Download The influence of biotic interactions on soil biodiversity

Ecology Letters, (2006) 9: 870–886
REVIEW AND
SYNTHESIS
David A. Wardle*
Department of Forest
Vegetation Ecology, Swedish
University of Agricultural
Sciences, SE 901-83 Umeå,
Sweden; and Landcare Research,
PO Box 69, Lincoln, New
Zealand
*Correspondence: E-mail:
[email protected]
doi: 10.1111/j.1461-0248.2006.00931.x
The influence of biotic interactions on soil
biodiversity
Abstract
Belowground communities usually support a much greater diversity of organisms than
do corresponding aboveground ones, and while the factors that regulate their diversity
are far less well understood, a growing number of recent studies have presented data
relevant to understanding how these factors operate. This review considers how biotic
factors influence community diversity within major groups of soil organisms across a
broad spectrum of spatial scales, and addresses the mechanisms involved. At the most
local scale, soil biodiversity may potentially be affected by interactions within trophic
levels or by direct trophic interactions. Within the soil, larger bodied invertebrates can
also influence diversity of smaller sized organisms by promoting dispersal and through
modification of the soil habitat. At larger scales, individual plant species effects,
vegetation composition, plant species diversity, mixing of plant litter types, and
aboveground trophic interactions, all impact on soil biodiversity. Further, at the
landscape scale, soil diversity also responds to vegetation change and succession. This
review also considers how a conceptual understanding of the biotic drivers of soil
biodiversity may assist our knowledge of key topics in community and ecosystem
ecology, such as aboveground–belowground interactions, and the relationship between
biodiversity and ecosystem functioning. It is concluded that an improved understanding
of what drives the diversity of life in the soil, incorporated within appropriate conceptual
frameworks, should significantly aid our understanding of the structure and functioning
of terrestrial communities.
Keywords
Aboveground, belowground, biodiversity,
herbivory, plant litter, predation, soil.
competition,
ecosystem
functioning,
Ecology Letters (2006) 9: 870–886
INTRODUCTION
Over the past several decades, many ecologists have focused
on trying to understand why different communities or
ecosystems differ in the diversity of organisms that they
contain (e.g. Hutchinson 1961; MacArthur & Wilson 1967;
Grime 1973; Tilman 1982). Historically, most of the effort
devoted to addressing this question in terrestrial ecosystems
has focused on aboveground plant and animal species.
However, it is well recognized that in most terrestrial
ecosystems the belowground biota supports a much greater
diversity of organisms than does the aboveground biota.
While the vast majority of species of soil biota have yet to be
Ó 2006 Blackwell Publishing Ltd/CNRS
described, several key groups (bacteria, fungi, nematodes
and insects) almost certainly contain several hundreds of
thousands to millions of species globally (De Deyn & Van
der Putten 2005). This diversity is also apparent at local
scales; for example, a few grams of soil may contain a few
1000 species of bacteria and several 100 species of
invertebrates (Torsvik et al. 1994; Wardle 2002). Although
soil ecologists have long recognized the need to understand
the mechanisms by which soil biodiversity is maintained
(Anderson 1975; Ghilarov 1977; Bruns 1995), it is only
comparatively recently that questions relating to the
maintenance and functional significance of soil biodiversity
have attracted widespread interest from ecologists. As such,
Review and Synthesis
there has been a recently growing body of theory about how
soil biodiversity may respond to local extrinsic stress and
disturbance factors (Wardle 2002; Bardgett et al. 2005b), and
on how belowground biodiversity interacts with aboveground biodiversity (Hooper et al. 2000; De Deyn & Van
der Putten 2005).
This review addresses the issue of how biotic drivers
(both above- and belowground) influence the biodiversity of
soil organisms, and explores the mechanisms involved.
Although there has been increasing recent research activity
on this topic, this work is spread diffusely through two
separate bodies of literature (i.e. the soil biology literature
and the ecological literature) and there have been few
attempts to conceptually synthesize it. Yet, an improved
understanding of this topic would greatly enhance our
understanding of terrestrial communities and ecosystems in
several ways. First, it would assist our knowledge of the
factors that influence soil food webs at a finer-scale levels of
resolution (e.g. species and genera) than at the broad-scale
functional or taxonomic scales that have characterized most
soil food web studies to date (e.g. Wardle & Yeates 1993; De
Ruiter et al. 1995). Second, it would enhance our understanding of feedbacks between aboveground and belowground biota at the community level and the degree to
which the two communities drive each other (Wardle et al.
2004a). Third, it should contribute usefully to our understanding of how soil biodiversity (and loss of biodiversity)
affects ecosystem functioning (Hooper et al. 2005), given
that an adequate understanding of how diversity affects
ecosystem functioning in a Ôreal worldÕ context requires us
to understand the factors that regulate biodiversity in the
first instance (Grime 1998). Fourth, it should help us to
better understand how global change phenomena influences
real communities and ecosystems, especially when global
change factors alter those biotic factors that influence soil
biodiversity.
In this review, I will draw together literature on how
biotic factors influence biological diversity within components of the soil community, and in doing so will explore the
mechanistic basis by which soil biodiversity is regulated by
biotic interactions. For the purposes of this review,
taxonomic richness, taxonomic evenness, and functional
diversity, will all be recognized as useful measures of soil
biodiversity. In this light it is recognized that different
measures of diversity, and different levels of resolution for
quantifying diversity, may be useful for answering different
questions (e.g. some will be more relevant to understanding
what structures communities; others will be more relevant
for understanding function). It is also recognized that
different levels of taxonomic resolution are generally applied
to different groups; for example, most studies on larger
invertebrates consider diversity at the species level, whereas
species level characterization is usually intractable for
Biotic drivers of soil biodiversity 871
procaryotes and other measures of diversity are used.
Components of the soil community (within which diversity
will be considered) will include broad functional and/or
taxonomic groups that are widely used in studies of soil
ecology (e.g. bacteria, saprophytic fungi, arbuscular
mycorrhizal fungi and oribatid mites). In reviewing this
topic I will first explore how soil biotic drivers resident in
the soil affect soil biodiversity. I will then consider the
effects of aboveground biotic drivers on soil biodiversity.
Finally I will explore how a conceptual understanding of the
influence of biotic drivers on soil biodiversity can enhance
our understanding of community and ecosystem ecology,
and in doing so will identify key gaps in knowledge and areas
in which future research could usefully contribute.
BIOTIC DRIVERS RESIDENT IN THE SOIL
Within trophic group interactions
Biotic drivers of soil biodiversity operate over a range of
spatial and temporal scales (Fig. 1). At the most local of
these scales, diversity of soil organisms can potentially be
regulated by interactions that occur among taxa within the
same trophic grouping. Such interactions are most likely to
have a role in structuring community attributes for those
groups of organisms that are resource regulated rather than
strongly consumer regulated in the soil food web, as the
community structure of these groups of organisms is most
likely to be regulated by competition. Different groups of
soil organisms differ markedly in the extent to which they
are regulated by resource availability as opposed to by their
consumers, although most groups are regulated to some
extent by both factors (De Ruiter et al. 1995; Wardle 2002).
However, most of the evidence for strong competitive
interactions in the belowground environment involves fungi
and the fungal-based energy channel of the soil food web
(Wardle 2002).
Although there is ample evidence in the literature for
competitive interactions in soil fungal communities, direct
evidence for competition as a determinant of fungal
diversity (i.e. through competitive exclusion) is scarce.
Indirect evidence, however, is apparent for studies that
reveal that the presence of a given saprophytic fungal
species (or group of species) on a substrate may effectively
exclude colonization of new saprophytic fungal species on
that substrate; this has been long recognized for both litter
substrates (Garrett 1963) and dead wood (Rayner & Todd
1979; Boddy 2000). Although this issue has seldom been
addressed for mycorrhizal fungal species (but see Wu et al.
1999; Kennedy & Bruns 2005), competitive exclusion may
also be important in determining ectomycorrhizal fungal
diversity at the scale of the individual host plant root tip, at
least if the majority of root tips are colonized by a single
Ó 2006 Blackwell Publishing Ltd/CNRS
872 D. A. Wardle
Review and Synthesis
Biotic drivers of soil biodiversity
Vegetation dynamics
Vertebrate herbivores
Plant community attributes
Invertebrate herbivores
Plant species attributes
Physical structures created by
other organisms
Dispersal by other
soil organisms
Predation by other
soil organisms
Interference interactions
among coexisting
organisms
Within group
belowground
diversity
Figure 1 The hierarchical nature of biotic factors that may
influence alpha-diversity within a given group of soil organisms.
Here, Ôwithin groupÕ can be applied to key trophic groups (e.g.
microbe-feeding nematodes) or taxonomic groups (e.g. fungi and
oribatid mites). ÔInterference mechanismsÕ apply primarily to
interactions among fungi, among bacteria, and between bacteria
and fungi; ÔpredationÕ by other soil organisms includes soil faunal
consumption of bacteria, fungi and other soil fauna. Note that the
right-hand axis is presented as a gradient, because while some
organisms and processes operate exclusively in the aboveground or
belowground compartments, others operate in both compartments
(e.g. plants that have both aboveground and belowground
structures; animals that spend time both above- and belowground).
Note that the relative positions of these drivers in terms of
temporal and spatial scale are only intended to be illustrative not
exact, and that some of these drivers operate across a range of
scales. Note also that several of these factors may interact to
influence diversity (not shown).
fungal species. For example, in a study for which tree
seedlings were inoculated with eight fungal species either
singly or in multiple species combinations, several fungal
species persisted only in the monoculture treatment,
presumably because they were competitively excluded from
colonizing seedlings when in combination with fungal
species with superior competitive abilities (Jonsson et al.
2001). Further, there is evidence that nitrogen fertilization
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can greatly reduce the diversity on plant roots of both
arbuscular mycorrhizal fungi (Egerton-Warburton & Allen
2000; Egerton-Warburton et al. 2001) and ectomycorrhizal
fungi (Lilleskov et al. 2002), probably in part because greater
resource availability favours competitive fungal species that
suppress subordinate species.
Another related within-trophic level effect, namely the
production by microbes of antibiotics, may also have a role
in influencing microbial diversity. Although the role of
antibiotics in structuring microbial communities has been
long recognized, their role in regulating diversity has seldom
been considered. However, there is some theoretical
evidence, founded on game theory, which predicts a role
for antibiotic production in promoting bacterial diversity
(Czárán et al. 2002). Conversely, antibiotic production by
resident fungal species may serve to reduce colonization by
new species, and it has long been recognized that soils
dominated by antibiotic-producing fungi can resist invasion
by new fungal species, including those that might operate as
plant pathogens (Wicklow 1981).
Resource regulation, and therefore within-trophic level
interactions (such as competition), is less likely to have a role
in regulating the diversity within groups of soil animals, e.g.
soil microarthropods; soil nematodes. Soil animal diversity
generally does not show a hump-backed response to
increases in disturbance intensity or resource availability
(Freckman & Ettema 1993; Wright & Coleman 1993;
Wardle 2002), indicating that factors that maximize soil
animal biomass or density do not promote dominance of
competitive species that reduce subordinate species by
competitive exclusion. As discussed later, the relatively low
intensity of competition among soil faunal taxa, and dearth
of evidence for competitive exclusion, may contribute to the
hyperdiverse nature of soil faunal communities.
Interactions within a given trophic level need not
necessarily be negative, and there has been increasing
recognition over the past decade of the role of positive
interactions such as facilitation in structuring ecological
communities (Callaway & Walker 1997). Facilitative interactions in soils have most frequently been identified for soil
fungi and the fungal-based energy channel. For example,
during decomposition of fresh dead plant material, those
fungal species that colonize first will break down recalcitrant carbohydrates such as cellulose into simpler forms,
thereby enabling subsequent colonization by sugar fungi
(Frankland 1969). The net result is greater fungal diversity
on the substrate over time. Further, Tiunov & Scheu (2005)
found that mixtures of fungal species greatly promoted
conversion of cellulose to CO2 despite some components
of the mixture being unable to utilize cellulose. This
outcome can only be explained by cellulose-degraders
breaking cellulose into simpler carbohydrates that can be
used by other species, and represents a type of facilitation
Review and Synthesis
that would serve to promote the diversity of fungal taxa
present.
Interactions across trophic groups
Regulation of major groups of soil biota through predation
is widespread in soil food webs (De Ruiter et al. 1995) and
there are many examples of regulation of densities of both
soil animals and soil microbes by their consumers (reviewed
by Wardle 2002). Further, consumption of microbes by soil
fauna is likely to be an important driver of soil microbial
community structure. Fungal-feeding fauna show a distinct
preference for some fungal taxa or hyphal types above
others; this has frequently been shown for saprophytic fungi
(e.g. Klironomos et al. 1992; Bonkowski et al. 2000), but
there is also evidence of this for both mycorrhizal
(Klironomos & Kendrick 1996) and plant-pathogenic
(Sabatini & Innocenti 2000) fungi. Further, fungal-feeding
fauna frequently prefer fungal species with certain functional attributes, such as primary colonizers of plant litter
(Klironomos et al. 1992) and those with pigmented hyphae
(Maraun et al. 2003). This is analogous to aboveground
herbivores showing preference for plant species that are
adapted for earlier successional sites and that have suites of
traits that differ from those of less-palatable later successional species (Grime 1979; Coley et al. 1985). If selective
feeding by fungal-feeding invertebrates can affect fungal
community composition and therefore the relative dominance of different fungal taxa, then effects on soil fungal
diversity are also likely. The influence of fungal grazers on
fungal diversity has seldom been tested, although McLean
et al. (1996) found a neutral effect of grazing by mites and
collembolan on fungal diversity in microcosms. Whether
shifts in fungal community composition resulting from soil
invertebrates has generally positive or negative effects on
fungal diversity remains little understood, but effects in
either direction may be predicted depending on whether the
invertebrates selectively suppress competitive dominant or
subordinate, species (Holt & Lawton 1994). As a parallel,
both positive and negative effects of aboveground grazers
on plant diversity have been commonly reported in the
literature (Proulx & Mazumder 1998).
Although regulation by consumers of soil dwelling groups
other than fungi is well recognized, the implications of this
for the community structure or diversity within these groups
have seldom been addressed. However, bacterial-feeding
nematodes preferentially feed on some bacterial taxa relative
to others (Ettema 1998), so there are likely implications for
bacterial community composition and diversity. Further,
while how the predatory protozoa inhabiting the aqueous
component of the soil affect the diversity of their prey
remains unknown, there are some relevant studies involving
protozoa in aqueous laboratory experiments; such studies
Biotic drivers of soil biodiversity 873
have shown that predatory protozoa can exert a variety of
effects on the diversity of both prey protozoa (Cadotte &
Fukami 2005; Jiang & Morin 2005) and bacteria (Steiner
2005) depending on context. However, the extent to which
predation of the major soil faunal groups by their predators
may influence their community structure and diversity
remains largely unknown.
Non-trophic interactions
Over larger spatial scales, soil invertebrates serve as agents
of dispersal of smaller soil organisms, principally microbes.
These include bacteria, and propagules of saprophytic,
pathogenic and mycorrhizal fungi (Visser 1985; Dromph
2003; Müller et al. 2003; Rantalainen et al. 2004a). Soil
microbes may be dispersed either through ingestion and
subsequent egestion or through physical attachment to the
body surface of the invertebrate. In the case of saprophytic
soil fungi at least, those taxa that are most likely to attach to
the animal’s body surface are often those that are fast
growing and establish readily in new microhabitats (Visser
1985), suggesting that dispersal may promote fungal
colonization and enhanced fungal diversity of fresh organic
matter. This provides an interesting parallel to the colonization–competition trade-off observed across species in
plant communities (Rees et al. 2001). The role of detritivorous invertebrates in promoting fungal colonization and
diversity through assisting their dispersal has also been
recognized in relation to woody substrates (Müller et al.
2003).
While small-bodied soil animals interact with microbes
primarily directly through predator–prey interactions, larger
bodied soil animals also influence microbes (and small
bodied soil animals) through altering the physical environment and creating structures that serve as habitats (Brown
1995; Lavelle & Spain 2001). For example, many
microarthropods transform litter into faecal pellets, earthworms create middens and casts, termites build mounds,
and ants produce mound nests. These structures all favour
some components of the soil biota at the expense of others
and therefore potentially influence soil biodiversity. For
example, earthworm casts have been shown to promote
diversity of fungal species (Tiwari & Mishra 1993; McLean
& Parkinson 1998a) and oribatid mites (Loranger et al. 1998;
McLean & Parkinson 1998b), although neutral effects of
earthworms on diversity of other faunal groups has also
been detected (Brown 1995). The most likely mechanism
through which earthworms promote diversity of other
groups (notably fungi) is through reducing the intensity of
competitive interactions, probably by suppressing dominant
competitive species within those groups (McLean &
Parkinson 1998a). Subterranean ant nests are known to
reduce the densities of soil-borne plant pathogens and
Ó 2006 Blackwell Publishing Ltd/CNRS
874 D. A. Wardle
fungal-feeding nematodes (Blomqvist et al. 2000), with
possible consequences for the diversity of organisms within
these groups, and for diversity within other groups that may
benefit through reduced pathogen and fungal feeder
densities. Ant mounds have also been recognized as greatly
altering the composition of the soil food web (Laakso &
Setälä 1998), and have been shown to promote microbial
functional diversity, probably by creating a heterogeneous
mosaic of organic matter and promoting habitat spatial
variability (Dauber & Wolters 2000).
PLANTS AND THEIR ABOVEGROUND CONSUMERS
AS BIOTIC DRIVERS
Effects of plant species and species combinations
Although there has been a long history in soil ecology of
studying the community structure of soil organisms in
relation to soil properties, over the past decade or so there
has been a greatly increasing interest in understanding how
plant identity, composition and diversity affects the soil
community. This has been instigated in part by increasing
recent interest in the so-called diversity-function issue (i.e.
how organism diversity affects community and ecosystem
processes), an issue that requires explicit integration of
aboveground–belowground feedbacks (Wardle et al. 2004a;
De Deyn & Van der Putten 2005; Hooper et al. 2005).
Plant species differ markedly in the belowground
communities that they support, and this has important
functional consequences (Hunt et al. 1988; Ayres et al. 2006).
As such, soils from under monocultures of different plant
species frequently support vastly different levels of diversity
of various groups of soil organisms, e.g. nematodes (De
Deyn et al. 2004; Vitecroft et al. (2005), mites (Badejo &
Tian 1999), endomycorrhizal fungi (Eom et al. 2000;
Johnson et al. 2003) and saprophytic microbes (Wardle et al.
2003b). Further, monospecific litters from different plant
species have been shown to support differing diversities of
decomposer invertebrates (Hansen 1999; Wardle et al.
2006). It is not well understood why different plant species
differ in the diversity of organisms that they support,
although this is likely to be driven by trait differences
between plant species. Plant species with different suites of
traits return organic matter of differing qualities to the soil
(Dı́az et al. 2004), which in turn has likely consequences for
attributes of the soil food web (Wardle et al. 2004a),
including taxonomic or functional diversity within major
groups of soil organisms.
Given that plant species usually coexist in mixtures rather
than occur singly, the issue then emerges as to whether
multiple plant species combinations support greater diversity of soil biota. It has long been recognized that increasing
plant diversity may potentially influence foliar herbivore
Ó 2006 Blackwell Publishing Ltd/CNRS
Review and Synthesis
diversity (Southwood et al. 1979; Siemann 1998) but the
issue of how diversity of soil organisms are affected by plant
diversity has attracted only relatively recent attention
(Hooper et al. 2000; Wardle 2002). In this light, several
recent studies have considered how live plant diversity
affects diversity within major groups of soil organisms
(Table 1). Most experimental studies have found diversity
within major belowground groups to be unrelated to live
plant diversity even when other community- and ecosystemlevel properties are related (e.g. Wardle et al. 1999, 2003b,
2006; Korthals et al. 2001; Porazinska et al. 2003; Carney
et al. 2004). This is also supported by observational evidence
across gradients of plant diversity (Broughton & Gross
2000; Hooper et al. 2000). This points to above- and
belowground biodiversity being somewhat uncoupled,
despite aboveground and belowground community structure frequently being linked (Wardle et al. 1999; Hooper
et al. 2000). Only two studies have found an effect of live
plant diversity on soil diversity, but one of these (Stephan
et al. 2000) incorporates an experimental design in which
Ôsampling effectÕ (Huston 1997) (i.e. the increased probability of including plant species with particular attributes in
more diverse mixtures) may explain the outcome. In the
other, De Deyn et al. (2004) did find greater soil nematode
diversity in diverse plant species mixtures than in corresponding monoculture treatments, presumably because of a
greater range of plant-derived resource types present. In
contrast, three of four studies that have involved the
manipulation of plant litter species richness through litter
mixing (Hansen 1999; Kaneko & Salamanca 1999; Armbrecht et al. 2004) have found a positive effect of litter
diversity on soil invertebrate diversity, with only one
(Wardle et al. 2006) giving inconsistent results. All three
studies used full monoculture litter treatments, and the
results therefore cannot be explained solely by sampling
effect. In particular, in the study of Armbrecht et al. (2004),
the use of rarefaction analyses and explicit testing for
patterns of spatial dependencies among experimental units
makes this work one of the most rigorous demonstrations
of an ecological effect of plant species diversity in the
literature.
For plant diversity to influence soil diversity, the most
likely mechanism would involve: (i) a more diverse plant
community returning a more heterogeneous mixture of
resources to the soil; and (ii) this more diverse resource
mixture in turn influencing soil biodiversity, e.g. through
promoting greater resource partitioning among the component soil organisms (Hooper et al. 2000; Wardle 2002). It is
unclear as to whether a more diverse mix of plants
necessarily produces a more heterogeneous mix of substrates, as a single plant species might be able to produce as
wide a range of tissue types (in terms of quality and chemical
composition) as would a whole range of plant species
Plant species richness
Plant species richness
Plant species richness
Plant species richness
Porazinska et al. (2003)
Wardle et al. (2003b)
Carney et al. (2004)
De Deyn et al. (2004)
PLFA, microbial phospholipid fatty acids.
Wardle et al. (2006)
Armbrecht et al. (2004)
Species richness
of leaf litter
Species richness
of leaf litter
Species richness
of twig litter
Species richness
of leaf litter
Plant species richness
Korthals et al. (2001)
Plant litter manipulation
Kaneko & Salamanca
(1999)
Hansen (2000)
None (plant
diversity gradient)
Plant species richness
Removal of plant
species
Barros in Hooper
et al. (2000)
Stephan et al. (2000)
Live plant manipulation
Wardle et al. (1999)
Reference
Plant diversity
manipulation
1–8
Yes
Yes
Partial
1–7
1 or 8
Yes
Yes
No
Yes
Yes
1–3
1–8
1–5
1–9
1 or 2
No
No
1–32
4 or 15
No
No
Monoculture
treatments?
10–43
3–8
Range of
species
richness
Deciduous forest
(North Carolina, USA)
Coffee agroecosystem
(Colombia)
Mixed forest (Banks
Peninsula, New Zealand)
Mixed forest (Matsue, Japan)
Tropical vegetation
(Costa Rica)
Grassland (the Netherlands)
Tropical pasture
(Manaus, Brazil)
Grassland (Lupsingen,
Switzerland)
Grassland (Planken Wambuis,
Netherlands)
Grassland (Konza
Prairie, KS, USA)
Grassland (greenhouse study)
Grassland (Waikato,
New Zealand)
Ecosystem type
Nematodes (genera),
macrofauna (species)
Twig-nesting ants (species)
Oribatid mites (species)
Oribatid mites (species)
Microbes (PLFAs), nematodes
(genera)
Microbes (PLFAs and catabolic
diversity), nematodes (genera)
Ammonium-oxidizing bacteria
(operational taxonomic units)
Nematodes (genera)
Nematodes (genera)
Microbes (catabolic diversity)
Microbes (PLFAs), nematodes
(genera), root feeding
arthropods (species)
Macrofauna (species)
Group(s) of soil
organisms and
level of resolution
Table 1 Summary of studies that have explicitly tested whether plant species diversity affects diversity of soil organisms
No consistent trends
Positive effect of diversity
Positive effect of diversity
Positive effect of diversity
Positive effect of diversity,
but composition more
important
Response to composition
but not diversity
No relationship
No response to vegetation
treatments
No consistent trends
Positive response
No relationship
No consistent relationships
Response of diversity of
soil organism group(s)
to plant diversity
Review and Synthesis
Biotic drivers of soil biodiversity 875
Ó 2006 Blackwell Publishing Ltd/CNRS
876 D. A. Wardle
(Hooper et al. 2000). Further, in the only study to date to
specifically investigate the ecological consequences of
substrate chemical diversity (Orwin et al. 2006), it was
found that increasing the diversity of carbohydrate types
added to the soil from one to eight compounds had no
consistent effects on either soil processes or on soil
microbial functional diversity. This was despite the composition of carbohydrates having important belowground
effects. Thus, even if live plants in a more diverse
herbaceous community released a wider diversity of
compounds to the rhizosphere than did a less diverse
community, then this would not necessarily promote soil
biotic diversity. Conversely, the diversity of physical types of
microhabitats in forested systems has been shown to
promote diversity of both soil invertebrates (Anderson
1978; Barker & Mayhill 1999) and ectomycorrhizal fungi
(Dickie et al. 2002). Different invertebrate species can
preferentially colonize litters with different physical structures (Hansen 1999) and different chemical compositions
(Wardle et al. 2006), meaning that in plant communities that
support a thick litter layer (notably in forested systems), a
greater diversity of litter types might indeed promote
invertebrate diversity. If this is the case, then plant diversity
would promote soil diversity mostly in those systems in
which a thick layer of litter was maintained and in which
plant species drove soil organisms through litter production
rather than through rhizosphere exudation.
There are also other possible mechanisms through which
plant diversity may affect soil diversity, although these have
not been addressed to date. For example, increasing plant
diversity has been shown in several instances to promote
plant productivity, particularly at low diversity levels
(Hooper et al. 2005). It is recognized that plant production,
and therefore the quantity of resources entering the soil,
promotes subsets of the soil biota, particularly those that are
regulated primarily by resource availability (Mikola & Setälä
1998). The implications of this for soil biodiversity are not
well understood, although Degens et al. (2000) found that
soils with a greater amount of basal resources present also
supported microbial communities with a greater functional
diversity. Further, there is recent evidence that the diversity
of bacteria in aquatic systems (some of which also occur in
the aqueous component of soils) can show hump-backed
relationships with ecosystem productivity (Horner-Devine
et al. 2003; Kassen et al. 2004).
Effects of foliar herbivores and their predators
Foliar herbivores are being increasingly recognized as
important indirect drivers of the belowground subsystem,
and both positive and negative effects of herbivores have
been reported, depending on the mechanism through which
the herbivores affect the decomposer subsystem (Bardgett
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Review and Synthesis
& Wardle 2003). Further, there are several examples of
studies that have shown both positive and negative effects
of herbivory on plant diversity (Proulx & Mazumder 1998).
The indirect effects of foliar herbivores on soil biodiversity
remains relatively unstudied, although a growing handful of
studies have addressed this question or at least provided
relevant data (Table 2). Most have focused on browsing
mammals, although one has investigated the effects of
localized invertebrate herbivory on the diversity of soil
organisms (Wardle et al. 2004c). Here, experimental planted
mesocosms were set up with eight aphid species, added
singly or in various multiple species combinations. Although
aphid species identity had important effects on some
belowground groups, the diversity of only one such group
(microbe-feeding nematodes, which are secondary consumers) was affected by the addition of aphids or aphid species
identity. Further, no group of soil organisms was consistently affected by aphid species diversity. The mechanistic
basis by which aphid species identity might indirectly
influence the diversity of a group of soil-dwelling secondary
consumers in the soil is unclear, but presumably involves
alteration by aphids of the nature of plant-derived resources
entering the decomposer food web.
Studies involving herbivore exclusion plots in the field
(Table 2) have most often found negative effects of
mammals on the diversity of various groups of soil biota,
e.g. arbuscular mycorrhizae (Gehring et al. 2002), microarthropods (Dombos 2001; Clapperton et al. 2002) and
macrofauna (Suominen 1999; Wardle et al. 2001). However,
two of the three studies that have considered how browsers
influence soil nematode diversity have found no detectable
effect (Wall-Freckman & Huang 1998; Wardle et al. 2001)
while the third found some positive effects (Stark et al.
2000). The mechanism by which mammals reduce soil biotic
diversity is unclear, but could involve changes in vegetation
composition and the relative dominance of different plant
species (Gehring et al. 2002) or physical disturbances to the
soil caused by the mammals (Doubos 2001; Clapperton et al.
2002). In this light, Wardle et al. (2001) found for a range of
forested sites throughout New Zealand that browsing
mammals consistently reduced the abundance and diversity
of various groups of soil macrofauna, apparently as a result
of mammal-induced soil disturbance. These effects occurred
even when the mammals did not adversely affect vegetation
density, vegetation diversity or diversity of litter types
present on the forest floor. Previous work suggests that soil
faunal diversity is generally only adversely affected by soil
disturbance (in contrast to predictions of the Ôintermediate
disturbanceÕ hypothesis) (Wardle 2002; Bardgett et al.
2005b), and in this light, consistent adverse effects of
mammal-induced soil disturbance on diversity of meso- and
macrofauna may be expected. These effects are less likely
to adversely affect the diversity of smaller-bodied soil
Aphids
Cattle
Range of herbivores
Cattle
Cattle
Reindeer
Moose
Reindeer
Sheep
Range of mammals,
mostly deer
Foliar herbivore type
PLFA, microbial phospholipid fatty acids.
Invertebrates
Wardle et al. (2004c)
Clapperton et al. (2002)
Gehring et al. (2002)
Stark et al. (2000)
Dombos (2001)
Wardle et al. (2001)
Browsing mammals
Leetham & Milchunas (1985)
Wall-Freckman & Huang (1998)
Suominen (1999)
Reference
Grassland (mesocosm study)
Prairie (southern Alberta, Canada)
Tropical forest (northern
Queensland, Australia)
Shortgrass prairie (Colorado, USA)
Shortgrass prairie (Colorado, USA)
Boreal forest (northern Finland)
Boreal forest (Finland and Sweden)
Boreal forest (Muonio, Finland)
Grassland (southern Hungary)
Rainforest (throughout
New Zealand)
Ecosystem type considered
Microbes (PLFAs and catabolic
diversity), herbivorous
nematodes (genera)
Microbe-feeding nematodes
(genera)
Microarthropods (species)
Nematodes (genera)
Gastropods (species)
Gastropods (species)
Nematodes (genera)
Collembola (species)
Nematodes (genera)
Gastropods (species),
beetles (species),
diplopods (family)
Mites (family)
Arbuscular mycorrhizal
fungi (species)
Group(s) of soil organism
and level of resolution
Table 2 Summary of studies that have explicitly tested whether foliar herbivores indirectly influence the diversity of soil organisms
Sometimes positive herbivore
effects
No effect
Reduction by herbivores
Reduction by herbivores of
spore diversity
No response
No response
Reduction by herbivores
Enhancement of relative diversity
Enhancement by herbivores
Reduction by herbivores
No response
Generally reduction by herbivores
Response of diversity of soil
group(s) to presence of herbivores
Review and Synthesis
Biotic drivers of soil biodiversity 877
Ó 2006 Blackwell Publishing Ltd/CNRS
878 D. A. Wardle
organisms such as nematodes that inhabit water films in
small pore spaces because these microhabitats are less likely
to be influenced by physical disturbance (Stark et al. 2000;
Wardle et al. 2001).
Although indirect effects of aboveground secondary
consumers (predators of herbivores) on the belowground
subsystem have been seldom studied, aboveground trophic
cascades (where predators indirectly affect plants by
influencing herbivore densities) can determine the nature
of organic materials entering the soil, with implications for
the soil community (Croll et al. 2005). In this light, two
studies have provided relevant data on how aboveground
predators may influence decomposer diversity through
cascading trophic effects. In the first, Dyer & Letourneau
(2003) found that manipulation of a top invertebrate
predator (which feeds upon herbivorous and possibly
detritivorous invertebrates), associated with a tropical shrub,
did not influence the diversity of shrub-associated decomposer fauna in any of three trophic levels. Diversity within
each level was instead affected by the amounts of resources
made available for the decomposer subsystem. In the
second, Wardle et al. (2005) established mesocosms with
plants and aphids, and with or without predators of the
aphids. The presence of top predators influenced the plant
community, and this in turn induced a cascading effect on
the abundances of organisms in each of three consumer
trophic levels of the soil food web. However, there was no
consistent effect on organism diversity within any of these
three trophic levels, indicating that soil biodiversity can be
highly buffered against interactions that occur aboveground.
Effects of aboveground changes over successional time
At larger temporal scales, e.g. in the order of decades to
millennia, changes in plant community composition due to
vegetation succession also cause shifts in soil communities.
These changes result from plant species replacing each other
over time through both biological (e.g. facilitation and
interference) and abiotic (e.g. changes in nutrient supply
from parent material) mechanisms. Feedbacks between
aboveground and belowground communities at these larger
scales have important implications for both community- and
ecosystem-level properties (Bardgett et al. 2005a). Few
studies have considered how soil communities change
during vegetation succession, but there is evidence that
during the first few decades of succession increases in plant
diversity and community productivity are closely matched
by increases in soil food chain length (Verhoeven 2002), and
the diversity of soil microbes (Sigler & Zeyer 2002; Tscherko
et al. 2003), soil invertebrates (Dunger et al. 2004; Hodkinson et al. 2004) and mycorrhizal fungi (Jumpponen et al.
2002). Further, these changes in soil community attributes
appear to be deterministic and consistent across successions,
Ó 2006 Blackwell Publishing Ltd/CNRS
Review and Synthesis
at least at a regional scale (e.g. hundreds of kilometres)
(Hodkinson et al. 2004). However, after the initial phases of
succession soil diversity need not continue to increase;
Chauvat et al. (2003) found for forest rotations that over
time the diversity of microbes and springtails actually
declined, apparently as a result of declining habitat diversity
and food abundance.
In the order of millennia or more, ecosystems without
significant disturbance can enter a state of ecosystem
ÔretrogressionÕ, in which vegetation succession ultimately
proceeds to a highly unproductive state in which available
nutrients, principally phosphorus, become very limiting
(Walker & Syers 1976). Although the implications of this for
the decomposer subsystem have been seldom explored (but
see Vitousek 2004; Wardle et al. 2004b), there is evidence
that microbial community structure may undergo substantial
changes during retrogression, such as from fungal to
bacterial domination (Wardle et al. 2004b). Little is known
about how soil microbial or faunal diversity changes during
retrogression, although Williamson et al. (2005) found
microbial functional diversity to decline and nematode
diversity to remain invariant across a 600 000 year retrogressive succession on terraces varying in time since uplift
from the ocean.
CONCEPTUAL INSIGHTS DERIVED FROM
UNDERSTANDING BIOTIC DRIVERS
It has previously been recognized that densities of soil
organisms are regulated by a diverse range of factors that
operate in a hierarchical manner across a range of spatial
(Ettema & Wardle 2002) and temporal (Bardgett et al.
2005a) scales. It is apparent from this review that the
diversity of life in the soil is also driven by a hierarchy of
biotic factors, ranging in spatial scale from localized
interspecific interactions at one end to vegetation succession
on landscapes at the other end (Fig. 1).
The wide spectrum of biotic factors driving soil biodiversity may help explain the hyperdiverse nature of soil
communities. Over 30 years ago, Anderson (1975) drew
attention to the Ôenigma of soil biodiversityÕ [a belowground
analogue of Hutchinson’s (1961) Ôparadox of the planktonÕ],
which highlights the issue as to how it is possible for soils to
maintain a high diversity of organisms without biotic
mechanisms such as competitive exclusion reducing diversity. It has previously been proposed that this diversity can
be explained in part by the diversity of niche axes in the soil
promoting considerable resource partitioning amongst
trophically equivalent organisms (Faber & Joose 1993;
Wardle 2002), coupled with a very low intensity of
competition within large subsets of the soil biota (Wardle
2002). The present review also addresses whether biotic
drivers (both below- and aboveground) may also serve to
Review and Synthesis
promote soil biodiversity across a range of spatial and
temporal scales (Fig. 1). Although there is a dearth of data
with which to explicitly or quantitatively test the importance
of the various mechanisms in Fig. 1 in driving soil
biodiversity, the available evidence suggests that many of
these mechanisms serve to maximize soil biodiversity at a
range of spatial and temporal scales, thus contributing to the
high biotic diversity present in the soil subsystem. Further,
the importance of many drivers that operate aboveground is
likely to vary across ecosystems, and an enhanced understanding of them should contribute usefully to determining
how and why soils differ in the biodiversity that they
support.
Aboveground–belowground feedbacks
This review has focused on drivers of soil biodiversity,
including those that are based aboveground. However, the
aboveground and belowground components strongly influence each other, suggesting that there may be important
feedbacks between the two. Just as there are several
examples of how aboveground biota (plants and their
consumers) affect soil communities (Tables 1 and 2), there
are also examples of how soil biota affect aboveground
communities, and these effects may propagate through
several trophic levels (reviewed by Van der Putten et al.
2001; Wardle 2002). Further, components of the soil biota
may influence plant diversity, either positively (e.g. Van der
Heijden et al. 1998; De Deyn et al. 2003) or negatively (e.g.
Brown & Gange 1989; Hartnett & Wilson 1999), depending
on whether or not they promote subordinate plant species
relative to dominant species (Ureclay & Dı́az 2003). One
study has also shown a positive response of plant species
diversity to arbuscular mycorrhizal fungal diversity (Van der
Heijden et al. 1998), although the mechanistic basis of that
result remains unclear. Nevertheless, given the range of
patterns reported in the literature on how belowground
biota affects plant diversity and how aboveground biota
affects belowground diversity, both positive and negative
feedbacks between above- and belowground biodiversity are
theoretically possible.
It is expected that the strength of feedbacks between
above- and belowground biodiversity will vary depending on
which groups of soil biota are considered. There is
increasing recent recognition that those soil groups most
directly associated with plant roots (e.g. mycorrhizal fungi,
root pathogens and herbivores) show a higher degree of
specificity than has been previously supposed (Wardle et al.
2004a). This means that a greater range of plant species
should be able to support a greater range of root-associated
biota, although the evidence for or against this prediction at
the plant community level is scarce. However, if this is the
case, then it provides evidence for niche partitioning among
Biotic drivers of soil biodiversity 879
components of the soil biota, and may provide a useful test
of niche-based models and approaches developed for
aboveground and other systems (e.g. Schoener 1974; Tilman
1982). Further, if components of the root-associated biota
show high specificity, then the community structure
(including diversity) of that biota should in turn strongly
affect community structure aboveground by affecting the
relative densities of different plant species (e.g. dominant vs.
subordinate) (Stampe & Daehler 2003; Ureclay & Dı́az
2003), potentially influencing plant diversity. A different
pattern is expected when decomposer soil biota are
considered. While decomposers do show some resource
specialization, this is driven more directly by differences
among plant-derived substrate types than by differences
among plant species, and decomposers are much greater
generalists than root-associated biota in their associations
with plant-derived resources. Further, different species
combinations of decomposer biota are only likely to
indirectly differ in their effects on the plant community,
simply through differentially influencing the supply of plantavailable nutrients from the soil. For this reason, it is
reasonable to predict stronger links and feedbacks between
plant diversity and the diversity of root-associated biota than
between plant diversity and decomposer diversity, although
insufficient data currently exists to adequately test this
prediction.
A greater understanding of linkages between aboveground composition and decomposer diversity requires an
understanding of the importance of regulation by resource
availability, relative to regulation by consumers in higher
trophic levels, in structuring soil food webs. The relative
importance of these factors has frequently been considered in the context of decomposer food web theory, and
most groups are structured by both to varying degrees
(e.g. De Ruiter et al. 1995; Mikola & Setälä 1998; Moore
et al. 2003). However, most of this work has focused at a
coarse level of resolution (i.e. major functional or
taxonomic groups) rather than at the finer degrees of
resolution needed for understanding drivers of soil
biodiversity. For example, significant responses of the
diversity of a group of organisms to plant community
attributes might be detectable at the species (or even the
genetic) level even when diversity at a coarser level of
resolution is unresponsive. The question of whether plant
community attributes drive decomposer diversity, and the
extent to which this is propagated through the decomposer food web, first requires knowledge of the extent to
which the diversity in each decomposer trophic level is
regulated by resource or food availability. However, it
is likely that the diversity within some trophic levels is
strongly resource regulated while that of others is less so,
and this explains why the diversity of different trophic
groupings may greatly vary in their response to aboveÓ 2006 Blackwell Publishing Ltd/CNRS
880 D. A. Wardle
ground biotic drivers (Wardle et al. 2003b; De Deyn et al.
2004) (Table 1).
Biodiversity and ecosystem functioning
Understanding the biotic drivers of soil biodiversity is
directly relevant to the so-called diversity-functioning issue,
which is focused on determining whether organism diversity
influences key ecosystem properties such as decomposition,
nutrient flow rates, productivity, and resistance and resilience to disturbances. This is because such information
informs on whether changes in biodiversity caused by these
drivers at the ecosystem level are sufficient to impact upon
these functions. A growing number of studies have
investigated how the biodiversity of belowground organisms
may impact upon key ecosystem functions (Hättenschwiler
et al. 2005; Hooper et al. 2005). There is evidence indicating
possible effects of mycorrhizal fungal diversity and/or
composition on ecosystem productivity at the species level
(e.g. Van der Heijden et al. 1998; Jonsson et al. 2001) and
even at the genetic level (Koch et al. 2006). Plant productivity has also recently been shown to respond to the
community structure (although not species richness) of root
herbivores (Brinkman et al. 2005). Further, it is likely that
those processes that can only be carried out by a small
number of specialized taxa (e.g. nitrification and symbiotic
nitrogen fixation) are susceptible to losses in the diversity of
these taxa (Wardle 2002). Meanwhile, decomposer and
nutrient mineralization processes are carried out by a diverse
range of taxa, suggesting a significant level of functional
redundancy in the decomposer biota. In this light, loss of
diversity of soil biota through experimental disturbances has
been shown to have little effect on decomposer processes
(Degens 1998; Griffiths et al. 2000), and belowground
processes driven by soil fauna have been shown to be
driven mainly by species identity and functional dissimilarities among faunal species than by species richness (Laakso
& Setälä 1999; Heemsbergen et al. 2004). Some studies have
shown decomposer processes to be influenced by species
diversity of both saprophytic fungi (Setälä & McLean 2004;
Tiunov & Scheu 2005) and invertebrates (Liiri et al. 2002),
but these effects are likely to become saturated at low levels
of diversity, probably well below those normally likely to be
encountered in real communities. Shifts in soil biodiversity,
such as those caused by the drivers listed in Fig. 1, are most
likely to significantly influence ecosystem functioning for
only those processes that are performed by a restricted
number of taxa, and are unlikely to strongly affect
decomposition or nutrient mineralization.
One habitat in which the diversity of decomposer
organisms may potentially influence ecosystem functioning
is in plant litter rather than in mineral soil. The issue of how
mixing of litter from different plant species in turn
Ó 2006 Blackwell Publishing Ltd/CNRS
Review and Synthesis
influences decomposer processes has been attracting recent
attention (Gartner & Cardon 2004; Hättenschwiler et al.
2005) and, as is apparent from Table 1, increasing litter
diversity may increase the diversity of microhabitats and
therefore decomposer faunal diversity. The presence of
decomposer fauna has in turn been shown in two recent
studies to exert important effects on how litter mixing
affects litter decomposition (Hättenschwiler & Gasser 2005;
Schädler & Brandl 2005). Whether the effects of litter
diversity on invertebrate diversity in turn influence litter
decomposition and nutrient dynamics remains unstudied,
but such effects remain possible at least if litter mixing
promotes significant resource partitioning (and hence
resource use complementarity) amongst different invertebrate taxa.
Concluding remarks
Although there are a growing number of studies that have
published data on how soil biodiversity may be influenced
by biotic drivers, much remains to be understood with
regard to the mechanistic basis of these effects. Such an
understanding is required for developing general principles
about what drives soil diversity. As discussed earlier, one
area that remains poorly known but that would strongly
contribute to this understanding at local spatial and
temporal scales involves the relative importance of resource
regulation and regulation by consumers in higher trophic
levels in regulating soil community structure within trophic
groups. At larger scales, further research is also needed
about relative role of different mechanisms through which
larger organisms (e.g. plants and earthworms) affect the
diversity within groups of smaller organisms, including
through altered resource supply (quantity and quality),
modifications of habitat structure (including habitat heterogeneity) and changes in the soil disturbance regime. Coupled
with this is a need for understanding of how abiotic factors
that can be altered by larger organisms may in their own
right affect the diversity of soil organisms.
There is a large and growing body of ecological theory
about the maintenance and regulation of community
diversity that has been developed mainly for aboveground
and aquatic systems. One of the key challenges in soil
ecology continues to be to better understand the extent to
which these theories apply to soil; to achieve this would in
turn provide a useful test of the generalities of these
theories. For example, well-known theories about diversity
responses to disturbance and stress gradients (e.g. Grime
1973; Connell 1978; Huston 1979) have seldom been
explicitly addressed for soils (Wardle 2002; Bardgett et al.
2005b). Similarly, as described earlier, there is much to be
found about how soil organisms and their diversity conform
to niche-based theories (e.g. Grime 1979; Tilman 1982; Rees
Review and Synthesis
et al. 2001) or the extent to which niche partitioning may
explain the hyperdiverse nature of soil communities. There
have also been few attempts to apply the principles of island
biogeography theory to understanding soil biodiversity (but
see Wardle et al. 2003a). Further, while trait-based approaches in plant ecology (and notably the issue of tradeoffs
among species between those with conservative vs. acquisitive resource strategies) are increasingly recognized as
important for understanding community and ecosystem
processes (e.g. Dı́az et al. 2004), the extent to which similar
principles apply to major groups of soil organisms has been
seldom addressed (but see Faber 1991, with regard to soil
faunal communities).
There are also several topics that have been gaining
significant recent attention in the ecological literature, and to
which a greater understanding of soil biodiversity may
usefully contribute. Some are discussed earlier; other
examples are as follows. First, there has been increasing
interest in how invasive organisms influence communities of
native organisms in the invaded habitat. A handful of studies
have shown that the diversity within key groups of soil
organisms may be influenced by community invasions of
alien plants (Belnap & Phillips 2001; Belnap et al. 2005),
earthworms (McLean & Parkinson 1998a,b) and browsing
mammals (Wardle et al. 2001). Although such studies point
to important above- and belowground consequences of
biological invasions (Wolfe & Klironomos 2005), too few
have been performed to develop general principles about
how alien organisms influence soil biodiversity or the
underlying mechanisms through which this happens.
Second, a growing number of studies have reported
responses of belowground community structure to key
atmospheric drivers of global change such as elevated CO2
(Niklaus et al. 2003; Yeates et al. 2003), temperature (Bardgett et al. 1999) and nitrogen deposition (Egerton-Warburton
et al. 2001; Wiemken et al. 2001). There are several
mechanisms by which these global drivers may affect soil
biota, both directly (through affecting the soil organisms
themselves) and indirectly (by influencing plant growth
characteristics, plant community structure, resource input to
the soil) and therefore potentially soil biodiversity. However,
it is unclear as to which of these mechanisms are important
in driving soil biodiversity and when a better understanding
of this would assist prediction of how biological communities respond to global change. Third, a better knowledge
of what drives soil biodiversity would contribute to greater
understanding of the ecological consequences of habitat
fragmentation and habitat size. Recent studies point to low
turnover of fungal diversity across large geographical
distances (Green et al. 2004) as well as to inconsistent
effects of habitat size and isolation on diversity of
decomposer biota (Wardle et al. 2003a; Rantalainen et al.
2004b) and arbuscular mycorrhizal fungi (Mangan et al.
Biotic drivers of soil biodiversity 881
2004). However, whether the size and isolation of fragments
containing groups of organisms known to drive soil biota
(e.g. vegetation) or habitat patch size, influences soil
biodiversity, remains little understood. Fourth, specifically
in relation to bacteria, it is recognized that habitat properties
(e.g. heterogeneity and resource availability) are important
drivers of bacterial diversification through adaptive radiation, and that that this radiation can occur over the matter
of days (Kassen et al. 2004). The issue of how biotic drivers
of resource and habitat properties (e.g. plants and earthworms) in turn drive the evolution of bacterial populations
and thus their diversification remains unexplored, but
investigations in this area would greatly aid our understanding of the interface between ecology and evolution in the
soil (Crawford et al. 2005).
Finally, our understanding of what drives soil biodiversity
has lagged well behind that for aboveground and many
aquatic systems, in part because of the physical complexity
of the soil environment and sheer numbers of types of soil
organisms present. The main impediment to an improved
understanding of soil biodiversity is in actually characterizing this diversity. For soil fauna and some microbial
components (notably fungi), this characterization requires
access to specialist taxonomic skills, and there are a
diminishing number of individuals worldwide who have
the necessary expertise. Bacteria pose a particular challenge,
as they do not lend themselves as easily to the classic
ÔspeciesÕ concept as do eucaryotes. Yet, they are undoubtedly an important group to understand from both a
community-level and an ecosystem-level perspective,
because their diversity probably rivals that of most groups
of eucaryotes, and because of their key role in a range of
biogeochemical processes. Despite the obvious difficulties
in quantifying soil microbial diversity (especially at fine
levels of taxonomic resolution), methodologies that might
yield useful insights in the future are rapidly evolving. In
particular, although currently available molecular approaches
have limitations in reliably assessing the relative abundance
of different microbial taxa (e.g. across systems or experimental treatments), over time these methods will probably
develop to a level where they can more successfully achieve
this. This will in turn greatly increase the range of ecological
questions to which they can be applied. In any case, an
improved knowledge of what drives the diversity of life in
the soil, incorporated within appropriate conceptual or
theoretical frameworks, should substantially enhance our
knowledge of the structure and functioning of real terrestrial
ecological communities.
ACKNOWLEDGEMENTS
Ian Dickie, Tadashi Fukami and Gregor Yeates made
helpful comments on earlier drafts, and three anonymous
Ó 2006 Blackwell Publishing Ltd/CNRS
882 D. A. Wardle
referees and J. Chase made helpful suggestions on a later
version.
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Editor, Jonathan Chase
Manuscript received 19 December 2005
First decision made 6 February 2006
Manuscript accepted 15 March 2006