Conservation of Soil Organism
Diversity under Global Change
CONSIDER
2002-2007
Thematic network CONSIDER (EVK2-CT-2002-20012)
Final document
(fourth periodic report, deliverable 48, DoW)
important factors influenced by man
conditions for
soil organisms
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Plant cover
Trophic interactions via the plant
Dead organic matter
Spatial separation
Coordination
Biological Institute University of Copenhagen, DK
Deptartment of Ecology, Lund University, S
Center Terrestrial Ecology, Heteren, NL
Institut Zoologie, Universität Darmstadt, D
Center Agriculture and Environmental Research, University of Reading, UK
Department of Ecology, University of Helsinki, FIN
Department of Soil Microbiology and Symbiotic Systems, Granada, ES
INRA, Agronomie et Environmrent, Nancy F
Department of Biology and Environmental Science, Jyväskylä, FIN
Biological Science, University of London, Holloway UK
Søren Christensen
Katarina Hedlund
Wim H. Van der Putten
Stefan Scheu
Simon Mortimer
Heikki Setälä
José-Miguel Barea
Christophe Robin
Juha Mikola
Alan Gange
Conservation of Soil Diversity
under Global Change
CONSIDER
2002-2007
Thematic network CONSIDER (EVK2-CT-2002-20012)
Final report
(fourth periodic report, deliverable 48, DoW)
Content
A
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A2
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A9
Conservation of Soil Diversity under Global Change………………………………..
Introduction………………………………………………………………………….
Diversity of soil organisms………………………………………………………….
Importance of soil biodiversity……………………………………………………...
Threats to soil biodiversity………………………………………………………….
Biodiversity – function relationship………………………………………………...
Plant biodiversity – soil biodiversity relationship…………………………………..
Soil organic matter – soil biodiversity relationship………………………………...
Spatio-temporal effects on soil biodiversity………………………………………..
Multitrophic interactions and soil biodiversity……………………………………..
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A10 Aboveground-belowground interactions as an organizing framework……………………
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A11 History of the aboveground-belowground interactions framework………………………… 10
A12 Linking empirical to modelling approaches………………………………………………… 10
A13 Mitigation activities…………………………………………………………………
A13-1 Dealing with effects of land use change…………………………………………
A13-2 Dealing with effects of climate change………………………………………….
B
The CONSIDER project in relation to needs and wishes expressed by the EU…….
B1 The EU policy………………………………………………………………………..
B2 The EU Thematic Strategy on Soil Protection………………………………………
B3 Visions expressed by the EU Commission, DG Environment………………………
B4 Wishes expressed by the EU Environmental Agency………………………………
C
Recommendations from CONSIDER to the EU Commission on Soil Biodiversity..
C1 Important properties of soil biodiversity…………………………………………….
C2 Specific statements, based on the work of CONSIDER…………………………….
C4 Possible approaches to mitigate biodiversity loss……………………………………
References ………………..……………………………………………………………….
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A: Conservation of Soil Diversity under Global Change
A1: Introduction
CONSIDER dealt with the most important anthropogenic activities that pose a threat
towards, or are being implemented to mitigate loss in, soil biodiversity. Threats are
habitat fragmentation and destruction and global climate change, whereas mitigation
activities include land abandonment and environmentally-friendly agriculture.
CONSIDER addressed these four topics, each at its own workshop. To further
strengthen the focus of discussions, CONSIDER has performed, during the course of
its workshops, assessments or multidisciplinary measurements at existing field
experiments of relevance to the theme of the workshop.
The four topical workshops were on Land Abandonment (Workshop 1), on Habitat
Fragmentation (Workshop 2), about Environmental Friendly Agriculture (Workshop
3), and Climate Change (Workshop 4). The synthesis is not only a listing of outputs
from the topical workshops but also involves dealing with questions like: Can
environmental friendly agriculture (e.g. reduced amounts of fertilisers and pesticides,
more organic matter left in the soil, more diverse crop cover) counteract the negative
effects of arable land, such as fragmentation of habitat of some soil organisms into
areas of sub-optimal size? How successful will this mitigation be compared to
establishment of larger set-aside areas for these soil organisms, i.e. can we improve
soil organism diversity by changing instead of terminating agriculture in an area?
The synthesis workshop aimed at giving an integrated/balanced view of the
importance of the four issues from the previous workshops. These integrative
discussions involving the end-users were based on the discussions at the 5´th
workshop and area also the basis of this synthesising paper on soil biodiversity to
include recommendations for future strategy.
A2: Diversity of soil organisms
Soil is composed of organisms spanning a size range of five orders of magnitude from
micro-organisms and microfauna in the µm range over insects, arachnids, molluscs
and worms in the mm to cm range to soil dwelling mammals measured in dm.
Similarly, the individual numbers of the smallest organisms amount to 1014 bacteria
m-2 soil surface distributed on 10,000 species via microfauna amounting to 107-108 m2
soil distributed on hundreds of species to 10,000 individuals m-2 of insects,
arachnids, molluscs and worms distributed on, say, 100 species and finally one
mammal m-2. This high diversity is not superseded by any other environment and
there are special problems when associating e.g. diversity and evenness indices to an
entity like the soil bacterial community (Hill et al. 2003). The high diversity in soil is
most likely caused by the special features of the environment. The spatial
heterogeneity of the soil environment probably reduces interactions among organisms,
minimising direct interactions such as competition (Giller 1996) and thereby enabling
high diversity among organisms that are not particularly selective in their food choice
(Setälä 2005). Also, biotic drivers from the very local spatiotemporal scale (like
competition and predation) to the large spatiotemporal scale (like plant succession)
promote soil biodiversity (Wardle 2006).
The huge diversity of soil organisms may not have much intrinsic value
(aesthetic, cultural, ethical, political), but the functional value of providing nutrients
for plant growth and removing dead material from the soil surface is evident. On top
of this come values that are not esteemed at present but may become evident in the
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future. This may involve e.g. enzymatic decomposer capabilities of commercial or
environmental value. Other values of a high soil biodiversity would arise if diverse
systems were more productive, more sustainable, more resistant to perturbation, or
more resilient following perturbation. For this to be the case, diverse systems should
(i) have a larger repertoire (toolbox) to play with, (ii) provide more interactions
among groups of organisms, and (iii) have a higher redundancy. It was the task of
CONSIDER to challenge these beliefs of the consequences of soil biodiversity and
furthermore to evaluate, as much as possible in quantitative terms, how much
biodiversity is necessary in the soil system.
A3: Importance of Soil Biodiversity
It is well known that species of soil organisms differ in their effects on the functioning
of ecosystems. To exemplify, all arbuscular mycorrhizae fungi (AMF) are important
for soil aggregation, but also the fungal species matters as different AMF species
interact differently with different plant species in producing water stable soil
aggregates (Piotrowski et al. 2004, Rillig and Mummey 2006). Bacterial communities
formed during 7-8 years after introducing AM fungi also differ as a function of the
AMF clade added (Rillig et al. 2006). Remarkably, these bacterial communities had
differential effects on soil aggregation in the absence of AMF (Rillig et al. 2005),
indicating that aggregate formation happened by a concerted action of AMF and
bacteria. The composition of the plant endoparasitic nematode community in soil
affects plant growth (Brinkman et al. Oikos 2005), whereas the presence of AMF can
reduce the attack of such pathogens (la Pena et al. 2006) as well as aboveground
insect herbivory (Wamberg et al. 2003). Other soil organisms may also reduce
aboveground herbivores as seen with soil nematodes and leaf suckers and their
parasitoids (Bezemer et al. 2005) and with root feeding insects and leaf chewers
(Bezemer et al. 2003). In contrast, insect root herbivores may stimulate aboveground
insect herbivores as well as their parasitoids (Masters et al. 2001). Soil macrofauna
can affect the relationship between litter diversity and decomposition in forests
(Hättenschwiler and Gasser 2005) and enchytraeids can be essential for the spread of
saprotrophic fungi through soil (Rantalainen et al. 2004). For macrofauna, the species
identity and the functional dissimilarity between species has been found to be more
important for decomposition, CO2 production, and litter mass loss than the diversity
of these animals (Heemsbergen et al 2004).
Evidence of the importance of meso- and macrofauna on soil functioning differs from
that of the importance of microorganisms and microfauna. This is because larger
organisms can be added to and removed from a rather undisturbed system, whereas
manipulating microbial populations requires pretreatments like sterilisation that can
dramatically alter the system under study. For microorganisms, the assembly
approach has demonstrated that not only functions, like decomposition, that are
carried out by a large fraction of the soil community, but also functions, like
nitrification, that are performed by a more specialised group of organisms are very
insensitive to diversity of organisms (Wertz et al. 2006). A large redundancy can thus
often be demonstrated; i.e. removing of what corresponds to 90% of the microfauna
species using chloroform fumigation did not affect decomposition of plant material
(Griffiths et al. Oikos 2000). Similarly, a community of 5 soil decomposer fungal taxa
was equally efficient in C mineralisation as compared to systems with 48 taxa of soil
decomposer fungi (Setälä and McLean 2004). However, even though soil
communities with reduced biodiversity performed well in decomposition of plant
material, soils with most reduced diversity (e.g. lacking functional groups of
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nematodes), were not resilient in their functioning when subjected to a stress like
heating (Griffiths et al. 2000). In another study, the same authors built up biodiversity
by adding different dilutions of soil suspensions to sterilised soil (Griffiths et al. SBB
2001) and found that in this case, less diverse soil communities were more robust in
their functioning to the stresses applied (Cu addition or heating) than in their previous
study (Griffiths et al. 2000). This discrepancy may be due to parts of microbiota not
being present alive in the inocula used by Griffiths et al. (2001) but being present in
the soil before organism removal started in the first study (Griffiths et al. 2000). This
demonstrates how removing vs. adding organisms when creating diversity gradients
for microorganisms may affect the results, and thus adds an extra problem to studies
of importance of microbial vs. macro-organism biodiversity.
A4: Threats to soil biodiversity
There have been dramatic declines in both range and abundance of many species
associated with farmland in Europe and there is growing concern over the sustainability of
current intensive farming practices (Hole et al. 2005). During the last 40 years, one-third
of the world‘s arable land has been lost by erosion, current loss rate being more than 10
million hectares per year (Pimentel et al. 1995).
Global change processes predicted over the next century involve climate change
and marked changes in land use of the society (Schröter et al. 2005). One of the major and
immediate threats to biodiversity, and therefore also to soil biodiversity, is land use
change. In an attempt to evaluate the importance of current land use changes, it is
important to place them in a historic context, i.e. to consider also those land use changes
that occurred previously. During the three preceding centuries, cropland and pasture areas
have increased 5-7 times. This change took place mainly during the 19th century in
temperate areas and about 100 years later in the tropical region (Goldewijk 2001). In this
light, the 10% increase in area covered by forests and the 13% decrease in the agricultural
area in Europe during 1960-2000 (FAO Statistics 2007) do not exceed the rates of change
in previous centuries. Predicted future reduction in agricultural area in EU is marked,
however, amounting to a 50% reduction up to year 2080 (Rounsevell et al. 2006). During
the last decade of the 20th century, the decrease in agricultural area in Europe was due to
increases in artificial surfaces (8.100 km2) and forests/semi-natural open lands (4.700
km2) (EEA 2006). Sometimes, changes in land use may distort the equilibrium dynamics
between vegetation and climate so that the original vegetation will not recover following
land abandonment: for instance, the change in cover and diversity of shrub species
prevented the reestablishment of the original oak forest in the Mediterranean areas
(Barbero et al. 1990). Decades of intensive agriculture, together with an increase in area
(resulting in habitat fragmentation), have also diminished biological diversity on arable
land, both above- and below-ground, but we know far less about the latter.
Climate is changing globally as a result of both human activity (emission of
greenhouse gases) and natural oscillations. Climate change, with expected changes in
temperature, rainfall distribution and increased CO2 concentration may well further
affect soil biodiversity and the sustainability of soil processes. Elevated CO2 is
predicted to increase net primary production (Wardle et al. 1998) and decrease litter
decomposability (Couteaux & Bolger 2000). These changes mediated by plants may
have positive effects (Yeates et al 2003, Hungate et al 2000), no effects (Markkola et
al 1996, Haimi et al 2005) or negative effects (Loranger et al 2004) on populations of
soil organisms. When combining these varying effects of CO2 with the other factors
of climate change, it is not surprising if complex interactions will occur. For primary
production, such complex interactions have been observed for the plant cover where
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knowledge of e.g. the effect of altered precipitation pattern and CO2 cannot accurately
predict the combined effect of altering CO2 and precipitation (Shaw et al. 2002). To
date, most studies of the effects of agricultural intensification and global change on
biodiversity have been dedicated to protect biodiversity of visible, aboveground
systems. However, agricultural intensification has also affected the hidden
biodiversity and sustainability of belowground systems where we often do not even
know the size of organisms (Smith et al. 1992). Severe nutrient leaching losses, soil
erosion or a decrease in soil organic matter can be the result. In the review emerging
from CONSIDER workshop 4, it is demonstrated how climate change affects soil
organisms (Lindberg et al. 200X) and it is suggested that interactions among climate
factors may affect the response of belowground organisms as demonstrated above
ground for plant production. Such interaction effects between elevated CO2 and
altered precipitation on the soil nematode fauna have also recently been reported
elsewhere (Andersen et al. in prep.).
A5: Biodiversity – function relationship
Both functional and ethical arguments strongly support the imperative for conserving
soil biodiversity (Hagvar 1998). However, with a few exceptions, the relationship
between biodiversity and ecosystem functioning has been investigated from the
aboveground perspective (Hector et al. 1999, Tillman 1999, Symstad et al. 2000), and
there is an urgent need for a belowground perspective (Mikola and Setälä 1998,
Wardle et al. 2000, Griffiths et al. 2000, Griffiths et al. 2001). In a meta-analysis of
studies that link biodiversity and functioning in ecosystems, the majority (338) of 448
studies were on terrestrial systems (Balvanera et al. 2006). Moreover, 258 studies, i.e.
the majority of the terrestrial ones, were on grasslands and most of these focused on
plants and to a much smaller extent on herbivores (Balvanera et al. 2006). The intense
focussing on grassland plants and aquatic microbial systems in laboratory conditions
potentially make conclusions on diversity-function relationships less relevant for
communities like soil biota with high diversity and many links (Duffy et al. 2002).
Some species may also be more important than others for ecosystem functioning as
revealed in the Ecotron work (Lawton 1994). In the soil, the unknown role of the
large number of very small soil organisms (the microbes) and the small number of
large organisms further complicates the understanding of the relationship between
species number and processes performed (Fitter 2005).
One of the very few studies on the importance of biodiversity of soil organisms
revealed that around eight AM species out of a pool of 23 are needed for optimal plant
diversity, growth, and phosphorus uptake (van der Heijden et al. 1998). However,
with this kind of experimental approach there is always the risk that certain species
have special properties that, rather than the diversity of organisms, can explain the
observations (Scheublin et al. 2007). For instance, Laakso and Setälä (1999)
demonstrated how presence or absence of a specific species of enchytraeid worm
could produce such apparent biodiversity effects. Even among microbes such effects
can be apparent: Bell et al. (2005) found that several single isolates of soil bacterial
performed better (respired more) than assemblages containing 72 species.
A6: Plant biodiversity - soil biodiversity
Vegetation affects biodiversity belowground through the quality and quantity of litter
input and the form of root exudates (Belnap and Phillips 2001, Ehrenfeld et al. 2001,
Wardle and Nicholson 1996). In the same manner, microbial biomass (Bardgett et al.
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1999), trophic structure of the soil community (Yeates 1999), and functions such as
production of CH4 (Ström et al. 2005) can be affected. Plant production as well as
nutrient uptake efficiency seem to be higher in diverse plant communities in tropical
(Hiremath and Ewel, 2001) and temperate ecosystems (Van Ruijven and Berendse
2005). Similarly, water use efficiency is higher in plant mixtures than monocultures
(Caldeira et al., 2001). The activity and biodiversity of soil organisms is known to
control the magnitude and chemical nature of nutrient fluxes that affect soil fertility
and plant growth (Beare et al. 1992, Lavelle 1997), as well as plant succession
(DeDeyn et al. 2003) including the relationship between rare and invasive plants
(Klironomos 2002). However, plant diversity effects on soil community diversity
appear to be idiosyncratic;in a plant diversity experiment, plant identity was found to
be important for nematode diversity than plant diversity (De Deyn et al. 2004).
The common experimentation performed during workshop 1 of CONSIDER
suggested that communities of soil organisms within the rhizospheres of various plant
species depended on the species of the plant, as well as on the diversity of the
surrounding plant community, which the plants were part of (Bezemer et al. 200X).
The relationship between plant species and soil organisms can further affect
succession following land abandonment. Shortly after land abandonment, the soil
community reduces the performance of the early succession plant species thereby
enhancing the rate of succession (Kardol et al. 2006). However, when succession
proceeds, the soil community provides a more positive feedback to the plant
community, thereby slowing down the succession process (Kardol et al. 2006).
Current status of knowledge of Plant biodiversity - soil biodiversity relationship
in relation to climate change and land use.
 The plant community is an important driver of soil community composition and
soil ecosystem processes and services.
 Soil organisms can influence the composition of the plant community and changes
therein.
 Soil organisms and aboveground organisms influence each other through their
influences on plant performance and plant community composition
 Plant identity is more important to soil diversity than plant diversity
 Soil organisms influence plant diversity, but whether or not this is due to soil
biodiversity is less clear
 Land use change can take place at high speed (e.g. conversion of pasture into
arable land or forest), but the conversion of soil communities requires
restructuring of the entire soil food web, which can take decades.
 Climate change may impact on plant diversity through changes in soil community
composition, with direct effects of soil organisms on plants through herbivory and
symbiosis and indirect effects through altered nutrient cycling
A7: Soil organic matter – soil biodiversity
Soil biodiversity is intimately bound to soil organic matter; litter and humus materials
form the basal resources of the belowground food web. Whereas the effect of elevated
temperature in climate change will undoubtedly reduce soil organic matter, the effect
of elevated CO2 is less certain, even though a reduced C sequestering in soil has been
observed (Heath et al. 2005). These observations are in line with the quite frightening
predictions by the latest earth system models when applied to specific areas of
temperate Europe (Smith et al. 2007). There are uncertainties, however, with regard to
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the dynamics of CO2 production and consumption in climate change scenarios, and
not the least for the circumpolar region (Sitch et al. 2007). So even though these
natural processes only constitute a few percent of the CO2 emissions from burning
fossil fuel (Zhuang et al. 2006), we do need to pay attention to them as well. To
maintain soil activity and productivity in arable systems, organic manuring,
undersowing and mulching are frequently practised methods. It is further known that
soil food webs consist of bacterial and fungal energy channels (Beare et al. 1995,
Moore and DeRuiter 1991) and that fungi tend to dominate in ecosystems with less
favourable litter input and discrete organic layers, whereas bacteria tend to dominate
in ecosystems with more favourable litter input and high below-ground input of root
exudates. The lack of more detailed knowledge of the effects of this kind of driving
forces on soil biodiversity is surprising considering that soil organisms are intimately
bound to essential ecosystem processes such as decomposition and mineralisation and
even formation of soil aggregates (e.g. Jungerius et al. 1999, Bossuyt et al. 2004) and
infiltration of water (Mando et al., 1996).
Current status of knowledge of Soil organic matter – soil biodiversity
relationship in relation to climate change and land use.
 Soil organic matter and decomposer community composition and functioning are
intimately linked.
 To fully exploit the potential of the decomposer food web for ecosystem
functioning it need to be fuelled by organic residues. Therefore, for a sustainable
management of agricultural systems, organic farming systems need to be adopted.
 Organic farming significantly increases the numbers and biomass of major
decomposer taxa thereby:
# fostering internal nutrient cycling
# increasing the fixation of carbon (by plants or how?) in soil organic matter
# improving aggregate stability and soil surface roughness resulting in reduced
soil erosion
# increasing water infiltration rates and water holding capacities of soils fostering
water capture and reducing soil erosion
 Increased soil organic matter concentrations do not necessarily result in increased
soil biodiversity; increasing soil biodiversity needs a more integrated approach
including:
# spatially structured agricultural fields
# reduced management intensity
# intelligent crop rotation systems
# reduced use of pesticides.
A8: Spatio-temporal effects on soil biodiversity
Spatial heterogeneity in soil organism distributions occurs on nested scales, and is
shaped by a spatial hierarchy of environmental factors, intrinsic population processes
and disturbance (Ettema and Wardle, 2002). Many soil organisms also exhibit
temporal heterogeneity due to their ability to form resistant, resting structures during
periods of poor substrate availability in soil (Felske & Akkermans 1998). We know
very little about how the relationship between soil biodiversity and soil processes
varies on spatial and temporal scales. This would be important, however, when
developing recommendations of the suitability of individual species, and effectiveness
of different techniques, in biodiversity restoration. At the microscale of soil structure,
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it seems to be advantageous for plants that organic resources that are mineralised at
different rates are separated by several mm in soil, whereas for decomposer microbes
a complete mix of the resources seems to be more beneficial (Jingguo and Bakken
1997). At this scale, we also know that mineral nutrients diffuse freely between
resources within a few days, whereas organisms in decomposer communities, such as
nematodes, may differ dramatically on resources separated only by a few mm
(Christensen et al. 2007). In contrast, very little is known of the mechanisms at larger
scales that are relevant to larger soil organisms. Soil macrofauna can stimulate
nutrient turnover and soil organic matter dynamics (Lavelle et al. 2006), thereby
acting as engineers that modify the environment of other soil organisms (Hedde et al.
2005, Velasquez et al. 2007) and even stimulating gene exchange among microbes
(Daane et al. 1996). Enchytraeids also act as vectors for the spread of saprotrophic
fungi through habitat corridors (Rantalainen et al. 2004). Although this effect of the
macrofauna is normally considered beneficial, there are examples where the activity
of macrofauna has been deleterious for ecosystem functioning through harmful effects
on soil structure (Chauvel et al. 1999). The spatial distribution of soil organisms may
also have profound effects on the plants; for instance, mycorrhizae was found to have
a heterogeneous distribution in disturbed sites, while older sites had less patchy
distribution of dense populations (Boerner et al. 1996). This means that in undisturbed
sites the hyphal networks of both AM fungi and ECM fungi will be larger, more
homogeneously distributed and give a higher probability of infecting plants, either
present in the seed bank or dispersing into the area.
The spatial issue is further complicated by interactions between soil and air.
Soil organisms serve as a major resource for many air-borne generalist predators of
foliar herbivores, including spiders, and staphylinid and carabid beetles. In times of
low supply of herbivore prey, these generalist predators switch over consuming soil
arthropods from the soil surface. At the onset of herbivore development in early
summer, the generalist predators are then able to switch to foliar herbivores as prey,
preventing insect pest outbreaks (Settle et al. 1996, Scheu 2001, Snyder and Wise
2001).
Current status of knowledge on Spatio-temporal effects on soil biodiversity in
relation to climate change and land use
 Many ecosystem services, such as soil aggregation, plant nutrient uptake and
water retention, are processed by mycorrhizal associations. Intensive
agriculture disrupts the spatial distribution of mycorrhizal associations, by
increasing their spatial heterogeneity and decreasing total abundance.
 Soil organisms have an ability to resist disturbance by dispersing in time,
through different dormant stages. This strategy is also used by pests in
monocultures, which may be counteracted by increased diversity of the soil
organisms.
 The links between above and belowground organisms are on different spatial
and temporal scales, which explains the problems of tracing evolutionary and
functional patterns between above- and belowground communities.
A9: Multitrophic interactions and soil biodiversity
Many rhizosphere microorganisms are closely associated (mutualistic or antagonistic)
with plant roots, whilst the free-living decomposer organisms are known to regulate
these interactions (Griffiths et al. 2007). This regulation includes (i) grazing on
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mycorrhizal fungi (Setälä 1995, Klironomos and Kendrick 1995), (ii) grazing on plant
pathogens (Curl 1988, Pussard et al. 1994), (iii) dispersal of plant-growth stimulating
micro-organisms (Doube et al. 1994, Lussenhop 1996), and (iv) dispersal of microorganisms antagonistic to root pathogens (Stephens and Davoren 1997). These effects
of belowground organisms on plant performance can further propagate to higher
trophic levels, as shown in studies where decomposer community has strongly
affected the performance of above-ground herbivores (Scheu et al. 1999, Bonkowski
et al. 2001). Supporting this, aboveground plant defence to natural enemies has been
found to be influenced by the complexity of the soil community (Bezemer et al.
2005).
It is also now known that the growth, reproduction and population dynamics of
organisms living in the soil environment can be profoundly affected by the presence
of aboveground herbivores (Gange and Brown 1997). However, with extremely few
exceptions, the strengths of the interactions between these organisms are unknown
and the role that natural enemies in one compartment (soil or above-ground) have on
the organisms in the other compartment has never been explored (Gange 2001, Van
der Putten et al. 2001). An important question is whether the interactions between
these spatially separated organisms are mediated by nutritional or defensive chemical
changes in the host plant (Van der Putten et al. 2001). Furthermore, it is possible, that
all of the interactions observed are mediated by the presence of fungi within the foliar
or root tissues of the plant (Gange 2001). The critical points are to discover the
strengths of the interactions between these spatially separated organisms, and to
determine whether observed changes in visible, above-ground groups, as a result of
land use change or climate change, can be used as predictors of changes in invisible,
subterranean organisms. In the evaluation of importance of these interactions on
plants and plant associated organisms, it is crucial to know what one group of
organisms means to the life of the other. There is probably no doubt that the plant
means everything for the plant-associated organism, and that mineralisation of plant
nutrients by decomposers is essential to the plant (Alphei et al. 1996). Recent
research, however, indicate that plant roots may only transfer a minor fraction of
carbon to the belowground soil organisms when compared to the respiration activity
of the root itself (Christensen, Bjørnlund, Vestergård 2007). Such information is
essential in the evaluation of the evolutionary significance of changes in the
rhizodeposition from plants.
Current status of knowledge re. Multitrophic interactions and soil biodiversity in
relation to climate change and land use

The CONSIDER programme has enabled us to determine that the diversity of
life above ground is strongly influenced by the diversity below ground.

Land use change, in terms of habitat loss or agricultural intensification, can
reduce soil biodiversity at all spatial scales.

We know that the identity of species in the soil profoundly influences growth
of above ground organisms, but we do not know the exact mechanism of this,
though we suspect it to be through a modification of plant chemistry

Conservation of soil biodiversity is critical, not just for maintaining a
sustainable soil, but for maintaining the composition of above ground plant
and animal communities too.
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A10: Aboveground-belowground interactions as an organizing framework
Terrestrial ecosystems consist of above and belowground subsystems which contain a vast
number of species that interact at various spatial and temporal scales. Recently, especially in
the areas of terrestrial nutrient cycling and plant defence, empirical studies have shown that
interactions between above or belowground species and communities have important
consequences for ecosystem processes (Wardle et al. 2004), and that species interactions in
the above and belowground subsystems can influence those in the opposite subsystem (e.g.
Fukami et al. 2006). However, the complexity of possible interactions between above and
belowground species and their variances in scale dependencies are enormous (Bardgett et al.
2005, De Deyn and Van der Putten 2005), which complicates the identification of general
patterns and the development of new theory. In this workshop we reviewed empirical studies
on above-belowground interactions and discussed how the development of testable
hypotheses will benefit from a coupled empirical-theoretical modelling approach. We propose
that such a combined empirical-theoretical approach will enhance our conceptual
understanding of population dynamics and their consequences for community interactions and
ecosystem processes in natural and managed ecosystems. We also review how such
approaches will enhance our capacity to predict future changes due to global (humaninduced) climate change.
A11: History of the aboveground-belowground interactions framework
Ecologists have long been aware that plant productivity and the development of plant
communities are influenced by soil fertility. For example, agricultural research has a well
established tradition of considering consequences of soil fertility for crop yield and the attack
of crop plants by their natural enemies, such as aboveground aphids. Likewise, in (semi)natural systems, studies as early as the nineteen seventies have shown that aboveground
herbivores may indirectly influence belowground herbivore and decomposition processes.
Despite this knowledge, already outlined in Hairston et al.’s 1960 green world hypothesis,
these earlier studies made little acknowledgement of the spatial and temporal scales of the
interactions in one subsystem as compared to the other. Also, ecological concepts developed
for one subsystem have rarely been applied to the opposite subsystem. For example, the
concept of tritrophic indirect interactions between plants, aboveground invertebrate
herbivores and their natural enemies has been almost exclusively developed and tested for
aboveground communities (Price et al. 1980), whereas a feeding guild and foodweb approach
to analyze fluxes of nutrient and energy has been strongly developed by soil ecologists (Hunt
1987, De Ruiter et al. 1995).
Less than 20 years ago, the issue of how above- and belowground species and communities
interact started to be investigated (A. Gange, V.K. Brown, G. Masters), and there is now a
growing body of literature from empirical studies in this area. However, with this increase in
the number of studies been done, there is growing uncertainty about the generality of
findings. For example, there is still no consensus or general prediction about if and why root
herbivores and their natural enemies may enhance or reduce the performance of shoot
herbivores and their natural enemies. The opposing effects observed (e.g. Masters et al. 1993
versus Bezemer et al. 2003) may depend on the model system used, initial herbivore densities,
abiotic or a variety of other environmental conditions. Experimental testing would require
many detailed case specific studies at a variety of temporal and spatial scales, and while
general patterns may exist, they tend to only be detectable at larger spatial or temporal scales
(Wardle et al. 2004).
A12: Linking empirical to modelling approaches
General patterns could also be observed using modelling to identify essential interactions on
which empirical efforts can then be concentrated in turn. Thereby, empirical studies of the
crucial interactions can establish the link to reality of patterns emerging during model
analysis. Models can be used to develop general concepts from small-scale experiments and
10
thereby contribute to the development of ecological theory on above- belowground
interactions in a scale-explicit and reality-proof way. To comply with this claim, we propose a
basic modelling framework that consists primarily of a combination of two linked subecosystems (e.g. Moore et al. 2003). These two systems are defined on the basis of the
primary energy source. The first is the primary producer based subsystem, consisting of roots
and shoots, above- and belowground herbivores and predators. These interactions involve
above and belowground primary and secondary plant compounds, direct and indirect
interactions and constitutive and induced defences. The second is the detritus based system,
consisting of dead organic material (detritus), primary decomposers (fungi, bacteria) and
detritivores (earthworms), microbivorous organisms and predators. This activity of the
detritus based system, which is mainly located below ground, has major consequences for
developing a conceptual framework on above-belowground interactions.
A13: Mitigation activities.
A13-1: Dealing with effects of land use change Just as the above-mentioned threats
are mainly related to agricultural activity, mitigation activities also deal with
agriculture. When agricultural land is abandoned by set aside, aboveground plant
community management can speed up the transfer towards more natural vegetation
(Hansson and Fogelfors 1998, Van Der Putten et al. 2000, Leps et al. 2001). Feedback
mechanisms occurring between above- and belowground communities guarantee that
soil organisms will also be affected by this process (Bever et al. 1997). A less drastic
mitigation activity compared to set aside is environmental friendly agriculture, where
crop residues are left on the soil surface to provide more organic matter and crop
cover can be more varied compared to the traditional monoculture. It is envisaged that
the effects of environmental friendly agriculture on soil organisms qualitatively
resemble the mechanisms operating following set-aside. The common
experimentation performed following workshop 3 of CONSIDER also showed that
elevated organic inputs stimulated the soil biota controlling organic matter
decomposition, and that the omission of pesticides and inorganic fertilisers strongly
stimulated the diversity of weeds, diptera larvae, and surface living predatory spiders
at the expense of leaf sucking aphids (Birkhofer et al. 20XX). These changes in
above- and belowground organisms are to be considered beneficial (for what?) and
occurred without any marked reduction in crop yield. With respect to global climate
change, the amounts of soil organic carbon being emitted to the atmosphere can be
markedly reduced – by up to 44% - if an improved agricultural soil management is
adopted (Smith et al. 2007). Such favourable standards of organic farming include:
reduced use of chemical pesticides and inorganic fertilisers; preservation of mixed
farming; higher number of crops grown in rotations; smaller field size; use of farm
yard and green manure; intercropping and undersowing; mechanical weeding; and
sympathetic management of non-cropped habitats (Hole et al. 2005). In Frick,
Switzerland, 21 years of organic farming have been shown to enhance soil fertility
and above- and below-ground biodiversity and on top of that to give a high energy
and nutrient efficiency. In this large-scale agricultural experiment, organic farming
used 34-53 % less fertilizers and 97 % less pesticides than conventional farming,
while the output was still 80 % of conventional yields (Mäder et al., 2002).
Current status of knowledge on consequences of land use change for soil biodiversity.
 Managing community composition and ecosystem processes and services after
land use change requires consideration of soil community composition and soil
biodiversity
11



Undesired vegetation development (including noxious weeds in vegetation and
biological invasions of exotic species) often depends, at least indirectly, on soil
organisms or soil community composition.
Management of soil organisms is constrained by long development times of soil
communities
Ecosystem management starts with managing soil communities
A13-2: Dealing with effects of climate change. Conservation of biodiversity and
mitigation of climate change provides a link between IPCC and CBD (convention on
biological diversity) and it is a challenge to bring these two communities together.
What is needed to conserve biodiversity is primarily the maintenance and restoration
of resilience as an essential element of adaptation to sustain the delivery of ecosystem
goods and services. Resilience being the ability of an ecosystem to maintain functions
after being perturbed will decrease the sensitivity. Biological factors, which confers
resilience includes genetic heterogeneity and ecosystem connectivity (”Report CBD
2005”; Eleventh meeting Montreal, 28 November - 2 December 2005 (Item 6.6 of the
provisional agenda; Report of the meeting of the ad-hoc technical expert group on
biodiversity and adaptation to climate change).
There is no reason to believe that most of the precautions taken with respect to
biodiversity in general (focus on reduction of CO2; awareness of general threats to
biodiversity to give synergistic impact) are not valid for soil biodiversity as well,
even though ”production of biofuels” will certainly not improve soil biodiversity; on
the contrary actually. It is suggested that mitigation of climate change effects on
biodiversity is done through land use change. However, afforestation and reforestation
activities can have positive, neutral or negative impacts depending on the ecosystem
being replaced and management options applied. The best opportunities for positive
effects of afforestation and reforestation activities can be achieved on degraded and
reclaimed lands with (i) natural regeneration and native species, (ii) minimal clearing
of pre-existing vegetation, (iii) minimal use of chemicals, (iv) extended rotation
lengths, and (v) low impact harvesting methods. Introducing trees into agriculture
(agroforestry) will have positive effects on soil biodiversity especially in the humid
tropics (Mutuo et al. 2005), and avoiding deforestation from the beginning can
provide the greatest biodiversity benefits (Braulio Dias,CBD, Brazil, Informal joint
meeting of the CBD-SBSTTA and UNFCCC-SBSTA, Montreal 30 November 2005).
Current status of knowledge on consequences of climate change for soil biodiversity.
 Studies of the impacts of climate change on soil biodiversity have utilized two
approaches: firstly, empirical studies of current distributions and modelling of
likely shifts in distribution, and secondly, experimental manipulations of climate.
 Increasing amount of work exists on the effects of changes in temperature and soil
moisture on the populations of soil organisms. A more limited body of work exists
on the interactions between these factors, and the implications of changes in the
abundance of soil organisms for ecosystem processes.
 Empirical evidence suggests that the effects of climate change are likely to be
most pronounced in high latitude and high altitude zones where soil food webs are
relatively simple and opportunities for distribution shifts are likely to be limited.
 Modelling work indicates that climate change is likely to have strongest effects
on the abundance of taxa, which have a high number of consumers, emphasising
the importance of consideration of multi-trophic interactions.
12
 In theory, changes in the distribution of species and functional groups as a result
of climate change can be compensated for by changes in the abundance and
distribution of other taxa, with no effect on ecosystem service delivery.
 More research is needed of the role trophic complexity in stabilising the provision
of soil ecosystem services in the face of climate change, and particularly of spatial
variability in soil food webs, the dispersal ability of soil organisms and species
redundancy in functional groups.
 Changes in climate are likely to have a significant impact on the carbon budgets
of European ecosystems. Increases in temperature will lead to increases in
decomposition rates if soil moisture levels are sufficient. In some areas of Europe
with highly organic soils, such as the peatlands of the Boreal areas, changes in soil
faunal populations as a result of increases in temperature are likely to have
significant effects on carbon storage.
 In managed ecosystems, changes in top down drivers (including those
encouraged as part of climate change mitigation policies) are likely to have more
dramatic effects on soil biodiversity and the ecosystem services it delivers than the
direct effects of climate per se.
 Afforestation and further abandonment of agricultural land have a potential to
benefit soil biodiversity, whilst in some geographical zones, declines in soil
fertility, soil organic matter content, soil moisture and the increased frequency of
fires may threaten the ecosystem services that soil organisms provide.
B: The CONSIDER project in relation to needs and wishes expressed by the EU.
B1: The EU policy
The common EU Policy on agriculture from the 1950’s has been governed by the
themes intensification and subsidies. During the last decade land abandonment and
marginalisation has been added as new themes to combat the overproduction in
agriculture within the EU.

The CONSIDER project timely addressed this shift in EU policy by
addressing land abandonment at one of its four topical workshops (WS1).
B2: The EU thematic strategy on soil protection
This was made public by the EU commission in September 2006 (Thematic Strategy
on Soil Protection, 2006). According to the strategy, further research is necessary to
close the gaps in knowledge about soil and to strengthen the foundation for policies.
The Commission intends to follow the recommendations from the stakeholder
consultation, on the following priority clusters:
A. processes underlying soil functions, e.g. (1) biomass production in agriculture
and forestry, (2) storing, filtering, transforming nutrients, substances and
water, (3) biodiversity pool for habitats, species, genes, (4) environment for
humans, (5) source of raw materials, (6) acting as carbon pool, and (7) archive
of geological and archaeological heritage
B. spatial and temporal changes in soil processes,
C. ecological, economic and social drivers of soil threats,
D. factors influencing soil eco-services, and
E. operational procedures and technologies for soil protection and restoration.
13
The CONSIDER project dealt with several of the above-mentioned priorities,
namely A(3), B, and E.
B3: Visions expressed by EU Commission, DG Environment
According to The European Commission, DG-Environment Unit Agriculture, Forests
and Soil (Niek de Wit), invited to Workshop 6 of CONSIDER, specific soil
biodiversity issues that need to be addressed are (De Wit 2006)
A. relationship Soil biodiversity  Soil functioning,
B. Aboveground  belowground interactions,
C. Land use effects on soil biodiversity
D. Use of Soil biodiversity as indicator of soil health/quality,
E. Increase of knowledge on biodiversity to use as tool in management strategies,
F. Risk assessment for Soil biodiversity in relation to soil use and pollution;
G. Use of Soil biodiversity to mitigate climate change effects, and
H. Improving Research infrastructure, finding best practices and identifying research needs.

The CONSIDER project prioritised its effort on many topics of the abovementioned list: Topic A is underlying all work-packages (WP1, 2, 3, and 4) of
the project, Topic B is directly addressed in WP4, and the contents of Topic C
were dealt at the Workshops 1 and 3.
B4. Wishes expressed by the EU Environmental Agency
At the visits to the EEA office in Copenhagen, it became clear that the agency wants
“clear examples showing that biodiversity matters” (Anne Rita Gentile, EEA Office,
Copenhagen).
At WS6 of CONSIDER we presented studies that clearly showed how
biodiversity matters for ecosystem functioning (particularly at section B: “The
importance of soil biodiversity – case studies”; see abstracts 3-7 at the end of
this document).
C: Recommendations from CONSIDER for the EU Commission on soil
biodiversity
C1:
Important properties of soil biodiversity.
Soil biodiversity is extremely high; most functions have many actors and a
great redundancy among generalists seems apparent. A probable explanation
for this are the spatially isolated sub-environments that characterise the soil
system.
 With respect to general functions like decomposition and nutrient
mineralisation, there is evidence that very few organisms are needed for the
functioning of the system. To maintain resistance and resilience of the soil
system, redundant species are, however, needed so that these can take over if
the original actors are disturbed.
 Research and conservation of soil communities and processes would benefit
from disregarding biodiversity as an operational term and instead explicitly
focusing on the different functions and species present in the soil.

14
Plant biodiversity
And soil biodiversity (WP1)
Plant identity overwhelms effects
of plant diversity on the soil
system and soil biodiversity
Soil organic matter
and soil biodiversity (WP2)
The anticipated increase in land use
intensity is expected to threaten soil
organic matter pools and the
functioning of the decomposer
system
New plants invading due to
climate change will have new
traits that affects soil biodiversity
The increase in temperature and
precipitation in Central Europe is
likely to result in reduced SOM of
arable systems thereby threatening
the functioning of the decomposer
system
For mitigating losses of organic
matter its return has to be
intensified by adopting organic
farming systems, crop rotations
including slow decomposing
species and breeds increasing
carbon retention
As above
Land use change
Climate
change
Mitigating effects on soil
biodiversity of
Climate
Land use change
change
Consequences for soil biodiversity of
C2: Specific statements, based on the work of CONSIDER:
Complex and long crop rotations
are more important in fighting
plant pests than having more
species at the same time: A long
crop rotation will improve pest
control
15
Spatio-temporal effects
on soil biodiversity (WP3)
Organisms with poor dispersal and
large individual distributions
(earthworms, AM-fungi, and
Basiodiomycetous fungi) are
negatively affected by fragmentation
and their recolonisation probabilities
are lower. This has effects on
reduced function of ecosystem
services as decomposition, nutrient
transfer and production of soil pores
Drastic climatic events, as drought
and flooding, will have major
changes on soil biodiversity mainly
through influence by loss of organic
matter
Multitrophic interactions
and soil biodiversity (WP4)
Agricultural intensification will
reduce soil biodiversity quickly
(over few years), but if the
change is positive, i.e. reversion
to natural habitat, the
concomitant positive effect on
the soil will be slow (takes
decades)
Heterogeneity is needed on a
landscape scale to ensure that main
ecosystem services are maintained
Land abandonment will restore
above-below ground community
interactions, but the process is
slow. Pesticide reduction and
removal must be done to hasten
the process.
Prevention of loss of organic matter
trough sustainable use of soils is
needed
Increasing soil biodiversity will
enable the community to resist
invasion, hence reducing pest,
weed and disease problems in all
types of community
Negative effects if niches for
invasive species are created and
no natural predators of these
invaders exist
C3: Future research questions based on the work of CONSIDER
 We need to identify key soil organisms providing specific ecosystem services.
At present we only have macrofauna acting as mixers and nitrifying bacteria
providing nitrate and thereby providing fast delivery of nitrogen to plant roots.
 How much redundancy is required to maintain general functions under altered
(stressed) conditions? How does this required level compare to the actual
diversity within functional groups in the soil system?
 We need to understand how to integrate knowledge on spatial and temporal
dynamics of soil organisns with climate change and land use, and how
cascading effects of increased carbon assimilation into soil will affect trophic
interactions in the soil biota.
 Do we have to establish and maintain ecological corridors between natural
sites (refugees) and the other land area of Europe to be able to fully benefit
from the biodiversity at the preserved sites?
 Ultimately we want to know if soil biodiversity can mitigate climate change
and especially if sustainable use of soils can both store carbon and restore
biodiversity at the same time?
 Recently, we have shown that soil organisms can influence plant community
composition and aboveground multitrophic interactions. The next step is to
identify where and how these effects express themselves, where they are most
influential and how they change due to global changes.
 Then, based on this knowledge, we can determine if these are necessary to be
counteracted by management and how that management should look like.
C4: Possible approaches to mitigate biodiversity loss
We need proper predictions. We are faced with some areas where we are now
becoming aware of the role of soil organisms (succession, biological invasions, plant
community composition/ diversity and above-belowground multitrophic interactions).
What is needed now is a better understanding of where and how these soil-borne
influences are most influential and how they react on global change. Then, based on
the predicted consequences, we can determine if these are necessary to be
counteracted by management and how that management should be.
With respect to the threats from land use and climate change, the possible actions can
be categorised into three groups: (1) Wait and see and find best approach, (2) Buffer
unwanted changes when possible, and (3) a Pro-Active approach.
(1) In the Wait and see –approach one should invest in protecting safer regions of the
world, where the effects of climate change and land use are less severe. In contrast,
those systems that should be most influenced should be studied intensively and the
diversity-functioning relationships at these sites should be related to the diversityfunctioning relationships at sites subjected to less severe changes. This approach
would reveal the impacts of climate and land use change on the biodiversity and
functioning of soil subsystems.
(2) In the Buffering approach, soil biodiversity is restored by abandoning agricultural
land and by linking these ex-arable fields to each other and to remaining agricultural
areas using ecological corridors. In specific cases, where an aspect of land
16
management is known to create problems for a group of soil organisms, action is
taken to avoid this (specific buffering action).
(3). The Pro-Active approach should involve mapping of soil biodiversity across
Europe to determine the hotspots of soil biodiversity and measures should be taken to
protect biodiversity in these areas. Particularly warm e.g. cities and south facing
slopes on the northern hemisphere) and cold (north facing slopes under dense plant
cover on the northern hemisphere) habitats, where the ‘future diversity’ might already
be present, should also be identified. The biodiversity hotspots and extreme habitats
should then be linked together with ecological corridors in an attempt to conserve soil
biodiversity under different land use and climate change.
CONSIDER suggests that the Pro-Active approach (3) is first used throughout Europe
to identify the diversity hot-spots. After these spots have been identified, the
Buffering (2) and the Wait and See -approach could be used under circumstances
where organisms cannot be identified, which would have a specific response to
climate or land use change,.
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