Conventional feed ingredients

Energy and protein are the main limiting requirements in all feeds. Energy sources constitute the largest component in poultry diets, followed by plant protein and animal protein sources. Cereal grains such as corn, wheat, barley, oats and sorghum are commonly used as energy sources in rations. Proteins are provided by both animal and plant origin sources, depending on what each country allows. Fish meal and soybean meal provide popular protein sources for poultry due to their amino acid profiles. Because of the consistent increase in cost of fish and soybean meals, the prices of poultry feed has been substantially increased (Tacon and Metian, Reference TACON and METIAN2008). A diet based on maize and soybean meal provides a good balance of all essential amino acids except methionine, which can be compensated by including synthetic methionine (Waldroup and Smith, Reference WALDROUP and SMITH2008). Soybean meal could be added up to 25-30% in broilers, breeders and laying hens (Ewing, Reference EWING1997; McDonald et al., Reference MCDONALD, EDWARDS and GREENHALGH2002). Such costs have, over the last decade, pushed many small stakeholders’ and subsistence poultry farmers out of the industry (Teguia and Beynen, Reference TEGUIA and BEYNEN2005).

Recent advances in animal production and processing technologies have further increased the demand for conventional feedstuffs like soybean by feed industry, agricultural product-dependent industries (confectionery and distillers) and food companies (Bolu and Adakeja, Reference BOLU and ADAKEJA2008). Thus, it is necessary to look for locally available, less conventional protein to substitute soybean meal in poultry ration (Chand et al., 2014). Commercial production of insect-based protein ingredients such as maggot meal, earthworm meal, silkworm pupae meal, meal worm and other insects would help subsistence and low capital farmers not only to cut down their production costs, but would also improve production efficiency.

Maggot meal

The housefly has a very high nutritive value, and has been previously used as a feed and food ingredient. This fly has been associated with disseminating various diseases and ailments in humans and animals. However, recently this animal has been increasingly recognised as a suitable insect candidate for mass production as a feed material (Uchewa, Reference UCHEWA2014). Maggots can be easily cultivated using different substrates, such as organic wastes that naturally attract housefly infestation and egg laying. Maggots are high in protein (42-62%) with digestibilities ranging from 60-72%, rendering it a good source of protein for monogastrics (Awoniyi et al., Reference AWONIYI, ALETOR and AINA2003a; Reference AWONIYI, ALETOR and AINA2003b).

Different production methods have been used by various researchers to produce maggot meal. Uchewa (Reference UCHEWA2014) adopted a method using bags full of attracting substrate (unspecified). The bags were watered periodically to prevent the substrate drying out. Fresh substrate was introduced in new empty bags to attract maggots, in this way the flies migrated from the old substrate and eggs were cultivated on the new substrate. Subsequently, the substrate was treated with hot water to kill the maggots, and then sun-dried for further processing. Offal, like any decomposing waste, attracts flies and creates an unhealthy environment. Nzamujo (Reference NZAMUJO1986) turned this challenge into an opportunity, creating a ‘fly hotel’ where offal was carefully spread over hundreds of small, square, netted open containers, encouraging flies to lay their eggs, and resulted in up to one ton of maggots being produced each week. The maggots, rich in protein, were harvested and were fed to fish and quail.

Aniebo et al. (Reference ANIEBO, ERONDU and OWEN2009) used cattle blood and wheat bran to produce maggots. The substrate was constituted by mixing 100 kg of cattle blood and 20 kg wheat bran spread on a floor space of 6 m² to a thickness of 3 cm. The odour of fresh blood and the subsequent fermenting substrate attracted flies. Fly eggs hatched into larvae within two days, and the maggots were allowed to grow for another two days. The mature maggots were harvested and sun dried until a constant weight was achieved. The dried maggots were milled into a meal using a hammer mill.

Yaqub (Reference YAQUB1991) used poultry droppings and animal carcasses to produce maggots, which were ready for harvesting five to eight days after egg laying. The maggots were then removed from the substrate using sieves and trays. The substrates containing the maggots were put on the sieve (mesh size of 5 mm) and placed over a tray and were exposed to the sun. Being phototoxic, the maggots moved away through the sieve into the tray, hence giving clean separation. The maggots were washed with water and dried in the sun, and then at 50°C for 24 h.

Samuel and Nyambi (Reference SAMUEL and NYAMBI2013) generated dried maggots from composted poultry droppings, cow dung, goat droppings, and other decaying animal waste materials. Akpodiete et al. (Reference AKPODIETE, OLOGHOBO and ONWADE1998) used fresh droppings from layer hens for maggot production, whereby the substrate was collected in plastic bowls (1 kg per fowl), and mixed with 100 ml of palm oil, and the bowls were then placed in an open shed. Houseflies laid eggs on them and the substrate was moistened by sprinkling with water daily to support larvae growth for six days before harvesting. Sufficient water was added to each bowl to completely submerge the droppings which allowed the maggots to float and be easily separated, which were then sieved, rinsed and freed of any debris. The maggots were roasted dried on a fire and milled in a laboratory hammer mill before being incorporated into diets. Other researchers have also produced maggots using poultry droppings (Okah and Onwujiariri, Reference OKAH and ONWUJIARIRI2012), which, in turn, offers a sustainable way for producing protein sources directly on the poultry farm using them.

Nutritive value of maggot meal

Maggot meal has been shown to be a good alternative protein source for fish, livestock and poultry, providing the essential amino acids with good biological value (Awoniyi, Reference AWONIYI2007). However, scientists have reported different compositions of the so-called ‘magmeal’. This large variation in its composition may be due to the differences in production and processing methods. Aniebo et al. (Reference ANIEBO, ERONDU and OWEN2009) reported that magmeal contained 47.6% crude protein (CP), 25.3% crude fat (8-12%) and 6.25% ash. Yaqub (Reference YAQUB1991) conducted proximate analysis of magmeal and reported 45% CP, 15% crude fat, 8% ash and 25% chitin. Maggot meal is of high biological value, as the CP ranges between 39-55% with crude fat from 12.5-21%. Magmeal is a rich source of phosphorus, trace elements and B complex vitamins (Teotia and Miller, Reference TEOTIA and MILLER1973). Awoniyi et al. (Reference AWONIYI, ALETOR and AINA2003b) reported that magmeal has 55.1% CP, 20.7% crude fat and 0.2% nitrogen free extracts. Maggot meal produced on poultry droppings by Okah and Onwujiariri (Reference OKAH and ONWUJIARIRI2012) contained 44.4% crude protein, 9.76% crude fat, 14.29% ash, 16.81% nitrogen free extracts, 0.03% Ca and 0.05% fat. Hwangbo et al. (Reference HWANGBO, HONG, JANG, KANG, OH, KIM and PARK2009) produced maggots in fresh poultry droppings and stated that it had a good amino acid profile, high CP (63.99%), essential amino acids (29.46%) and high CP digestibility (98.50%).

Use of maggots in poultry rations

Various researchers have used maggot meal as a protein source in livestock and poultry, replacing fish meal, soybean meal, groundnut, meat meal, blood meal either completely or partially (Awoniyi et al., Reference AWONIYI, ALETOR and AINA2003a). Akpodiete et al. (Reference AKPODIETE, OLOGHOBO and ONWADE1998) conducted a trial using the Nera breed of laying chickens to determine the replacement value of magmeal for fish meal. Inclusion of magmeal had no significant impact on daily feed intake, hen-day egg production, egg weight, FCR, liveability or external and internal egg quality characteristics. However, albumen weight (as a percent of egg weight) was significantly high in birds fed diets containing either fish or magmeal. Egg yolk cholesterol and Ca concentration were significantly reduced with increased levels of magmeal in the diet. It was therefore concluded that magmeal can replace fish meal in layer diets without adverse consequences on performance or egg quality.

Awoniyi et al. (Reference AWONIYI, ALETOR and AINA2003a) replaced 25, 50, 75 and 100% fishmeal with magmeal in the diet of broiler chickens. The diet where 25% of fish meal protein was replaced with magmeal was the most efficient in terms of average weekly weight gain and protein efficiency ratios. The live, dressed and eviscerated weights as well as the relative length, width and weights of the pectoral and gastrocnemius muscles of the chickens at nine weeks were not significantly influenced by the diets. It was concluded that maggot meal can be used as an inexpensive replacement for fish meal in broiler ration.

A 35-day feeding trial was conducted by Okah and Onwujiariri (Reference OKAH and ONWUJIARIRI2012) to evaluate the performance of finisher broilers fed magmeal as a replacement for fish meal. Five diets were formulated so that magmeal replaced fish meal at 0, 20, 30, 40 and 50%. Chickens fed the control diet consumed less feed (P<0.05) and gain less body weight as compared to 40-50% maggot meal feed. Those fed magmeal had better FCR than those fed the control diet, demonstrating that magmeal can be a cheaper protein source, which can successfully replace expensive fish meal.

Hwangbo et al. (Reference HWANGBO, HONG, JANG, KANG, OH, KIM and PARK2009) studied the utilisation of maggots as a feed supplement for the enhancement of broiler performance. They investigated the effects of maggot supplementation on meat quality and performance in Ross broilers. The birds were fed a basal diet (control) or this same diet supplemented with 5, 10, 15 and 20% magmeal. It was observed that the increasing level of maggot supplementation caused a linear increase in live weight gain, however FCR was not improved, indicating increased feed intakes. The diets supplement with 10 and 15% maggots were the most efficient. In maggot-fed broilers, breast muscle lysine and tryptophan levels were significantly higher than the control group. Téguia et al. (Reference TÉGUIA, MPOAME and OKOUROU MBA2002) found that up to 6.75 g/kg fish meal in the starter ration and 20 g/kg fish meal in the grower-finisher ration could be totally replaced by house fly maggot meal. The overall positive effects of maggot meal on animal performance and product quality could be due to the improved digestibility and availability of essential amino acids.

Earth worm

Yaqub (Reference YAQUB1991) successfully produced earthworms from waste to feed catfish (Heterobranchus isopterus). Three pits were filled with poultry droppings and loamy soil was added to the droppings to simulate the natural environment for earthworms. The pits were covered with plastic sheets to prevent the substrate from being saturated by rain water. They were watered to keep the substrates moist for the best results. Earthworms were ready for harvesting in five to eight days. Brown (Reference BROWN1995) and Brown et al. (Reference BROWN, DOUBE and EDWARDS2004) reported that fungi represent important food sources for earthworms and a number of studies have shown that earthworm preferentially consume litter that is extensively colonised by fungi. Sogbesan and Ugwumba (Reference SOGBESAN and UGWUMBA2008) cultured earthworm using a mixture of saw dust (30%), rice bran (20%), mushroom (Pleurotus sajor caju) (20%), Centrosema pubescens leaves (15%) and poultry droppings (15%). Barcelo (Reference BARCELO1988) produced earthworms using a mixture of fresh manure from cattle, swine, goats and chickens, Leucaena leucocephala leaves, sawdust, rice hull and rice bran. The substrate was fermented by keeping it moist and turning every day to allow the heat generated to escape from the pile. When heat production stopped, an equal proportion of L. leucocephala leaves and the animal manure were placed in experimental boxes. A mixture of sawdust, rice hull and rice bran at a proportion of 55, 35 and 10% respectively were placed in separate boxes and served as another substrate. Each box was supplemented with either 0, 100, 200, 300 or 400 g fermented kitchen scraps. After harvesting, direct heating or freezing were used for killing earthworms prior to drying. Sherman (Reference SHERMAN2003) mentioned in his book regarding earthworm production, that earthworms required a temperature of 60 to 80°F, moisture content 60 to 85%, pH of 6.8 to 7.2 and can survive in a relatively low O₂ and high CO₂ or in dissolved O₂ within water.

Nutritive value of earthworms

Watson (Reference WATSON1957) determined the chemical composition of the earth worm cuticle and found that approximately 80% was CP, which contained a high proportion of hydroxyprolyl and glycyl residues. The remainder of the cuticle was chiefly composed of polysaccharides, which, when hydrolysed, yielded galactose and small amounts of pentoses and hexoses. Sogbesan and Ugwumba (Reference SOGBESAN and UGWUMBA2008) reported that earth worm contained (on DM basis) 63.0% CP, 5.9% crude fat, 8.9% ash, 0.43% Na, 0.53% Ca, 0.62% K, 0.94% P and 1476 kJ/100g of metabolisable energy. Furthermore they determined the essential amino acid composition of earthworm meal and found that it contained Arg 2.83, His 1.47, Iso 2.04, Leu 4.11, Lys 6.35, Let 5.30, Phe 6.26, Thr 4.43 and Val 4.43 g per kg protein. Finke (Reference FINKE2002) reported that earthworm contained 10.5% CP, which compromised Arg 0.61%, Met 0.19%, Lys 0.66%, Thr 0.47%, Trp 0.09%, crude fat 1.2% and ash 0.6%. Reinecke et al. (Reference REINECKE, HAYES and CILLIERS1991) in South Africa evaluated protein content of three species of earthworms and reported a CP content of 66.1%, 58.4% and 61.6% for Eisenia fetida, Eudrilus eugeniae and Perionyx excavatus respectively, compared to 61% for fish meal. Paoletti et al. (Reference PAOLETTI, BUSCARDO and VANDER JAGT2003) reported large amounts of CP (64.5 to 72.9%), essential amino acids, total fatty acids (6.6 to 10.5 mg/g dry weight of crude fat), Ca (1020-7070 μg/g dry weight) and Fe (1050-2990 μg/g dry weight). Tiroesele and Moreki (Reference TIROESELE and MOREKI2012) carried out proximate analysis of earthworm meal and found that it comprised 63.0% CP, 5.9% crude fat, 1.9% crude fibre, 11.8% NFE and 8.9% ash.

Nutritional value of earth worms

There is very little information on the use of earthworm meal in poultry diets however, Prayogi (Reference PRAYOGI2011) conducted a study in Indonesia and found that 10% earthworm meal could replace a large portion of the fish meal in the diet with no adverse effect on body weight gain and FCR. However, feed intake was reduced at a 15% inclusion level. Sharma et al. (Reference SHARMA, PRADHAN, SATYA and VASUDEVAN2005) argued that heavy metals and other pollutants may be taken up by the worms and can be passed on to the birds consuming them. Tiroesele and Moreki (Reference TIROESELE and MOREKI2012) demonstrated the potential utilisation of earthworms as alternative feed resources in terms of protein, mineral and essential amino acid contents for smallholder poultry production. Prayogi (Reference PRAYOGI2011) conducted a trial to evaluate the effect of replacing fishmeal with earthworm meal in quail rations. Quail were supplemented with 0% of earthworm meal and 15% of fish meal (control), 5% of earthworm meal and 10% of fish meal, 10% of earthworm meal and 5% of fish meal and 15% of earthworm meal and 0% of fish meal in the diet. Increased earthworm supplementation decreased feed consumption, although supplementation with 10% earthworm meal gave good growth performance in terms of FCR and body weight gain. Son and Jo (Reference SON and JO2013) supplemented earthworm meal to seven day old broiler chicks to determine its effect on growth performance and nutrient digestibility. Chicks were fed diets containing 0%, 0.2% and 0.4% of earthworm meal for six weeks. High feed intake, weight gain and nutrient digestibility was observed when the chicks were fed diets containing 0.4% earthworm meal. Son (Reference SON2009) reported that supplementing 0.2 to 0.6% earthworm meal in laying hens diet, improved laying performance and egg quality, especially the ratio of egg yolk n-6/n-3 fatty acids. Heavy metals, namely, As (4.41 ppm), Cd (1.23 ppm), Cr (1.18 ppm), Hg (0.00ppm) and Pb (3.39 ppm) were detected in earthworm meal, respectively, but were not detected in meat or eggs and did not affect quality. Barcelo (Reference BARCELO1988) reported that increasing levels of earth worms from 6% to 14% in broiler rations and concurrently decreasing levels of fish meal from 14% to 6% tended to improve FCR.

Silkworm pupae

Silkworms are the waste product of silk industry. The pupae are sun dried, powdered and used as silkworm pupae meal (SWPM), and a number of studies have reported its use as an alternate protein source in poultry rations. Dutta et al. (Reference DUTTA, DUTTA and KUMARI2012) and Khatun et al. (Reference KHATUN, HOWLIDER, RAHMAN and HASANUZZAMAN2003) used SWPM in Rhode Island Red (RIR) and straight run Arber Acres broiler chicks. Khatun et al. (Reference KHATUN, AZMAL, SARKER, RASHID, HUSSAIN and MIAH2005) conducted a study to evaluate SWPM in a feeding trial using layer chicks (RIR pure line). Silkworms were collected and the upper silk layer was discarded by heating with baking powder solution for 30 minutes and then washed in clean water, sun dried, and ground to a powder. Wijayyasingth and Rajaguru (Reference WIJAYYASINGTH and RAJAGURU1977) obtained silkworm pupae which were ground to open the chitinous coverings and the enclosed powdered pupal matter released.

Nutritive value of silkworm meal

Wijayyasingth and Rajaguru (Reference WIJAYYASINGTH and RAJAGURU1977) determined the chemical composition of SWPM and found that it consisted 8.50% moisture, 19.47% crude fat, 63.3% CP, 3.10% crude fibre and 4.50% ash. Mlcek et al. (Reference MLCEK, ROP, BORKOVCOVA and BEDNAROVA2014) reported that SWPM contained quality protein and essential nutrients, a balanced ratio of amino acids and unsaturated fatty acids. Hertrampf et al. (2000) reported that it contained 88.9% dry matter, 89.6% organic matter, 55.1% CP, 23.2% crude fat, 3.8% ash, 5.5% crude fibre and 6.4 NFE. Andrew (Reference ANDREW2009) found that SWPM consisted 60.7% moister, 229 kcal/kg energy, 23.1% CP, 14.2% crude fat and 1.5% ash. On average, SWPM has 50-60% CP, 25-35% crude fat, 8-10% sugars, and traces of vitamin E, B1 and B2, nicotinic acid, pantothenic acid, Ca, P, Cu, Fe and Se.

Silkworms as a protein source for poultry

Dutta et al. (Reference DUTTA, DUTTA and KUMARI2012) used various levels of SWPM in gradual replacement for fish meal. They found that a linear increase of SWPM in the poultry feed caused a corresponding decrease in cost per unit of feed. Khatun et al. (Reference KHATUN, HOWLIDER, RAHMAN and HASANUZZAMAN2003) replaced fish meal with SWPM in diets for straight run Arber Acres broiler chicks. Four iso-nitrogenous and iso-energetic diets formulated with either 6% fish meal + 0% SWPM; 4% fish meal + 2% SWPM; 2% fish meal + 4% SWPM; or 0% fish meal + 6% SWPM. Their results showed that growth rate, FCR, liveability, meat yield and profitability increased in a linear manner with increasing levels of SWPM. Khatun et al. (Reference KHATUN, AZMAL, SARKER, RASHID, HUSSAIN and MIAH2005) conducted a study to evaluate SWPM on growth and egg production performance in young RIR layer. The study revealed that profitability, growth and egg production performance was significantly higher for diets with 6% SWPM as compared to 0% and 8% SWPM. Feed cost/kg gradually declined with increasing inclusion of SWPM and efficiency of the birds receiving SWPM was improved compared to the control. Hence, SWPM could be an excellent substitute for more costly protein ingredients in layers rations, leading to increase profitability. Wijayyasingth and Rajaguru (Reference WIJAYYASINGTH and RAJAGURU1977) found that SWPM was suitable as a substitute for fish meal in trials examining the performance of broiler starters, broiler finisher and laying hens. As an extra benefit they found improved reproductive performance in layers fed SWPM diets.

Mealworm

The lesser mealworm (Alphitobius diapernis) is one of the most important and widespread pests in commercial poultry production. The adult beetle is known as the darkling beetle, litter beetle or black bug. The lesser mealworm can be grown on spilled feed, manure, bird cadavers and cracked eggs, and infests a wide variety of stored products like wheat, barley, rice, oatmeal, soybeans, cowpeas, peanuts, linseed, cottonseed, oilseed, tobacco and drugs (Loftin and Corder, Reference LOFTIN and CORDER1914). The yellow mealworm has been shown to be an acceptable protein source for broiler chickens. They can be grown on waste materials including fruits, vegetables and cereals in various combinations (Veldkamp et al., Reference VELDKAMP, VAN DUINKERKEN, VAN HUIS, LAKEMOND, OTTEVANGER, BOSCH and VAN BOEKEL2012). Tang et al. (Reference TANG, DAI and LIU2010) cultured yellow mealworms on a diet of wheat bran, whole wheat flour, and brewer's yeast (50:45:5 w/w) at 26±1°C and 55±5% relative humidity with a photoperiodic of 12 hours light and 12s hour darkness. Ramos-Elorduy et al. (Reference RAMOS-ELORDUY, AVILA GONZALEZ, ROCHA HERNANDEZ and PINO2002) reared mealworms (Tenebrio molitor) on low-nutritive waste products and fed them to broiler chickens. Mealworms transformed the low-nutritive waste products into a high-protein source, which showed the potential of mealworms as a promising and sustainable source of alternative protein for poultry rations.

Nutritive value of mealworm

Veldkamp et al. (Reference VELDKAMP, VAN DUINKERKEN, VAN HUIS, LAKEMOND, OTTEVANGER, BOSCH and VAN BOEKEL2012) reported that yellow mealworm (Tenebrio molitor) contained 44-69% CP and 23-47% crude fat. Yellow mealworm larvae contained 53.4% CP on dry matter basis as compared to 67.9% CP in lesser mealworm and 45.0% CP in super (larger) meal worm larvae. Yellow mealworm pupae had a crude fat content of 33.8%, whereas that of lesser mealworm larvae was lower at 20.7% and the super meal worm larvae contained 41.4%.

Abd-Rahman-Jabir et al. (Reference ABD-RAHMAN-JABIR, RAZAK and VIKINESWARY2012) determined the chemical composition and nutrient digestibility of super worm meal in their work on fish feed formulations, and found it had a lower content of CP (42.83%) compared to fish meal (52.64%). The super worm meal contained a high percentage of crude fat (40.01%) along with high quality protein and this made it a suitable replacement for fish meal. Super worm meal contained seventeen amino acids. The total amount of the essential amino acids found in super worm meal and fish meal were 199.20 and 288.40 mg/g CP, respectively.

Ramos-Elorduy et al. (Reference RAMOS-ELORDUY, AVILA GONZALEZ, ROCHA HERNANDEZ and PINO2002) grew mealworms on low-nutritive waste products and fed these to broiler chickens. The mealworms were able to transform the low nutritive waste products to a high protein diet. Soybean meal (protein content 55%) was reduced to 31, 26 and 20% of the diet and replaced by 0, 5 and 10% of mealworm, respectively. The basic feed source, sorghum (with 9% protein) was 61 to 64% of the diet (by weight), and did not change in the three treatments. Performance was maintained with the replacement by super worm meal.

Acknowledgement

The authors extend their appreciation to the Deanship of Scientific Research at King Saud University for funding this work through research group No. RG-1436-021.