Insects Such as Termites Hold a Promising Future for the African Catfish (Clarias gariepinus)

Abstract

Due to the high cost of fishmeal, it has been desirous to search for alternative sources of protein which are cheap and can replace fishmeal without compromising the growth and well-being of cultured fish. The use of insects such as termites to totally or partially replace fish meal is indeed innovative since most insect-based diets are known to inhibit the growth of cultured fish species due to some underlying factors. However, termite meal has been applauded for its good nutritional quality (crude protein and lipids, mineral composition, fatty, and amino acids) comparable to fishmeal. The concentration of phytate and tannin which could otherwise inhibit nutrient digestibility and growth of fish can be eliminated through proper processing techniques. Interestingly, concentrations of other anti-nutrients such as oxalate, trypsin inhibitor, lectin, and hydrocyanic acid in termites are known to be negligible and as such may not affect the digestibility and absorbance of essential nutrients.

1. Introduction

Fish is a staple food in many nations around the world, and in many Asian and African nations, consumption patterns for fish and rice are similar [1]. A stronger contribution from aquaculture is expected to increase the annual consumption rate of fish from 20 kg per person in 2016 to 37.8 kg per person in 2030 [2]. The increased demand for high-value protein, which is anticipated to nearly double by 2050 as a result of the rapidly expanding population in developing nations, is one of the major nutritional problems around the world [3].

Recent research has focused on ensuring sustainable aquaculture in order to supply this constantly growing need for protein while staying within environmental constraints. Farmers now run the risk of being blackmailed and may give up aquaculture in favor of more lucrative endeavors due to the unsustainable rise in the price of beef meal, fishmeal, and soybean meal. This is because expensive fish meal and other expensive protein sources account for 60–70% of the cost of aquaculture operations [4]. These trends amply demonstrate the need for increasing the production of alternative sources of protein, such as insects, which are less expensive, readily available, trustworthy, and sustainable. Aquaculture is still the sector of animal food production that is expanding at the fastest rate.

Despite being in its infancy, aquaculture has produced a large majority of insects, many of which were laboratory experiments. However, insects have a bright future, especially for fish nutrition and sustainable aquaculture. Because of the excellent quality and quantity of protein and fat they provide, humans and domestic animals, including fish, have recently developed an overwhelming appetite for insect-based diets [5]. Numerous catfish species and other fish species have shown outstanding growth responses to insect-based diets, according to recent studies [6, 7]. When it comes to the aquaculture production rate among other fish species raised in Africa, catfish and tilapia are competitors. Due to their rapid development rates, tolerance to a wide variety of water quality, good sensory quality of their meats, and high desire and acceptance by consumers, catfish of the Clarias and Heterobranchus genera are popular choices.

Many studies on the potential of insects in aquafeed use houseflies, mealworms, and soldier flies in their trials [8, 9, 10], but very few studies use termites [11]. The Isoptera order and family of termites are eusocial insects that live in colonies with reproductive castes as their leaders [12]. They are significant players in the early stages of plant litter decomposition in tropical habitats, especially in Africa’s deserts and rain forests. Furthermore, termites have contributed significantly to the staple foods of the majority of African and Asian countries, where there are more than 2.5 billion insect eaters [2]. They are among the most nourishing insects and the second most consumed insect order after Orthoptera [13]. They have been thoroughly examined for great quality and quantity of lipids, crude protein, and fatty acids. Edible termites such as those in the genus Macrotermes are generally safe and good for feed, but some Noditermes and Cubitermes species have been known to be hazardous to farm animals.

Crude protein, lipids, and fatty acids are abundant in edible termites, as are well-balanced essential amino acids such as lysine, threonine, and histidine. In addition to being rich in minerals like magnesium, manganese, potassium, iron, zinc, and phosphorus, they are also high in vitamins [14]. As a result, it has been suggested that termite meals compete favorably with fish meal in encouraging the growth and welfare of farmed fish. Unfortunately, termites can only be found in nature during particular months or seasons. For instance, they can be found during the alate or swarmer nuptial flights or at the beginning of the rainy season. The apterous reproductive adults can be seen in huge numbers close to light sources during swarming since they are drawn to light by nature. They now land, drop their wings, move in pairs into a crack in the ground, seal it shut, and mate to start a new colony. Poor villagers in certain African nations collect termites for food using a broom and a pail of water as they are drawn to their lights.

In addition to humans, fish are known to eat live termites that fall into their ponds. This opportunistic feeding takes place when live food is in plentiful supply in fish farms. The mouths of fish and other vertebrates have been modified to prefer insect prey. For instance, the broad mouths of African sharptooth catfish (Clarias gariepinus) and African giant catfish (Heterobranchus longifilis) allow them to swallow complete insects [15].

Termite meal is a crucial component that has been employed frequently to compound feeds in animal farms in nations like Cambodia, Thailand (Southeast Asia), Nepal (South Asia), Kenya, and Zambia (East Africa), as well as Togo, Burkina Faso, and Ghana (West Africa) [16]. Termites can be simply and inexpensively harvested [17]. Rural fish farmers can reduce the high cost of fish meal and other animal and plant proteins used in aquafeed by employing termites instead of cottonseed cake and soybean meal. Numerous authors have already discussed the usage of termites in food and feed [14, 18, 19, 20]. Studies [11, 21] found that African giant catfish (H. longifilis) and African sharptooth catfish (C. gariepinus) fed termite-based diets with an ideal inclusion level of 50% crude protein experienced excellent growth performance and nutrient utilization.

2. Field harvesting, farming, and processing methods

2.1 Termite harvesting in the field

Various techniques are used for harvesting termites in the field. These techniques, however, are based on the termite genus. The two most efficient techniques for Macrotermes are fractional termite mound demolition and trapping [13]. The majority of farmers that collect termites for animal feed use a variety of environmentally friendly trapping techniques that protect termite mounds [22].

In general, termite collecting involves using old clay, iron, or plastic containers, occasionally calabashes, or baskets fashioned from nypa or other palm leaves. These containers hold termite baits made of organic materials including plant detritus, crop residues, and animal droppings [23]. The containers are typically put upside down and close to termite colonies. To consume the substrates and become stuck, the termites enter the container. In addition to using a trapping system, collecting termites is another option available in the wet season, particularly following a significant downpour when adult winged termites swarm in April and October. Locals notice them because they are drawn to light naturally.

Despite being classified as seasonal insects, termites can be sustainably induced to be present even during the dry season, potentially ensuring a supply throughout the year [24]. Termite mounds in western Kenya are owned by farmers and passed down through inheritance. This has made the termite industry quite profitable in certain places [25].

Farmers use live termites in Southeast Asia to feed their farmed fish. They either collect the termites directly from the field or purchase them for 0.27 USD per kg from local markets [4]. By suspending a fluorescent lamb above fish ponds, mainly during the months of March and April and August and September, termites can be fed directly to the fish. Insects are taken as prey in fish ponds by the fish because they are drawn to light and its reflection in the water. Field-caught termites such as Trinervitermes species are frequently used as fish bait in Zambia [4]. Although termite rearing has historically been considered to be a very challenging task and frequently not advised due to high methane gas emissions, reports show that termite rearing contributes the least to global methane emissions when compared to rice cultivation, cattle production, mining, use of fossil fuels, and burning of biomass [26, 27].

2.2 Termite farming

Seasonal insects like termites can be grown in a controlled environment to produce them year-round [28, 29]. Typically, the production of eggs, larvae, and sustaining progenitors is the first risky step in insect farming [30]. Environmental management practices must be strictly followed during termite rearing in enclosures for the best possible growth and development. The importance of factors including ambient temperature, relative humidity, photoperiod, feed quality, and mitigating the spread of disease must not be understated [29, 31].

Such situations could be addressed by contacting a reliable technical advisory/supervision team for assistance with long-term intensive insect farming. Due to their destructive habits and reputation as pests among farmers, most research has focused on finding ways to remove termites rather than domesticating them for food. Due to this failure, termite farming is now only in the infantry or laboratory trial stage throughout the world. The termite laboratory rearing described in a 1991 publication is a unique one [32]. A subterranean termite’s small-scale raising is described in the paper (Reticulitermes speratus). However, according to recent studies, termite farms are also present in Kenya and India. With a price of Sh 12 per 150 g dry weight on the local market, Kenya is a major producer of termites [25].

2.3 Processing methods

The termite meal is dried in the sun to prevent the nutrients from being destroyed by potential overheating during laboratory drying with an autoclave or other drying equipment [33, 34]. However, autoclave can still be cautiously employed especially during the wet season to ensure availability of raw materials for sustainable production of termite meals. Processing methods for the world’s supplies of fish meal include drying and grinding, employing chemicals to extract some of the nutritious components, boiling, or fermentation. The quantity of protein available, the makeup of the resultant amino acids, and the digestibility are all determined by these processing methods [33].

3. Nutritional composition of termites

3.1 Proximate composition

Table 1 obtained from a 2013 study [24] depicts the relative composition of four species of edible termites consumed in western Kenya. The moisture content ranged from 6.5 to 8.8 g/100 g. However, an earlier study from the same region reported a lower content of 1.7 g/100 g [35]. The degree of moisture content of any dried food is greatly influenced by the drying environment, among other things. Due to the fact that some of the meals are dried on the ground, water may collect around them rather than drain away, making the drying process difficult [36]. The protein content of the termite species ranged from 33.5 to 39.3 g/100 g, which is comparable to the dried termite protein value of 35.70 g/100 g previously reported [35].

	Mendi termite	Sugarcane termite	War-like termite	Fungus-growing termite
Moisture	6.5	5.0	5.1	8.8
Protein	39.3	33.5	39.7	37.5
Lipid	44.8	46.6	47.0	47.3
Total ash	7.6	4.6	4.7	7.2
Dietary fibre	6.4	6.6	6.2	7.2
Carbohydrate	1.9	8.7	2.4	0.7

Table 1.

Proximate composition of edible termites (g/100 g).

Except for moisture content, which is in wet weight basis, other compositions are as per dry weight basis of winged termites [24]. Mendi termite (Macrotermes subhyalinus). Sugarcane termite (Pseudacanthotermes militaris). War-like termite (Macrotermes bellicosus). Fungus-growing termite (Pseudacanthotermes spiniger).

Termites have excellent protein quality that is advantageous for human and animal nutrition [5], even though these values are lower than those recorded in fish (70.6 g/100 g) and soybean (51.8 g/100 g) [37]. As can be seen in Table 1, the termites’ lipid content varied from 44.8 to 47.3 g/100 g. Another study [38] found 19.70–24.10 g/100 g for various termite species in Nigeria, while a previous study [35], also recorded 53.4 g/100 g for sun-dried termites. Termites should be defatted prior to use as meal in order to bring the lipid content of termites to the levels reported in fish (9.9) and soybean (2.0) [37].

As reported, the ash content in termites ranges from 4.6 to 7.6 g/100 g [24]. However, a study found a value for dried termites as low as 4.8 g/100 g [35]. The presence of high levels of ash in termites may result from persistent ash contamination of the soil during harvest and drying. Before such food samples are analyzed, sorting is a method to eliminate any visibly present soil, dust, and other physical pollutants. The average value of 15.8 g/100 g reported for fish [37] is lower than the ash content of termites, which is also lower. The carbohydrate content per 100 grams varies from 0.7 to 8.7 g. However, another study [39] recorded a value of up to 29.0 g/100 g. The range of dietary fiber per 100 grams is 6.2 to 7.2 g. Because chitin and cellulose have structural similarities, the fiber seen in insects is actually chitin [24]. Insects may therefore have high fiber content because of chitin.

3.2 Amino and fatty acids

From the reports on catfish nutrition and nutrient requirements, termites possess all the essential amino acids, such as histidine, methionine, and lysine, required for the sharp-tooth catfish to grow to their full potential [40, 41]. Because termite-based diets may not require the addition of methionine, lysine, or any other essential amino acid, they have an advantage over other insects in this regard. Ten amino acids are required for proper fish nutrition: arginine, histidine, isoleucine, leucine, lysine, methionine, phenylalanine, threonine, tryptophan, and valine. According to the developmental stage (larva, pupa, prepupa, and imago), the type of diet, and the rearing conditions, the amount of protein in insect bodies varies. As a result of these variations, the amino acid content can also vary [15].

According to the data in Table 2, termite oil has a higher percentage of unsaturated fatty acids than polyunsaturated fatty acids (PUFA). The most common fatty acid in the lipid fraction of termite species was oleic acid [24].

	Mendi termite	Sugarcane termite	War-like termite	Fungus-growing termite
Capric acid	0.0	0.2	0.2	0.3
Caprylic acid	0.0	0.0	0.4	0.4
Lauric acid	0.0	0.0	0.2	0.2
Myristic acid	1.1	0.0	1.2	0.8
Palmitic acid	27.7	26.0	38.4	28.0
Palmitoleic acid	4.2	5.8	0.6	3.2
Stearic acid	6.3	5.9	9.5	6.1
Oleic acid	48.6	50.3	41.7	49.3
Linoleic acid	10.8	11.5	5.0	10.5
Linolenic acid	1.4	0.2	0.9	0.8

Table 2.

Fatty acid composition of edible termites.

Compositions are as per dry weight basis of winged termites [24]. Mendi termite (M. subhyalinus). Sugarcane termite (P. militaris). War-like termite (M. bellicosus). Fungus-growing termite (P. spiniger).

3.3 Mineral composition

Termites are a great source of minerals like calcium, iron, and zinc, as indicated in Table 3. The contribution of micronutrients, which are well known to be lacking and generate serious public health concerns in poor people in developing nations, is particularly significant while focusing on the nutritional significance of edible insects [42]. Iron and zinc deficiency are major public health issues, particularly for mother and infant health [43]. In general, reports on the amounts of zinc and iron in different insects show that they are a valuable source of these minerals [44, 45].

	Mendi termite	Sugarcane termite	War-like termite	Fungus-growing termite
Ca	58.7	48.3	63.6	42.9
Fe	53.3	60.3	116.0	64.8
Zn	8.1	12.9	10.8	7.1

Table 3.

Mineral composition of edible termites (mg/100 g).

Compositions are as per dry weight basis of winged termites [24]. Mendi termite (M. subhyalinus). Sugarcane termite (P. militaris). War-like termite (M. bellicosus). Fungus-growing termite (P. spiniger).

3.4 Anti-nutrient composition

The presence of antinutrients, which are typically linked with undigested cellulose in the intestines of insects, is one of the factors that restricts the use of insects as food for fish and other animals. Antinutrients can prevent nutrient digestion, which can have a negative impact on fish growth. Degutting, however, is a method for removing these anti-nutrients from insect guts. Additionally, it has been found that oven drying the termites before using them as animal feed successfully removes anti-nutrients such as phytic acid and antioxidant polyphenols without harming the vital nutrients [46]. Additionally, termites are said to have minimal or no concentrations of additional anti-nutrients such as calcium oxalate, trypsin inhibitor, lectin, and hydrocyanic acid [47].

4. Growth response and nutrient digestibility

4.1 Growth response

The catfish, H. longifilis has been observed to perform well in terms of growth when fed with diets containing termite meal [21]. In other studies, the growth of African catfish was not adversely affected when termite meal was used to partially or entirely replace fish meal [11].

4.2 Nutrient digestibility

One of the main concerns of stakeholders who purchase insects in aquafeed is the nutritional digestibility of nutrients by fish fed insect meal. This worry is frequently brought on by the presence of chitin from the exoskeleton, which may decrease perceived digestibility and, as a result, the growth of farmed fish. However, the amount of chitin is dependent on the species and stage of the insect’s growth [48]. It is questionable whether fish can digest chitin because some fish do so better than others.

It is interesting to note that catfish have a critical adaptive system for breaking down insect chitin. Many catfish have chitinase in their gastrointestinal tracts (GIT), which facilitates the ingestion of insects. Chitin from insects and crustaceans must be broken down by the enzyme chitinase, which is produced by the pancreas and the gastric glands. Termites and other arthropods have been a part of natural fish diets for a long time, as evidenced by the digestive enzyme chitinase, buccal organ alterations, and behavioral adaptations of fish like catfish [15].

In insects, the digestibility of proteins and amino acids (AAs) might vary depending on how much of the AAs are bonded to chitin or scleroderoprotein, which are mostly found in adult insect cuticles. The chitinolytic activity of enzymes like chitinase in the stomach and chitobiase in the intestine, which are present in the gastrointestinal tracts of many fish species that feed on insects and other macroinvertebrates like shrimp and crabs, allows these proteins or amino acids to be available for fish nutrition.

5. Conclusions

Due to their adaptability and capacity to adjust their amino acid and fatty acid profiles and transform cellulose into protein, termites are one of the best alternatives to fish meal when replacing it partially or entirely. Fishmeal is expensive, so it has been desirable to look for cheaper protein alternatives that can take its place without hindering the growth of farmed fish. Termite meal has received praise for having an excellent nutritional content that is comparable to fish and soybean meals (crude protein and lipids, mineral composition, fatty and amino acids). Chitin, a growth inhibitor for many farm animals, can be spontaneously broken down by catfish into useful components.

With the right processing methods, the concentration of phytate and tannin that could otherwise prevent fish from absorbing nutrients and growing can be reduced. It is interesting to note that other anti-nutrient quantities in termites, such as oxalate, trypsin inhibitor, lectin, and hydrocyanic acid, are known to be minimal and may not have an impact on the digestion and absorption of vital nutrients.

Acknowledgments

The authors appreciate Dr. Edet’s reading of the manuscript’s first draft and her helpful comments, which helped to make the article better.