ARTICLE IN PRESS
Pedobiologia 50 (2007) 463—477
www.elsevier.de/pedobi
The feeding ecology of earthworms – A review
James P. Curry, Olaf Schmidt
School of Biology and Environmental Science, University College Dublin, Belfield, Dublin 4, Ireland
KEYWORDS
Oligochaeta;
Food preferences;
Ingestion;
Assimilation;
Earthworm–
microbial
interactions;
Stable isotopes
Summary
Current knowledge of earthworm feeding ecology is reviewed, with particular
reference to food selection, ingestion, digestion and assimilation, and the use of
novel techniques to advance understanding of the functional significance of these
processes.
Traditional research methods including direct observation of feeding behaviour, gut
content analysis, choice tests, and litter bags have provided a wealth of information
on earthworm feeding. However, there is a lack of the mechanistic, quantitative
information required to characterise adequately their functional role in soil
ecosystem processes such as soil C sequestration and loss, decomposition of organic
residues, the maintenance of soil structure and trophic interactions with plants and
microorganisms.
Stable isotope ratio analysis of light elements (C, N, and S) offers a powerful
research tool to reveal and quantify trophic relationships of earthworms in soil food
webs, while molecular techniques can further enhance understanding of the
interactions between earthworms and microorganisms and their functional
significance.
& 2006 Elsevier GmbH. All rights reserved.
Contents
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Food preference and selection . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Food ingestion rates . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Digestion and assimilation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Novel approaches . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Isotope techniques . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Molecular techniques . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Future directions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Corresponding author.
E-mail address: [email protected] (J.P. Curry).
0031-4056/$ - see front matter & 2006 Elsevier GmbH. All rights reserved.
doi:10.1016/j.pedobi.2006.09.001
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464
Introduction
While there is a considerable volume of published
information on the feeding ecology of earthworms,
there are still many aspects which are not fully
understood. The importance for soil fertility of soil
and organic matter ingestion and turnover by
earthworms has long been acknowledged (Lee,
1985; Lavelle and Spain, 2001; Edwards, 2004),
but many aspects of the interactions between
earthworms, microorganisms, plant roots, various
forms of organic matter and soil mineral constituents and their implications for processes such as
carbon cycling (Zhang and Hendrix, 1995; Jegou
et al., 1998; Bossuyt et al., 2004; Pulleman et al.,
2005) are still poorly understood.
Our understanding of earthworm feeding ecology
is grounded in the careful observations of early
naturalists such as Charles Darwin and Gilbert
White, subsequently refined and extended by
many workers using a wide range of techniques
such as gut content analysis, choice chamber/arena
tests, palatability tests of various kinds including
indirect assessment of foods in growth studies,
litter bag studies, and, more recently, by the
increasing use of novel isotopic, molecular and
related methods.
This paper reviews the current state of knowledge of earthworm feeding ecology and considers
emerging research issues and the potential benefits
which may flow from the application of novel
techniques to their study.
Food preference and selection
The diet of earthworms mainly consists of organic
material in various stages of decay (Lee, 1985).
Dead plant tissue comprises the bulk of the organic
matter consumed, but living microorganisms, nematodes and other microfauna, mesofauna and
their dead remains, are also ingested. Most species
also consume mineral soil fractions to a greater or
lesser degree and seem to prefer organic–mineral
mixtures over pure organic materials (Doube et al.,
1997). The presence of sand grains in particular is
known to facilitate assimilation of nutrients from
organic matter in the case of litter-feeding earthworms, probably by enhancing the grinding action
of the gizzard (Marhan and Scheu, 2005a). This
grinding action may also contribute to the breakdown of ingested mineral grains (Suzuki et al.,
2003) and the greatly accelerated dissolution of
clay minerals as has been shown to occur in
synthetic sediments (Needham et al., 2004).
J.P. Curry, O. Schmidt
A convenient and functionally useful classification based on feeding habits divides earthworms
into detritivores which feed at or near the soil
surface on plant litter and mammalian dung, and
geophages which feed deeper in the soil and derive
their nutrition from soil organic matter and dead
roots ingested with large quantities of soil (Lee,
1985). Various subdivisions within these two broad
groups have been proposed. The currently widely
used classification of Bouché (1977) divides the
detritivores into two groups, the epigeics which are
restricted to the surface, organic-rich, soil horizons, and anecics which feed preferentially on
surface litter but live in burrows in the mineral soil.
The geophages (endogeics sensu Bouché, 1977) may
also be subdivided into groups such as polyhumics,
mesohumics and oligohumics on the basis of their
feeding strategies in relation to soil organic matter
(Lavelle, 1981).
Analysis of the digestive tract contents (generally
the crop and gizzard) in earthworms has revealed
the presence of a wide range of organic materials
(Bouché and Kretzschmar, 1974; Piearce, 1978;
Ferrière, 1980; Judas, 1992; Bernier, 1998; Mariani
et al., 2001). Piearce (1978) found fragments of
grass and other plant leaves, roots, algal cells,
earthworm setae, seeds, fungi, protozoa, fragments of arthropod cuticle, and amorphous humus,
in a range of species from a permanent pasture in
Wales. While there was considerable overlap in the
diets of the different species, Piearce concluded
that the six species examined fell into five separate
dietary groups distinguishable on the basis of the
nature, particle size and quantities of organic and
mineral materials ingested.
While earthworms as a group feed on a wide
range of materials, many studies using a range of
techniques including gut content analysis, choice
chambers, palatability tests, bait removal methods, and litter bags have demonstrated significant
levels of food selection by different species.
Earthworms can show distinct preference for
different kinds of plant litter (Satchell, 1967),
and preference can vary between species. Neilson
and Boag (2003) offered soil and foliage of seven
plant species to six earthworm species from
Scottish upland pasture soil and found that Lumbricus terrestris preferred litter of Poa annua to
other types of plant litter and soil; Octolasion
cyaneum preferred soil, while the other species
tested (Aporrectodea caliginosa, Ap. longa, Allolobophora chlorotica and L. rubellus) displayed no
obvious food choices. The particle size of organic
material is known to strongly influence earthworm
growth rates and fecundity (Boström and LofsHolmin, 1986; Lowe and Butt, 2003), presumably
ARTICLE IN PRESS
The feeding ecology of earthworms
because finer material is more readily ingested and
assimilated than coarse, although it is not known
whether earthworms actively select finer material
in preference to coarse.
Protein- and carbohydrate-rich litters seem to be
preferred to litters with lower protein content,
possibly because litter N and carbohydrate contents
are strongly correlated and earthworms show a
strong preference for litter with high soluble
carbohydrate content (Satchell, 1967). Freshly fallen leaves of many trees including oak, beech, larch,
and spruce are unpalatable to earthworms but
become acceptable after a short period of weathering and microbial degradation of distasteful
substances, notably phenolic compounds (Satchell,
1967). Hendriksen (1990) evaluated leaf litter
preference on the basis of the numbers of earthworms found below litter bags containing different
litters in a pasture field and found that detritivores
(Lumbricus spp.) were more selective in their
choice of litter than geophages (Aporrectodea
spp.). Litter preference by Lumbricus spp. was
significantly correlated with C:N and phenolic
content, while the preferences of geophages were
not correlated with palatability. Schönholzer et al.
(1998) also found that palatability of leaves
of Taraxacum officinale, Hypericum perforatum,
Dipsacus silvestris and Miscanthus sinensis to
L. terrestris was largely determined by the C:N
ratio. A reduction in the palatability of senescent
leaves of H. perforatum during the first week of
decomposition was attributed to the presence of
toxic plant metabolites.
When offered a choice between infected and
non-infected materials, L. terrestris preferred
leaves and paper discs inoculated with microorganisms and showed distinct preferences for different
types of inoculum (Wright, 1972; Cooke and Luxton,
1980). Three earthworm species (Al. chlorotica,
Ap. longa and L. terrestris) were offered a choice
of mixtures of soil and small wheat straw fragments, which had been inoculated individually with
six saprotrophic fungi and all showed preferences
between the six fungal species (Moody et al.,
1995). Early straw decomposers, capable of utilising water-soluble sugar and cellulose, were preferred in most cases to lignin-decomposing fungi
characteristic of the later stages of decomposition.
Likewise, Bonkowski et al. (2000) demonstrated
that the preferences of five earthworm species for
a range of soil fungi followed a general pattern,
irrespective of ecological group. However, Maraun
et al. (2003) concluded that earthworms, like most
fungal-feeding decomposer animals, appear to be
food generalists rather than specialists, with a
preference for dark pigmented fungi (Dematiacea)
465
which often comprise up to 60% of fungal isolates
from soil and are generally of high food quality. The
nutritional significance of such preferences is
uncertain, as to date there is little direct evidence
to support the general assumption that fungi and
other microorganisms are a major food source for
earthworms (see for example Wolter and Scheu,
1999). However, recent developments in molecular
methods provide excellent tools for addressing
this and related aspects of earthworm nutrition
(see below).
In addition to fungi, other components of the soil
microbiota which may constitute a significant part
of the diet of earthworms include protozoa, algae,
and nematodes. Amoebae can form a significant
proportion of the diet of earthworms (Bonkowski
and Schaefer, 1997). Algae are often present in gut
contents, but the capacity of earthworms to
assimilate C from algae growing on the soil surface
has only recently been confirmed experimentally by
tracing 13C from isotopically labelled CO2 into body
tissue of Al. chlorotica in the absence of higher
plants (Schmidt et al., 2003). Earthworms may
ingest considerable numbers of nematodes (Dash
et al., 1980; Yeates, 1981), and have been
associated with a reduction in nematode populations under some circumstances (Hyvönen et al.,
1994; Ilieva-Makulec and Makulec, 2002). The
question of whether these organisms are actively
preyed upon by earthworms or accidentally ingested with organic matter is still an open one. In a
multiple choice feeding experiment, Bonkowski and
Schaefer (1997) found evidence that Ap. caliginosa
may actively search for locations with high protozoan (naked amoebae) densities in beech forest
soil. However, these microfauna are associated
with hotspots of biological activity such as the
rhizosphere or decaying plant residues in the soil
and it seems more likely that they are accidentally
ingested with dead organic matter by earthworms
which feed preferentially in microsites rich in
decaying organic matter (Bolton and Phillipson,
1976; Lee, 1985).
Earthworm–plant interrelationships remain an
active topic for research (Brown et al 1999; Scheu,
2003). There is some uncertainty regarding the
degree to which earthworms feed on living root
material. Bouché and Kretzschmar (1974) concluded from crop and gizzard content analysis that
Ap. rosea and Al. chlorotica were root feeders in
pasture, while Ap. caliginosa was a root feeder in
forest soil. Deep-dwelling soil species are believed
to consume considerable amounts of dead root
material (Lee, 1985). Radiotracer studies using 32P
provided some evidence for ingestion of living
white clover roots by L. terrestris (Baylis et al.,
ARTICLE IN PRESS
466
J.P. Curry, O. Schmidt
1986), and earthworms have been observed feeding
on root hairs in rhizotron studies (Gunn and
Cherrett, 1993). However, there is no evidence
that earthworms feed extensively on living roots or
are attracted towards root exudates; it seems more
likely that fine roots and root hairs are ingested
incidentally while feeding on rhizosphere soil.
Clarifying the nutritional exploitation, if any, of
rhizodeposits by earthworms remains a challenging
task for research. For example, Milcu et al. (2006)
hypothesised recently that higher plant diversity,
with unchanged root and shoot biomass, resulted in
a larger biomass of Ap. caliginosa because more
diverse plant mixtures provide earthworms with
nutritionally higher-quality root-derived C resources. In this context, a novel belowground
olfactometer device designed by Rasmann et al.
(2005) to test nematode responses to plant root
signals could likewise be suitable to study earthworm responses to plant signals and trophic earthworm–rhizosphere interactions (Fig. 1).
While the nutritional importance of plant seeds
ingested by earthworms is unknown, several studies
have investigated the effects of earthworms on the
dispersal and viability of ingested seeds and
implications for vegetation dynamics (Piearce
et al., 1994; Willems and Huijsmans, 1994; Decaëns
et al., 2003; Smith et al., 2005).
Most kinds of animal dung are highly attractive
and nutritious food sources for earthworms (Barley,
1959; Marhan and Scheu, 2005b; Lowe and Butt,
2005). A number of species aggregate under dung
pats or seek out dung-rich patches in the soil
(Hughes et al., 1994). Protocols are now available
to produce animal manures that are either distinct
in their 13C composition resulting from designed
C3/C4 photosynthetic plant-type diets (Dungait
et al., 2005) or 15N labelled, in bulk or different
N fractions (Powell et al., 2004); the use of such
manures has potential for quantifying the participation of different earthworm species in the
incorporation and decomposition of animal manures under realistic field conditions. Knowledge of
dung feeding behaviour of earthworms is also
relevant in the assessment of their possible role
in the transmission of livestock diseases including
bovine tuberculosis (Muldowney et al., 2003;
Fischer et al., 2003).
Food ingestion rates
Figure 1. Belowground olfactometer designed to test
nematode responses to plant root signals. Reproduced
from Rasmann et al. (2005) with permission by the Nature
Publishing Group.
Table 1.
Organic matter ingestion rates can be very
variable (Table 1), depending on factors such as
favourableness of environmental conditions for
Organic matter ingestion rates
Guild (1955)
Barley (1959)
Hendriksen (1991)
Hendriksen (1991)
van Rhee (1963)
van Rhee (1963)
van Rhee (1963)
Curry and Bolger (1984)
Raw (1962)
Needham (1957)
Shipitalo et al. (1988)
Shipitalo et al. (1988)
Shipitalo et al. (1988)
Shipitalo et al. (1988)
Species
Material
Ingestion rate
(mg DM g1 FM d1)
Aporrectodea caliginosa
Ap. caliginosa
Lumbricus festivus
Lumbricus castaneus
Lumbricus terrestris
Ap. caliginosa
L. castaneus
L. terrestris
L. terrestris
L. terrestris
L. terrestris
L. terrestris
Lumbricus rubellus
L. rubellus
Cattle dung
Sheep dung
Cattle dung
Cattle dung
Grass, alder leaves
Grass, alder leaves
Alder leaves
Salix leaves
Apple leaves
Elm leaves
Alfalfa/clover
Corn leaves
Alfalfa/clover
Corn leaves
40
80
c.12
c.22
10–17
12
33
9–15
2.6–16.5
27 (max. 80)
12–13
6
36–52
18
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The feeding ecology of earthworms
Table 2.
467
Soil ingestion rates
Species
Type of soil
Ingestion rate
(mg DM g1 FM d1)
Barley (1959)
Scheu (1987)
Scheu (1987)
Curry et al. (1995)
Curry et al. (1995)
Boström (1988)
Bolton and Phillipson (1976)
Aporrectodea caliginosa
Ap. caliginosa
Octolasion lacteum
Ap. caliginosa
Lumbricus terrestris
L. terrestris
Aporrectodea rosea
200–300
2105
1880
2353
713
490–3500
1000–2000
Martin (1982)
Martin (1982)
Martin (1982)
Lavelle (1974)
Ap. caliginosa
Aporrectodea trapezoides
Lumbricus rubellus
Megascolecidae/Eudrilidae
Pasture
Beechwood mull
Beechwood mull
Arable land
Arable land
Arable land
Mull soil under bramble
(Rubus fruticosus).
Sandy soil7added OM
Sandy soil7added OM
Sandy soil7added OM
Tropical savanna
earthworm activity, food quality, and palatability.
Leaf consumption rates as high as 80 mg dry
mass g1 fresh mass d1 have been reported for
L. terrestris (Needham, 1957), van Rhee (1963)
reported rates ranging from 10 mg g1 fresh
mass d1 for high-quality litter to 66 mg g1 fresh
mass d1 for litter of poor quality, while Barley
(1959) reported a mean dung consumption rate by
Ap. caliginosa of 80 mg g1 fresh mass d1. However, these estimates have been mainly derived
from culture experiments with earthworms maintained under favourable conditions. The range of
12–17 mg dry mass of grass litter g1 fresh mass d1
reported by van Rhee (1963) for six species under
seminatural conditions may be more typical for
temperate grassland earthworms, while dung consumption in the field by L. festivus and L. castaneus
appears to be of a similar magnitude (Hendriksen,
1991).
Soil consumption rates (usually estimated from
egestion or cast production rates) are equally
variable, reflecting the feeding habits of the
earthworm species and the organic matter content
and quality of the soil (Table 2). Estimates range
from 200 to 300 mg dry soil g1 fresh mass d1 for
Ap. caliginosa in a New Zealand loam soil (Barley,
1959) up to 34 g g1 d1 for juvenile Millsonia
anomala feeding on organic matter-poor tropical
soil, although 7–10 g g1 d1 may be more typical
for tropical geophagous earthworms such as the
common invasive species Pontoscolex corethrurus
(Lavelle and Spain, 2001). Soil consumption rates of
1.0–2.5 g dry mass g1 fresh mass d1 appear to be
typical for temperate geophagous species (Bolton
and Phillipson, 1976; Scheu, 1987; Boström, 1988;
Curry et al., 1995), although higher rates have been
reported (e.g., Martin, 1982; see Table 2). Some
species such as the epigeic L. rubellus and the
topsoil-dwelling Ap. trapezoides can compensate
3750–4090
2630–4190
1920–3010
6700
for inadequate soil organic matter content to an
extent by increasing soil consumption rates, but
this does not seem to be the case for true endogeic
species such as Ap. caliginosa (Martin, 1982;
Boström, 1988).
Juvenile earthworms have higher relative soil
consumption rates than adults, reflecting their
higher energy requirements (Bolton and Phillipson,
1976; Scheu, 1987; Boström, 1988; Curry et al.,
1995). Soil consumption/egestion rate increases
with temperature to an optimum level, which
appears to be about 15 1C for Allolobophora/
Aporrectodea spp. in temperate soils (Bolton and
Phillipson, 1976; Scheu, 1987; Boström, 1988; Curry
et al., 1995; Daniel et al., 1996) and about 10 1C for
L. terrestris (Curry et al., 1995), although Whalen
et al. (2004) recorded increasing rates of soil
egestion with temperature up to 20 1C by Aporrectodea and Lumbricus juveniles. Soil consumption
appears to be at a maximum at moisture tensions at
or somewhat above field capacity, and is generally
limited in drier soils and in saturated soils (Lee,
1985; Scheu, 1987; Hindell et al., 1994). It may
increase with increased burrowing activity in
compacted soil (Larink et al., 2001).
Digestion and assimilation
Significant enzymatic activity occurs in the guts
of earthworms (Parle, 1963; Neuhauser et al.,
1978; Barois and Lavelle, 1986; Loquet and Vinceslas, 1987), but it is not clear how much of this
originates from the worms themselves and how
much is due to the gut microflora. Cellulase activity
has been detected in gut wall extracts of several
species (Urbasek, 1990), but probably most of the
enzyme activity in the gut is due to ingested
microflora (Lattaud et al., 1998). While simple
ARTICLE IN PRESS
468
carbohydrates and proteins are probably readily
digested, it appears that earthworms are able to
digest relatively little of the cell wall constituents
of the plant litter they ingest – some cellulose,
some simple phenolic materials, but probably no
lignin (Satchell, 1967; Lee, 1985; Brown and Doube,
2004). Studies on the interrelationships between
earthworms and microorganisms have often yielded
inconclusive results, possibly because of methodological constraints. An interesting innovation in this
context is the use of image analysis to quantify the
origin and fate of microorganisms ingested by
L. terrestris, with decomposing leaves of T.
officinale (Schönholzer et al., 1999). Most studies
seem to indicate that the microbial composition of
the earthworm gut reflects that of ingested soil or
plant residues, but some species with specialised
feeding habits may possess a distinctive gut
microflora (Satchell, 1967; Lee, 1985; Brown and
Doube, 2004). Novel molecular techniques offer
considerable prospects for yielding greater insights
into such interrelationships and their functional
significance (see below).
Earthworms assimilate nutrients and energy from
a wide range of ingested materials with variable
efficiency, depending on the species and the nature
of the ingested material. Earthworm feeding
strategy is generally one of high consumption and
low assimilation of poor-quality food material.
Thus, the geophagous species Ap. rosea consumes
large amounts of soil, literally eating its way
through the soil (Bolton and Phillipson, 1976).
Although it ‘grazes’ the walls of burrows, and
preferentially selects more organic-rich fractions of
soil, the overall food quality of the ingested
material is poor and the assimilation efficiency is
correspondingly low (less than 2.5% of ingested dry
organic matter, approx. 1% on an energy basis,
Bolton and Phillipson, 1976). Assimilation efficiency
for tropical geophagous earthworms appears to be
somewhat higher (3–19% of ingested soil organic
matter), for reasons that seem to reflect a high
level of microfloral activity in the gut (Lavelle and
Spain, 2001; see below). Assimilation efficiencies
can be considerably greater for litter-feeding
species feeding on high-quality material. Daniel
(1991) studied leaf litter consumption and assimilation by juvenile L. terrestris and reported
assimilation efficiencies of 43–55% for dandelion
leaves under favourable temperature and moisture
conditions, while Dickschen and Topp (1987) reported assimilation efficiencies for L. rubellus of
about 30% when fed on larch litter and 70% when
fed on alder leaves. However, these values seem
unrealistically high in the context of the field
situation as, when given a choice, litter-feeding
J.P. Curry, O. Schmidt
earthworms will always consume mineral soil to a
greater or lesser degree (Doube et al., 1997) and
admixture with soil will have the effect of reducing
assimilation efficiency.
As already mentioned, one of the main factors
likely to influence food digestibility is the degree of
microbial involvement in the process. The relationship between earthworms and microorganisms may
be regarded as a mutualistic one, the nature and
intensity of which varies with functional group
(Lavelle and Spain, 2001). Epigeic species which
consume considerable amounts of raw organic
matter have a broad range of enzymatic capacities,
probably mainly originating from ingested microflora. Anecic species such as L. terrestris form
‘middens’ by collecting and dragging surface litter
into the mouths of their burrows where it is
amenable to microbial colonisation and degradation (the ‘external rumen’), with mutually beneficial consequences for earthworms and microflora.
The significance of mutualistic digestion, resulting
from the interaction between earthworms and
microflora ingested with the soil while the soil
passes through the gut, is more problematical in
the case of endogeic earthworms (Barois and
Lavelle, 1986; Lavelle and Spain, 2001). Microbial
activity is considered to be greatly stimulated by
favourable conditions (moisture content, pH, high
concentration of mucus) in the anterior part of the
gut; in the midgut this enhanced microbial activity
results in the digestion of soil organic matter, and
the products of this digestion are partially absorbed
in the posterior part of the gut. It has been
suggested that this process could result in 3–19%
of soil organic matter being assimilated from
organic matter-poor tropical soil during a gut
transit time of 30 min to 2–4 h, although this
remains to be demonstrated directly (Lavelle and
Spain, 2001). However, it is difficult to understand
how even enhanced microbial activity could significantly influence the dynamics of organic matter
breakdown within such a short time in the earthworm gut. This and other aspects of the ‘sleeping
beauty’ hypothesis (Lavelle and Spain, 2001) merit
further investigation. Another way in which organic
matter assimilation could be enhanced is through
reingestion of casts, which has been suggested to
occur frequently among anecic earthworms in
temperate soils (Bouché et al., 1983).
Novel approaches
The potential of isotope and molecular techniques to enhance understanding of earthworm
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The feeding ecology of earthworms
469
feeding ecology and food web interactions is
particularly exciting, and some examples of the
application of these approaches in earthworm
feeding studies are considered here.
Isotope techniques
Stable isotope techniques measure ratios of
stable isotope pairs such as 13C/12C (carbon),
15
N/14N (nitrogen) and 34S/32S (sulphur), usually
by isotope ratio mass spectrometry (IRMS) (Scrimgeour and Robinson, 2004). The strengths of these
techniques are that they can be applied to study
real, undisturbed food webs in the field, they
reflect assimilated, rather than ingested, dietary
components, and they can be used to quantify
matter fluxes between earthworms and their
environment as functional processes. Two broad
approaches have been found useful in soil ecological studies, namely natural abundance and tracer
addition methods.
Natural abundance methods measure the ratios
of naturally occurring stable isotopes. Since earthworms are either detritivores or geophages, this
approach relies on known isotopic differences
between potential food sources for earthworms,
rather than isotopic fractionation associated with
classic trophic steps (DeNiro and Epstein, 1981). A
number of studies have successfully used natural
isotopic source differences to explore the feeding
ecology of field populations of earthworms. Martin
et al. (1992) exploited the distinct 13C compositions
associated with vegetation shifts from C3 to C4
photosynthetic type vegetation in France, and from
C4 to C3 in Ivory Coast, to investigate the ability of
earthworms to assimilate soil organic pools of
different ages, while Briones et al. (2001) similarly
exploited land-use changes involving maize (C4)
and grassland (C3) vegetation in Spain and England.
While earthworms generally showed a preference
for fresh over older material, different ecological
and age groups appeared to consume organic
matter of different quality. Schmidt and Ostle
(1999) used natural isotopic differences between
cattle slurry (which was naturally enriched in 15N
after storage) and other potential food sources to
ascertain the assimilation of N derived from slurry
by Ap. caliginosa and Ap. longa in the field.
Schmidt et al. (1997) found that the N isotope
ratios in earthworm ecological groups reflected
isotopic changes in the vegetation, in this case the
presence of clover (N2-fixing legume) in a wheatclover cropping system. More importantly, 15N
concentrations in ecological groups also reflected
feeding on plant litter or soil organic matter (see
Figure 2. Natural abundance 15N isotope ratios in wholebody tissue of five sympatric earthworm species were
strongly correlated with degree of surface litter feeding
as assessed by mucus analysis after 14 d feeding on 15Nlabelled maize in field plots (r ¼ 0:953, Po0:01, n ¼ 5)
(O. Schmidt and J.P. Curry, unpublished).
also Fig. 2). Thus, gradual differentiation in feeding
by earthworms on organic materials decomposed to
a different degree probably mirrors shifts (fractionation) in 15N associated with microbial processing
of food sources, termed ‘trophic distance from the
primary organic matter source’ by Hendrix et al.
(1999a).
Combined C and N isotope ratios were more
effective in separating earthworm feeding groups
in set-aside arable land in Ireland than were the
patterns of C and N isotopes considered separately
(Schmidt et al., 2004). The seven lumbricid species
present were clearly divided into two groups, one
comprising mainly litter-feeding species (Lumbricus
spp. and Satchellius mammalis), and the other soilfeeding species (Al. chlorotica, Ap. caliginosa, Ap.
longa, Ap. rosea and Murchieona minuscula). While
the data suggested a high degree of overlap
between species within the soil-feeding group,
the variability was such that interspecific differences in food selection and ecosystem functions
could not be ruled out. Combined 13C and 15N
analysis has also been used successfully to analyse
trophic relations of non-lumbricid earthworms.
Hendrix et al. (1999a, b) used 13C and 15N to
explore patterns of resource utilisation and partitioning by native earthworms in subtropical savanna and forest ecosystems in northern Florida, and
by native and exotic species in tropical ecosystems
in Puerto Rico. Uchida et al. (2004) combined
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470
stable isotope analysis (13C and 15N) with gut
content examination to investigate the previously
unknown feeding ecology of megascolecid earthworms in Japanese forests. Generally, stable
isotope analysis has tended to confirm and further
refine conventional ecological classification systems (Briones and Schmidt, 2004).
J.P. Curry, O. Schmidt
Enriched stable isotope tracer methods have
been used to measure C and N assimilation and
turnover rates in earthworms (e.g., Bouché and
Ferrière, 1986; Curry et al., 1995) and to quantify
the effects of earthworm feeding on elemental
flows between soil compartments including plant
litter (Zhang and Hendrix, 1995; Postma-Blaauw
Figure 3. Fate of 15N and 13C secreted by isotopically labelled individuals in different gut sections and fresh casts in
(A) Lumbricus terrestris and (B) Octolasion cyaneum (O. Schmidt, unpublished).
ARTICLE IN PRESS
The feeding ecology of earthworms
et al., 2006). Most such studies have been
conducted under laboratory conditions or by
reintroducing labelled earthworms into artificial
field enclosures. The objective of a recent field
study in Ireland was to quantify over one active
season (12 weeks) in situ N and C assimilation from
surface plant litter by undisturbed earthworm
populations, comprising a range of species representing different ecological groups, using a combination of stable isotope natural abundance and
enriched methods (O. Schmidt and J.P. Curry,
unpublished). These studies showed that while
there was preferential assimilation of litter N by
anecic as compared to endogeic species, most
members of all ecological groups utilise surface
litter as an N and C source. The study also
confirmed firstly, that natural 15N abundance is a
sensitive measure of the soil-litter feeding gradient
and secondly, that cutaneous mucus, having a fast
turnover, is a better indicator of current dietary
input than whole-body tissue (Fig. 2).
Additional laboratory-based studies were focused
on the intestinal C and N metabolism in earthworms, with the objectives of identifying and
quantifying the sources of C and N and tracing
their fate during gut transit and in casts
(O. Schmidt, unpublished). The main trends are
illustrated by the examples presented in Fig. 3.
Large amounts of worm-derived 13C and 15N were
detected in the foregut of both the endogeic
species O. cyaneum and the anecic L. terrestris.
However, the sharp drop in 13C and 15N in the
midgut and hindgut observed in both species
indicated that the reabsorption of worm-derived
intestinal C and N is rapid and efficient during gut
passage. Casts were slightly but significantly
enriched in 15N, which suggests that losses of
intestinal C, but not N, in casts are small (Fig. 3).
An issue of significance in relation to the mutualistic digestion hypothesis mentioned earlier that
remains to be explored is the role of the intestinal
mucus as a primer for microbial activity in the
earthworm gut.
Recently, 14C measurements by accelerator mass
spectrometry (AMS) have been applied to soil
organisms to determine the age of assimilated
C. This approach, which exploits the decline in
atmospheric 14C from nuclear weapons testing
since the mid-1960s, can estimate the time of
origin of organismal C younger than 40 yr with a
precision of about 1 yr (Hobbie et al., 2002).
Briones and Ineson (2002) and Briones et al.
(2005) analysed enchytraeid and lumbricid worms
from a blanket bog and woodland soil, respectively,
in Britain. Epigeic species were found to have
lowest body radiocarbon concentrations, indicating
471
that they had assimilated recently fixed C (0–3 yr
old); endogeics had assimilated older (5–8 yr old)
material, while anecics appeared to have assimilated a higher proportion of older, more mineralised organic matter than expected.
Molecular techniques
Molecular techniques may help to distinguish
between the sources of enzyme activity indigenous
to earthworms and that associated with exogenous
microorganisms ingested with food, currently an
area of considerable uncertainty. In a recent study,
Egert et al. (2004) used terminal-restriction fragment length polymorphism (T-RFLP) analysis to
study the bacterial and archaeal community structure in soil, guts, and fresh casts of L. terrestris
feeding in soil with and without beech litter
amendment. Analysis of the T-RFLP profiles revealed only minor, although statistically highly
significant, differences between the communities.
However, the existence of an abundant indigenous
gut microflora appeared unlikely. Similarly, Horn
et al. (2006) concluded from comparative sequence
analysis that denitrifying microbial populations
found in the gut content of four lumbricid species
were regular soil microorganisms rather than
endemic to the gut. Singleton et al. (2003), using
both conventional (direct counts, culturability
studies) and molecular (RNA profiles, fluorescent
in situ hybridisation (FISH)), found that a significant
fraction of prokaryotes remaining in the intestine
after casting were tightly associated with the
intestine wall. The microbial community tightly
associated with the intestine was dominated by a
small number of phylotypes, and this association
was opportunistic rather than obligate.
Future directions
Progress has been made in the mechanistic,
quantitative analysis (Jager et al., 2003) and
modelling (Jager, 2004) of the various parameters
necessary to describe the feeding activity of
ecotoxicological test species (Eisenia spp.) in
artificial substrates; the challenge is to apply
equally rigorous approaches to studying the
feeding, including food selection and composition, by soil-dwelling earthworm species in real
soils.
The selection and ingestion of food materials by
individual earthworms is still not well understood;
multiple-choice feeding experiments with improved experimental design (Arthur, 1965; Prince
ARTICLE IN PRESS
472
et al., 2004) and in situ bait feeding experiments
for geophagous species (e.g., van Gestel et al.,
2003) are required to improve understanding of
these important processes. Knowledge of selective
feeding by earthworms on certain organic matter
pools would be useful because it is likely to affect
the mineralisation or stabilisation of such pools
(Marhan and Scheu, 2005b). Also, selectivity for
groups of organisms, or patches containing these
groups, could be a major factor determining the
effects of earthworms on these and other, nonselected organisms. For instance, Jørgensen et al.
(2005) have described an innovative molecular
approach to test selective foraging on soil fungi
by collembolans in undisturbed soil, an approach
that could be applied to earthworms. Since the
fungal diversity based on 18S rDNA sequences in soil
was 33 times higher than that in gut contents of
Protaphorura armata, the authors concluded that
this collembolan species is highly selective when
foraging on soil fungi. Berg et al. (2004) have
recently used activity measurements of three
carbohydrases to classify 20 Collembola species
from grassland soils into feeding guilds; such a
systematic, metabolic fingerprinting approach has
not yet been pursued for earthworms.
Little is known about ontogenetic changes in the
food and feeding behaviour even of the moststudied earthworm species and thus possible agespecific nutritional constraints on population dynamics. For example, juvenile stages of marine
deposit-feeding polychaete worms have been
shown to be more susceptible to food limitation
than conspecific adults, creating food-related
recruitment bottlenecks (Hentschel, 1998). In a
study of Ap. longa, a species that could be
expected to show ontogenetic dietary changes,
isotopic data provided only limited evidence for
such ontogenetic or intraspecific feeding specialisation (Schmidt, 1999).
Recent development of simple, rapid labelling
techniques has enhanced the accessibility of
isotope tracer approaches for earthworm studies.
Grass and other herbaceous plants, for instance,
can be isotopically labelled using a simple urea
leaf-feeding method (Schmidt and Scrimgeour,
2001), while earthworms themselves can be labelled by feeding them soil amended with 15Nenriched mineral compounds and 13C glucose
(Dyckmans et al., 2005). The development of
mobile systems for 13CO2 pulse-labelling has greatly
facilitated belowground C tracer experiments in
the field (Ostle et al., 2000), an approach that has
great potential for studying the feeding ecology of
earthworms, especially in relation to rhizosphere
processes, under field conditions.
J.P. Curry, O. Schmidt
Many aspects of earthworm–microbial interaction require further study, including selection and
ingestion rates for different microbial groups and
the interactions which occur during transit of
ingested soil and organic matter through the gut,
and the potentially significant contribution of
denitrification proceses in the gut to N2O emission
from soils (Drake et al., 2006). Molecular techniques offer considerable potential for animal–
microbial studies. For instance, recent work has
demonstrated the enormous microbial diversity
which occurs in the human intestine (Eckburg
et al., 2005), while Suh et al. (2005) isolated over
650 yeasts from the guts of beetles, at least 200
being hitherto undescribed taxa. Molecular and
isotopic techniques used in combination offer
considerable potential for unravelling complex
earthworm–microbial–organic matter interrelationships, for example possible structural changes
in the gut microflora and functional consequences
for nutrient assimilation by earthworms induced by
variation in food resource quality.
Lipid analysis, alone or in conjunction with
compound-specific isotope analysis, appears to
have considerable potential as a novel tool in soil
food web studies. According to Chamberlain et al.
(2004) lipids such as fatty acids and sterols are ideal
for such studies. This approach has proven to be
especially useful for small invertebrates such as
Collembola (Chamberlain et al., 2004; Ruess et al.,
2004, 2005a, b); the evaluation of its utility for
larger invertebrates including earthworms is in
progress (Sampedro et al., 2006). A related
approach which may have applications in identifying earthworm food sources concerns the relationship between amino acid profiles in earthworms
and those in the soil (Donovan et al., 2005).
Ecological stoichiometry – the study of the
balance of elements in ecological processes – has
recently being receiving attention in regard to
freshwater and marine detritus-based ecosystems
(Cross et al., 2003; Moe et al., 2005) but has been
little considered in relation to terrestrial ecosystems (Pokarzhevskii et al., 2003). Since organisms
often require elements (notably C, P, and N) in
ratios which differ from those provided by their
food, this mismatch may have implications for
earthworm feeding and food chain relationships.
For example, Tiunov and Scheu (2004) demonstrated, in a laboratory experiment with
O. tyrtaeum, that C availability controls the growth
of detritivorous earthworms and their effect on N
mineralisation. Availability of assimilable C was
found to greatly influence the growth of the
geophagous tropical earthworm species Millsonia
anomala: when water-soluble organic matter was
ARTICLE IN PRESS
The feeding ecology of earthworms
added to soil, ingestion rate decreased sharply
while growth was significantly improved as a result
of the decreased ‘cost’ of processing soil (Lavelle
et al., 1980).
Other biochemical fingerprinting methods based
on Fourier transform infrared spectroscopy (FT-IR)
have been proposed as high-throughput tools for
monitoring environmental impacts on microbial
communities in earthworm casts (Scullion et al.,
2003). These methods could also be used for
comparing feeding and food selection by coexisting
earthworm species under varied environmental
conditions (e.g., different food quality, habitats,
interspecific competition).
While most of the focus in earthworm feeding
ecology has understandably been on food web
relationships and implications for nutrient cycling
and soil fertility, other areas and applications which
merit attention include the potential impact of
earthworms on soil-borne plant pathogens (Friberg
et al., 2005) and mycorrhizal fungi (Gormsen et al.,
2004), the earthworm-mediated distribution of
biocontrol agents in the soil (Singer et al., 1999),
and the interactions between earthworms and
transgenic plants or their litter (Saxena and
Stotzky, 2001; Zwahlen et al., 2003). As is the case
with many other soil animal groups, earthworms
are usually studied in isolation, but the few
published studies of interactions with other organisms affecting feeding by earthworms had surprising outcomes (e.g., Humphries et al. 2001; Zimmer
et al., 2005; Milcu et al., 2006). For instance, the
presence of fungal endophytes substantially increased the nutritional value of grass leaves for
E. fetida (Humphries et al. 2001) and springtails
were found to enhance the nutrition of Ap.
caliginosa from non-litter sources (Milcu et al.,
2006).
Coming back to Darwin, there is renewed interest
in the feeding activities of earthworms and their
roles in earth surface processes of importance in
archaeological sites, including the transport of soil,
stones and seeds, and the production of calcium
carbonate granules which may have preserved
palaeo-environmental information (Canti, 2003).
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