Agriculture, Ecosystems and Environment, 24 (1988) 235-247 235

Elsevier Science Publishers B.V., Amsterdam - - Printed in The Netherlands

Interactions between E a r t h w o r m s and Micro-

organisms in Organic-matter B r e a k d o w n

CLIVE A. EDWARDS' and K.E. FLETCHER 2

~Ohio State University, Columbus, OH 43210 (U.S.A.)
2The Horticultural Institute, Wellesbourne, Warwickshire CV35 9EF (Gt. Britain)

ABSTRACT

Edwards, C.A. and Fletcher, K.E., 1988. Interactions between earthworms and microorganisms
in organic-matter breakdown. Agric. Ecosystems Environ., 24: 235-247.

The digestive system of earthworms consists of a pharynx, oesophagus and gizzard ('reception
zone') followed by an anterior intestine that secretes enzymes and a posterior intestine that ab-
sorbs nutrients. During progress through this digestive system there is a dramatic increase in
numbers of micro-organisms of up to 1000 times. There is experimental evidence that micro-
organisms provide food for earthworms. Bacteria are of minor importance in the diet, algae are of
moderate importance; protozoa and fungi are major sources of nutrients. Worms, produced under
sterile conditions, could live on individual cultures of certain bacteria, fungi and protozoa, but
grew best on various mixtures of microorganisms.
Symbiotic interactions between earthworms and microorganisms break down and fragment
organic matter progressively, finally incorporating it into water-stable aggregates. The mineral
nutrients in earthworm casts and lining earthworm burrows are in a form readily available to
plants. There is evidence that interactions between earthworms and microorganisms not only
provide these available nutrients, but stimulate plant growth indirectly in other ways.
There are some studies that show that earthworms can disperse pathogenic microorganisms
and influence the viability of fungal spores and nematode cysts. Earthworms have complex inter-
actions with microorganisms that can lessen or increase plant disease attack.

INTRODUCTION

T h e r e is a b u n d a n t e v i d e n c e t h a t i n t e r a c t i o n s b e t w e e n e a r t h w o r m s a n d mi-
c r o o r g a n i s m s are of m a j o r i m p o r t a n c e in t h e d e g r a d a t i o n of organic m a t t e r
a n d t h e release of m i n e r a l n u t r i e n t s into soil ( E d w a r d s a n d L o f t y , 1977; Lee,
1985). H o w e v e r , t h e n a t u r e of t h e s e i n t e r a c t i o n s , a n d t h e role of m i c r o o r g a -
n i s m s in t h e n u t r i t i o n of e a r t h w o r m s is still f a r f r o m clearly d e f i n e d a n d de-
p e n d s m a i n l y u p o n c i r c u m s t a n t i a l evidence. T h e a v a i l a b l e d a t a d e m o n s t r a t e
t h a t c e r t a i n m i c r o o r g a n i s m s are killed d u r i n g p a s s a g e t h r o u g h t h e e a r t h w o r m
gut, w h e r e a s o t h e r s p r o l i f e r a t e . N e i t h e r t y p e of o b s e r v a t i o n c o n f i r m s w h e t h e r
m i c r o o r g a n i s m s are i m p o r t a n t as i t e m s of e a r t h w o r m diet. T h e a i m o f t h i s

0167-8809/88/$03.50 © 1988 Elsevier Science Publishers B.V.

236

work is to review our current knowledge of microbial-earthworm interactions

and attempt to generalize their importance in the maintenance of soil structure
and fertility and their role in dynamic soil processes.

DIGESTION IN EARTHWORMS

The digestive systems of earthworms from different species, genera and fam-
ilies differ in detail, but their guts have a common basic structure. We still
know relatively little about the process of digestion of the wide range of ma-
terials that pass through the earthworm gut, and these may well differ between
different species. Some species such as Lumbricus terrestris L. depend mainly
upon intact organic wastes for nutrition, whereas other species, such as Eisenia
foetida (Savigny), appear to prefer organic matter in an advanced stage of
decomposition and some appear to extract their nutrients from finely frag-
mented organic matter intimately mixed with soil; typical of these is Allolobo-
phora caliginosa (Savigny).

Digestive system

Earthworm digestive systems are relatively simple, consisting of a buccal

chamber, pharynx, oesophagus, crop, gizzard and intestine. The buccal cavity
has a musculature which permits it to be extruded to allow sensory structures
on its surface to reach potential food. It appears to be able to exert a suctorial
action and to take material in and pass it down the pharynx to the oesophagus,
which has calciferous glands that secrete calcium. This in turn passes into the
crop, which is large and prominent in lumbricids, and ends in a grinding giz-
zard. The position of the gizzard is further forward in megascolecids, eudrilids
and most glossoscolecids than in lumbricids. Behind the gizzard lies the intes-
tine, which is a simple cylindrical tube, with a typhlosole, lined with an epi-
thelium of columnar cells. There are usually 4 well-defined regions of the
intestine, a contractile anterior part which secretes mucus and proteins, fol-
lowed by a middle intestinal region which is ciliated and contains glandular
cells, and then by a posterior intestine lined by a peritrophic membrane and
which ends at the anus.

Passage of food through the digestive system

In lumbricids, food adheres to mucus extruded by the buccal epithelium.

Pressure on the wall of the buccal cavity is released, which establishes a partial
vacuum. The pharynx exerts a further suction and the food enters the pharynx,
which also functions as a force pump, reinforcing oesophageal peristalsis and
propelling food as far as the gizzard. Ciliary action augments muscular con-
traction in the anterior oesophagus. The crop contracts more frequently than
 237

the gizzard and both act as a force pump for transport of materials through the
intestine. The presence of solid material appears to be the stimulus for con-
traction in both regions, and there is no difference in the physical state of their
contents (Arthur, 1965). The folds of the crop regulate the rate of movement
of material into the gizzard, prevent regurgitation, and may assist in the mixing
of food. A sphincter of circular muscles controls the passage of food from giz-
zard to tubular intestine. The sac-like dilations of the anterior intestine undergo
rhythmic expansion and contraction. Intestinal ciliary mechanisms do not ap-
pear to act in propelling food along the intestine. Movements of the body wall
during locomotion aid in passing materials down the gut, and there is also
peristaltic activity. The time taken for food to pass through the gut can vary
from 3 to 4 h in E. foetida to 12-20 h in L. terrestris (Edwards and Lofty, 1977).

Digestive enzymes

Most studies of digestive enzymes in earthworms have been limited to the

lumbricids. Protease, lipase, amylase, lichenase, cellulase and chitinase activ-
ities have been described (Laverack, 1963). A variety of other carbohydrases
have been reported for several species. The biochemical properties of these and
of the other digestive enzymes were reviewed by Jeuniaux (1969). In many
cases, the presence of an enzyme in digestive-organ extracts and that of the
same enzyme in the intestinal lumen has not been confirmed. Thus it is still
uncertain whether there is an extraceUular digestive function for many enzymes.
There is a general proteolytic activity of the intestinal fluid of L. terrestris
after stimulation of glandular cells in the anterior intestine (Millott, 1944;
Heran, 1956). Van Gansen (1962) reviewed secretions in several lumbricids
and proposed the following pattern: (1) the pharyngeal gland secretes and acid
mucus and an amylase, but probably no proteolytic enzyme; (2) amylase and
two proteases are active in the crop, gizzard and anterior intestine; (3) the
middle intestine secretes a neutral mucus and probably some chitinase (De-
vigne and Jeuniaux, 1961). Parle (1963) substantiated an endogenous source
for chitinase activity and presented evidence that cellulase is secreted by the
lumbricid rather than by microorganisms occurring in the digestive tract.
Intestinal homogenates (Segments 20-60) and the digestive fluid contain
trypsin, a protease has been isolated from the digestive fluid and carboxypep-
tidase A and B activities have been observed in intestinal homogenates and
digestive fluid (Bewley and DeVillez, 1968).

Nutrient absorption

There is probably increasing absorption of nutrients along the length of the

intestine, and the posterior intestine, with its characteristic peritrophic mem-
brane, appears to be a major zone of absorption (van Gansen, 1962). Certainly,
238

most areas of the gut can absorb chemicals, but we still lack detailed knowledge
of these processes.

MICRO-ORGANISMSAS FOOD FOR EARTHWORMS

Most of the evidence that microorganisms can provide food for earthworms
is circumstantial and comes from field studies.

Populations in earthworm intestines

A wide range of microorganisms, including bacteria, algae, protozoa, acti-

nomycetes, fungi and even nematodes, are found commonly throughout the
length of the earthworm gut. For instance, Bassalik (1913) reported more than
50 species of bacteria from the earthworm gut. The species of microbes in the
gut are usually very similar to those in the surrounding soil or organic matter
upon which the earthworms feed (StSckli, 1928; Teotia et al., 1950; Rusch-
mann, 1953; Ponomareva, 1953, 1962; Schultz and Felber, 1956; Zrazhevskii,
1957; Went, 1963; Parle, 1963; Atlavinyte et al., 1971 ). This is positive circum-
stantial evidence that earthworms depend upon microorganisms for food; if
microorganisms were used to digest food, the species found in the gut would be
likely to differ from those in the surrounding soil.
The numbers of most species of microorganisms increase dramatically dur-
ing passage through the gut. Stockli (1928) reported great increases in total
numbers of bacteria and actinomycetes (Table 1 ).
Similarly, Ponomareva (1953) found that numbers of actinomycetes, pig-
mented bacteria and other bacteria of the Bacillus cereus group increased as
food moves backwards along the earthworm intestine. One of the most detailed
studies of earthworm nutrition to date was that of Parle (1963), who also re-
ported that actinomycetes and bacteria multiply as they pass through the gut
of L. terrestris, A. caliginosa and A. longa, with about 1000 times more of these
organisms in the hind gut than the foregut. Supporting evidence that multi-
plication in numbers of microorganisms occurs during passage of materials
through the gut comes from the many reports of greatly increased numbers of
microorganisms in the casts of earthworms, compared with those in the soil

TABLE 1

Numbers ( × 106) of microorganismsin different parts of the intestine of L. terrestris (St~ckli,

1928)
Taxa Foregut Midgut Hindgut
Actinomycetes 26 358 15 000
Bacteria 475 32 900 440 700
 239

which the worms had consumed. Increases in numbers of microorganisms re-

ported in casts compared with surrounding soil ranged from about twice (Ghi-
larov, 1963), three times (Zrazhevskii, 1957), five times (Teotia et al., 1950;
Atlavinyte et al., 1971), and thirteen times (Ponomareva, 1953). Unless mi-
croorganisms are multiplying extremely rapidly during passage through the
gut, such increases would be evidence that earthworms are not using these
microorganisms as food. However, not all types of microorganisms have been
reported to increase in numbers during passage of materials through the gut.
Parle (1963) reported that populations of yeasts and fungi did not proliferate
during passage through the gut, although those of actinomycetes and bacteria
did. Domsche and Banse (1972) reported the total destruction of fungi during
passage through the earthworm gut and this was supported by Dash et al.
(1979), who reported digestion of various species of microfungi in different
regions of the gut of the tropical earthworm, Drawida calebi. Species that were
not digested were those that produced antibiotics, such as Aspergillus spp. and
PeniciUium sp., or that had thick-walled, multi-layered spores, such as Thie-
lavia terricola. In other studies, Dash et al. (1980) reported that the size of
hyphal fragments decreased during passage through the earthworm gut. Ko-
zlovskaya and Zhdannikova (1961) found that of the kinds of microorganisms
found in earthworm casts, spore-forming bacteria and actinomycetes predom-
inated and populations of fungi were much lower. Not all species of bacteria
survive passage through the earthworm gut in a viable form. For instance, Day
(1950) reported that numbers of BaciUus cereus var mycoides decreased during
passage through the gut, and Escherichia coli (Brusewitz, 1959), and Serratia
marcessens (Day, 1950) were also killed during passage through the gut.

Experimental evidence

There have been relatively few conclusive data from experiments involving
feeding earthworms differentially with microorganisms.
When individual L. terrestris were allowed to feed on discs of apple leaves
inoculated with the bacterium Pseudomonas aeruginosa, they consumed about
35 % more than when offered uninoculated leaf disks (Wright, 1972 ). However,
in a similar experiment, where Pseudomonas fluorescens was cultured on disks
of filter paper, L. terrestris did not feed on these preferentially, compared with
their feeding on disks with no bacteria. However, when the bacterium was
substituted by two species of fungi, Mucorhiemalis and PeniciUium sp., the
earthworms consumed more filter paper disks with fungi than they did those
without (Cooke and Luxton, 1980). In later experiments (Cooke, 1983), L.
terrestris preferred disks inoculated with Fusarium oxysporum, Alternaria so-
lani and Trichoderma viride, but were not attracted to disks inoculated with
Cladosporium cladosporoides, Poronia pili[ormis, Chaetomion globosum and
Penicillium digitatum. The evidence that the earthworms were attracted to
240

specific fungi was reinforced because there was a strong correlation between
the number of fungi on the disks and the degree of selection. The attraction of
earthworms by fungi was confirmed by Piearce (1978), who found that fungi
and algae were a significant component of the food of 6 lumbricid species. At-
lavinyte and Pociene (1973) also demonstrated that earthworms grew best in
soil with green and blue-green algae.
Several workers have reported that nematodes could be important in the diet
of earthworms. Piearce and Phillips (1980) reported that although they could
find living nematodes in the crop and gizzard of L. terrestris they did not find
any in the pharynx and oesophagus. Dash et al. (1980) considered that ne-
matodes were part of the diet of Lampito mauritii.
The best experimental evidence that microorganisms are important in the
diet of earthworms, comes from studies on E. foetida, a species common in
decaying organic matter, but which can also live in soils with a large amount
of organic matter. In the first of these studies, Miles (1963) hatched individual
E. foetida from microbiologically sterile cocoons and introduced them into soils
that had been inoculated with bacteria and fungi. He found that this species
would grow successfully only when protozoans were added to the cultures.
Piearce and Phillips (1980) and Rouelle (1983) exposed a ciliate Colpidium
campyulum and the amoebae, Saccamoeba stagnicola, Thecamoeba sp. and
Acanthomoeba triangularis to the digestive juices orE. [oetida and L. terrestris
and found that they were killed and digested. Duhlinska (1979) also consid-
ered protozoa to be essential components of the diet of E. [oetida. More recent
work has reported that the presence of various microorganisms in the diet
increased the growth of E. [oetida. Neuhauser et al. (1980) reported weight
increases in the presence, but not the absence of, each of 7 species of micro-
organisms; two bacteria, two protozoa and three fungi. Feeding on live cultures
resulted in greater increases in weight when bacteria and fungi were provided,
but not with the protozoa. Growth of worms fed Euglena gracilis was not sig-
nificantly different, whether live or dead organisms were offered, whereas E.
[oetida grew better when given dead cultures of Tetrahymena pyriformis than
when provided with live cultures. Flack and Hartenstein (1984) reported that
E. foetida grew well when fed many species of protozoa and bacteria although
growth rates with protozoa present were about 20% faster than when bacteria
occurred. Hand and Hayes (1988) also reported growth of E. foetida in the
presence of bacteria and fungi, with good growth occurring in the presence of
Acinetobacter sp. Trichoderma sp. and Mucor spp. However, these workers also
reported that certain species of bacteria (Flavobacterium spp., Streptomyces
spp., Pseudomonas fluorescens) had a toxic effect on E. foetida, causing 100%
mortality within 7 days. The presence of simple nutrients, e.g. casein and glu-
cose also reduced the growth rate of E. [oetida, and if protein was present at a
concentration of 0.5%, or sucrose at 0.1%, 100% mortality occurred within 4
days (Neuhauser et al., 1980). Although the above workers all reported that
 241

E. foetida could grow on various species of microorganisms, there appear to be

deficiencies in the techniques they employed. Most did not use controls with
no microorganisms, and they used microorganisms obtained from scientific
suppliers for their feeding experiments, which were usually totally different
from those found in the environment of the worm. Also, no attempts were
made, except by Hand and Hayes (1988), to rear worms axenically that were
internally and externally free of microorganisms, or to try and culture worms
in sterile environments. Thus, any microorganisms added to cultures of worms
were added to a resident, stable, mixed population of microorganisms. The
reported growth of E. foetida in the presence of various added microorganisms
may have been due to the worm feeding on the added organism, but could easily
have occurred through a shift in the microbial population or nutrient balance,
caused by the addition of an alien microorganism to the resident population.
Moreover, these experiments were very short term, all lasting 2 weeks or less.
A detailed study on the role of microorganisms in the diet of E. foetida was
made at Rohamsted Experimental Station as part of our research programme
(Morgan, 1985). After organic matter was leached with water, individual E.
foetida grew in it more slowly than in unleached material, and if it was heated
at only about half the rate in unheated organic matter. This is at least circum-
stantial evidence that microorganisms are involved in the growth of the earth-
worms. In subsequent experiments, young individuals were hatched sterile from
cocoons, surface-sterilized with carbencillin and then kept in a cellulose me-
dium treated with this antibiotic for 7 days.
When young individual E. foetida were offered 18 species of bacteria and
actinomycetes in pure culture nearly all the worms died within 6 weeks, and
even those surviving on Citrobacter freundii and Pseudomonas sp. had lost
weight (Table 2 ). The reason for lack of success may have been unpalatability,
but could also have been due to production of metabolites or other antagonistic
materials by the bacteria.
In a second series of experiments, young individual E. foetida were kept in
16 pure cultures of fungi in cellulose. In 6 of the cultures, all of the worms died
within 10 days, in three others they were all dead after 6 weeks. However, they
survived in cultures with some species of AspergiUus, Ascobolus sp. and Tri-
choderma sp. In two cultures with Arthrobotrys sp. and Cladosporium herbarum
the worms continued to grow over a period of 14 weeks (Table 2; Fig. 1 ).
Thus, it seems likely that E. foetida can utilize fungi as a food source. The
earthworms appeared to be very sensitive to changes in their environment
caused by the fungi. This is possibly due to a build up of metabolites in the
liquid fraction of the media. Eisenia foetida appeared to prefer non-sporulating
species which are not known to produce antibiotics; such preferences were also
reported for D. calebi (Dash et al., 1979 ). It is quite possible that in its natural
environment E. foetida is selective about the organisms it digests, even though
a whole range of organisms are ingested. It may be that E. foetida prefers pro-
242

TABLE 2

G r o w t h o f E. foetida o n p u r e c u l t u r e o f m i c r o o r g a n i s m s in cellulose 1

Bacteria Weight Fungi Weight

after 6 weeks after 6 weeks

Aeromonas hydrophila • Aspergillus flavus •

Acinetobacter vat. lwoffi • AspergiUus [umigatus I •
Actinomycete • Aspergillus furnigatus II --
Alcaligenes sp. • Aspergillus terreus --
Bacillus cereus vat. mycoides • Arthrobotrys sp. + +
Bacillus macroides • Cladosporiurn herbarum + +
C D C gp II F • F u s a r i u m sp. •
C D C gp V • Oidium sp. *
Citrobacter f r e u n d i i -- Penicillium sp. I •
Enterobacter agglornerans • Penicillium sp. II •
Flavobacterium I • F 18 •
Flavobacterium meningosepticum • F 19 •
Flavobacterium II • Ascobolus sp. --
Pseudomonas aeruginosa • Trichoderma sp. --
Pseudomonas 17 -- C 6 •
Pseudomonas 16 • C 13 --
Serratia marcescens •
Serratia rubidaea •

1Symbols used; • dead; -- s o m e w e i g h t lost; + + g a i n in weight.

0.24L o Control
I • Cl herborum

~ 0.20 A. A Artnrobotrys sp.

~ o.161- ~ •

~0.12

~ 0.04

0,00 I , I , , , , ,
0 2 4 6 8 10 12 14
Time (weeKs)

Fig. 1. G r o w t h o f E . foetida o n Cl. herbarurn a n d A r t h r o b o t r y s sp. L i n e a r r e g r e s s i o n a n a l y s i s gave

c o r r e l a t i o n coefficients ( r ) of: c o n t r o l r = 0 . 9 7 ; Cl. herbarum, r = 0 . 8 4 ; Arthrobotrys sp., r = 0 . 8 4 .

tozoa, only taking fungi when no protozoa are available, or the worm may re-
quire a mixed diet including both protozoa and fungi to fulfill its nutrient
requirements.
To test the importance of protozoa as a food source for E. foetida, several
 243

cultures of protozoa were set up on cellulose. These included Euglena gracilis,

Tetrahymena pyriformis and Ochromonas minuta. Only E. gracilis kept worms
alive for more than 5 weeks. On the basis of these experiments, it did not seem
that this limited selection of protozoa were important in the diet of E. foetida.
However, when worms were grown in cellulose cultures with both bacteria and
these protozoa they survived and grew larger.
Thus, most of the accumulated evidence indicates that earthworms are de-
pendent upon a range of microorganisms in their nutrition and that probably
fungi are the most important microbes as food. It seems likely that protozoa
are also important in their diet but that bacteria and actinomycetes are much
less important.

EARTHWORMS AND THE DISPERSALOF MICRO-ORGANISMS

There have been relatively few experimental studies on the importance of

earthworms in dispersing microorganisms. There seems little doubt that they
must play an extremely important role in this dispersal, since there are many
reports of the large number of microorganisms in earthworm casts. Probably
those species of earthworms such as L. terrestris andAllolobophora longa, which
have relatively permanent burrows in soil are less important in dispersing mi-
croorganisms than those species such as A. caliginosa and A. chlorotica which
move continuously through the upper layers of soil. Hutchinson and Kamel
(1956) demonstrated this experimentally, by showing that fungi spread much
more rapidly through soil when earthworms were present.

Dispersal of beneficial microorganisms

Probably one of the most important activities of earthworms is to commi-

nute organic matter as it passes through their guts, and in this process to ex-
pose the material to a broad spectrum of microorganisms which can multiply
readily on the increased surface area. Because of the universitality of this in-
teraction, and the difficulty of quantifying such interactions, there is little ex-
perimental evidence on its importance. However, there is good evidence of the
importance of earthworms in dispersing propagules of vesicular-arbuscular
mycorrhizae (Rabatin and Stinner, 1988).

Dispersal of harmful microorganisms

Many thick- and thin-walled fungal spores lose little viability during passage
through the intestines of earthworms (Hoffman and Purdy, 1964), e.g. spores
of dwarf bunt (TiUetia controversa) lost none of their viability in passage
through worms. Earthworms can also disperse spores of harmful fungi such as
Pythium (Baweja, 1939), and Fusarium (Khambata and Bhatt, 1957). Thorn-
244

Populationsof
Plant
Patl~ogens
TrQnsmiss;on/~ Dispersal Adverse

Eartt~worms~ I~Microorganisms
/ 1
Beneficial
~ !utrlent/Or::ir::=e r
Release

Fig. 2. Interactions between earthworms and microorganisms.

Dorsal view Lateral view

Fig. 3. The digestive system of a lumbricid.
 245

ton (1970) isolated viable spores of 15 species of phycomycetes from the guts
of lumbricids. Similarly, Rao (1979) concluded t h a t theMegascolex insignis, a
tropical earthworm, could spread viable spores of Pythium aphanidermatum,
a common disease of papaya.
Earthworms may also have an adverse affect upon the spread of fungi, for
example the ascospores of Ventura inaequalis (Coke). Wint, which causes ap-
ple scab, are released from perithecia on overwintering dead leaves lying on
the soil surface in the spring, and these infest the new growth (Hirst et al.,
1955). However, a large population of L. terrestris removes many of these leaves
from the soil surface during the winter, thus preventing at least a proportion
of the ascospores from being able to infect trees.
Earthworms also influence attacks by nematodes on plants. Ellenby (1945)
reported significant increases in hatchability of cysts of the golden cyst ne-
matode (Heterodera rostochiensis) after passage through the gut of A. longa.
Yeates (1981) reported reductions in nematode populations of 37-66% in soils,
when earthworms were introduced into them. He considered it likely t h a t the
earthworms were feeding on nematodes, but these changes could be due to the
earthworms spreading fungi t h a t are of major importance in controlling ne-
matode populations (Kerry, 1988).

CONCLUSIONS

Clearly, the interactions between earthworms and microorganisms are com-

plex (Fig. 2). T h e y are extremely interdependent and we are only just begin-
ning to appreciate the importance of these interactions. The current weight of
evidence is t h a t the beneficial interactions outweigh the effects of dispersal of
pathogens, but a great deal more research is needed in this important area.

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