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Earthworm meal

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Description
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Common names 

Earthworm, common earthworm, lob worm, worms, nightcrawler (USA), dew worm, grandaddy earthworm (Canada), redworm, brandling worm, panfish worm, trout worm, tiger worm, red wiggler worm [English]; ver de terre, lombric, ver de terre commun, ver de fumier [French]; regenworm [Dutch]; Regenwurm; Kompostwurm, Mistwurm, Stinkwurm [German]; verme rosso californiano [Italian]; dżdżownica; kompostowiec różowy [Polish]; minhoca [Portuguese]; Навозный червь [Russian]; lombriz de tierra, lombriz de tierra comun; lombriz roja [Spanish];الخرطون; دودة حمراء[Arabic]; איסניה פטידה[Hebrew]; 蚯蚓 [Chinese];シマミミズ [Japanese]; ஐசீனியா பெட்டிடா [Tamil]; کرم ایزینیا فتیدا [Farsi]

Related feed(s) 
Description 

Earthworm meal consists in processed worms reared for vermicomposting, a method of composting that consists in the conversion of fruit and vegetable wastes, animal dung, methanizer residues or sewage into organic soil amendments for agriculture and horticulture, which are produced by the worms and deposited on the surface as wormcast (castings). The protein-rich earthworms are a byproduct of vermicomposting. They can be used in farm animal feeding, especially poultry, pigs and aquaculture species. Rearing earthworms could be a way to reduce wastes and feed/food competition. It could be easier to grow earthworms than insects from an economic and energy point of view as the many earthworm species are adapted to broader temperature ranges than insects (Tedesco et al., 2019).

Species

There are about 4000 species of earthworms. A handful of species has been used for vermicomposting as they display suitable characteristics like tolerance of a wide range of environmental and management conditions, short life-cycles, high reproductive rates, and good composting rate. Eisenia andrei, Eisenia fetida (also spelled Eisenia foetida), Dendrobaena veneta, Perionyx excavatus and Eudrilus eugeniae are the only extensively used species for vermicomposting. Among those 5 species Eisenia andrei and Eisenia fetida are quite similar (red striped worms) and often confused. In the wild, they can be found together but in vermicomposting installations it is advised to separate the two species as being mixed reduces their viability (Dominguez et al., 2011).

Morphology and life cycle

Earthworms are segmented, bilaterally symmetrical invertebrates, displaying indeterminate growth after sexual maturity and reaching up to 30 cm in length. Earthworms have a digestive tract with a mouth, a crop and a gizzard, intestine and anus. The circulatory system consists in blood vessels and several pairs of hearts (5 in Lombricids). Earthworms have no lungs and respiratory exchanges are done through the skin. Earthworms are hermaphroditic: they reproduce by copulation between two individuals at the level of an external gland – the clitellum – producing the cocoon where the eggs are laid. The cocoons are tiny and lemon-shaped, usually deposited near ground surface, and deeper when dry conditions occur. The period of incubation before hatching is variable, depending upon species and environmental conditions. Recently hatched earthworm are unpigmented but they need only a few days to get their adult colour. Under favourable conditions, they reach maturity in several weeks. The clitellum is an indicator of maturity (Dominguez et al., 2011).

Uses

Earthworms have been used for a long time. They have been eaten by early humans and used a baits for fishing and hunting. Native Americans, Aborigenes in Australia and Maori in New-Zealand ate earthworms. Native Americans dried/smoked and stored earthworms for winter use after they had been put in water or fed on special feed in order to offload gut dirt and become tastier (Deane, 2020). Earthworms were known for their ethnomedicinal properties in China and cited in the Divine Farmer’s Materia Medica Classic around 200 B.C-200 A.D (Yu Shen, 2010). In early populations, earthworm were also already used as baits for fishing and hunting. By the 18th century, earthworms were referred to as a feedstock for domestic animals and Charles Darwin was the first to document their importance for the breakdown of organic matter. The industrial production of earthworms as fishing baits started in the 20th century in the United States, notably in California. The use of earthworms as vermicomposters began in the late 1930s, but this activity did not develop as these businesses were pyramid schemes. A renewed interest arose in the 1970s in Germany, the United States and in the United Kindgom. Today, the main use of earthworms is to produce vermicompost and to provide protein for farm animals and fish. One of the advantages of vermicomposting is that the process does not produce off-odours, unlike other composting processes. Earthworms are able to decompose several classes of wastes coming from human, animal or industrial activity (Edwards, 2011). Earthworms are edible and can be boiled, fried, roasted, sauteed, put in meatloaf and used in culinary specialties over the world (Deane, 2020).

Distribution 

Earthworms are cosmopolitan animals, but some families are endemic to some regions. The Lumbricidae family includes most of the European, North American and West Asian genera like Eisenia, Lumbricus, Dendrodrilus, Dendrobaena. In Africa, the Eudrilidae are present in West Africa and the Microchaetidae, in South Africa. In Australia and eastern Asia, the Megascolecidae family is mainly present while the Glossoscolecidae are native to Central and South America. Apart from their geographical localisation, earthworms are divided into 3 ecological categories:

  • Epigeic earthworms that live above the ground. They are litter dwellers and litter transformers. They feed on coarse particulate organic matter, and excrete castings that are mainly organic matter.
  • Endogeic earthworms live in horizontal burrows in the top soil layers and consume soil matter. They excrete organomineral faeces.
  • Anecic earthworms live in deep vertical burrows and consume litter matter that they drag into their burrows.

Depending on the place where vermicomposting is done, different earthworm species can be used because their optimal growth rate varies with temperature.

Temperate regions

Eisenia fetida, Eisenia andrei, Dendrodrilus rubidus, Dandrobaena veneta, Lombricus rubellus and Drawida nepalensis are paleoartic species and they are the most suited to the range of temperature found in temperate regions.

  • Eisenia species are used for vermicomposting. They have optimal growth rate at 25°C and at 85% moisture. Under such conditions, they can reproduce after only 45-51 days, the hatchability of the cocoons is 72-82% and the time for young Eisenia earthworms to reach sexual maturity is between 21 and 30 days. They can live 4.5 to 5 years in controlled conditions, but their lifespan is much shorter in the wild (Dominguez et al., 2011).
  • Lombricus rubellus survives cold conditions, it lives in the soil layer and is also referred to as a possible species for vermicomposting. It is often replaced by Eisenia in commercial products.
  • Dandrobaena veneta is a large earthworm that is not very prolific (low hatching viability and low young earthworms/cocoon) but that grows quickly and produces heavy individuals (0.92 g vs 0.55 g for Eisenia spp.), a suitable trait for protein production in vermicomposting facilities (Dominguez et al., 2011).

Tropical and subtropical regions

Species like Eudrilus eugeniae and Perionyx excavatus are used for vermicomposting in tropical and subtropical regions.

  • Eudrilus eugeniae is a large epigeic earthworm native to Africa that is also extensively used as fishing bait in North America. It has poor tolerance of temperature changes and its optimal growth rate is between 25-30°C with 80-82% moisture. Eudrilus eugeniae cannot be reared outdoors outside from tropical and subtropical areas, Despite its poor handling tolerance, it is a valuable and prolific species whose individuals can live up to 3 years.
  • Perionyx excavatus is found in tropical South-East Asia and was introduced to Europe and North America. Though it does not grow during winter, it has a valuable resistance to higher temperatures and it keeps growing on a broader range of temperature, from 4°C to more than 30°C (Dominguez et al., 2011).
  • Hyperiodrilus euryaulos has been referred to as a prolific fast growing earthworm in the semi-arid zone of Nigeria (providing 200 earthworms from one egg in 3 weeks) (Sogbesan et al., 2007).
Processes 

Vermicomposting requirements

Earthworms can be raised on a broad range of systems: in beds, boxes, pits, cement troughs, and windrows. Their requirements are minimal but important:

Litter

Earthworms need a stable, well-aerated and moist litter (>50% moisture) with a favorable C:N ratio. The litter should not decompose too quickly and should not heat as it can be deleterious to earthworms. The litter can be made of different materials : horse dung, cow dung, pig manure, poutlry litter or peat moss, compost, maize silage, maize stover, chopped bark, wheat straw, oat straw, hay, papers, paper pulp, sludge, cardboard, corrugated cardboard, etc. The litter should be relatively shallow so that earthworms can colonize all their habitat.

Feed sources

Earthworms are voracious and able to consume 50 to 100% of their body weight in one day. They can ingest a broad variety of feeds but they are particularly fond of already degraded organic matter, notably cattle and rabbit dung. Pig manure is readily consumed when dried. Poultry litter is less appreciated due to its high temperature and high protein content, which can be deleterious to earthworms (GEORG, 2004 cited by Munroe, 2008; Gaddie et al., 1975). Other suitable feed include kitchen wastes (when not too rich in nitrogen and fat), precomposted food wastes, sewage biosolids (earthworms are reported to destroy toxic substances), legumes haulms, grains, algae (when thoroughly rinsed to limit salt content), chopped corrugated cardboard etc. Feeds should be distributed regularly and in amounts small enough to prevent fermentation and a rise in temperature that may kill the worms. Quickly composting the wastes before vermicomposting can help to obtain optimal temperature, moisture, ammonia and salt content (El Boushy et al., 2000).

Density and yield

Initial earthworm density should be in the 2.5–5 kg/m² range to ensure an optimal reproduction rate. The earthworm population under favorable conditions may double within 30-60 days. An earthworm facility sown with 10 kg of earthworms can yield 20 kg after 30 days, 40 kg after 60 days and,more than 40 tons in 12-24 months. Yields of 1 kg fresh earthworm per 2 kg calf manure (DM) were reported and it was suggested that a herd of 100 cows producing 3 t manure/day would yield 42 kg earthworm protein/day and 15 t/year (Fosgate et al., 1972).

Vermicomposting systems

Various vermicomposting techniques are used. Most of them consist in making shallow bed layers or windrows of variable width and of limited height (50-90 cm, never more than 1 m) with animal or crop wastes that can range from almost-liquid slurries to straw-based mixtures or relatively dry poultry litter. For efficient vermicomposting, the bed layers moisture and temperature should be monitored and kept to 80-90% moisture and between 15 and 25°C, the latter being reported to be optimal .

Earthworms are seeded after a prior period of composting. As the earthworms are growing, the wastes are added in thin layers of substrate to prevent heating, the overall system should be shaded and constant moisture should be kept by watering and drainage. It requires one month for the vermicompost to get ready. The earthworms can then be harvested (GEORG, 2004 cited by Munroe, 2008; Dominguez et al., 2011; Edwards et al., 2011; Misra et al., 2003; El Boushy et al., 2000).

Here are some examples of vermicomposting systems:

  • In the Philippines, earthworms were grown in pits (3 m x 4 m x 1 m depth) drained with bamboo poles to prevent earthworms from being waterlogged. The bed layer was filled with organic residues (straw, crop residues, green weeds, leaves or animal manure) and left for a week to precompost. Earthworms were added and started to burrow. The pits were covered to prevent sunshine and to keep the substrate with adequate moisture. After 2 months, the pits could be partially (66-75%) emptied and the worms were removed by hand or sieving. The yield was 10 kg castings per 1 kg of earthworms. The earthworms were used in new pits, sold for the same purpose sold or as livestock feed, fish feed, or human food (Misra et al., 2003).
  • In Cuba, vermicomposting was done in cement troughs. Bed layers were made of 7.5-10 cm layers of one-week old manure. The worms were added and a new layer of manure was added every 10 days to provide new feed. After 2 months, the worms were separated from the compost (Misra et al., 2003).
  • In Canada, vermicomposting was done in static outdoor windrows. The litter was made of cardboard and the feeds were poultry and bovine manure. Earthworms were seeded in August and they spent all winter in the windrows under 1 m snow. By next summer the population had been multiplied by 5. The vermicompost was of high quality. Protein rich feeds maintained heat in the windrows during the canadian winters. After harvest, new windrows were set along the old ones so that the earthworms could migrate to the new litter (Munroe, 2008).
  • Continuous systems have been developped in Australia. Earthworms are placed in raised containers, about 3 m wide. The feed (biosolids) is sprayed above the worms without disturbing them. The small particles of vermicompost fall through the screen at the bottom of the container. Such systems could process 2-3 t of wastes per day (Bogdanov, 1996).

Earthworm harvest

Eartworms can be harvested using different methods. The many difficulty is that the worms are embedded in the vermicompost, a moist and sticky. The worms must be separated from the castings when they are intended as bait or feed, which can be done manually, by migration, or mechanically (Bogdanov, 1996).

Manual harvesting

Manual harvesting is a time-consuming activity that can be done in smallholder units. The compost is laid on the ground in a relatively thin layer and the earthworms burrow to flee the light. The upper layer is removed repeatedly until the worms can be harvested in the lowest layer where most animals can be found (Misra et al., 2003).

Migration and screening

There are several harvesting methods based on combining migration and screening. Three of them are reported below.

  • The vertical top-down migration system can be achieved when vermicomposting has been carried out in continuous vertical systems with a wire mesh bottom. The container is lit from above and earthworms, fleeing the light, are collected at the bottom (Munroe, 2008).
  • The vertical bottom-up migration system consists in placing the grid and attractive feed materials (peat moss + coffe pomace or fresh bovine dung) above the earthworm layer. This technique can be done with boxes or with onions bags (bags with wide mesh), as done in Cuba. The earthworms are climbing to the fresh feed and can be collected (Cracas, 2000). One constraint of the technique is that some feed remains with the worms that do not come as clean as they are with other techniques. This can be alleviated by removing most of the excess feed after the harvest (Munroe, 2008)
  • The push-pull method developed in India consists in pushing the earthworms out of the vermicompost of coconut leaves with the help of a repellent (mustard) and to subsequently pull them thanks to an attractant (cow dung). The method was found to be effective and able to save manpower (Gopal et al., 2019).
  • The horizontal screening technique consists in attracting earthworms to a pre-weighed substrate, such as peat moss, and forcing them through a screen. Once they have passed through the screen, the worm-free compost is removed and another batch of vermicompost replaces it. The operation is repeated until the weight of the receiving substrate reaches the required weight (corresponding to the desired weight of worms + the weight of the substrate at the start) (Munroe, 2008).
Mechanical harvesting

Mechanical harvesting is efficient. It is done with inclined rotary drum screens 2.5-3 m long x 30-60 cm in diameter. The screen is metallic with variable grid size. The drum is electrically powered. The vermicompost is fed by the high extremity of the drum. As the drum rotates, castings pass through the screen and earthworms are collected at the bottom (Bogdanov, 1996).

Preparting earthworms for animal feeding

Washing and blanching

The earthworms should be washed thoroughly and left in water for a duration ranging from 30 min to 8 h, so that they evacuate the residual wastes from their guts. They can later be blanched in boiling water.

Dry feed

Earthworm meal is made by drying (natural or artificial) and then grinding the worms. In smallholders units, earthworms are dried by laying them out in the sun or by using an artificially drying system, sometimes without prior washing or blanching. The ash content of the final meal is directly correlated to the amount of soil contamination. Heating the worms at 120°C for one hour was found to reduce bacterial count and to improve growth in rats (Velazquez et al., 1986). In Nigeria, the earthworms were thoroughly rinsed in water and kept in a bowl for 30 min to let them evacuate residual undigested contents. The worms were then blanched in hot water and oven-dried at 80°C for 3 h. After drying, the worms were milled with hammer milling machine into a powder, packed as dried earthworm meal in airtight plastic bowls and stored at 0-20°C for further use (Sogbesan et al., 2007).

Other drying methods include immersion in acetone (1 hour) followed by air- or oven drying (95°C), and freeze-drying. A comparison of drying methods found that they resulted in slightly different dry matter yields (g of dried product per 100 g of fresh worms):15.2% (hot air), 11.6% (oven), 13.5% (freeze-drying), 12.8% (acetone) (Edwards, 1985).

Wet feed

Earthworms can be ensiled with formic acid or mixed with molasses or with molasses and sorghum (El Boushy et al., 2000; Ortega Cerrilla et al., 1996).

Environmental impact 

Earthworms in the wild

In terms of biomass and overall activity, earthworms dominate the world of soil invertebrates, including arthropods. They play a major role in the soil structure as they induce soil movement, nutrient flow, water movement, and plant growth. While not essential to soil health, they are a proven indicatorsf healthy soils (Labenz, 2014).

Waste reduction and soil amendment

Earthworms are waste managers as they break down organic materials. They are not only composting these materials, but they also provide good quality and sanitized soil amendment (vermicompost) and supplemental protein source (the earthworms) to feed farm animals and aquaculture species (Edwards et al., 2011; Sinha et al., 2010; Eastmann et al., 2001; Eastmann, 1999). Vermicomposting with the help of earthworms in a viable method for turning organic wastes into a viable supplemental protein source, while enhancing soil characteristics. Thanks to waste digestion by earthworms, the vermicompost is free of pathogens and as safe as conventional compost without the need of high temperature (Sinha et al., 2010; Eastmann et al., 2001; Eastmann, 1999).

Nutrient leaching prevention

Thanks to its high humic matter and physical structure, vermicompost has a high water capacity retention and prevents nutrients from being lixiviated with water in the soil (Munroe, 2008).

Pasture fertility enhancement and soil sanitization

Earthworms used for vermicomposting are epigeic species. They do not survive for long in the soil as it is not loose enough to be colonized. The cocoons contained in the vermicompost are quite resistant to soil conditions and can survive and develop in pasture stands provided they receive fresh faeces from grazing livestock. They are able to transform animal faeces into valuable castings and enhance the fertility status of the stand . It has been reported that the earthworms that develop from the cocoons are able to destroy the pathogens that could be brought in the faeces, which has a sanitization effect on the soil and on the water that passes through the soil (Appelhof, 2003 cited by Munroe, 2008).

Nutritional aspects
Nutritional attributes 

Earthworms have a high protein content and are mainly used as a source of protein in monogastric animals diets. The composition of earthworms is highly variable and depends on the species, substrate and process.

The protein content of earthworms ranges from about 30% to more than 70% DM. Lumbricus terrestris was found to contain about 33% DM of protein vs 57% for Perionyx excavatus (Vodounnou et al., 2016). Protein content was higher for worms raised on pig manure than for those raised on sheep manure (51% vs 43% DM) (Vodounnou et al., 2016). Their amino acid content is particularly valuable for animal feeding and they provide lysine, methionine+cystine, phenylalanine and tyrosine in good amounts. Its essential amino acids profile (lysine and methionine) can be better that that of meat or fish meal (Edwards, 1985). In rats, it was reported that earthworm meal had slightly lower protein efficiency than soybean meal. The process undergone by the earthworms could alter the amino acid profile and the essential amino acid index. High (105°C vs 40°C) drying temperatures decreased protein efficiency (Koreleski et al., 1994).

Ash content can be extremely variable, with values ranging from about 4% to more than 40% DM, as it depends on amount of residual soil present on the worms after the harvest. It also depends on substrate: mineral content was 21% DM for earthworms grown on poultry manure and 13.5% for those grown on pig manure (Vodounnou et al., 2016). Some earthworms have been found to be rich in iron (Zhenjun et al., 1997). It should be noted that a high mineral content will affect negatively the energy content.

Earthworms contain variable amounts of fat (4-19% DM) with valuable long chain fatty acids. They contain vitamins, notably niacin and vitamin B12 (Edwards et al., 2011).

Potential constraints 

Heavy metals and contaminants

Vermicomposting facilities often receive sewage from both domestic and industrial sources that might be contaminated by medicines and heavy metals. These contaminants may be detrimental to earthworm growth, survival and reproduction. Earthworms are able to accumulate a number of metals in their body (Morgan, 2011). However, earthworms do not act like plant accumulators. It was shown that Zn and Cu uptake was counter-balanced by excretion while Cd and Pb had low excretion and could thus accumulate more easily (Spurgeon et al., 1999). It has been hypothezised that heavy metal accumulation in earthworms depends on bioavailable heavy metals in the substrate. It was suggested to lower heavy metal bioavailability through pH modification or additives (Li et al., 2010).

Feed safety

Rats fed on 10% earthworm meal showed no signs of morbidity, mortality, or deteriorated health parameters. No effects were observed on their reproduction or lactation. Only their gonads were found to be heavier. It was concluded that earthworm meal could be safely used in animal feeding (Ibanez et al., 1993).

Coelomic fluid of Eisenia fetida

The coelomic fluid of earthworms moistens their skin and allows them to move in the ground. In Eisenia fetida, the foul-smelling yellow coelomic fluid is excreted when the worms are stressed, and it plays a role of deterrent for predators (Musyoka et al., 2019). The coelomic fluid of Eisenia fetida was found to be safe for 42 species of invertebrates (larvae and aquatic adults) but it was toxic to vertebrates, including fish (11 species), toad tadpoles (Bufo japonicus formosus), reptiles (lizard Japanula polygonata, soft shelled turtle Trionyx japonicus), birds (Japanese quail) and mammals (mouse and rat). The toxicity occurs at low levels (0.2-2%) and within 10 to 225 min depending on the species. This toxicity can be alleviated by heating the coelomic fluid, hence the necessity of blanching the earthworms (Kobayashi et al., 2001).

Pigs 

There have been few trials using earthworms in pig diets. It should be a safe and digestible protein source for pigs.

Digestibility

Earthworm meal was found to be very palatable and highly digestible for pigs, with digestibility coefficients of 80%, 92% and 72% for energy, protein and dry matter respectively, and a digestible energy of 12.8 MJ/kg DM. Earthworm meal was comparable to soybean meal in pig diets (Vieira et al., 2004).

As feed additive in piglets

Earthworm meal was used as a feed additive in weanling piglets diet at levels of 0.4% 0.8% and 1.6% in the feed. All levels had positive effects on growth rate and health. The lethality was reduced (Apsari et al., 2019).

Poultry 

Earthworms are commonly consumed by poultry in free-range rearing systems (Khan, 2018; Blair, 2008). They are sometimes harvested or produced at small scale and used in fresh form in family poultry production (Tiroesele et al., 2012). At larger scale, earthworm meal can be included in complete diets as dried meal.

The protein content of earthworm meal is high, and its amino acid profile is well adapted to poultry requirements. It is close to that of fish meal, with a high content in essential amino acids , such as lysine, threonine or methionine (Son, 2009; Blair, 2008; Sugimura et al., 1984). Digestibility is reported to be high (Rezaeipour et al., 2014).

Broilers

Several studies showed that earthworm meal can be used in broiler diets with success. Growth performance is generally maintained when earthworm meal is introduced in broiler diets, and it even increased in some cases (Gholami et al., 2016; Nalunga, 2019). Inclusion levels up to 6-10% were used with success in growers (Das et al., 1990; Loh et al., 2009, Sugimura et al., 1984). However, in some cases, the highest inclusion levels led to reduced growth (Gunya et al., 2019). Feed intake is sometimes reduced by earthworm meal inclusion, leading to an improvement in feed efficiency (Loh et al., 2009; Nalunga, 2019; Das et al., 1990). In other cases, feed intake can be increased (Gholami et al., 2016; Gunya et al., 2019). In younger animals some authors report a reduced growth with 4-8% earthworm meal in diets (Janković et al., 2015). Other studies used 1 to 5% earthworm meal with no negative effects on growth performance and feed efficiency (Bahadori et al., 2017; Mekada et al., 1979; Rezaeipour et al., 2014). Somes studies reported an improvement in growth performance with very low inclusion (0.2 to 0.4%) of earthworm meal, which could suggest a probiotic effect rather than a nutritional improvement (Son, 2009). Use of fresh earthworms led to lower performance than earthworm meal, but this could be due to different feed formulation (Jankovic et al., 2015). In slow growing chickens, growth performance were equivalent to a control diet when either fresh or dried earthworms were supplied (Taboga, 1980). No detrimental effect was observed on carcass yield and composition (Nalunga, 2019). Physico-chemical parameters of meat were not affected by earthworm meal (Gunya et al., 2019; Jankovic et al., 2015). Sensory characteristics of meat was not negatively affected by use of earthworm meal and some sensory parameters were even improved (Nalunga, 2019).

From the results above, earthworm meal can be considered as a suitable ingredient for broiler feeds which can be used up to 8 to 10% with adequate feed formulation. In younger animals the level should be limited to 5%.

Layers

Laying performance was maintained with the use of fresh earthworms in diet, at a level equivalent to 5% of diet DM. Egg quality was not degraded by the use of earthworms (Mekada et al., 1979). An experiment with 0.3 to 0.6% earthworm meal in layer diets improved rate of lay but decreased slightly egg weight. In this experiment with very low inclusion rates, no problems of contamination with heavy metals were recorded (Son, 2009). In growing pullets, use of 1 to 5% earthworm meal slightly improved growth and feed conversion. Heavy metals were higher in earthworm meal diets, and this increase was also recorded in pullet livers, but not in muscle, so that earthworm meal used is considered as safe (Zang et al., 2018).

Quails

Earthworm meal could succesfully replace fish meal in quail diets (Dioson, 1984). In meat quails, the use of 5 to 10% earthworm meal in substitution to fish meal allowed similar growth performance, lower feed intake and better feed efficiency, while a level of 15% earthworm meal led to decreased growth performance (Prayogi, 2011). In another experiment the use of 6% earthworm meal resulted in similar body weight, while dressing percentage was slightly improved. Chemical composition of meat was altered, with lower fat and higher protein content, which could be due to feed composition (Morón-Fuenmayor et al., 2008). In laying quails, earthworm meal was successfully used in replacement of fish meal (Silvestre, 1984). The use of very low earthworm meal levels slightly improved laying performance, probably due to a probiotic effect rather that nutrient content itself (Istiqomah et al., 2017).

Rabbits 

Rabbit manure makes a high quality compost that is often used as a substrate for earthworm production, either alone or mixed with plant by-products (Aubert et al., 1987; Schley et al., 1987; Mpoame et al., 1994; Samkol et al., 2008). Earthworms produced with this system may be used as protein source, for instance for poultry (Djossa et al., 2014). Earthworm are rich in proteins, have a well-balanced amino acid profile and are rich in vitamins and minerals. However, earthworms raised using rabbit manure should never be used to feed rabbits due to obvious health reasons, since there is a risk of recontaminations with pathogen agents.

Earthworms produced with non-rabbit substrate have been studied as raw material in rabbit feeding. The inclusion of earthworm meal at 3% in low cost growing rabbit feeds (about 10% of the total dietary proteins) resulted in good economical performance without health problem (Nieves et al., 2001). In a study conducted in Mexico, the introduction of earthworm meal in a growing rabbit diet (18% proteins) in order to represent 30% of the total dietary proteins, resulted in growth performance (growth rate, feed intake, feed conversion ratio) similar to that obtained with the control diet based on conventional protein sources. Apparent DM digestibility was 5% higher than the control diet (Orozco Almanza et al., 1988). Despite these interesting results, additional experiments on the use of earthworm meal in rabbit feeding would be welcome.

Minks 

Minks were given 1 kg earthworm meal/day in order to replace fish meal in their diet. After a week to get used to the new feed, feed intake was similar to what was observed with fish meal. Production performance (precocity of mould and quality of fur) was improved when compared to an equivalent amount of fish in the diet (Bao, 1983).

Fish 

Earthworms have a high protein content and a good amino acid profile close to that of fish meal and for those reason they have been regularly assessed to replace this costly protein source in fish feeds (Vodounnou et al., 2016; Nguyen et al., 2015; Pucher et al., 2014; Dedeke et al., 2013; Istiqomah et al., 2009; Nguyen et al., 2005). Earthworms contain prostaglandins which could have a role in fish and shell fish gonads maturation. Using earthworms products in their diet could improve growth, fecundity of broodstock, maturation and egg sizes (Ramu, 2001 cited by Sogbesan et al., 2007).

There may be differences in nutritive value and suitability depending on the earthworm species and on the fish species. Earthworm meal from Eisenia fetida has been tested in a broad range of fish diets from low level (10%) to high level (100% as a fish meal replacer). It has been generally shown to have positive effect on growth, reproduction, digestibility, stress, survival, feed conversion ratio, feed utilization and assimilation efficiency, but not on all tested fish species (Mohanta et al., 2016; Chaves et al., 2015; Sakthika et al., 2014; Knights, 1996; Ganesh et al., 2003; Stafford et al., 1985). Positive effects have been found to be more consistent with earthworm meal from Perionyx excavatus species (Nguyen et al., 2015; Chaves et al., 2015; Pucher et al., 2014).

Common carp (Cyprinus carpio)

In India, earthworm meal from Perionyx excavatus fed to common carps was found to be a satisfactory replacer for fish meal and no difference in overall quality of the edible portion was observed (Nandeesha et al., 1988). In Vietnam, a replacement trial included increasing levels (0%, 50% or 100%) of sun dried earthworm (Perionyx excavatus) meal in common carp diet. The fish grew better when fed on 50% or 100% in comparison to fish meal. It was suggested that large zooplankton could also benefit from earthworm meal and subsequently provide supplemental feed to the carps (Pucher et al., 2014). Perionyx excavatus resulted in similar or higher growth rate, protein efficiency and energy retention compared to fish meal (Nguyen et al., 2015). However, Perionyx excavatus meal should be thermally treated in order to reduce antinutritional factors that may depress growth (Pucher et al., 2014).

In Brazil, it was possible to replace commercial fish meal based diet of common carp postlarvae with a feed containing 33% earthworm meal and a blend of different fruits. The mixture had lower crude protein but higher fat content than the commercial diet. There was no difference in growth, weight gain and fish tissue between fish fed on both diets. It was suggested that the earthworm-based diet had a higher assimilation efficiency than the fish meal-based diet in postlarval carps, and it was reported to be economically and environmentally suitable (Chaves et al., 2015).

Nile tilapia (Oreochromis niloticus)

In Brazil, the trial described above for carps was done on Nile tilapia with the same positive results in terms of performance and economic and enviromental suitability (Chaves et al., 2015). However, in an earlier study in Egypt, earthworm meal used to replace fish meal in tilapia diets (25, 50, 75 and 100% substitution) depressed feed intake, growth, and feed conversion (Sayed, 1998). In the Philippines, processed earthworm meal from Perionyx excavatus and Eudrilus eugeniae was an efficient and cost-effective replacement for fish meal in the diets of the cage-cultured Nile tilapia (Guerrero, 2009). It was suggested that unprocessed earthworm biomass could replace "trash fish" in carnivorous fish diets in a cost-effective way (Cruz, 2006).

Rainbow trout (Onchorhynchus mykiss)

Results about the use of earthworm meal in rainbow trouts have been inconsistent. Some trials have been negative. In an early trial in Canada, final body weight was found to decrease linearly with increasing levels of freeze-dried earthworm meal (Eudrilus eugeniae) in the diet despite of a good protein digestibility. It was suggested that some unidentified essential compound was lacking in earthworm meal (Hilton, 1983). Similar results have been observed when frozen or freeze-dried Eisenia fetida worms were offered to trouts. Those products were totally unpalatable and yielded little or no growth when compared to the commercial fish diet (Tacon et al., 1983). This issue was confirmed when fingerling rainbow trouts were fed earthworm meal (Eisenia fetida), resulting decreased intake and nitrogen utilization. An inhibitory effect of some earthworm components on digestive enzyme activity was suspected (Cardenete et al., 1993).

Other trials have been more positive. In Scotland, up to 30% dried earthworm meal (Eisenia fetida) could replace herring meal in rainbow trout diets without any adverse effect on fish performance. There was an increase in body fat from 5 to 20% dietary inclusion (Stafford et al., 1985). In Italy, a 25-30% inclusion rate was determined to be the acceptability level or earthworm in rainbow trouts. Below this threshold, good productive performance could be achieved without affecting the quality of the final food products (Parolini et al., 2020). In Iran, no deleterious effect on blood parameters and overall health were found when rainbow trouts fingerlings were fed on earthworm meal (Eisenia fetida) replacing 25% fish meal (Razzaghi et al., 2018).

Frozen earthworm from Lumbricus terrestris and Allolobophora longa were reported to yield better or equal fish growth than commercial trout pellets (Tacon et al., 1983).

Siluriforms

Striped catfish (Pangasianodon hypophtalmus)

In Vietnam, a comparison of the digestibility in striped catfish fingerlings of different animal and plant protein sources found that earthworm meal (no species indicated) had the lowest apparent digestibility, which reducess its value as a replacer of fish meal in the feed (Da et al., 2013).

Bagrid catfish (Mystus montanus)

In India, earthworm meal (Eisenia fetida) made from worms grown on water hyacinth and fed in small amounts to Mystus montanus had positive effect on body weight gain, specific growth rate, feed conversion ratio and protein efficiency ratio (Sakthika et al., 2014).

African mud catfish (Clarias gariepinus)

In Nigeria, feeding African catfish fingerlings up to 70% earthworm meal (Alma millsoni) replacing fish meal was found to be suitable for optimal growth, nutrient utilization, and feed cost reduction (Monebi et al., 2015). Similar results were obtained when diets containing 50-70% earthworm meal (Eudrilus eugeniae) was fed to fingerlings of the mud catfish hybrid [male] Heterobranchus longifilis × [female] Clarias gariepinus) called Heteroclarias (Monebi et al., 2013).

Snakehead fish (Channa spp.)

Snakeheads of all stages from fry to adult could be fed on earthworms (De Silva, 1989).

Crustaceans 

Shrimps

White shrimp (Penaeus vannamei)

White shrimps relish live earthworms as shown in this video of shrimp culture in Vietnam:

 

In China, white shrimp (Penaeus vannamei) were fed a 4:1 mixture of earthworm meal (Eisenia fetida) and soybean meal fermented with Bacillus subtilis to increasing methionine content, as a potential total replacer of fish meal. Fermentation with Bacillus subtilis increased the palatability of the mixture and shrimp growth performance. Up to 80% fish meal could be replaced. The fermentation was effective as a health promotor of shrimps which kept healthy after being challenged with Vibrio alginolyticus (Chiu et al., 2016). Though it had been suggested that earthworm feeding could have a promoting effect on gonad development in white shrimp breeding parents as it is the case in fin fish and shell fish, this fact could not be confirmed experimental (Chen et al., 2011)

Chinese shrimp (Fenneropenaeus chinensis)

Earthworms could be satisfactorily fed to Chinese shrimps and promoted good growth and high survival rate due to disease resistance towards viruses or bacterial infections (that can be brought by clams or commercial feeds for example)(Zhang et al., 2009).

Prawns

Freshwater prawn (Macrobrachium malcolmsonii and Macrobrachium idella)

In India, freshwater and brackishwater prawn (Macrobrachium malcolmsonii) could be fed on soybean or live feeds like mussels or earthworm but also on a mixture of the 3 feeds (soybean, mussels and earthworms) over a period of 30 days. The best results for growth performance and feed efficiency were obtained on the blended diet (Thirumurugan et al., 1999). In the Philippines, earthworm meal (Perionyx excavatus and Eisenia eugeniae) has been found to be an efficient and cost-effective replacement for dried fish (Therapon plumbeus) in freshwater prawn Macrobrachium idella (Guerrero, 2009).

Red claw crayfish (Cherax quadricarinatus)

In Thailand, earthworm fragments (Eudrilus eugeniae) included in brood crayfish diet resulted in shortest incubation times and in highest number of free living juveniles. However, the juveniles were of the smallest size and earthworm meal was not recommended to feed crayfish (Kiriyakit et al., 2018).

Nutritional tables
Tables of chemical composition and nutritional value 

Avg: average or predicted value; SD: standard deviation; Min: minimum value; Max: maximum value; Nb: number of values (samples) used

Main analysis Unit Avg SD Min Max Nb  
Dry matter % as fed 90.2 4.2 77.1 95.2 20  
Crude protein % DM 57.9 8.8 32.5 71.3 46  
Crude fibre % DM 2.4 2 0.2 7.8 19  
Neutral detergent fibre % DM 14   7.7 20.9 4  
Acid detergent fibre % DM 5.4   0.6 12.7 3  
Ether extract % DM 9 4.2 0.9 18.5 42  
Ash % DM 14.9 11 3.7 45.7 38  
Starch (polarimetry) % DM 0       1  
Total sugars % DM 0.3       1  
Gross energy MJ/kg DM 20.2 3 16.1 24.4 6 *
               
Amino acids Unit Avg SD Min Max Nb  
Alanine g/16g N 5.4 1 3.7 6.8 10  
Arginine g/16g N 6.8 1.7 3.5 9.6 16  
Aspartic acid g/16g N 9.6 1.3 7.5 11.6 11  
Cystine g/16g N 1.1 0.4 0.7 2 10  
Glutamic acid g/16g N 12.8 1.5 9.7 15.3 12  
Glycine g/16g N 5.2 0.7 4 6.3 11  
Histidine g/16g N 2.6 0.5 1.4 3.4 17  
Isoleucine g/16g N 4.5 0.7 3.2 6.7 16  
Leucine g/16g N 7.8 1.5 5.4 10.7 17  
Lysine g/16g N 7 0.9 5.4 8.5 20  
Methionine g/16g N 1.8 0.4 1.1 2.7 19  
Methionine+cystine g/16g N 3   3.1 3.8 4 *
Phenylalanine g/16g N 3.9 0.7 3 5.1 16  
Phenylalanine+tyrosine g/16g N 7.2   6.7 8.8 4 *
Proline g/16g N 3.2 0.9 1.9 4.5 10  
Serine g/16g N 4.5 1.1 3 7.7 16  
Threonine g/16g N 4.1 0.8 2.3 5.5 18  
Tryptophan g/16g N 1 0.3 0.6 1.3 5  
Tyrosine g/16g N 3.3 0.5 2.7 4.1 14  
Valine g/16g N 5.1 1.1 3.5 8.1 16  
               
Fatty acids Unit Avg SD Min Max Nb  
Myristic acid C14:0 % fatty acids 2.8   2.1 3.8 4  
Palmitic acid C16:0 % fatty acids 8.7 4.3 5.1 14.8 5  
Palmitoleic acid C16:1 % fatty acids 6.2       1  
Stearic acid C18:0 % fatty acids 11.6 6.7 6.3 19.9 5  
Oleic acid C18:1 % fatty acids 14.2 3.8 10.6 19.2 5  
Linoleic acid C18:2 % fatty acids 7.2 2.1 4.8 10.2 5  
Linolenic acid C18:3 % fatty acids 2.9 3.1 0 6.6 5  
               
Minerals Unit Avg SD Min Max Nb  
Calcium g/kg DM 14.9 14.1 1.8 60.3 23  
Phosphorus g/kg DM 9.8 3.3 5 16.3 20  
Potassium g/kg DM 12.2 6.1 5.8 22 9  
Sodium g/kg DM 7.49 3.25 4.3 11 6  
Magnesium g/kg DM 2.2 1.2 0.6 4.7 12  
Sulfur g/kg DM 10.5       1  
Manganese mg/kg DM 97 86 8 269 11  
Zinc mg/kg DM 269 334 28 1300 12  
Copper mg/kg DM 125 246 8 812 12  
Iron mg/kg DM 548 531 6 1498 9  
Selenium mg/kg DM 2       1  
               
Pig nutritive values Unit Avg SD Min Max Nb  
Energy digestibility, growing pig % 93.4       1 *
DE growing pig MJ/kg DM 18.9         *
MEn growing pig MJ/kg DM 17.3         *
NE growing pig MJ/kg DM 10.9         *
Nitrogen digestibility, growing pig % 85       1  
               
Poultry nutritive values Unit Avg SD Min Max Nb  
AMEn cockerel MJ/kg DM 14.4         *
AMEn broiler MJ/kg DM 14         *
               
Rabbit nutritive values Unit Avg SD Min Max Nb  
DE rabbit MJ/kg DM 17.1         *
MEn rabbit MJ/kg DM 14.8         *
Energy digestibility, rabbit % 84.7         *
Nitrogen digestibility, rabbit % 79.8         *

The asterisk * indicates that the average value was obtained by an equation.

References

Babiker, 2012; Bahadori et al., 2017; Barker et al., 1998; Barrows et al., 2015; Chiu et al., 2015; Dedeke et al., 2013; Finke, 2002; Gonzalvo et al., 2001; Gunya et al., 2016; Gunya et al., 2019; Hilton, 1983; Ibanez et al., 1993; Istiqomah et al., 2009; Istiqomah et al., 2017; Janković et al., 2015; Koh et al., 1985; Mekada et al., 1979; Mohanta et al., 2016; Monebi et al., 2016; Nalunga, 2019; Nguyen et al., 2005; Nguyen et al., 2015; Ordaz-Lugo et al., 2015; Orozco Almanza et al., 1988; Ortega Cerrilla et al., 1996; Pucher et al., 2014; Reinecke et al., 1991; Schultz et al., 1977; Sogbesan et al., 2008; Son, 2009; Stafford et al., 1984; Sugimura et al., 1984; Sun et al., 1997; Tacon et al., 1983; Vieira et al., 2004

Last updated on 03/11/2020 23:24:25

References
References 
Datasheet citation 

Heuzé V., Tran G., Sauvant D., Bastianelli D., Lebas F., 2020. Earthworm meal. Feedipedia, a programme by INRAE, CIRAD, AFZ and FAO. https://www.feedipedia.org/node/665 Last updated on November 3, 2020, 23:27

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