Applied Soil Ecology 10 (1998) 263±276
Functional aspects of soil animal diversity in agricultural grasslands
Richard D. Bardgetta, Roger Cookb,*
a
School of Biological Sciences, 3.614 Stopford Building, University of Manchester, Oxford Road, Manchester M13 9PT, UK
b
Institute of Grassland and Environmental Research, Aberystwyth, SY23 3EB, Wales, UK
Received 5 July 1997; accepted 14 March 1998
Abstract
There has been recent interest in the characterization of soil biodiversity and its function in agricultural grasslands. Much of
the interest has come from the need to develop grassland management strategies directed at manipulating the soil biota to
encourage a greater reliance on ecosystem self-regulation. This review summarises information on selected groups of soil
animals in grasslands, the factors in¯uencing their abundance, diversity and community structure and their relationships to the
functioning and stability of grassland ecosystems. Observations on the impacts of agricultural managements on populations
and communities of soil fauna and their interactions con®rm that high input, intensively managed systems tend to promote low
diversity while lower input systems conserve diversity. It is also evident that high input systems favour bacterial-pathways of
decomposition, dominated by labile substrates and opportunistic, bacterial-feeding fauna. In contrast, low-input systems
favour fungal-pathways with a more heterogeneous habitat and resource leading to domination by more persistent fungalfeeding fauna. In view of this, we suggest that low input grassland farming systems are optimal for increasing soil biotic
diversity and hence self-regulation of ecosystem function. Research is needed to test the hypothesis that soil biodiversity is
positively associated with stability, and to elucidate relationships between productivity, community integrity and functioning
of soil biotic communities. # 1998 Elsevier Science B.V.
Keywords: Collembola; Earthworms; Ecosystem processes; Fertilizer; Functional diversity; Land management; Livestock grazing;
Nematodes
1. Introduction
Grasslands, including steppes, savannas and prairies are important terrestrial ecosystems covering
about a quarter of the Earth's land surface. The
development of agriculture has been very closely
linked with these grassland systems in western Europe
where they form the backbone of the ruminant livestock industry. In the UK for example, approximately
*Corresponding author. Tel.: +44 1970 828255; fax: +44 1970
828357; e-mail: [email protected]
0929-1393/98/$19.00 # 1998 Elsevier Science B.V. All rights reserved.
PII S0929-1393(98)00125-5
50% of the land area comprises agricultural grassland
with rough and hill grazings, permanent grazings and
temporary silage grasslands completely dominating
the landscape of much of western and northern Britain
(Gordon and Duncan, 1994).
Grasslands build soil systems different from those
of forests and other vegetation types, even from the
same parent material. A key feature of grasslands is
their high turnover of shoot and root biomass, and
consequent large pool of labile organic matter at the
soil surface. In contrast to many terrestrial ecosystems, heavy herbivore loads are also a characteristic
264
R.D. Bardgett, R. Cook / Applied Soil Ecology 10 (1998) 263±276
feature of grasslands. This signi®cantly in¯uences
plant growth and species composition of grassland,
since herbivores consume as much as half the annual
above-ground net primary production and one fourth
or more of annual below-ground net primary production (Detling, 1988). As a result of these relatively
high rates of consumption, it has been suggested that
the structure of grasslands is the result of numerous
interactions, many of which are either direct effects of,
or mediated by, herbivores (McNaughton, 1983). Herbivores also have a profound in¯uence on nutrient
pathways in grasslands by short cutting both litter
return and soil recycling processes; a large percentage
of nutrients taken up by plants in grazing ecosystems
is cycled directly through animal excreta, resulting in
accelerated soil incorporation, particularly of nitrogen
and phosphorus (Ruess and McNaughton, 1987).
Therefore, soils of grazed grasslands tend to have
small amounts of dead litter on the soil surface but
have large amounts of organic nitrogen and carbon
(Bardgett, 1996). These features combine to produce a
soil environment that sustains an abundant and diverse
faunal and microbial community.
There has been much recent interest in the characterization of soil biodiversity and its function in
agricultural grasslands (see Bardgett, 1996). Much of
this interest has come from the need to develop grassland management strategies directed at manipulating
the soil biota to encourage a greater reliance on
ecosystem self-regulation than on arti®cial inputs such
as fertilizers and pesticides (Yeates et al., 1997). We
are investigating the effects of some of these key
changes in management on the populations and communities of some soil animals in grassland with a view
to determining how changes in these may be related to
changes in the grassland ecosystem and its functioning, through the interactions between animals and
micro¯ora. In this review, we give an account of
information on the more abundant faunal groups in
temperate grasslands, especially microarthropods and
nematodes. We have not dealt with protozoa in our
work and extensive information on the larger fauna is
widely available (Edwards and Bohlen, 1996). For
nematodes and microarthropods, we consider; (1) the
factors in¯uencing their abundance, diversity and
community structure; (2) their importance in terms
of the functioning and stability of grassland systems;
and (3) future directions for research. This review may
contribute to a mechanistic understanding of the
important processes and stability of grassland ecosystems.
2. The diversity of soil animals in grasslands
The diversity of fauna in grassland soils is very rich.
In general, the nematodes, microarthropods and annelids are the most abundant in terms of both number and
biomass. As in all ecosystems, soil organisms are
classi®ed by width into macrofauna (greater than
2 mm diameter), mesofauna (between 100 mm and
2 mm diameter) and microfauna (less than 100 mm
diameter). This section of the review will focus on one
important group of organisms within each of these
three categories, namely earthworms, microarthropods and nematodes, respectively. Other soil animals,
including species of insects and nematodes which
have particular importance as pests of agricultural
grassland plants have been considered elsewhere
(Clements and Cook, 1997; Cook and Yeates, 1993).
2.1. Macrofauna ± earthworms
The summary of density and biomass of grassland
soil fauna (Table 1) shows that the Lumbricidae form
the greatest biomass (70±80% of the total) of the
animals of temperate grasslands. Densities of the order
of 60±150 mÿ2 have been recorded in highly productive lowland pastures (Yeates et al., 1997) to as high as
400±500 mÿ2 in soils of limestone and other grasslands (Svendsen, 1957; Coulson and Whittaker, 1978).
However, much lower earthworm densities of 5±
10 mÿ2 have been recorded in acidic, upland grassland
soils in the UK (Bardgett et al., 1993a). The number of
species in a given grassland earthworm community
ranges from 1 to 15, but most communities contain
around 3 to 6 species (Edwards and Bohlen, 1996).
Several schemes have classi®ed earthworms into
major ecological groups, based mainly on differences
among species in burrowing and feeding activities,
and vertical strati®cation in soil. Perhaps the most
widely used classi®cation is that of Bouche (1977)
who recognized three major ecological groups of
earthworms: (1) epigeics, which feed on decomposing
plant material in the litter layer; (2) anecics, which
form permanent or semi-permanent vertical burrows,
R.D. Bardgett, R. Cook / Applied Soil Ecology 10 (1998) 263±276
265
Table 1
The mean population density (numbers mÿ2) and mean biomass (g mÿ2 dw) of animals in different grassland soils in UK and Ireland
Group
Limestone grassland1
ÿ2)
Lumbricidae
Enchytraeidae
Nematoda
Collembola
Acarina
Tipulidae
Acid, upland grassland1
ÿ2
ÿ2
Lowland grasslands
ÿ2
Density (n m
Biomass (g m )
Density (n m )
Biomass (n m )
Density2 (n mÿ2)
Density3 (n mÿ2)
390
80 000
3 300 000
46 000
33 000
120
23.2
4.1
0.14
0.15
0.35
4.1
4
200 000
3 900 000
23 000
45 000
2 500
0.04
4.60
0.18
0.05
0.32
1.96
360
5 800
34 000
105 000
106 000
60±150
6 500
4 000 000
5 400
114 000
Source of information: 1Coulson and Whittaker (1978); 2Curry, 1969; 3Yeates et al., 1997.
and feed primarily on decomposing plant material
pulled downwards from the litter layer; and (3) endogeics, which inhabit the mineral soil horizons and
consume soil and obtain nourishment from humi®ed
organic matter. In temperate grasslands, without a
distinctive litter layer, the majority of species
(approximately 70%) are anecic and only a small
proportion are epigeic, or surface dwelling (Lavelle,
1983).
2.2. Mesofauna ± microarthropods
Numerically, microarthropods (Collembola, Acari
and Protura) are the most abundant non-aquatic faunal
groups in soils of most ecosystems. Recorded densities of soil microarthropods are as high as
300 000 mÿ2 in old, permanent grasslands with dense
root systems and high organic matter content. In
contrast, densities as low as 50 000 mÿ2 have been
recorded in soils of temperate acidic grasslands and
semi-arid grassland (Bardgett and Grif®ths, 1997).
Collembola (springtails) and Acari (mites) usually
account for up to 95% of total numbers of microarthropods (Seastedt, 1984). In temperate grasslands, the
biomass of mites and springtails is often reported to be
similar, whereas in tropical grasslands the biomass of
mites can be two to ®ve times that of springtails
(Petersen and Luxton, 1982; Bardgett and Grif®ths,
1997).
In terms of species diversity, Siepel and van de
Bund (1988) reported that there were up to 108 species
of microarthropods in 500 cm2 soil of an unmanaged
Dutch grassland. Assuming everyone of these has an
unique niche, according to the hypervolume model
(Hutchinson, 1957) and that competitive exclusion
reduces niche overlap (Hardin, 1960), this implies
tremendous variation in resources in soil (Siepel,
1994). This vast diversity, moreover, is subject to
considerable spatial and temporal variation. Direct
observation of microarthropods in rhizotrons (exposed
in situ soil sections) has shown densities at least twice
as high around roots as in the bulk soil (Lussenhop,
1992). With respect to seasonal variation, microarthropod numbers in grasslands tend to be greatest in
summer and lowest in winter (King and Hutchinson,
1976; Bardgett et al., 1993a). In general, seasonal
variations are related to soil moisture status, temperature and availability of plant residues, and rapid
increases in microarthropod numbers are not uncommon in the surface soil after episodic rainfall events
(Greenslade, 1981).
Numbers of microarthropods are generally greater
in the surface soil than in lower horizons. In a range of
upland grassland soils, Bardgett et al. (1993a) found
that 92±98% of Acari and Collembola were extracted
from the upper 0±2 cm soil, which included the litter
layer. Other studies have also shown that active microarthropods tend to concentrate in the upper soil horizons and litter layer (e.g. Hutson and Veitch, 1983)
and only certain microarthropod groups, such as the
Prostigmata (Acari) are found at greater depths (Perdue and Crossley, 1990). The species composition of
the microarthropod community is also strongly in¯uenced by soil depth. Two morphological types of
microarthropods which dwell at different depths in
the soil can be differentiated (Wallwork, 1976). In
general, larger more active genera, adapted to an open
and often dry habitat, predominate in the surface soil
and/or litter layer. These genera (e.g. Collembola of
the genera Entomobrya and Tomocerus, and Acari
266
R.D. Bardgett, R. Cook / Applied Soil Ecology 10 (1998) 263±276
(Hermannia) can withstand desiccation, and have
strong pigmentation, well-developed eyes and long
appendages. At greater soil depth, genera are generally smaller, weakly pigmented, often lack eyes and
have soft bodies with short appendages, e.g. the
collembolans Onychiurus and Tullbergiinae, and the
smaller forms of cryptostigmatid or oribatid mites.
As with most soil faunal groups, microarthropods of
grassland soils occupy all trophic categories of belowground detritus food-webs (Moore et al., 1988). However, most microarthropods in grassland soils can be
regarded as either microphages, feeding on soil micro¯ora (fungi, bacteria, actinomycetes and algae) and/or
as detritivores, scavenging dead organic matter and
plant litter (Bardgett et al., 1993c). Microarthropods
have been calculated to obtain 51% of their energy
from the bacterial pathway and 26% and 24% from the
fungal and root pathways in shortgrass steppe in North
America (Moore et al., 1988). Some microarthropods
are also known to be predators e.g. certain prostigmatic mites and carnivorous Collembola (Isotoma
sp.), the latter feeding on rotifers and eggs of nematodes (Wallwork, 1976). An extensive review of the
feeding biology of microarthropods has been prepared
(Petersen and Luxton, 1982).
2.3. Microfauna ± nematodes
Nematodes are very abundant in grassland soils,
where population densities can be as high as 10
million mÿ2 in highly productive lowland grasslands
(Yeates et al., 1997) or as low as 1 million mÿ2 in
acidic, infertile upland grassland soils (Bardgett et al.,
1997a) and blanket bog (Coulson and Whittaker,
1978). Yeates et al. (1997) recognized 75 taxa in
Welsh lowland grasslands and Hodda and Wanless
(1994a) some 154 species in English chalk grassland.
However, in both of these studies only a proportion of
these taxa and species were present in individual
replicate samples. Nematode families can be allocated
to different feeding groups from knowledge of the
relationship between feeding and mouth and gut morphology (Yeates et al., 1993). In temperate agricultural
grassland, nematode populations are dominated by
plant-feeders with bacterial feeders also abundant
(Fig. 1). Omnivores and fungal-feeders are usually
similar, smaller proportions of the total nematode
population and predators the least abundant. Three
grassland studies in Britain have shown differences
between the feeding groups in taxonomic diversity,
with less diversity relative to abundance in plantfeeding and fungal-feeding nematodes than in other
trophic groups (Fig. 1). Occurrence of the different
trophic groups is subject to considerable spatial variation. In chalk grassland, fungal-feeding species were
widespread but only a few species occurred commonly
in samples; omnivores/predators occurred less frequently per sample; bacterial feeders were more uniformly distributed than the plant feeders which were
very aggregated (Hodda and Wanless, 1994a, b).
Nematode populations may be described by both
traditional and speci®c indices to show responses
which may characterise anthropogenic impacts on
grassland soils. Yeates (1982) applied traditional
population indices to pasture nematode populations
and concluded that the use of supraspeci®c taxa was
valid since, even at speci®c level, most taxa could not
be allocated to practically de®ned niches. He concluded that the nematode fauna represents the sum of
numerous populations, being neither a community of
interacting species nor a guild of species exploiting a
resource. The nematode fauna interacts with other
biota over a range of trophic levels and a variety of
food webs, in¯uencing energy and nutrient ¯ows. This
approach is supported by the conclusions that indices
of nematode taxonomic richness, diversity, trophic
diversity and trophic structure do not show differences
between systems, although they may contribute to
understanding food web and ecosystem processes
(Freckman and Ettema, 1993).
The maturity index (Bongers, 1990; Korthals et al.,
1996) weights nematode species mean abundance by
colonizer-persister (c-p) scale, related to r and K life
strategies. This has been used to distinguish nematode
population response to disturbance (e.g. tillage, manuring, and toxic impacts of xenobiotics). The MI index
re¯ects the maturation of communities. Two types of
responses of nematode populations may lower the MI
value, type I when taxa with low c-p values
(ˆcolonisers) increase and others do not and, type
II when taxa with high c-p values (persisters) decrease
disproportionately more than others. Type I examples
seem to relate to increased nutrient availability as a
result of temporally increased microbial activity and
type II responses, which have been less often documented, may re¯ect long term toxicity and low food
R.D. Bardgett, R. Cook / Applied Soil Ecology 10 (1998) 263±276
267
Fig. 1. The relationship between relative abundance (% all nematodes) and the proportion of taxa in four trophic groupings of nematodes from
three types of grassland. Data from permanent grassland (~ and, Yuen, 1966); chalk grassland (^ and, Hodda and Wanless, 1994a and Hodda
and Wanless, 1994b, b) and grazed pastures (& and &, Yeates et al., 1997). Nematode groups: plant-feeding and plant-associated, pf;
bacterial-feeding, bf; omnivores and predators, o and p; fungal-feeding, ff.
availability. Because increases in c-p1 taxa may follow eutrophication in stressed and unstressed systems
leading to an increased MI in both cases it has been
suggested that omitting c-p1 taxa will give a more
useful index of nematode population responses
(Korthals et al., 1996). Comparison of the original
MI and MI2-5 may also discriminate between stress
responses. More detailed examination of the responses
of the different taxa is needed both experimentally and
by community analysis to visualise the shifts in pro-
portions of the coloniser/persister species (de Goede et
al., 1993; Korthals et al., 1996).
3. The effects of land management on animal
diversity in grasslands
Land management affects soil animal populations
by: (1) altering the quality and quantity of detritus and
non-detritus inputs, and; (2) by in¯uencing the soil
268
R.D. Bardgett, R. Cook / Applied Soil Ecology 10 (1998) 263±276
microhabitat in terms of soil physical and chemical
qualities. The diversity of feeding habits and habitat
preferences of soil fauna in grasslands implies that
responses to management will be complex and may be
limited to various speci®c groups of organisms. In
grasslands, the key management variables that
strongly in¯uence the above soil properties are the
application of fertilizers (organic and inorganic) and
the activities of grazing ruminant livestock. In managed grasslands however, it is often dif®cult to separate the response of the soil fauna to these
management variables, since changes in the two often
occur together i.e. increased fertilizer use increases
herbage production and hence livestock stocking densities. However, certain generalizations can be made
by a `systems' approach to understanding the effects
of management intensity on soil faunal diversity. We
will illustrate the effects of grassland management on
two key faunal groups, the nematodes and microarthropods, by reference to our work and other studies
on: (1) effects of changes in livestock stocking density; (2) effects of fertilizer application to grassland,
and; (3) effects of changes in broad-scale management
from intensive to less intensive, or organically managed grassland systems. Effects of pesticides and
tillage on soil fauna will not be considered since these
are not normal management practices in grassland
systems.
3.1. Effects of livestock grazing
Changes in livestock grazing pressure substantially
modify the environment for soil and litter inhabiting
microarthropods and nematodes, affecting their abundance, diversity and spatial distribution. For example,
increased sheep stocking density on an Australian
pasture (10, 20, 30 sheep haÿ1) severely reduced
numbers of Collembola in the surface soil (King
and Hutchinson, 1976; King et al., 1976). Likewise,
reductions in Collembola numbers were associated
with increased sheep stocking density of a lowland
perennial ryegrass (Lolium perenne) grassland (Walsingham, 1976). These responses were attributed to
changes in soil pore space and surface litter, both of
which were reduced with increased sheep grazing
intensity. Much of the activity of soil microfauna is
also controlled directly by available pore space and
this is affected by a number of management practices,
such as livestock grazing, as well as intrinsic soil
characteristics.
Studies by Bardgett et al. (1993a) of sheep-grazed
upland grasslands presented a different story. Numbers of Collembola and Acari in the surface soil were
found to decline along a gradient towards less sheep
grazing. In the same study, the short- and long-term
cessation of sheep grazing on a wide range of upland
grassland types, resulted in signi®cant reductions in
the abundance of total Collembola and the dominant
collembolan species Onychiurus procampatus
(Fig. 2). Similar responses of nematode fauna of
upland grasslands to cessation of livestock grazing
were reported by Bardgett et al. (1997a) (Fig. 3) when
reductions in nematode abundance in ungrazed grasslands were related to quantitative and qualitative
changes in available food resources. In particular,
an associated reduction in microbial abundance was
thought to suppress populations of microbial-feeding
nematodes in ungrazed grassland. This suggestion is
in agreement with Freckman et al. (1979) who also
found that numbers of nematodes, in particular bacterial-feeders, were higher in grazed than ungrazed
annual grassland. This effect has been attributed to
reductions in the abundance of soil micro-organisms,
which in turn are related to decreased soil temperature
and moisture content (Freckman et al., 1979), and to
the removal of extra N from animal excreta. Changes
in root biomass (Sohlenius et al., 1987) and reductions
in the input of plant litter (King and Hutchinson, 1983)
have also been shown to in¯uence nematode abundance in ungrazed grassland soils.
There is evidence that root-feeding and other soil
fauna may be indirectly affected by above-ground
grazing through herbivore effects on patterns of root
exudation and plant carbon allocation. Ingham and
Detling (1984), studying a North American prairie,
reported that root-feeding nematodes consumed 5±
25% annual below-ground net primary production and
were more abundant in grazed than ungrazed areas.
Subsequent laboratory studies (Ingham and Detling,
1986) provided strong evidence that these changes
were related to enhanced C allocation to the roots of
defoliated Bouteloua curtipendula. It was hypothesised that this would lead to increased rates of root
exudation (low molecular weight C compounds, secretions, polysaccharide mucilages and lysate) which in
turn represents a high-quality nutrient source for the
R.D. Bardgett, R. Cook / Applied Soil Ecology 10 (1998) 263±276
269
Fig. 2. The effects of removing sheep grazing for 2 years (G, grazed; U, ungrazed) on the abundance (mean number mÿ2 SE) of (a) total
Collembola, and (b) the fungal-feeding collembolan Onychiurus procampatus in the surface soil of four upland grassland sites, representing a
gradient of sheep management intensity, in Cumbria, UK;*,***ˆP<0.05, P<0.001, respectively; nˆ5. (After Bardgett et al., 1993a).
growth and maintenance of rhizosphere organisms,
including microfauna. Increases in root exudation
linked to both plant defoliation and to enhanced
below-ground herivory by root-feeding nematodes
(Yeates et al., 1997) have recently been shown to
increase rhizosphere microbial biomass and activity
and, presumably, microbial-feeding microfauna.
Further studies are required to assess the generality
of these ®ndings with respect to both plant and
nematode species variation.
3.2. Effects of fertilizer applications
The application of both organic and inorganic
fertilizers to grasslands has been shown to affect
microarthropods and nematode populations. Additions of nitrogenous fertilizers to organic grassland
soils increased total Collembola numbers by some
65% (Coulson and Butter®eld, 1978). Likewise, Bardgett et al. (1993a) found twice as many Collembola
and mites in the surface soil of a fertilised (NPK)
upland grassland as in adjacent unfertilized grassland. Increases in microarthropod numbers on
application of phosphate (King and Hutchinson,
1980) and nitrogenous fertilisers (Edwards and Lofty,
1969) to lowland temperate grasslands have also been
reported.
Negative effects of inorganic fertilisers have also
been reported. The abundance and species diversity of
microarthropods declined following the application of
nitrogenous fertiliser to grassland (Siepel and van de
Bund, 1988). These authors also reported changes in
microarthropod community structure with fertilisers
reducing the proportion of euedaphic collembolans in
favour of hemiedaphic and especially epedaphic
forms. At high fertilizer levels, mite species with
longer life cycles were also less abundant and phoretic
species, with short generation times, more abundant.
It is widely reported that the application of organic
manures to grassland increases nematode numbers,
due to increased substrate availability, plant growth
and altered soil conditions (Bardgett and Grif®ths,
1997). These effects can also be highly irregular, both
spatially and temporally; hot spots of buried plant
material were found to produce rich habitats for
nematodes with up to 3000 gÿ1 dry matter (Grif®ths
et al., 1991), but responses varied with the characteristics of the organic manures. Inorganic fertilisers also
have variable effects, with reports of both reduced
(Sohlenius and Wasilewska, 1984) and enhanced
270
R.D. Bardgett, R. Cook / Applied Soil Ecology 10 (1998) 263±276
Fig. 3. Seasonal variation in numbers of nematodes (mean number
mÿ2104 SE) in grazed and ungrazed (37 years) plots of two
upland grasslands types at Llyn Llydaw and Cwm Idwal,
Snowdonia, UK. The two grassland types are (1) Agrostis-Festuca
on brown earth soils, and (2) Nardus-dominant on acidic podzolic
soils. *,**,*** ˆ P<0.05, P<0.01, P<0.001, respectively (nˆ4).
(After Bardgett et al., 1997a).
nematode populations (Beare et al., 1989; Sohlenius
et al., 1987).
3.3. Management systems
As previously mentioned, the effects of individual
management inputs to grassland on soil fauna are
dif®cult to separate from one another. In view of this,
most research has focused on general shifts in faunal
diversity in response to changes in management systems, for example from an intensive fertilized grassland system to an organic grassland system with no
fertilizer inputs and lower stocking densities.
Generally, nematode faunal diversity increases as
management inputs decrease, largely due to a positive
impact of low-input management on the diversity of
the ecosystem and detrital inputs. For example, Wasilewska (1995) showed that a ¯oristically diverse community of six grass species, representative of a lowinput grassland system, encouraged a more mature
stage of nematode succession compared with a cocksfoot (Dactylis glomerata) monoculture which had a
greater proportion of plant feeders. The greater
diversity of nematodes was related to the increased
diversity of available food resources of plant roots and
litter inputs into soil under mixed species of grass.
Similarly, Siepel (1996) found that the density and
species diversity of microarthropods was approximately twice as high in low-input as in high-input
grassland sites. The microarthropod community of
low-input sites was dominated by fungivorous grazers,
whereas in the high-input sites these organisms were
largely absent being replaced by bacteriovores. The
microarthropod community of the high-input sites also
consisted of very opportunistic species with sexual
reproduction and good dispersal capacities (i.e.
r-strategists).
These ®ndings also relate well to those of Yeates et
al., (1997) who compared intensively managed grasslands with adjacent sites on the same parent material,
that had been managed under organic prescriptions
(i.e. no inorganic fertilizers) for several years. Nematode populations were larger in the organically-managed grassland systems and fungal-feeders were twice
as abundant as in conventionally managed soils
(Fig. 4). This change was also mirrored in a shift in
the soil microbial community towards fungal dominance (Yeates et al., 1997). Taxonomic diversity
relationships were not affected by these management
differences, except that there were relatively more
omnivore taxa in organic systems (Fig. 4).
Maturity indices, calculated from these population
data (Yeates and Cook, 1997) for various subsets of
nematodes show some of the impacts of management
as well as site (soil texture) effects (Fig. 5). Indices are
higher (that is indicative of more mature populations)
in organic systems, a phenomenon better shown by
non-plant feeding, fungal feeding and all microbial
feeding nematodes. When r-strategists (c-p 1) were
excluded these differences disappeared, emphasising
the conclusion that these respond to nutrient enrichment in the conventionally-fertilized sites (Fig. 5,
Korthals et al., 1996).
R.D. Bardgett, R. Cook / Applied Soil Ecology 10 (1998) 263±276
271
Fig. 4. Relative abundance and taxonomic composition of trophic groups in nematode populations from grassland systems managed
conventionally or organically; }, predators; ~, fungal feeders; &, omnivores; ^, bacterial feeders; &, plant feeders).
Fig. 5. Maturity indices for nematode populations and groups in grassland on three soil textures under contrasting conventional (conv) and
organic (org) managements (data from Yeates and Cook, 1997).
The above changes appear to corroborate the existence of bacterial- and fungal-based compartments
(sensu Moore et al., 1996) in soil communities of
managed grasslands. Intensively managed grasslands
appear to correspond to the `fast cycle' dominated by
labile substrates and bacteria, while less productive,
organically fertilized grasslands relate to the `slow
cycle' dominated by more resistant substrates and
fungi (Coleman et al., 1983). There is some indication
that the two extremes may promote different levels of
diversity in soil fauna; if `slow' cycles have greater
heterogeneity in organic substrates and successional
272
R.D. Bardgett, R. Cook / Applied Soil Ecology 10 (1998) 263±276
decomposition, they would favour a more diverse soil
community, whereas `fast' cycles, dominated by inorganic nutrients which may reduce the number and
complexity of available resources (e.g. less plant
species diversity and reduced application of organic
manures), would promote a fast growing faunal and
microbial community of limited diversity. Such
changes are broadly consistent with those during
successional development of an ecosystem (Odum,
1969, 1985) when larger organisms become dominant
during succession and maturation. Fungi are several
orders of magnitude larger than bacteria (Swift et al.,
1979). In grasslands, therefore, shifts from bacterial to
fungal pathways in less intensively managed systems
are likely to be related to the development of ecosystem complexity during succession, in particular
increased build-up and conservation of soil nutrients.
This may contribute to increased ef®ciency and order
of a more stable ecosystem.
In above-ground plant and animal communities,
hump-backed relationships (Fig. 6) are found between
species diversity and disturbance or between diversity
and productivity (Grime, 1979). Such relationships are
likely to apply to soil biotic responses to environmental gradients (Wardle and Giller, 1997). In grasslands systems where management has been removed,
it is evident that highly stable, uniform environments
with abundant resources favour dominance of particularly competitive species, that is, competitive exclusion (sensu Grime, 1979; Austin, 1987). Changes in
management intensity lead to changed soil environmental conditions, expressed as stress. Studies of the
soil fauna of grasslands where agricultural management has been removed (Bardgett et al., 1993a; Freckman et al., 1979), or is absent (Ingham and Detling,
1984) indicate a hump-backed relationship between
species diversity and abundance and agricultural disturbance. Moderate stress, such as in organically
managed, low-input systems, may reduce the likelihood of competitive exclusion and allow other
organisms to proliferate. At the other extreme, severe
stress imposed by intensive agriculture clearly leads to
a reduction in soil faunal diversity (Fig. 6).
In view of the above, low-input systems may be
analagous to some intermediate point in a community
succession, resulting in a compromise between youth
and maturity. Such a state may be maintained or
enhanced by short-term pertubations or regular
resource pulses associated with application of manures from grazing animals and/or other sources. Such
systems are often referred to as pulse-stabilized subclimaxes sensu Odum (1969), that is, a developmental
stage below, or short of, the climax that would develop
in the absence of a pertubation. If such relationships
do hold true, then low-input farming systems may be
optimal for an increase in soil biotic diversity and
hence self-regulation of ecosystem function. The
removal of management altogether, however, may
be the worst management system for maintaining soil
biodiversity.
4. Functional implications of changes in faunal
diversity
Fig. 6. Hypothetical model of the effects of management intensity
on the diversity of soil fauna in agricultural grasslands. Where the
stress is mild, such as in ungrazed grasslands, it is hypothesized
that competitive species can predominate resulting in a lack of
diversity. When stress increases, in the form of agricultural
management, these species lose competitive advantage and more
species can proliferate. At high levels of stress, associated with
intensive grassland farming, progressive extinction of species leads
to a loss of diversity.
Although the contribution of fauna to total soil
respiration is low (Petersen and Luxton, 1982), it is
becoming increasingly apparent that soil animals have
a profound impact on soil processes through their
in¯uence on the composition and activity of the soil
micro¯ora. Several microcosm studies of grassland
systems have shown that the presence of soil animals,
such as nematodes or Collembola, can directly affect
the biomass and activity of the microbial community
R.D. Bardgett, R. Cook / Applied Soil Ecology 10 (1998) 263±276
through feeding on fungi and bacteria (e.g. Bakonyi,
1989; Bardgett et al., 1993a, b) or indirectly by
comminution of organic matter, dissemination of
microbial propagules, and the alteration of nutrient
availability (as reviewed by Grif®ths and Bardgett,
1997). Indeed, the action of invertebrates generally
leads to an increase in nutrient availability as a result
of increased soil microbial activity and the excretion
of excess ingested nutrients that are no longer required
for production (e.g. 90% of ingested N by nematodes
is not used and is excreted into the soil environment).
Such increases in nutrient availability have been
linked to plant productivity, and studies have shown
that plants grown in the presence of microbial-feeding
nematodes contain more N than plants grown in their
absence (Ingham et al., 1985). Such links have not
been demonstrated for microarthropods in grassland
soils, but evidence from studies of forest ecosystems
suggests that their feeding-activities are likely to
enhance nutrient availability in grassland ecosystems
(e.g. Ineson et al., 1982).
The above studies, however, have been concerned
with understanding the impacts of particular species or
trophic groups of animals on soil processes; based
largely on presence or absence. They do not address
the question of the importance of soil animal biodiversity in the functioning of grassland or other ecosystems. Soil ecosystems contain many speci®c
interactions at different spatial and temporal scales
within food webs. Studies of food-web complexity in
grassland systems have been conducted in relation to
system stability and nutrient cycling (e.g. de Ruiter et
al., 1994, 1995). These studies rely on the aggregation
of species into functional groups i.e. based on food
choice and life history parameters (sensu Moore et al.,
1988). In doing so, therefore, they do not consider the
importance of the taxonomic composition within each
functional group in relation to the degree of species
redundancy. In addition, it is becoming increasingly
apparent that static patterns of food web assembly are
sensitive to the number of taxa in each functional
group; webs with different numbers of species may
work in subtly different ways (Lawton and Brown,
1994). Despite these limitations, many of which are
inherent to the study of soil communities, these studies
have greatly progressed our understanding of the
importance of complexity in soil communities in
relation to ecosystem functions.
273
In our opinion, the central question to be addressed
is how soil biodiversity in¯uences the stability of soil
ecosystems ± both in terms of their structure and their
function. A large body of literature has accumulated
on the importance of diversity±stability relationships
in above-ground plant and animal communities and it
is evident that the hypotheses provided for aboveground communities are equally applicable below
ground (Wardle and Giller, 1997). The central hypothesis of these studies (e.g. McNaughton, 1988; Pimm,
1984) is that more diverse, or complex systems are: (1)
more resistant, i.e. better able to maintain a state in a
¯uctuating environment and (2) more resilient, i.e.
better able to return to a ground state when displaced
(McNaughton, 1994). There is growing empirical
evidence to support this hypothesis when considering
the productivity of plant communities (McNaughton,
1977, 1985; Frank and McNaughton, 1991; Tilman,
1996; Naeem et al., 1995) and clearly similar information is urgently required if we are to answer the
question ± how does soil biodiversity in¯uence the
function of grassland and other ecosystems?
5. Conclusions
From this review, it is clear that soils from grassland
systems contain an abundant and diverse fauna, much
of which has been characterized for a range of natural
and managed grassland ecosystems. Agricultural
management is a common feature of grassland systems, particularly in western Europe, and an increasing body of information is accumulating on how
various management practices common to grassland
systems affect both the abundance and diversity of soil
faunal communities and populations. In general,
intensive management of grassland, with large inputs
of inorganic fertilizers and livestock stocking densities
impacts negatively on the diversity, but not necessarily
the density of soil fauna. These management systems
tend to favour opportunistic, bacterial-feeding fauna
with sexual reproduction and good dispersal capacities
(i.e. r-strategists). They are also characterized as
having `fast' cycles dominated by labile substrates
and bacterial decomposition pathways. In contrast,
low-input systems with a more heterogeneous habitat
and resource, contain a more diverse fauna, characterized by species that are more persistent and, in gen-
274
R.D. Bardgett, R. Cook / Applied Soil Ecology 10 (1998) 263±276
eral, fungal-feeders. Such systems are characterized
by `slow' cycles, dominated by more resistant substrates and fungal decomposition pathways. Although
relatively little information is available on the diversity of fauna in unmanaged grasslands, evidence
points to a reduced density and diversity of fauna in
these soils.
The above changes in fauna along management
gradients suggest that, as with other plant and animal
communities, a hump-backed relationship between
species diversity and abundance, and disturbance
may occur (sensu Grime, 1979). This review suggests
that a highly stable, uniform environment with abundant resources, such as an unmanaged grassland,
favours dominance of particularly competitive species, forcing competitive exclusion. Moderate stress,
however, such as in organically managed, low-input
systems, may reduce the likelihood of competitive
exclusion and allow other organisms to proliferate. At
the other extreme, severe stress imposed by intensive
agriculture clearly leads to a reduction in soil faunal
diversity. On the basis of this information, we suggest
that low-input farming systems are optimal for an
increase in soil biotic diversity and hence self-regulation of ecosystem function.
This review highlights the wealth of information
concerning the functional importance of individual
species or functional groups of soil fauna in grassland
systems. However, there is a lack of information about
the functional importance of faunal biodiversity, in
terms of faunal complexity, in grassland soils. We
recommend that future studies should consider the
role of soil faunal diversity in terms of diversity±
stability relationships (sensu Pimm, 1984; McNaughton, 1988). Such studies are in accordance with
those of above-ground communities and will provide
simple experimental systems to assess the importance
of soil faunal and microbial diversity in terms of a
changing environment ± i.e. its resistance and resilience to environmental change. In particular, research
should address the central hypothesis that soil biodiversity is positively associated with the stability,
measured in terms of the productivity, community
integrity and function, of soil biotic communities.
An understanding of these relationships is essential
if we are to project the role of biodiversity as a
contributor to preserving ecosystems in a changing
environment.
Acknowledgements
We acknowledge funding from: UK Ministry of
Agriculture Fisheries and Food; Biotechnology and
Biological Sciences Research Council; Scottish Of®ce
for Environment, Agriculture and Food; and EU Contract ERB ENV4-CT 95 0017. We are also grateful to
many colleagues present at the Soil Biodiversity
Workshop held at Schloss Rauischholzhausen, University of Giessen, Germany 1996 for their discussions
and to Lijbert Brussaard, Tryggve Persson and Wim
van der Putten for their helpful comments on this
paper.
References
Austin, M.P., 1987. Models for the analysis of species' response to
environmental gradients. Vegetation 69, 35±45.
Bakonyi, G., 1989. Effects of Folsomia candida (Collembola) on
the microbial biomass of a grassland soil. Biol. Fertil. Soils 7,
138±141.
Bardgett, R.D., 1996. Potential effects on the soil mycoflora of
changes in the UK agricultural policy for upland grasslands. In:
Frankland, J.C., Magan, N., Gadd, G.M. (Eds.), Fungi and
Environmental Change. British Mycological Society Symposium, Cambridge University Press, pp. 163±183.
Bardgett, R.D. and Griffiths, B., 1997. Ecology and biology of soil
protozoa, nematodes and microarthropods. In: van Elsas, J.D.,
Wellington, E., Trevors, J.T. (Eds.), Modern Soil Microbiology.
Marcell Dekker, New York, in press.
Bardgett, R.D., Frankland, J.C. and Whittaker, J.B., 1993a. The
effects of agricultural practices on the soil biota of some upland
grasslands. Agric. Ecosyst. and Environ. 45, 25±45.
Bardgett, R.D., Whittaker, J.B., Frankland, J.C., 1993b. The effect
of collembolan grazing on fungal activity in differently
managed upland pastures ± a microcosm study. Biol. Fertil.
Soils 16, 255±262.
Bardgett, R.D., Whittaker, J.B., Frankland, J.C., 1993c. The diet
and food preferences of Onychiurus procampatus (Collembola)
from upland grassland soils. Biol. Fertil. Soils 16, 296±298.
Bardgett, R.D., Leemans, D.K., Cook, R., Hobbs, P.J., 1997a.
Seasonality of soil biota of grazed and ungrazed hill grasslands.
Soil Biol. Biochem., in press.
Bardgett, R.D., Keiller, S., Cook, R., Gilburn, A., 1997b. Dynamic
interactions between microorganisms and fauna in upland
grassland soils amended with sheep dung ± a microcosm study.
Soil Biol. Biochem., in press.
Beare, M.H., Blair, J.M., Parmelee, R.W., 1989. Resource quality
and trophic responses to simulated throughfall: effects on
decomposition and nutrient flux in a no-tillage agroecosystem.
Soil Biol. Biochem. 21, 1027±1036.
Bongers, T., 1990. The Maturity Index: an ecological measure of
environmental disturbance based on nematode species composition. Oecologia 83, 14±19.
R.D. Bardgett, R. Cook / Applied Soil Ecology 10 (1998) 263±276
BoucheÂ, M.B., 1977. StrateÂgies lombriciennes. In: Lohm, U.,
Persson, T., (Eds.), Soil Organisms as Components of
Ecosystems. Ecological Bulletins, Stockholm, 25, pp. 122±132.
Clements, R.O., Cook, R., 1997. Pest damage to established grass
in the UK. Agric. Zool. Rev. 7, 157±179.
Coleman, D.C., Reid, C.P.P., Cole, C.V., 1983. Biological
strategies of nutrient cycles in soil systems. Adv. Ecol. Res.
13, 1±55.
Cook, R., Yeates, G.W., 1993. Nematode pests of grassland and
forage crops. In: Evans, K., Trudgill, D.L., Webster, J.M.
(Eds.), Plant Parasitic Nematodes in Temperate Agriculture.
CAB International, Wallingford, UK, pp. 305±350.
Coulson, J.C., Butterfield, J.E.L., 1978. An investigation of the
biotic factors determining the rates of plant decomposition on
blanket bog. J. Ecol. 66, 631±650.
Coulson, J.C. and Whittaker, J.B., 1978. Ecology of moorland
animals. In: Heal, O.W., Perkins, D.F. (Eds.), Production
Ecology of British Moors and Montane Grasslands. Springer,
London, pp. 52±93.
Curry, J.P., 1969. The qualitative and quantitative composition of
the fauna of an old grassland site at Celbridge Co. Kildare. .
Soil Biol. Biochem. 1, 221±227.
Detling, J.K., 1988. Grassland and savannas: regulation of energy
flow and nutrient cycling by herbivores. In: Pomeroy, L.R,
Alberts, J.J. (Eds.), Concepts of Ecosystem Ecology: A
Comparative View, pp. 131±148.
Edwards, C.A., Bohlen, P.J., 1996. Biology and Ecology of
Earthworms. 3rd ed. Chapman and Hall, London.
Edwards, C.A., Lofty, J.R., 1969. The influence of agricultural
practices on soil micro-arthropod populations. In: Sheal, J.R.
(Ed.), The Soil Ecosystem, Systematics Association, London,
pp 237±247.
Frank, D.A., McNaughton, S.J., 1991. Stability increases with
diversity in plant communities: empirical evidence from the
1988 Yellowstone drought. Oikos 62, 360±363.
Freckman, D.W., Duncan, D.A., Larson, J., 1979. Nematode
density and biomass in an annual grassland ecosystem. J. Range
Manage. 32, 418±422.
Freckman, D.W., Ettema, C.H., 1993. Assessing nematode
communities in agroecosystems of varying human intervention.
Agric. Ecosyst. Environ. 45, 239±261.
de Goede, R.G.M., Bongers, T., Ettema, C.H., 1993. Graphical
presentation and interpretation of nematode community structure:c-p triangles. Meded. Fac. Landbouwwet. Univ. Gent 58,
743±750.
Gordon, I.J., Duncan, P., 1994. Objectives for production and
conservation in grasslands: effect of large ungulates. In:
Haggar, R.J., Peel, S. (Eds.), Grassland management and nature
conservation. British Grassland Society Occasional Symposium
No. 28. British Grassland Society, pp. 20±32.
Greenslade, P., 1981. Survival of Collembola in arid environments:
observations in South Australia and the Sudan. J. Arid Environ.
4, 219±228.
Griffiths, B.S., Bardgett, R.D., 1997. Interactions between microbial feeding invertebrates and soil microorganisms. In: van
Elasas, J.D., Wellington, E., Trevors, J.T. (Eds.), Modern Soil
Microbiology. Marcell Dekker, New York, in press.
275
Griffiths, B.S., Young, I.M., Boag, B., 1991. Nematodes associated
with the rhizosphere of barley (Hordeum vulgare). Pedobiologia 35, 265±272.
Grime, J.P., 1979. Plant Strategies and Vegetation Processes. Wiley,
New York.
Hardin, G., 1960. The competitive exclusion principle. Science
131, 1292±1297.
Hodda, M., Wanless, F.R., 1994. Nematodes from an English chalk
grassland: species distribution. Nematologica 40, 116±132.
Hodda, M., Wanless, F.R., 1994. Nematodes from an English chalk
grassland: population ecology. Pedobiologia 38, 530±545.
Hutchinson, G.E., 1957. Concluding remarks. Cold Spring Harbour
Symp. Quant. Biol. 22, 415±427.
Hutson, B.R., Veitch, L.G., 1983. Mean annual population densities
of Collembola and Acari in the soil and litter of three
indigenous South Australian forests. Aust. J. Ecol. 8, 113±
126.
Ineson, P., Leonard, M.A., Anderson, J.M., 1982. Effect of
collembolan grazing upon nitrogen and cation leaching from
decomposing leaf litter. Soil Biol. Biochem. 14, 601±605.
Ingham, R.E., Detling, J.K., 1984. Plant-herbivore interactions in a
North American mixed-grass prairie III. Soil nematode
populations and root biomass on Cynomys ludovicianus
colonies and adjacent uncolonized areas. Oecologia 63(3±7),
313.
Ingham, R.E., Detling, J.K., 1986. Effects of defoliation and
nematdoe consumption on growth and leaf gas exchange in
Bouteloua curtipendula. Oikos 46, 23±28.
Ingham, R.E., Trofymow, J.A., Ingham, E., Coleman, D.C., 1985.
Interactions of bacteria, fungi, and their nematode grazers:
effects on nutrient cycling and plant growth. Ecol. Monogr. 55,
119±140.
King, L.K., Hutchinson, K.J., 1976. The effects of sheep stocking
intensity on the abundance and distribution of mesofauna in
pastures. J. Appl. Ecol. 13, 41±55.
King, L.K., Hutchinson, K.J., 1980. The effects of superphosphate
and stocking intensity on grassland microarthropods. J. Appl.
Ecol. 17, 581±591.
King, L.K., Hutchinson, K.J., 1983. The effects of sheep grazing on
invertebrate numbers and biomass in unfertilized natural
pastures of the New England Tablelands (NSW). Aust. J. Ecol.
8, 245±255.
King, L.K., Hutchinson, K.J., Greenslade, P., 1976. The effects of
sheep numbers on associations of Collembola in sown pastures.
J. Appl. Ecol. 13, 731±739.
Korthals, G.W., De Goede, R.G.M., Kammenga, J.E., Bongers, T.,
1996. In: Van Straalen, N.M., Krivolutsky, D.A. (Eds.),
Bioindicator Systems for Soil Pollution. Kluwer Academic,
Dordrecht, pp. 85±94.
Lavelle, P., 1983. The structure of earthworm communities. In:
Satchell, J.E. (Ed.), Earthworm Ecology from Darwin to
Vermiculture. Chapman and Hall, London, pp 449±466.
Lawton, J.H., Brown, V.K., 1994. Redundancy in ecosystems. In:
Schulze, E.D., Mooney, H.A. (Eds.) Biodiversity and Ecosystem Function. Springer, London, pp. 255±268.
Lussenhop, P., 1992. Mechanisms for microarthropod ± microbial
interactions. Adv. Ecol. Res. 23, 1±33.
276
R.D. Bardgett, R. Cook / Applied Soil Ecology 10 (1998) 263±276
McNaughton, S.J., 1977. Diversity and stability of ecological
communities: a comment on the role of empiricism in ecology.
Am. Nat. 111, 515±525.
McNaughton, S.J., 1983. Serengeti grassland ecology: the role of
composite environmental factors and contingency in community organization. Ecol. Monogr. 53, 291±320.
McNaughton, S.J., 1985. Ecology of grazing ecosystems: the
Serengeti. Ecol. Monogr. 55, 259±294.
McNaughton, S.J., 1988. Diversity and stability.. Nature (Lond.)
333, 204±205.
McNaughton, S.J., 1994. Biodiversity and function of grazing
ecosystems. In: Schulze, E.D., Mooney, H.A., (Eds.), Biodiversity and Ecosystem Function, Springer, London, pp. 361±
383.
Moore, J.C., Walter, D.E., Hunt, H.W., 1988. Arthropod regulation
of micro- and mesobiota in below-ground detrital food webs.
Annu. Rev. Entomol. 33, 419±439.
Moore, J.C., de Ruiter, P.C., Hunt, W.H., Coleman, D.C.,
Freckman, D.W., 1996. Microcosms and soil ecology: critical
linkages between field studies and modelling food-webs.
Ecology 77, 694±705.
Naeem, S., Thompson, L.J., Lawler, S., Lawton, J.H., Woodfin,
R.M., 1995. Empirical evidence that declining species diversity
may alter the performance of terrestrial ecosystems. Philos.
Trans. R. Soc. Lond. B Biol. Sci. 347, 249±262.
Odum, E.P., 1969. The strategy of ecosystem development. Science
Wash. D.C. 164, 262±270.
Odum, E.P., 1985. Trends expected in stressed ecosystems.
Bioscience 35, 419±422.
Perdue, J.C., Crossley, D.A., 1990. Vertical distribution of soil
mites (Acari) in conventional and no-tillage agricultural soils.
Biol. Fertil. Soils 9, 135±138.
Petersen, H., Luxton, M., 1982. A comparative analysis of soil
fauna populations and their role in decomposition processes.
Oikos 39, 287±388.
Pimm, S.L., 1984. The complexity and stability of ecosystems.
Nature (Lond.) 307, 321±326.
Ruess, R.W., McNaughton, S.J., 1987. Grazing and the dynamics
of nutrient and energy regulated microbial processes in the
Serengeti grasslands. Oikos 49, 101±110.
de Ruiter, P.C., Neutel, A.N., Moore, J.C., 1995. Energetics,
patterns of interaction strengths, and stability in real ecosystems. Science Wash. D.C. 269, 1257±1260.
de Ruiter, P.C., Neutel, A.N., Moore, J.C., 1994. Modelling food
webs and nutrient cycling in agro-ecosystems. Trends Ecol. and
Evol. 9, 378±383.
Seastedt, T.R., 1984. The role of microarthropods in decomposition and mineralization processes. Annu. Rev. Entomol. 29,
25±46.
Siepel, H., 1994. Structure and Function of Soil Microarthropod
Communities. Unpublished PhD Thesis, University Wageningen.
Siepel, H., 1996. Biodiversity of soil microarthropods: the filtering
of species. Biodivers. Conserv. 5, 251±260.
Siepel, H., van de Bund, C.F., 1988. The influence of management
practices on the microarthropod community of grassland.
Pedobiologia 31, 339±354.
Sohlenius, B., BostroÈm, S., Sandor, A., 1987. Long term dynamics
of nematode communities in arable soil under four cropping
systems. J. Appl. Ecol. 24, 131±144.
Sohlenius, B., Wasilewska, L., 1984. Influence if irrigation and
fertilization on the nematode community in a Swedish pine
forest soil. J. Appl. Ecol. 21, 327±342.
Svendsen, J.A., 1957. The distribution of Lumbricidae in an area of
Pennine Moorland. J. Anim. Ecol. 26, 409.
Swift, M.J., Heal, O.W. and Anderson, J.M., 1979. Decomposition
in terrestrial ecosystems. University of California Press,
Berkely.
Tilman, D., 1996. Biodiversity: population versus ecosystem
stability. Ecology 77, 97±107.
Wallwork, J.A., 1976. The Distribution and Diversity of Soil
Fauna, Academic Press, London.
Walsingham, J.M., 1976. Effect of sheep grazing on the
invertebrate population of agricultural grassland. Soc. Proc.
R. Dublin Soc. 11, 297±304.
Wardle, D.A., Giller, K.E., 1997. A quest for a contemporary
ecological dimension to soil biology. Soil Biol. Biochem., in
press.
Wasilewska, L., 1995. Differences in development of soil nematode
communities in single and multi-species grass experimental
treatments. Appl. Soil Ecol. 2, 53±64.
Yeates, G.W., 1982. Variation in pasture nematode populations over
thirty-six months in a summer dry silt loam. Pedobiologia 24,
329±346.
Yeates, G.W., Cook, R., 1997. Nematode fauna of three Welsh soils
under conventional and organic grassland farm managements
In: De Goede, R., Bongers T. (Eds.), Nematode communities of
northern temperate grassland ecosystems, DEGREE, in press.
Yeates, G.W., Bongers, T., De Goede, R.G.M., Freckman, D.W.,
Georgieva, S.S., 1993. Feeding habits in soil nematode families
and genera ± an outline for ecologists. J. Nematol. 25, 315±331.
Yeates, G.W., Bardgett, R.D., Cook, R., Hobbs, P.J., Bowling, P.J.,
Potter, J.F., 1997. Faunal and microbial diversity in three Welsh
grassland soils under conventional and organic management
regimes. J. Appl. Ecol. 34, 453±471.
Yuen, P.R., 1966. The nematode fauna of the regenerated woodland
and grassland of Broadbalk wilderness. Nematologica 12, 195±
214.