production practices. The high cost of fish feed is also contributing to the low productivity and limited diversity of species farmed [
9]. The challenge facing the aquaculture industry is to reduce the cost of feed and the industry’s environmental footprint, while maintaining product quality and value [
8].
There is a need for groundbreaking solutions to produce more food and improve nutrition. This presents a serious task to researchers, who must devise ways to provide protein that can feed the growing human population while limiting the negative environmental impacts of agricultural production [
10]. Furthermore, programs of action must be economically viable and environmentally sustainable [
7]. To improve the sustainability of aquaculture it is important to identify feed formulations and production techniques that are not dependent on fish meal as the source of protein. Alternative protein sources will play an important role in aquaculture feed development. The “bioeconomy” in particular, the blue bioeconomy, will be paramount to the success of such initiatives.
The Danish National Bioeconomy Panel [
11] defined the bioeconomy as covering the development of renewable biological resources. It also includes the conversion of resources and waste generated from them into other products. Value added to the products will give rise to materials like food for humans, feed for animals, bio-based products, and bioenergy. A fundamental mission of the bioeconomy is to ensure the security of food for a growing human population in which protein supply for humans via fish production plays a key role [
3]. The bioeconomy promotes the resourceful use of biomass for feed, food, biomaterials, and bioenergy [
11]. Interestingly, there has been a paradigm shift in the aquaculture industry, as more attention is now paid by researchers and industry to alternative protein sources for aquafeed production [
7]. This is in a bid to provide more viable and sustainable aquaculture operations with regards to feed production [
12,
13]. In light of this, the blue bioeconomy remains critical to ensuring smooth and sustainable aquaculture.
The “blue bioeconomy” includes any economic activity linked to the use of renewable aquatic biological resources to create products [
3]. The aquatic biomass used in developing these products can include fishery residue, shellfish, crustaceans, and algae [
14]. The blue bioeconomy offers efficient and sustainable options targeted at maximizing productivity, efficient bioresource utility, and effective production cost [
3]. In practice, various researchers in the field of aquaculture have reported the efficacy of many unconventional protein sources of plant and animal origin that could replace fish meal and other conventional protein sources in aquaculture diet. Some of the alternatives that have been suggested include algae meal, blood meal, poultry offal, insect meal (black solider fly, grasshopper), housefly (
Musca domestica) maggot meal, cashew nut waste, Bambara nut and African yam bean [
12,
13,
15,
16,
17].
Alternative protein sources can provide solutions to problems faced by small-scale farmers such as high costs of production [
18] and the resultant loss in revenue due to low farm-gate prices. The Nordic Council of Ministers [
19] indicated that the use of alternative protein sources will boost local production, preserving jobs locally and generating new jobs as well. Using alternative protein sources will bring about the reduction in importation of nutrients and broadly enhance the bioeconomy. The bioeconomy is set to play a major role in the shift to cleaner and more energy-efficient production processes as we transition from a fossil fuel-based economy to one based on renewable and biological resources [
20]. Alternative protein sources for humans and fish production are important in securing the food and nutrition security for the increasing world population [
21]. Highlighting the need to embrace the bioeconomy, this study presents house fly maggot meal as an efficient alternative protein source and quality bioresource. We also assessed the effect of maggot meal diets on the gonadal development of African catfish (
Clarias gariepinus), which belongs to the family Clariidae [
22].
Aquaculture and catfish farming offer viable opportunities for employment and help toward poverty alleviation. Above all, the sufficient provision of aquatic meat can help to cater for the growing demand of protein, as capture fisheries are no longer sustainable [
23]. A number of cultivatable catfish species have been identified:
C. gariepinus, Clarias anguillaris,
Heterobranchus longifilis,
Heterobranchus bidorsalis,
Clarias isheriensis,
Clarias submarginatus,
Chrysichthys nigrodigitatus,
Bagrus sp., and
Synodontis sp. [
24].
C. gariepinus is a freshwater air-breathing aquaculture species [
25], known as a prominent commercial fish cultured both within and outside tropical and subtropical regions [
26,
27]. The FAO [
6] predicted that 62% of the overall world aquaculture production will be made up of freshwater species like carp, catfish, and tilapia by 2030. In Africa,
C. gariepinus is of economic importance and is a relished aquatic food with high dressing percentage [
28,
29].
The maturation of fish gonads and broodstock culture are important aspects of aquaculture management and practices [
30]. In fish reproduction, these factors have an impact on the broodstock efficiency and facilitate fish production. Food is nutritionally acknowledged to havea substantial effect upon the development of the gonads, fecundity, and egg and larval quality of fish. According to Idowu [
31], the egg diameter of fish is indirectly influenced by environmental factors such as temperature and food availability, and large eggs have an increased proportion of yolk. The larvae produced from larger eggs are also larger and have a better chance of survival in the face of adverse environmental conditions [
32].
Ogunji et al. [
33] reported that the high price of fish meal in world markets has necessitated the search for substitute protein sources. Housefly maggot meal—unlike other alternative protein sources, especially plant sources—can replace up to 100% of fish meal in the diets of Nile tilapia (
Oreochromis niloticus) and African catfish [
33,
34,
35,
36,
37]. Similarly, Kroeckelet al. [
38] observed that black soldierfly meal (
Hermetia illucens) might be a feasible alternative protein source for the partial replacement of fish meal in juvenile turbot (
Psetta maxima).
The effects of maggot meal substitution on egg development in terms of oogenesis, vitellogenesis, oocyte maturation, and ovulation have not been determined in African catfish. Since gonadal development and fecundity of fish are greatly affected by broodstock nutrition [
39], we also assessed the quality of maggot meal for use in broodstock diets. Specifically, we aimed to determine the effect of housefly maggot meal (magmeal hereafter) on the gonadal development of
C. gariepinus and the histology of developing gonads.
4. Discussion
The crude protein content of the diets used in this study (40.79 ± 0.41%) is comparable to values reported previously. The FAO [
47] reported that the propensity of
C. gariepinus toward carnivorous feeding habits means they require a relatively high dietary protein intake, in the order of 40–50% crude protein on a dry weight basis. Ali and Jauncey [
48] reported that
C. gariepinus fed with 35–40% protein diets displayed higher growth rates than those fed with low percentages of protein. Although the crude fat values used were lower than values reported by [
49], they were within the values recommended by Alegbeleye et al. [
50].
The growth performance of fish fed a maggot meal supplemented diet (D2–D4) was apparently increased, although results were not statistically significant. The SGR and MWG were not significantly different from the control; however, the highest values of SGR and MWG were recorded among fish fed Diet 4, which had the highest proportion of maggot meal in the diet. The SGR values fall within the range for similar species fed animal- and plant-based experimental diets that enhanced the development of the gonads [
51]. The results of this study corroborate previous observations that maggot meal, like other animal protein sources, is well accepted and utilized by the fish [
36,
52].
It has been suggested that the strong growth and nutrient utilization capacity of fish fed a maggot meal supplemented diet stems from its high biological value (i.e., nutrient composition) [
49]. Similarly, working with another insect larvae, Kroeckel et al. [
38] reported that the incorporation of black soldierfly meal protein in the diet of juvenile turbot (
Psetta maxima) is a feasible alternative protein source for the partial replacement of fish meal. Renna et al. [
53] observed that partially defatted
Hermetia illucens larvae can be included up to 40% as a feed ingredient in trout diets without impacting survival, growth performance, condition factors, somatic indices, dorsal fillet physical quality parameters, and intestinal morphology of the fish.
Our study is one of few that have assessed the effect of insect meal diets on gonadal development. The gonadosomatic index (GSI), an index of gonad size relative to fish size, is a good indicator of gonadal development in fish [
54]. The GSI was higher in fish fed the maggot meal diet compared with the control diet, although there were no statistically significant differences among the feeding groups. In addition, The GSI also increased with increase in the period of feeding trial. These values were similar to those reported for
C. gariepinus by Ekanem et al. [
50]. In another study, Al-Deghayem et al. [
55] reported the lowest GSI values for male
C. gariepinus (0.282 ± 0.13) and the highest GSI result for females (17.266 ± 6.89). Mature gonads were histologically observed when the mean gonadosomatic index of the female experimental fish was 18.05 ± 2.40 and the ripe eggs were observed when the gonadosomatic index of the female experimental fish was 18.10 ± 0.70. GSI values for males in this study were lower than in the females. Hashmi et al. [
54] found that GSI varies with individuals of the same species and that values for females are usually higher than males of the same size because ovaries are larger than testes.
In this study, we assessed the development of the gonads of
C. gariepinus fingerlings fed maggot meal supplemented diets for six months. The gonads developed in line with changes that were reported for catfish and some other teleosts [
56,
57,
58,
59,
60]. The oocyte developmental stages observed were the chromatin nucleolar, perinucleolar, cortical alveolar, vitellogenic, and maturation/hydration stages. The five male developmental stages detected were spermatogonia, primary spermatocytes, secondary spermatocytes, spermatids, and spermatozoa. Previous studies reported that the oogonia of
C. gariepinus proliferated and turned into primary oocytes, which subsequently grew within the follicles, formed cortical alveoli, entered vitellogenesis, underwent maturation/hydration and finally ovulated [
31,
39]. In this study, the observed changes were similar to those reported for teleosts [
61,
62], although ovulation was not observed at the end of this study. This may have been because the feeding trial began with fingerlings and the experiment lasted for 24 weeks (i.e., six months). The period of the feeding trial was shorter than the 12 months adopted by Çek and Yilmaz [
63].
On week 12 of the experiment, when the average weight of fish was 29.17 ± 1.60 g, the male and female gonads appeared as ribbon-like structures. These structures were attached to the dorsal lateral lining of the peritoneal cavity. Such thread-like structures are undifferentiated gonads that can finally form either male or female gonads [
63]. This marks the beginning of the development of the gonads in
C. gariepinus. Ogunji and Rahe [
64] reported that at the end of larval development of the African catfish (
H. longifilis) the gonads were not developed. In this study we found that African catfish gonads may begin development after 12 weeks.
Faster gonadal development was observed in fish groups fed high dietary maggot meal inclusion levels (
Table 5 and
Table 6 and
Figure 1,
Figure 2,
Figure 3,
Figure 4 and
Figure 5). It is possible that the good nutrient profile of maggot meal [
49] may have played a role in making the experimental diets suitable for feeding
C. gariepinus broodstock. Indeed, Bromage [
39] reported that gonadal development and fecundity in fish are greatly affected by broodstock nutrition in several species. The ovaries were in the resting stage from onset of the experiment until week 12 (i.e., three months into the feeding trial). The gonads of fish fed diet D1 developed to chromatin nucleolar stage between week 12 and 16, while those fed diets D2 and D3 were already developed to the perinucleolar stage, and fish fed with diet D4 were developed to the cortical alveoli stage.Guraya [
65] reported that sex differentiation occurs when the newly formed ovary is first distinguishable.
The genital papillae were observed in males at week 16 of the experiment when the weight of the fish ranged from 35.16–49.56 g. The fish fed with diets D1, D2, and D3 were observed to have gonads that were developed to the spermatogonia stage (
Figure 4a–c), while fish fed diet D4, which contained the highest proportion of maggot meal, already had gonads developed to primary spermatocytes (
Figure 4d). This represents a shorter rearing period than the 12 months of rearing suggested by Gupta [
61]. In week 24, fish fed diets D1 (control) and D2 were both observed to be in the secondary spermatocytes stage, while those fed diet D3 were in the spermatids stage. It is important to note that free spermatozoa were first observed in fish fed with diet D4. This was detected when the fish had a mean weight of 90.94 ± 13.58 g. Schulz et al. [
66] stated that maturity is related to age in
C. gariepinus, but in this study we observed that maturity was more related to size and diet rather than age, in accordance with the findings of [
64], in which it was reported that complete metamorphosis of
H. longifilis is determined by the size rather than the age of larvae.
5. Conclusions
Food production systems are reported to be negatively impacted by the global human population increase, climate change, devastating natural disasters, disease pandemics, and religious and political crises [
2]. As such, there is a need to support the achievement of the Sustainable Development Goals, especially SDG goal 2, and combat any setbacks in terms of food production and accessibility of affordable protein. Aquaculture is an important component of food security [
18] and has attracted increased research attention.
To realize more sustainable aquaculture that can provide a nutritionally adequate and relatively inexpensive and highly accessible protein supply, feed formulation and production techniques must be improved. The reliance on fish meal as a protein source for feed production should change and the use of alternative protein sources should be encouraged. The bioeconomy will play a crucial role in this process. While the bioeconomy promotes the resourceful use of biomass for feed, food, biomaterials, and bioenergy, the blue bioeconomy is aimed at any economic activity linked to the use of renewable aquatic biological resources to create products. In this study, maggot meal supplemented diets resulted in increased growth rates, albeit statistically non-significant. The development of the gonads in experimental fish fed maggot meal supplemented diets was also recorded earlier than in the control. These results suggest that maggot meal is a potentially important feedstuff in broodstock nutrition, which can help to improve catfish production.
Interestingly, maggot meal has previously been established to be a quality alternative protein source. Using this feedstuff to facilitate earlier maturation of broodstock (before the established one year of maturity as reported for African catfish) [
67] is important for more efficient fish production.
Maggot meal can be recommended as a suitable alternative protein source for supplementing fish meal in the diet of C. gariepinus broodstock, thus bringing aboutan improvement of fish seed development.