Introduction

Protein can be obtained from many feedstuffs such as meat and fish meals, cereal grains and legume by-products such as soybean meal. Usually, fish meal is commonly used as the most popular protein source for poultry production, and it is frequently the preferred source of protein because of its balance of essential amino acids (Advisory Committee on Animal Feeding Stuffs 2001). Nevertheless, the fish meal has a nutritional constraint in its usage, for example, the high content of histamine that can cause a defect on the gizzard of the poultry (Miculec et al. 2004). The fish meal is also known to cause tainting of chicken meat depending on quantities used and stages of feeding (Swick 1999). Feed cost has constituted about 60–70% of poultry production (Hinrichs and Steinfield 2007; Tiroesele and Moreki 2012). In the least cost feed formulation, the protein content of feed ingredient is the most expensive feed ingredient because conventional feeds are scarce and limited. Though, nutritionists choose ingredients that are high in protein to meet the nutrient requirements of chickens of different categories (Bhatti et al. 2002).

Fishmeal and soybean have been used worldwide as a source of protein for poultry. They are the conventional sources of animal protein in the poultry industry. They have been treasured for their balanced amino acids, and palatability (Davis et al. 2005; Antolovic et al. 2012). Due to the rise in prices of high-quality conventional animal feed required for poultry and competition for feed-in human diets as well as animal husbandry, these feedstuffs are becoming limited and scarce.

Since there is a restriction on the availability of conventional feed for chickens, researchers have come up with alternative protein sources of poultry feed. These alternatives are able to supply adequate essential and non-essential amino acids to enable their synthesis. Moreover, it has been reported that the possible use of some alternative animal protein feedstuff to substitute fishmeal such as earthworms can be a solution (Istiqomah et al. 2009; Ogello et al. 2014).

Earthworms Eisenia fetida have been found to be a good source of protein (Korstecka and Pączka 2006; Sogbesan and Ugwumba 2008). Earthworms with an important high protein component are used to feed chickens, pigs, rabbits, and as a dietary supplement for fish species (Kostecka and Pączka 2006; Stafford and Tacon 1985; Sabine 1986; Mason et al. 1992). The nutritive potential and utilization of earthworm E. fetida as poultry feed ingredients have not been documented in South Africa. Therefore, the objective of this review is to create attentiveness on the nutritional value of E. fetida as a source of protein for poultry.

Description of Eisenia fetida

Eisenia fetida worm belongs to the family of lumbericidae and genus Eisenia, which is known by other names such as the tiger worm, garlic worm, flatworm, cadillac worms and worm for fishing bait (Fadaee 2012). These worms are red, purple or brown in colour and yellowish in their abdomen. The number of its segment is about 80–110 and it is between 23–130 mm in length (Fig. 1). During puberty, the genital belt reaches to 7–9 pieces in between parts 24, 25, 26 or 32.

Fig. 1
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Eisenia fetida image (Schuld 2004)

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Growth of Eisenia fetida

Eisenia fetida growth depends on population density and food rationing (Singh et al. 2013). Their weight increases faster with a decrease in the population density (Garg et al. 2005). On the other hand, Ton et al. (2009) observed that the growth rate of earthworms depends heavily on the type and quality of the substrate. Normally, the growth cycle of worm E. fetida takes 40–60 days for the juvenile to develop into a mature or adult worm (Fadaee 2012). Adult worm weight is approximately 1.5 g at 50 to 55 days. After coming out of the cocoon they are able to reproduce. Adult worms can create a cocoon every three days on average and after 23 days, one- third of newborns come out of the cocoon (Fig. 2). For optimum growth of worms, they require temperatures that range between 15 to 20 ˚C, moisture content from 89 to 90%, oxygen, ammonia content of waste lower than 0.5 mg/g, salt content that is less than 0.5% and pH that ranges from > 5 and < 9 (Sherman 2003).

Fig. 2
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Growth cycle of earthworm Eisenia fetida (Venter and Reinecke 1988)

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Reproduction of Eisenia fetida

Eisenia fetida is hermaphroditic which means that each worm has both female and male reproductive organs (Dynes 2003). Eisenia fetida can reproduce by both sexual and asexual reproduction. They have a high reproduction rate due to their hermaphrodite nature, which allows each individual to produce 9 cocoons, each containing up to 20 eggs at least every 14 days (Musyoka et al. 2019; Tripathi and Bhardwaj 2004). The majority of the species reproduce by cross-fertilisation, although some reproduce cocoon parthenogenetically. In sexual reproduction, worms mate by joining their citellums together with the heads pointing in opposite directions. After copulation and long after the worms separate each worm secretes three eggs or their cocoon from citellim. It takes approximately four days for the formation of cocoon after mating has occurred (Reinecke and Alberts 1988). Incubation lasts for about 23 days for worms to hatch (Fig. 3). Three hatchlings are produced from each cocoon and it takes 20 to 40 days for mature worms to develop citelli (Reinecke and Alberts 1988). According to Edwards and Bohlen (1996), a cocoon takes about 3 to 5 months to hatch.

Fig. 3
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Lifecycle/reproduction cycle of the earthworm Eisenia fetida (Venter and Reineck 1988)

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Feeding earthworms

Earthworms feed on organic matter (Yadav and Garg 2009), including animal waste, plant waste, and urban waste. Animal manure is the main source of feed for E. fetida (Gunadi and Edward 2003). This was also substantiated by Sherman (2003) who specified that cattle horse, rabbit, swine, dairy and beef manure are excellent feed for earthworms, but poultry manure is not recommended because of its high protein and mineral content. It has been found by many authors that they grow faster in cattle manure (Atiyeh et al. 2000; Nagavallmma et al. 2004; Singh et al. 2013). Cattle dung has lower ammonia levels (Ton et al. 2009) and it is rich in nitrogen which enhances the rapid growth of E. fetida (Sharma et al. 2005). They are usually found in areas rich in organic matter, such as the upper topsoil layer, in the forest under piles of leaves or decaying logs, or in piles of manure.

Eisenia fetida nutrient composition

Protein Content of Eisenia fetida

Eisenia fetida is rich in crude protein as shown in Table 1. Crude protein of E. fetida differs with treatments applied on it (Table 1) Eisenia fetida are mostly featured by their high protein content that ranges between 58 and 71% dry weight (Zhenjun et al. 1997; Tiroesele and Moreki 2012). Eisenia fetida has been found to have the highest crude protein content than other earthworm species (Tiroesele and Moreki 2012). Eisenia fetida has 66.8% of crude protein while Eudrilus eugenia (E. eugenia) has 58.38% and Perionyx excavates (P. excavates) has 61.68%. This differs with the study of Sogbesan and Ugwamba (2008) who found that the crude protein for Hyalophora euryalus (H. euryaulis) is lower than 69.8% for P. excavates (Guerrero 1983) and 67.68% for E. fetida (Reinecke and Alberts 1987) but higher than 56.4% and 61.8 for E. fetida reported by Tacon (1994). This variation of protein content may be attributed to the different mediums used to grow earthworms.

Table 1 Crude protein of Eisenia fetida with different treatments
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Amino acid content of Eisenia fetida

Eisenia fetida has been found to have high amino acid values as compared to other earthworm species (Tiroesele and Moreki 2012). It is better quality in all quantities of the amino acid as shown in Table 2. Earthworm protein is high in essential amino acids compared to other common feeds (Zhenjun et al. 1997). Eisenia fetida contains 20 out of 24 major amino acids, including the ten essential amino acids (Albarran 1996). Segovia (1996) reported that the content of amino acid may be practically 6% of the worm’s dry weight hence; E. fetida is one of the best-known sources of amino acids. Eisenia fetida is rich in lysine which is limiting in many feed stuff and methionine and isoleucine (Albarran 1996; Anitha and Jayraaj 2012). Moreover, it has been also reported by Gabriel et al. (2010) that earthworms have an amino acid composition which is very similar to that of fishmeal and potentially superior to meat meal and contains essential amino acids as phenylalanine, leucine, lysine, methionine and valine (Gabriel et al. 2010).

Table 2 Amino acid profile of earthworm Eisenia fetida
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Fatty acid profile of Eisenia fetida

Eisenia fetida contains appropriate levels of desirable fatty acids and a high amount of omega 3 that distinguish it from other non-conventional feeds (Fadaee 2012). The fat content of worm meal has been reported to range from 5–20% of dry matter (Edward 1988). A number of mono and polyunsaturated fatty acids are in fairly high concentration in worm meal (Table 3). These fats are of special interest of nutrition benefits to poultry feed.

Table 3 Fatty acid profile of freeze-dried and oven-dried Eisenia fetida Gunya et al. (2016)
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Minerals and vitamins of Eisenia fetida

Eisenia fetida contains an adequate mineral content as shown in Table 4, and an excellent range of vitamins which are a valuable component of poultry feed (Vielma et al. 2001). Essential elements such as Copper (Cu), Manganese (Mn) and Zinc (Zn) are about one to six times higher in earthworm meal than in soybean and fishmeal (Zhenjun et al. 1997). Furthermore, Zhenjun et al. (1997) have reported that the iron content of earthworm fluid is ten times than that of soybean and fishmeal. This feature of earthworm fluid could be exploited to produce special iron (Fe) supplementation for poultry feed production (Zhenjun et al. 1997). Earthworm body is rich in vitamin A and vitamin B compounds 0.1 mg vitamin A, 0.25 mg vitamin B1 and 2.3 mg vitamin B2 per 100 g. It can be concluded that the earthworm E. fetida can be used for mineral and vitamin supplementation in addition to protein supplementation, in poultry feed.

Table 4 Mineral composition of Eisenia fetida
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Eisenia fetida as a source of feed for chickens

Eisenia fetida are natural feed for chickens. They can be used as an alternative non-conventional protein source (Bou-Maroun et al. 2013) due to their palatability to chickens (Tiroesele and Moreki 2012). They can be produced and harvested with ease, and they can be produced by simple methods from many kinds of organic material (Tuan and Focken 2009). Several studies have reported that E. fetida are very nutritious for poultry (Barcelo 1988; Reinecke and Viljoen 1991; Istiqomah et al. 2009; Tiroesele and Moreki 2012; Gunya et al. 2016). It is one of the substitutes that can be used instead of fishmeal and soybean because they have a protein content of 64–76% which is greater than the one for fishmeal (45%) and meat meal (51%) (Resnawati 2004). Moreover, it has been reported that the protein content of earthworm meal is close to that of Peru fishmeal and higher than that of Chinese fish meal, hen egg and soybean meal (Dedeke et al. 2013).

The use of E. fetida as a sustainable protein-rich feed ingredient in poultry diet is precisely feasible. They can be reared on low-grade bio-waste and can turn this bio-waste into high-quality protein (Parolin et al. 2020). In addition using earthworm meal as a source of protein for livestock especially for chickens is that they have an excellent chemical composition (Reinbeck et al. 1991), including essential amino acids, especially lysine which is not found in other feed stuff (Anitha and Jayraaj 2012; Tiroesele and Moreki 2012). It has been found that earthworms contain a large amount of protein (64.5—72.9%), essential amino acids (4.95–5.70 g/100 g) (Dedeke et al. 2010) total fatty acids (6.6 to 10.5 mg/g), calcium (1020–7070 μg/g) and iron (1050–2990 μg/g) for chickens. This was also supported by Korstecka and Pączka (2006) and Sogbesan and Ugwumba (2008) who reported that E. fetida is an excellent source of protein, rich in essential amino acids and vitamins. Moreover, they can be used as a substitute for fish meal and soya bean meal, due to their high protein content which ranges between 64–76% (Prayogi 2011). The dietary use of worms has already been analysed for poultry because they are already part of their natural diet. According to Reinecke et al. (1991), E. fetida can be harvested, dried and utilised as a protein source for poultry. There is a contradiction in results found by some researchers regarding earthworm use as poultry feed. Reinecke et al. (1991) found it to be a satisfactory source of protein for growing broilers whereas Koh et al. (1984) reported decreased performance. This difference may be due to the different inclusion levels of earthworm meal used as a protein supplement. The earthworm E. fetida has high-quality protein content along with antimicrobial and antioxidant that could be used as a feed supplement in broiler diet (Rezaeipour et al. 2014). Moreover, it has been reported that it has no anti-nutrient factor which declines performance of broilers (Reinecke et al. 1991). Furthermore, it has been found that growth performance of broilers fed diets containing earthworm meal is equal to that fed fishmeal (Rezaipour et al. 2014). This is in agreement with the observation by Boushy et al. (2000) who found that birds fed on earthworm meal as the major source of protein in the diets have all grown at rates equal to or better than those fed conventional protein meal. Resnawatti (2004) observed that earthworm E. fetida meal in feed up to 5% level has no significant effect on broiler body weight. Dried worm meal included up to 10% in broiler starter diet based on sorghum and soybean meal could be used without negative effects on feed consumption, weight gain and feed efficiency (Ramos-Elonduy et al. 2002). The improvement of body weight of broilers fed with earthworm meal may be attributed to the antibacterial characteristics of earthworm meal (Gunya et al. 2019; Julendra et al. 2012). According to Valembois et al. (1982), the coelomic fluid and the cocoon albumen of the earthworm Eisenia fetida andrei are demonstrated to possess an antibacterial activity. The antibacterial activity and the already known hemolytic activity are due, to the same lipoproteic molecules. The antibacterial activity (bacteriostatic effect) is only directed against the highly pathogenic soil bacteria.

Limitations of Eisenia fetida as poultry diet

Despite their importance, it has been reported that earthworms have limitations as poultry feed. Above 5% worm meal in diets, some researchers have reported a reduction of feed consumption to chickens (Yaqub 1997). Earthworms are the main intermediate of the internal parasite in free range chickens (LeeMaster 2007). Chickens may pick up parasites directly by ingesting earthworms which carry the eggs of internal parasites specifically roundworms and cecal worm nevertheless, processing of works like drying can limit the intake of the parasite. Internal parasites have a negative impact to chickens that can result in poor growth rate and feed efficiency, decrease egg production and even death in severe infections (Gabanakgosi et al. 2012). Earthworm production is economically feasible with high technology rearing methods (Edward and Arancon 2010). However, current methods of harvesting earthworms from organic waste are labour-intensive. This has been regarded as the greatest barrier to the successful commercial production of earthworm protein. Hence, earthworm as a source of protein has not been adopted commercially in developing countries (Edward and Arancon 2010). The earthworm meal is produced at an economical price, and additionally, the value of vermicompost produced can also be taken into account as complimentary income (Edward and Arancon 1994). Therefore, there is a need to come up with most efficient earthworm harvesting methods for the reason that its economic value is extremely valuable as feed for poultry as fishmeal because of its amino acids, fatty acids, minerals and vitamins content (Edward and Arancon 1994).

Conclusion

In conclusion, understanding the description, feeding, growth and reproduction is vital for production of earthworms which can then be used as animal feed. The advantage of utilising E. fetida as chicken feed are that they grow very rapidly, low inputs are required, and they convert organic matter diet into high-quality protein feed. Protein is an important nutrient in poultry diets that cannot be comprised. Earthworm E. fetida had demonstrated a potential and equal protein substitute which can be used as a protein source for poultry diets. In addition, E. fetida has a potential to be used as a protein source to poultry. It has a crude protein content that ranges between 60–70%, which is more than of fish and meat meal currently used in the poultry industry. Besides its good protein, it is better in quality in all amino acids and lysine which is limiting in many feed stuffs. Eisenia fetida contain vitamins and minerals, hence it can also be used as mineral and vitamin supplement. Furthermore, this study provide awareness about benefits of earthworm as a feed source for poultry and its use could play an important role in the sustainable of poultry production.