1. Introduction
Sustainable food systems improving nutrition and reducing malnutrition are urgently needed to meet the surging demand for protein sources around the world. One such sustainable food system is the farming and consumption of crickets [
1,
2]. Crickets are considered an alternative and sustainable food because they have a short life cycle, are prolific, and require far smaller quantities of water, feed, and space to raise than conventional livestock [
3,
4]. Moreover, farming crickets have been reported to cause less environmental damage than livestock, as they release fewer greenhouse gases [
5]. Additionally, crickets are reported to be more nutritious than livestock [
6].
Edible crickets have been a major source of nutrients for millions of people globally; over 60 species have been identified as being excellent human foods [
7,
8,
9,
10]. In Madagascar, the
G. madagascarensis cricket is consumed as a nutrient-rich food resource [
11].
Gryllus madagascarensis is a brown field cricket found in and around grasslands and farmlands in the high plateau of Madagascar. Both sexes of this cricket have a short lifecycle and are highly nutritious, making the species a suitable candidate for farming. Although this cricket could represent a potential source of nutrients that can help address the food insecurity, malnutrition, and poverty in Madagascar’s households, its farming faces a plethora of challenges including a lack of identified cricket feeds. Farmers also lack information on how different feeds used in rearing crickets impact the biology of
G. madagascarensis. Moreover, cricket producers and consumers lack details on the nutrition content of
G. madagascarensis fed on different feeds and how they compare with the required allowable intake to mitigate malnutrition in Madagascar. These questions form the basis of our study.
The type of feed used has been reported to be a key environmental factor influencing the population growth and nutrition content of farmed crickets [
12,
13,
14,
15]. To make cricket farming affordable, farmers require cheap, accessible, and sustainable feeds [
16]. In Madagascar, chicken feed is the main feed source used to farm crickets [
11,
17]. Farmers use chicken feed because of its high protein content, balanced essential amino acids (EAA), abundant essential fatty acids (EFA), range of minerals, and easily digestible energy [
18] The chicken feed used by the farmers to feed crickets is usually expensive and unsustainable [
19,
20]. Chicken feed is expensive due to the high cost of the protein-rich soybeans and fish meal, which are commonly added to other ingredients to make chicken feed [
21]. The rising cost of chicken feed, combined with uncertainty in the availability of supplies, has forced cricket farmers and feed manufacturers to seek its replacement in inexpensive, abundant, readily available alternative feed sources.
Weeds and agro-byproducts have been proposed as promising alternative materials for formulating cricket feeds [
15]. The main advantages of using weeds and agro-byproducts for formulating cricket feed are their local availability, abundance, inexpensive nature, sustainability, and capacity to provide nutrients for crickets [
18,
20]. Several studies have reported on the potential use of crop residues and weeds as single cricket feeds [
22]. However, no previous research has attempted to formulate feeds for edible crickets in Madagascar from weeds and agro-byproducts, making this the first study. From this perspective, formulating a reliable, robust, and sustainable feed requires a clear scientific understanding of the effect of different formulated feeds on cricket growth, survival, reproduction, and feed utilization. Moreover, the nutrient composition of the developed feeds and their impact on the nutrient content of crickets need to be unraveled. Thus, our study aimed to determine the development, survival, growth, reproduction, feed consumption rates, and feed conversation ratios of
G. madagascarensis fed on various feeds formulated from weeds and agro-byproducts available in central Madagascar. In addition, this study compared the nutrition content of the various formulated feeds with chicken feed and the nutrition content of the crickets fed on each feed. Lastly, this study compared the cost of each formulated feed to chicken feed. The best-performing feed regarding cricket nutrition, availability, and cost is recommended for cricket farming across Madagascar, and more generally, the African mainland, where the weeds and agro-byproducts studied thrive.
4. Discussion
The increasing cost of the chicken feed used to feed crickets has become a major obstacle to farming crickets for many households. Researchers worldwide are urged to develop alternatives to chicken feed for cricket culture. One of the available options is to use organic side streams as feed for crickets. Feeds formulated from weeds and agro-byproducts are being investigated as feed for crickets for human and animal consumption [
37]. The present research revealed that feeds formulated from weed and agro-byproducts are promising alternatives to replace chicken feed for farming
G. madagascarensis in small-scale and large-scale cricket farm conditions. Feed composition has been reported to influence cricket feed consumption, phenotype, fecundity, and nutrition content [
38]. Our study findings showed variations in development growth, survival, reproductive performance, feed efficiency, the nutrition content of
G. madagascarensis, and cost of production when the insects are reared on formulated feeds from single-plant product powders formulated from weeds and agro-byproducts.
The current study has demonstrated that development time was impacted by the type of feed used to rear
G. madagascarensis. Our study revealed that
G. madagascarensis grown on the reference feed took 29 days (4 weeks) to complete the nymphal cycle through the eclosion period to adult crickets. The short development time recorded differed from the seven weeks reported by [
17], who grew
G. madagascarensis collected from the wild on a reference feed of 20% protein content. The variation in development could be due to the differences in the nutrition content of the feeds and rearing room conditions such as humidity, temperature, and light period. On the other hand, our study has shown that
G. madagascarensis nymphs reared on nine different formulated feeds took ~28 to 41 days (4 to 6 weeks) to reach the adult stage. The difference recorded was due to differences in the nutrient content of the formulated feeds. For instance, the percentage of protein in cricket feeds has been reported to influence their development [
39,
40,
41]. Development time decreases when crickets are reared on high-protein feeds [
3,
19]. The shortest development time was associated with CFC, which has a protein content of 24.5%, and CFE, consisting of 23.5% protein. The longest development time was recorded in CFH, which has a protein level of 13.5%. In the current study, higher protein levels did not drastically shorten the development time, as seen with
G. madagascarensis fed CFB (protein content 25.0%) and the reference feed (protein content 28.0%). Previous studies also reported that speeding up development in crickets requires a diet that has more carbohydrates and less fat [
41]. In the present study, CFC, with 27.8% carbohydrates and 3.8% fat, and CFE, with 42.2% carbohydrate and 2.1% fat, led to the shortest development time relative to the reference feed, with a carbohydrate content of 43.7% and 3.4% fat. By contrast, CFJ, linked to the longest development time, had the highest levels of carbohydrates (56.6%) and the lowest level of crude fat (1.3%). This indicates that to achieve faster development, these crickets require a feed with an optimum ratio of protein to carbohydrate to fat. Proteins in a feed are important since they contain the amino acids required for the synthesis of cricket proteins [
41]. On the other hand, carbohydrates and fats provide energy, which is required for molting, searching for food and water, mating, and other metabolic activities.
Gryllus madagascarensis nymph development time to the adult stage in the current study was shorter (28–41 days) than the development time of nymphs of
Gryllus bimaculatus (36–48 days),
Gryllodes sigillatus (34–60 days),
Acheta domesticus (42–49 days),
Gryllus assimilis (44–64 days), and
Scapsipedus icipe (65–107 days) [
2,
19,
39,
42,
43,
44].
Feed is reported to impact the survival rate of crickets [
3,
45]. In the current study,
G. madagascarensis reared on the formulated and reference feeds showed a survival rate ranging between 66 and 98%. However, the highest survival rate (98%) occurred in
G. madagascarensis reared on CFG, CFE, and CFC feeds, as well as the reference feed (CFA). The lowest survival rate was reported in crickets raised on CFD (66%). The differences in the survival rate of
G. madagascarensis observed in the current study could be linked to the differences recorded on the formulated and the reference feed. Previous studies reported that crickets reared on formulated diets, which were well balanced in nutrients, experienced reduced mortality [
27,
45,
46]. Moreover, similar reports indicated that when crickets were grown on low-quality formulated feeds, nymph mortality increased because their nutritional needs were not met [
45,
47]. Therefore, the higher survivorship observed with feeds CFG, CFE, and CFC, having a protein content ranging between 21.5 and 24.4%, indicated that these feeds possessed optimum percentages of nutrients required by the
G. madagascarensis cricket compared with other feeds. The survival rate on CFG, CFE, and CFC was similar to that of the reference diet. Our findings are consistent with previous research, which indicated that crickets such as
A. domesticus reared on feeds with over 20% protein tended to have high survival rates of up to 96% due to decreased damage during development [
20,
41,
46]. Apart from protein, crickets also require carbohydrates, fiber, fat, and mineral elements for survival. The current studies indicated that
G. madagascarensis reared on feeds with carbohydrates (27.8–42.2%), fat (2.1–6.3%), and fiber (10.6–22.7%) led to the highest cricket survival rates. Our results are consistent with previous studies that indicated that crickets required carbohydrates ranging from 32 to 47% and fat (3.2–5.2%) to have a high survival rate. Additionally, crickets need optimal mineral elements to survive. From the present study, the highest survivorship was recorded in
G. madagascarensis reared on formulated feed CFG, CFE, and CFC, with levels of iron ranging from 171.1 to 881.4 mg/kgDM, copper (6.8–9.7 mg/kgDM), zinc (37.1–64.2 mg/kgDM), manganese (35.9–79.3 mg/kgDM), sodium (1939.3–2399.9 mg/kgDM), magnesium (0.2%), calcium (0.9–1.1%), phosphorus (0.2–0.3%), and potassium (1.2–1.6%) compared with other formulated feeds and the reference feed. Minerals such as calcium and magnesium play a vital role in insect physiology. To survive, insects require optimum amounts of sodium and iron, whereas excess or inadequate amounts of these two minerals lead to mortality [
48,
49]. On the other hand, when insects like ants are fed on feeds with higher protein content, there is a decreased survival rate due to high mortality [
50]. Therefore, while preparing feeds for crickets, the ingredients should be mixed in a manner that results in optimal nutrient levels that will enhance their survival. The weeds and agro-byproducts used to formulate CFG, CFE, and CFC (heterogenous feeds) show their potential as substitutions for chicken feed in cricket production.
Feeds are reported to significantly affect cricket body mass and length [
40,
51]. Determination of the feed with optimum nutrients to promote large, heavy bodies in
G. madagascarensis is a paramount factor for boosting production, profits, and sustainable farming of this cricket. The results of the present study demonstrate that
G. madagascarensis body length and wet body mass were greater in crickets fed on feed with moderately high quantities of protein than those fed on feeds where the protein level was too high or too low. For instance, the result of the current study demonstrates that the heaviest body masses and largest body sizes were attained by crickets fed CFG, which has a protein content of 21.5%—which is intermediate compared with other formulated feeds and the reference feed. The body mass and length of the crickets decreased when the insects were fed a diet either too high in protein, as with CFA (reference feed), which has a protein content of 28.0%, or too low in protein, such as CFJ (13.5% protein). Crickets fed on feeds with optimum nutrients result in crickets whose body length doubles during the juvenile molting, resulting in an exponential expansion of length from one juvenile stage to the other, until the last juvenile stage, where the body content accumulates [
19]. From our findings, CFG feed seems to contain the optimum combination of nutrients required to grow the largest and heaviest
G. madagascarensis, the ultimate goal of cricket farmers. The results of the current study corroborate early reports that suggest that feed with optimum nutrients leads to an increase in feed consumption in crickets, which in turn leads to an increased metabolic rate and body content accumulation [
38].
The feed conversion ratio (FCR) is a good indicator of the feed quality and efficiency of farmed crickets to make use of it. Previous studies have reported crickets to be high-feed converters [
14]. Comparing the impact of different formulated feeds on the FCR of
G. madagascarensis, our findings revealed that when the protein and mineral content of the feed is increased to the optimum level, the FCR decreases.
Gryllus madagascarensis fed on feeds CFG, CFE, and CFC had the lowest FCR compared with other formulated feeds and the reference feed. The small FCR showed by crickets fed on CFG, CFE, and CFC demonstrated that they converted the feed offered to them efficiently into biomass. The small FCR also shows that CFG, CFE, and CFC had high nutrition quality compared with other formulated and reference feeds. Crickets fed on CFJ, with its too-low protein content, and CFA, with its too-high protein content, exhibited high FCR, indicating that these groups were less efficient at converting feed to body mass. The FCR reported in this study is within the range of the FCR reported previously [
14,
44].
The type of feed influences the cost of feeding crickets [
14]. Many cricket farmers desire to use cheaper feeds to obtain higher returns on their investment. One way to achieve this is by determining the cost of producing one kilogram of live crickets. In the present study, the cost of feeding per kg live mass gain in
G. madagascarensis reared on feed CFH and CFG was significantly (7-fold) lower than feed CFJ and the reference feed. However, crickets fed CFH recorded a lower mean body weight and consumed more feed than crickets fed CFG. This has huge implications for income, while feeding CFG with intermediately high crude protein content may make it somewhat expensive to produce a kilogram of crickets, even though less feed is required than if using CFH. Also, feeding crickets on CFG will lead to a higher yield than other feeds. Therefore, feeding farmed crickets with feed CFG may be cheaper in the long run than using a feed too low or too high in crude protein.
The nutritional content of feed offered to the crickets has been reported to influence their reproductive yield. For instance, crickets fed on feed rich in protein will lay more eggs, have a short preoviposition period, their eggs will take less time to hatch, and egg hatch percentage will be high. In the present study, preoviposition duration, fecundity, egg incubation period, and egg hatchability in
G. madagascarensis reared on different formulated diets varied across the feeds. In this case, the shortest preoviposition, highest fecundity, shortest egg incubation period, and highest hatchability were recorded with
G. madagascarensis females fed on CFG. This was likely caused by the higher protein content, moderately high carbohydrate content, high ash content, high fiber content, high iron, high sodium, high calcium, and high phosphorous of CFG. This combination of nutrients has been reported to lower preoviposition time and egg incubation period and increase egg laying and egg hatchability in other cricket species [
19,
41]. On the other hand, the lowest preoviposition and fecundity, longest egg incubation period, and lowest egg hatchability were recorded in females fed CFJ. This feed contained the lowest quantity of protein, was high in carbohydrates, and was low in ash, iron, phosphorus, manganese, sodium, and calcium content, which corroborates previous reports [
52]. Further, studies on
G. assimilis and
G. sigillatus have shown that crickets fed on diets rich in high-quality proteins, carbohydrates, iron, and phosphorus will have larger, quicker-maturing ovaries able to accommodate more eggs than crickets fed low-quality diets [
41]. It is important to note that
G. madagascarensis, which produces 1130.6–2554.10 eggs, is comparable in fecundity to
G. bimaculatus,
S. icipe,
G. assimilis, and
A. domesticus reared on weeds and agro-byproducts [
53].
Different studies have reported feeds to have varying influences on the nutrition content of crickets [
13,
16]. Crickets fed on highly nutritious feeds have been reported to be a good source of protein, fat, and fiber (chitin). Our results show that
G. madagascrensis reared on feeds with varying nutrition content led to variation in the nutrition content of the cricket across the formulated feeds and the reference diet. Additionally, the nutritional analysis of
G. madagascarensis fed on formulated feeds revealed that protein was the major component, averaging 66.78%, followed by fats, fiber, moisture, ash, and carbohydrates. The nutrient content obtained from the crickets fed various feeds in our study is in tandem with previous studies, where reported protein varied from 59.70 to 75.00%, carbohydrate from 1.13 to 11.90%, fiber from 4.60 to 8.68%, fat from 8.00 to 23.80%, and ash from 3.79 to 5.40% [
54]. Crickets fed CFF (22.5% protein) had the highest protein content, followed by crickets fed CFG (21.5% protein), while crickets fed CFJ (13.5% protein) had the least nutrient content. Crickets reared on CFC had the highest fat content compared with the other feeds. Fat is a source of metabolic energy for human beings. Fat from crickets can be used as a raw material for industries manufacturing cooking oils and cosmetics. Therefore, farmers who want to produce crickets for fat extraction should feed CFC to their crickets. The findings demonstrate that crickets reared on CFG resulted in crickets with the highest fiber level, lacking in animal protein sources. Cricket fiber comes in the form of chitin, which has been reported to have human health benefits. For instance, chitin in crickets has been reported to serve as a prebiotic component enhancing the growth of
Bifidobacterium animalis in the digestive system of human beings, required for digestion and assimilation of food [
55,
56]. Moreover, chitin in edible crickets has been reported to reduce swelling in the gastrointestinal lining and improve the function of the heart [
56]. Additionally, chitin is reported to be an immune booster of eosinophils, macrophages, and T helper cells found in the lungs and gut [
57].
Feed is reported to influence the level of mineral elements in crickets [
6]. Minerals are important for the normal functioning of the cricket body [
58].
Gryllus madagascarensis reared on the nine formulated feeds and reference feeds varied in their content of mineral elements. This was due to differences in the nutrition content of various weeds and agro-byproducts used in formulating the feeds.
Gryllus madagascarensis reared on CFG with seven mixed ingredients was richest in potassium, calcium, magnesium, phosphorus, iron, zinc, and manganese compared with crickets reared on other formulated feeds. Crickets reared on CFI exhibited the lowest mineral element content. This could be because CFI is nearly homogeneous since it consists of one agro-byproduct and baking powder. Previous studies have demonstrated that when crickets are fed on a single-plant product, they always suffer deficiencies in some mineral elements [
19]. This implies that no single-plant product can supply sufficient mineral elements to meet the requirements of crickets. To overcome the deficiency, several plant products should be blended to attain a feed with diversified mineral elements, as found in CFG. The current study further demonstrated that potassium was the major mineral element, followed by phosphorus and sodium in
G. madagascarensis. This finding is similar to a previous study conducted on
A. domesticus [
14].
The current study revealed that when
G. madagascarensis was fed different feed formulations, the resulting adult crickets varied in their fatty acid content.
Gryllus madagascarensis grown on CFG and CFC were the richest in fatty acids. Linoleic acid formed the major fatty acid component, followed by oleic and palmitic acid, in crickets fed the formulated and the reference feeds. This result differs from the findings in [
58], which reported oleic acid as the major fatty acid, followed by linoleic and palmitic acid in
A. domesticus. Even when fed on different diets,
G. madagascarensis was shown to be a good supplier of alpha-linolenic acid (omega-3 fatty acids) and linoleic acid (omega-6 fatty acids), both essential fatty acids. The level of essential fatty acids (EFAs) obtained in this study was comparable to the results reported by [
8] for
A. domesticus. On the other hand, the reported fatty acids in this study were higher than those found in
G. bimaculatus (4.25–27.92%) and
G. assimilis (26.81%) [
59]. Essential fatty acids in edible crickets are important as they reflect the quality of insect oils [
60]. The ratio of polyunsaturated fatty acids (PUFA) to saturated fatty acids (SFA) varied according to the feed consumed by
G. madagascarensis. In our study, the ratio of PUFA to SFA was low and within the range of the 5:1 ratio recommended for health [
61]. These low PUFA-to-SFA ratios help prevent obesity, asthma, high blood pressure,
Diabetes mellitus, and some cancers [
61].
Regarding the cost of formulating one kilogram of the feeds, the current study demonstrated that the formulated feeds made from single-plant products from weeds and agro-byproducts incurred different costs. Formulated feeds were four to six times cheaper than the reference diet. CFG and CFF feeds were the most affordable to make compared with other feeds. This could be because using several single-plant products in feed formulation requires less of a particular agro-byproduct, especially those that might be expensive, reducing the final cost of the feed. The reference feed was the most expensive, making it the most inaccessible, unaffordable, and unsustainable feed choice for resource-poor farmers. By contrast, feeds formulated from weeds and agro-byproducts provide a cost-effective benefit but are still able to satisfy the dietary demands of
G. madagascarensis. Despite formulated feeds varying in their nutritional components, they generally provide enough nutrients for
G. madagascarensis. The global search for cheap feed suitable for farming edible crickets has been triggered by the extremely high cost of chicken feed, which has discouraged many people from farming crickets [
62]. We recommend that cricket farmers in Madagascar, a country rich in a variety of weeds and agro-byproducts, make use of these locally available and less expensive ingredients to develop feeds for their crickets while reducing the cost of cricket farming. Since supplies of weeds and agro-byproducts have seasonal limitations, cricket farmers are advised to harvest them in season, rinse them with clean water, sun dry them, then mill them into powders and pack them in hermetically sealed bags before storing them for future use. Further, weeds and agro-byproducts are bulky, requiring a lot of space for drying and storage in the case of large-scale cricket farming. To overcome such limitations, large-scale farmers can construct stacked wooden driers to make use of the sun, especially in areas where space for drying harvested weeds is limited. Moreover, large-scale farmers can construct simple barns on the farm to store the milled weeds and agro-byproducts. Wide adoption of this method can be encouraged with awareness campaigns among cricket farmers.