R. Soc.Lond. B 310, 299-307 (1985) Phil. Trans.

Printed inGreat Britain

299

Production offeedprotein from animalwasteby earthworms

By C. A.
EDWARDS

Rothamsted Experimental Station, Harpenden, AL5 2JQ, U.K. Hertfordshire The 84 Mt of cattle waste, 9 Mt of pig waste and 4-5 Mt of poultrywaste produced annually in the U.K. create seriousdisposal problems. Research at Rothamsted since 1980 has shown that the earthwormEiseniafoetida and other species can break down these wastes rapidly under controlled conditions to provide valuable horticultural composts and high-grade protein suitable foranimal feed. The conversion of animal wastes into earthworm tissue is very efficient, a tonne ofsuitable animal wastes producing up to 100 kg of worms,equivalent on a dry-mass oftheorderof 10 %. Earthwormdrymatteris 60-70 % basis to a conversionefficiency proteinwith a highercontentof essentialamino acids, such as lysineand methionine, than eithermeat or fishmeal. The otherconstituents ofwormsare 6-11 % fat,5-21 % carbohydrate,2-3 % mineralsand a range of vitamins,of which niacin and vitamin B12are ofparticularvalue. Thus wormsare a valuable potentialsource ofanimal feed if theycan be produced economically. Machinery forharvestingworms,methodsof processingtheminto animal feedand successfulfeedingtrials with fishand chickens are described.
1. INTRODUCTION

The large amounts of organic wastes produced by intensiveanimal production in the United Kingdom, which include 84 Mt ofcattle waste, 9 Mt of pig waste and 4-5 Mt ofpoultrywaste, cause major problems in disposal and a considerable potential for pollution of waterways. Charles Darwin (i 88I) was the firstto emphasize the very important role that earthworms play in breaking down organic matter. The importance of earthwormsin processingorganic matter in compost heaps is well known but less familiaris the great abundance and value of earthwormsin the breakdown process in trickling sewage filters (Terry I95I). Work in recentyearsin the U.S.A. (Hartensteinetal. I979; Neuhauser etal. I979) has shown can be used to break down activated sewage sludgesto finely divided materials, thatearthworms and even more recentlyat Rothamsted that earthwormscan be used to break down animal, vegetable and industrialorganic wastes to usefulcomposts (Edwards I983). The first to suggestthat earthwormscontained sufficient proteinto be considered as animal it in but is the last ten years that fulleranalyses Lawrence & Millar food were only (I945), of the body tissuesof earthwormshave been available to support this conclusion and the first successfulanimal feedingtrial was by Sabine (I978). 2.
FOOD
VALUE OF WORMS

Since the initial work of Mclnroy (I 971), therehave been a number of analyses of the constituents of the tissuesof different species of earthworms(Schulz & Graff I977; Sabine I978; Yoshida & Hoshii 1978; Mekada et al. 1979; Taboga 1980; Graff 1982). The overall composition of earthworm tissues does not differgreatly from that of many vertebrate tissues (table 1). [ 153 ]

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300

C. A. EDWARDS

The essentialamino acid spectrumofearthwormtissuescompares well with thosefromother currentlyused sources (table 2). Clearly the mean amounts of essential amino acids recorded are very adequate fora good animal feed as recommended by F.A.O.-W.H.O., particularly phenylalanineand tyrosine, in termsoflysineand thecombinationsofmethionineand cysteine, all of which are importantcomponentsof animal feeds.In addition, earthwormtissuescontain a preponderance of long-chain fattyacids, many of which non-ruminant animals cannot synthesize,and an adequate mineral content (figure 1). They have an excellent range of vitamins and are rich in niacin which is a valuable component of animal feeds (table 3).
drymass percentage 0.8 0.2 0.4 0.6 ......................

(a) potassium phosphorus calcium magnesium

17

1.0

(b) essential(long chain) (shortchain) Enon-essential

FIGURE

drymass percentage 8 4 6 2 _

10

acids in earthworms. (b) fatty 1. (a) Mineralsin earthworms;

TABLE 1. COMPOSITION OF EARTHWORM TISSUE

water protein fat carbohydrate minerals grossenergy

78-88% 60-70% 6-11 % 5-21 % 2-3 %

(drymatter) (drymatter) (drymatter) (drymatter)

16-24 kJg-' (drymatter)

TABLE

2.

ESSENTIAL AMINO ACID CONTENT (GRAMS PER 100 g PROTEIN) OF EARTHWORM TISSUE

essential amino acid

W.H.O.-F.A.O. Schulze Yoshida requirements mean & Mekada & ofessential aminoacids Mclnroy Graff Sabine Hoshii et al. Taboga Graff Rotham- ofall sted analyses (I98O) (I982) (I978) 1957-65 1973 (I97I) (I978) (I979) (I977) 2.0 4.2 4.8 4.2 2.2 2.8 2.8 1.4 2.8 4.2
a

arginine cysteine histidine isoleucine leucine lysine methionine phenylalanine threonine tryptophan tyrosine valine

4.0 7.0 6.5

a
b

4.0 1.0 5.0

b

6.9 4.5 0.8 1.6 4.3 4.7 4.3 8.7 5.0 5.9 8.7 1.9 1.6 3.4 4.4 5.2 6.9 1.3 1.4 4.4 2.7 3.0 5.1 5.1 5.2 3.0 5.1 +cysteine. a 3. Total formethionine + tyrosine. phenylaniline b 6.0 Total for 6.1 1.8 2.2 4.6 8.1 6.6 1.5 4.0 5.3

6.1 1.4 2.3 4.7 8.2 7.5 1.8 3.5 4.7

4.2 2.3 1.6 2.6 4.8 4.3 2.2 2.3 3.0

7.3 1.8 3.8 5.3 6.2 7.3 2.0 5.1 6.0 2.1 4.6 4.4

6.1 1.4 2.3 4.7 8.2 7.5 1.8 3.5 4.7 3.0 5.2

6.5 0.7 3.0 4.1 8.3 6.5 2.8 4.0 5.6 0.7 3.5 4.7

6.0 1.5 2.6 4.3 7.2 6.8 2.0 3.8 5.2 1.4 3.2 4.7

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TABLE 3. VITAMIN

PROTEIN

FROM ANIMAL
PER KILOGRAM)

WASTE
OF EARTHWORM TISSUES

301

COMPOSITION

(MILLIGRAMS

niacin riboflavin (B2) pantothenic acid (B complex) thiamin (Bl) pyridoxine (B6) folicacid biotin(B complex)
vitamin B12

358 147 16 15 2 0.5 0.35

4

3. GROWTH

OF WORMS

IN ANIMAL

WASTES

The lifecycles of fourspecies of worms that grow and reproduce well in organic wastes have been investigated thoroughly at Rothamsted. These are Eisenia foetida (Savigny), Eudrilus veneta excavatus eugeniae (Kinberg), Perionyx (Gates) and Dendrobaena (Rosa). The growthpatterns of individual worms or whole populations followedsigmoid curves and the maximum protein productionper unit timehas been achieved by inoculatinglarge volumes of animal wastes with relativelysmall numbers of young worms. Dry-matterconversion ratios of waste to worms as high as 10 % forcattle and pig waste and 5 % forpoultrywastes have been achieved readily in the laboratory and would seem to be feasible ultimatelyon a fieldscale. These earthwormscan withstand many adverse environmentalfactorsand on the basis of our research we have defined theirenvironmentalrequirementswithinbroad limits (table 4).

TABLE

4.

NECESSARY

CONDITIONS

FOR GOOD

GROWTH

OF

EIsENIA FOETIDA IN ANIMAL WASTES

aerobicity less than0.5 mgkg-' ammoniacontent salt content lessthan0.5 % 15-20 'C temperature moisture content 80-90 % pH 5-9

4. METHODS

OF PRODUCTION

The natural habitat ofwormsthat break down organic matteris in heaps ofdecaying organic matter and compost heaps. These habitats follow a natural microbial decomposition process with a successionof micro-organisms and wide changes in temperature, with up to 70 ?C being attained quite commonly. In such habitats, worm colonization is limited by temperature, populations are localized and biomass productivityis low. To produce earthworms,as a must be controlledenvironmentally and potentiallycommercialsource ofprotein,such systems waste added periodicallyto enable earthwormsto colonize all of the organic matterand utilize in which theyfeed to the maximum. the micro-organisms Animal wastes range fromalmost liquid slurriesthroughstraw-based mixturesto relatively dry and finelydispersed mixturessuch as those produced by laying chickens over deep litter systems.These wastes must be brought to a suitable moisturecontent and temperatureand the ammonia and salt contentsreduced to acceptable levels by leaching, compostingor some other method, beforethe worms can be grown successfully.

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302

C. A. EDWARDS

Once these conditions are attained, worms may be grown by a varietyof methods such as in ground-based beds of different sizes, in batch systemsin boxes or crates or even in trickling filter systemssimilar to those used in sewage disposal. The choice of a systemdepends mainly on economic considerations, such as the cost ofaddition of wastes to breedingcontainers,worm harvestingand handling. It is outside the scope of the presentpaper to deal with the technologyof worm production in detail, but it has been found that the growthof worms in beds filledwith animal waste to a depth of about 50 cm in successive shallow layers at regular intervals by automatically operated gantries is easy to manage. In colder climates some form of insulated housing is necessary. Different formsof batch production in crates or boxes are useful in some circumstances and systems ofcontinuous processingof wastes with automatic addition and removal of wastes are being developed currently. The technology to maximize worm and compost production is an evolving one, but with the current engineering input holds considerable promise for development into highly productive non-laborious systems.The rapid rate of conversion of organic wastes growth and multiplication of earthworms, and -theefficient into earthwormtissue protein, means that systemscan be developed that use a minimum of labour or sophisticated technology. Moreover, earthworms seem to have few diseases, predators or parasites that mighthinder maximum protein production. The efficient productivityof earthwormprotein depends mainly upon detailed knowledge of the population dynamics of the appropriate species, and upon the engineeringof suitable production systemsthat involve small labour inputs. Considerable progresshas been made towards the achievement of both these aims in research at Rothamsted and the National InstituteforAgriculturalEngineering,Silsoe.

5.

HARVESTING

OF

EARTHWORMS

FROM

ANIMAL

WASTES

the animal As the individual earthwormsand earthwormpopulations grow, theyfragment wastes into finer and finer particles, producing eventually a peat-like material that has considerable potential in horticulture.A major problem is that worms grow best at relatively high moisture levels (80-90% moisture content) and it is not easy to separate worms mechanically fromthe finelydivided organic matter at such high moisturecontents. Machinery forseparating worms fromfullyworked organic materials has been developed at Rothamsted and the National InstituteforAgriculturalEngineering,Silsoe (Phillips I985) of thismachineryin termsofpercentage recoveryofwormsis very and patented. The efficiency high. The machine that has been developed will at present separate worms fromabout one tonne of waste per hour and this machine is being automated and scaled up to increase this throughput.Until this automation has been achieved and until a rapid rate of separation of wormsfromwaste is possible, the productionofproteinforanimal feedfromwormswill remain an uneconomic process. Fortunately,it seems quite likelythat thisaim will be achieved within the coming year.

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6.

PROTEIN
OF

FROM ANIMAL
WORMS FOR ANIMAL

WASTE
FEED

303

PROCESSING

The worms collected fromthe separating machinerymay have small particles of waste on theirbodies and are likelyto contain waste in theirguts. Hence, the first stage ofall the methods of processingtested is to wash the worms thoroughlyand leave them standing in water fora minimum of three hours, to completelyevacuate the residual waste in theirguts. Various methods of processingthe worms foranimal feed have been developed and tested. Two of the methods tested produced a paste product and the fourothers a dry worm meal; all of thesewere acceptable fordifferent uses and the ultimatechoice of a method of processing must depend upon (i) the type of feed required, (ii) the cost of production of the protein, (iii) minimal loss of dry matterand (iv) minimal loss of nutrientvalue. Pastes (i) The first method tested was to blanch the worms in boiling water forone minute and incorporate 30 % molasses togetherwith 0.3 % potassium sorbate to produce a paste. The a loweringof the water activityto about Aw 0.90 and the addition of potassium molasses effect sorbate reduces thisfurther to approximatelyAW 0.65. At thislevel, the growthof yeasts and moulds is inhibited,permitting indefinite storage of the product. (ii) Another wet method tested was to incorporate 3 % formicacid with the worms with thoroughhomogenization,then to allow it to ensile and eventuallyproduce a verystable paste or liquid product. Dry meals (i) In this method a dry protein meal was produced by blanching worms in boiling water forone minute, then air-dryingand grinding. and grinding (ii) A dry meal was produced by freezingworms quickly, then freeze-drying them. (iii) Another dry meal was produced by first killingworms by immersingthem in acetone forone hour and then air- and oven-dryingthem at 95 ?C beforegrinding. (iv) A fourthtype of dry meal was produced by killingworms,dryingthem in an oven at 95 ?C and grinding. All the methods tested gave a good product that could be used but there were variations in the dry-matter yield (grams ofdry product per 100 g fresh worms). Killing wormsin boiling water and thendryingthemin an oven resultedin thelowestdrymatterof 11.6 %. Freeze-drying produced a meal with 13.5% dry matter. Killing worms in acetone then drying them in air produced a dry matterof 14.5 %, but aftersubsequent oven dryingthisfellto 12.8 %. Killing and dryingthe worms in a hot-air oven gave the greatestdry-matter yield of 15.2 %. The effects of the different processingmethods on the amounts of essential amino acids are summarized in table 5. Most of the methodshad relativelylittleeffect on the amounts ofamino acids in the product although the lysine content was decreased slightly by ensiling with molasses, with the use of formicacid and by freeze-drying, compared with other methods. Clearly, a stable proteinfeedcan be produced by any of the methodsand the choice of method must depend on the use to which the protein is to be put.

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304
TABLE 5. AMOUNTS OF ESSENTIAL AFTER

C. A. EDWARDS
AMINO ACIDS DIFFERENT (GRAMS PER 100 g PROTEIN) IN WORM TISSUES

PROCESSING

METHODS

amino acid arginine cysteine histidine isoleucine leucine lysine methionine phenylalanine threonine tyrosine valine

molasses ensiling 6.5 0.3 2.8 4.2 7.3 5.4 1.6 3.0 4.8 2.0 5.1

formic acid ensiling 6.7 0.5 2.7 4.3 7.1 5.9 1.1 2.8 5.1 2.4 4.9

processing method freeze-dried acetone-dried heat-dried 6.4 0.5 2.7 4.0 6.9 5.7 1.2 3.1 8.5 4.0 4.7 7.0 0.3 2.5 4.3 7.5 6.1 1.2 3.2 5.1 2.8 5.0 3.8 0.5 2.3 4.4 8.3 6.2 1.1 3.1 5.5 2.8 5.5

blanchand heat-dried 4.1 0.4 2.3 4.3 8.5 6.5 0.9 3.6 5.6 3.0 4.6

7.

ANIMAL

FEEDING

TRIALS

The main outlets suggested forutilization of earthwormprotein have been in fish-farming and as protein supplementsin poultryand pig feeds. trials (a) Fish-feeding The first trialsinvolvingthe feedingof earthwormsto fishwere by Tacon etal. (i 983), who used worms produced at Rothamsted to feed trout.The growthof troutfed only on E.foetida, Allolobophora longa (Ude) and Lumbricus terrestris L. was compared with that of fishfed on a commercial ration. Fish fed with frozenA. longaand L. terrestris grew as well or better than fishfed on commercial troutpellets. Trout did not grow well on a whole diet of freeze-dried E. foetida,although they grew much betteron E. foetidathat had been 'blanched' in boiling water beforefreezing(Stafford& Tacon I985). Dried earthwormmeal derived fromE.foetida which had not been blanched could replace the fishmeal componentofformulatedtroutpellets at levels of inclusion between 5 and 30 % without affecting growth of trout. The conclusion that both as a reached was earthwormshave potential complete feed or protein supplement for trout or other fish. Hilton (I983) reported that trout did not grow well on another earthworm species, Eudrilus eugeniae,but there are some doubts about his experimental techniques, because other formsof protein supplement currentlyused commercially,such as blood meal, would have also been unsuccessfulif used in the same way that he used worm protein.Guerrero (i983) reportedthat Tilapia fishgrew betteron diets containingearthworm protein supplementsfromPerionyx excavatus (Perrier) than those with fishmeal supplements. trials (b) Chicken-feeding The first trials which assessed the growthof chickens on earthwormprotein were reported by Harwood (I976) and Sabine (I978). They compared the use ofworm meal with meat meal as a proteinsupplementforchickensand found no significant in growthon the two difference diets. Similar resultswere reported by Taboga (I980) and Mekada et al. (I979), who also reported that when worms were fed to older birds, egg production was maintained. Jin-you etal. (I 982 a) reportedthat chickensfed on earthwormsput on weight fasterthan those given other diets (including fishmeal), had more breast muscle and consumed less food.

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FEED

PROTEIN

FROM

ANIMAL

WASTE

305

These resultshave been confirmedby our collaborators at the Poultry Research Centre, Edinburgh and reported by Fisher (I985). In these experiments,chickens grew well, had a good mass gain per unit of food and an excellent nitrogenretentionwhen fed on diets with levels of worm meal from72-215 g kg-' (figure2).

500 *z400-

-.

300200 100 0 (b) 500 400 -.....

bFn

1 ...

7.20/

14.4%

2150/

300bIL

cn

200 1?t 100 01 0 14.4/ 7.2% levelofwormmeal

.. ....

21.5%

FIGURE2. Growth ofchickens on an earthworm protein diet. (a) Nitrogen retention; (b) massgain.

trials (c) Pig-feeding There have been only two trials reporting the growth of pigs on earthworm protein supplements.Harwood & Sabine (I978) and Sabine (I978) showed that in feedingtrialswith both starterand grower pigs, animals fed on an earthwormprotein supplement grew equally well and had similar feed conversion ratios to those grown on commercial rations.Jin-you et al. (i982b) reported that piglets grew better on earthworm protein supplements than on others,and that older pigs had accelerated weaning, earlier oestrusin sows, increased disease resistanceand a decreased incidence of white diarrhoea.

8.

ECONOMICS

OF PRODUCTION

OF EARTHWORM

PROTEIN

There have been studies of the economics of production of earthworm protein (Fieldson I985). The general conclusionswere that earthwormproductionhad the best prospectsofgood profitswhen done by larger farmerswith considerable amounts of animal wastes. The most importantcriterionis that the worm meal must be produced at an economic price, although the value ofthe compost must be taken into account. Currently, the only labour-intensivepart
22

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306

C. A. EDWARDS

of worm protein production is the harvestingprocess and this remains the main barrier to commercial production, but seems likelyto be resolved in the near future. In a computeranalysisofthe economic value ofearthwormmeal (table 6), based on itsamino acid, fattyacid, mineral and vitamin content,it emerged that it is extremelyvaluable as feed forparticular animals such as eels and young turkeysand has about the same value forfish, pig and poultryfeed as fishmeal or meat meal.
TABLE

6.

VALUE

OF EARTHWORM MEAL FOR DIFFERENT ANIMAL FEEDS animal maximum value/(? r71) 130 183-218 220-249 1011 338 404 2000

cows ducks broiler chickens turkey(starter) turkey(finisher) trout eels

Considerable thanks are due to J. M. Hill for amino acid analyses, M. E. Putnam, Roche Co. forvitamin analyses and A. Niederer, Meat Research Institute,New Zealand, for help with earthwormprocessing.
REFERENCES

mould the action Darwin,C. i 88i The formation ofvegetable through 326 pp. London: Murray. ofworms, Edwards,C. A. i 983 Earthworms, organicwasteand food.Span26, 106-108. ofearthworm on animalwastes.In Proc. Fieldson, R. S. I985 The economic viability culture Int.Conf. Earthworms, Cambridge (ed. C. A. Edwards& E. F. Neuhauser).Cambridge:D. Ball & Co. (In thepress.) In Proc. value ofearthworm meal forpoultry. Fisher, C. x985 The nutritional Int.ConfEarthworms, Cambridge (ed. C. A. Edwards& E. F. Neuhauser).Cambridge:D. Ball & Co. (In thepress.) der Regenwurmarten und Eudrilus hinsichtlich ihrer Graff, 0. 1982 Vergleich Eiseniafoetida eugeniae Eignungzur aus Abfallstoffen. Proteingewinnung Pedobiologia 23, 277-282. in thePhillippines. In Earthworm and useofPerionyx excavatus as a protein resource R. D. I 983 The culture Guerrero, ecology (ed. J. E. Satchell),pp. 309-313. London: Chapman & Hall. on the potential E. F. & Kaplan, D. L. I 979 A progress use ofearthworms Hartenstein, R., Neuhauser, report in sludgemanagement. Proc. 8thNat.Conf. onSludge Composting, Florida, March 1979, pp. 238-241. Information Transfer Inc. Proc.Austr. Harwood, M. I976 Recoveryof proteinfrompoultrywaste by earthworms. & Stockfeed Poultry Conf., Sydney, pp. 138-143. value ofwormmeal. Proc. Harwood,M. & Savine,J. I 979 The nutritive Austr. Poultry & Stock feedConf,Sydney, March1978, pp. 164-171. offreeze-dried wormmeal as a replacement forfish Hilton, J. W. I983 Potential meal in trout dietformulations. Aquaculture 32, 277-283. Jin-you, X., Xian-Kuan, Z., Zhi-ren, P., Zhen-yong, J., Yan-hua,G., Hong-bo,I., Xue-yan,H. & Qiao-ping,X. research on thesubstitution ofearthworm forfish meal in feeding broilers. J. So. China I982 a Experimental Normal Coll.1, 88-94. Jin-you, X., Xi-cong, H. & Wen-xi, L. x982b An observation on theresults ofusingearthworms as supplementary foodforsuckling pigs.J. So. ChinaNormal Coll. 1, 1-8. content ofearthworms. Lawrence,R. D. & Millar,R. H. I945 Protein Lond.3939, 517. Nature, as foodforman and domestic Mclnroy,D. M. I97i Evaluationoftheearthworm Eiseniafoetida animals.Feedstuffs 43, 46-7. ofgrowing Mekada, H., Hayashi,N., Yokota,H. & Okomura, J. I 979 Performance and laying chickens feddiets earthworms. Sci. 16, 293-297. containing JapanPoultry E. F., Hartenstein, R. & Kaplan, D. L. I979 Second progress Neuhauser, on potential use ofearthworms report in sludgemanagement. Proc.Nat. ConfonSludge Composting, Maryland. (9 pages.) Information Transfer Inc. in the breakdown V. R. I985 Engineering of animal wastesby earthworms. Phillips, problems Proc.Int.Conf. Earthworms, Cambridge (ed. C. A. Edwards& E. F. Neuhauser).Cambridge:D. Ball & Co. (In thepress.)

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FROM ANIMAL

WASTE

307

in Sludge value of earthworm meal. In Proc.Conf.Utilization Sabine, J. I978 The nutritive of Soil Organisms N.Y. (ed. R. Hartenstein), Management, Syracuse, pp. 122-130. 0. 1977 ZurBewertung vonRegenwurmmehl ausEiseniafoetida als Eiweissfuttermittel. Schulz,E. & Graff, (Savigny) 27, 216-218. Landbauforsch. Volk. E. A. & Tacon, A. G. J. I985 The use ofearthworms as foodforrainbowtrout Salmo Proc. Int. Stafford, gairdneri. Conf. Earthworms, Cambridge (ed. C. A. Edwards& E. F. Neuhauser).Cambridge:D. Ball & Co. (In thepress.) value ofearthworms forchickens. Brit.Poultry Sci. 21, 405-410. Taboga, L. 1980 The nutritional Tacon, A. G. J., Stafford, E. A. & Edwards,C. A. I 983 A preliminary investigation ofthenutritive value ofthree terrestrial lumbricid worms forrainbowtrout. Aquaculture 35, 187-199. R. J. 1951 The behaviour Terry, and distribution ofthelarger worms in trickling filters. J. Proc. Inst. Sewage Purif., pp. 16-25. Yoshida,M. & Hoshii,H. I978 Nutritional value ofearthworms for poultry feed.Japanese Poultry Sci. 15, 308-311.

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