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Soil biodiversity, biological indicators and soil ecosystem services—an

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Soil biodiversity, biological indicators and soil ecosystem

services—an overview of European approaches
Mirjam Pulleman1, Rachel Creamer2, Ute Hamer3, Johannes Helder4,
Céline Pelosi5, Guénola Pérès6 and Michiel Rutgers7

Soil biota are essential for many soil processes and functions, Introduction
yet there are increasing pressures on soil biodiversity and soil The Convention on Biological Diversity (CBD; URL:
degradation remains a pertinent issue. The sustainable http://www.cbd.int/) and the Millennium Ecosystem
management of soils requires soil monitoring, including Assessment [1] have underlined the relationships between
biological indicators, to be able to relate land use and biodiversity loss and a decline in the capacity of ecosystems
management to soil functioning and ecosystem services. Since to support human well-being. Being the legally binding
the 1990s, biological soil parameters have been assessed in an international agreement for the conservation and sustain-
increasing number of field trials and monitoring programmes able use of biological diversity, the CBD has stimulated a
across Europe. The development and effective use of demand for indicators suited to monitor trends in the state
meaningful and widely applicable bio-indicators, however, of biodiversity and natural resources [2]. Soils are a natural
continue to be challenging tasks. This paper aims to provide an resource that must be secured for future generations, as
overview of current knowledge on the characterization and rates of soil formation or recovery are often too slow to cope
assessment of soil biodiversity. Examples of biological soil with current rates of soil loss and degradation. Soils also
indicators and monitoring approaches are presented. host an enormous biodiversity, in terms of abundance,
Furthermore the value of databases for developing a better numbers of species and functions of organisms. The organ-
understanding of the relationship between soil management, isms and their interactions are fundamental to many soil
soil functions and ecosystem services is discussed. We processes and functions, including organic matter
conclude that integration of monitoring approaches and data decomposition, nutrient cycling, soil structure formation,
sets offers good opportunities for advancing ecological theory pest regulation and bioremediation of contaminants. In
as well as application of such knowledge by land managers and aggregated form these processes and functions relate to
other decision makers. ecosystem services that are essential to humans, such as
Addresses food production, climate regulation and provision of clean
1
Wageningen University, Department of Soil Quality, PO Box 47, 6700 water [3,4,5] (Figure 1). Although biodiversity that is
AA Wageningen, The Netherlands
2
Teagasc, Johnstown Castle, Wexford, Ireland
‘hidden’ belowground has long received little attention,
3
Dresden University of Technology, Institute of Soil Science and Site this attitude has started to change. Loss of soil biodiversity
Ecology, Pienner Strasse 19, 01737 Tharandt, Germany caused by the expansion, intensification and mechaniza-
4
Wageningen University, Laboratory of Nematology, The Netherlands tion of agriculture has been identified as a major problem
5
INRA (National Institute of Agronomical Research), UR251 PESSAC, F-
across Europe. Related pressures include soil erosion,
78026 Versailles cedex, France
6
University Rennes, 2 rue du Thabor, CS 46510 35065 Rennes Cedex, organic matter decline, compaction, contamination, salini-
France zation and climate change [6,7].
7
National Institute for Public Health and the Environment, Laboratory for
Ecological Risk Assessment, PO Box 1, 3720 BA Bilthoven, The Different EU policies, e.g. on water quality, pesticide use,
Netherlands
waste management or nature conservation, contribute in
Corresponding author: Pulleman, Mirjam ([email protected]) some way to soil protection. However, regulations are
very specific to the threat of concern and do not consider
soil biodiversity as such, nor the wider context of soil
Current Opinion in Environmental Sustainability 2012, 4:xx–yy quality. The adoption of the EU Soil Thematic Strategy
This review comes from a themed issue on Terrestrial systems in 2006 was a first step towards a coordinated approach to
Edited by Saskia Keesstra and Gerben Mol ensure the protection of soils in Europe [8]. Further
integration of soil biodiversity conservation into EU
legislation, however, is hampered because the level of
knowledge has been considered insufficient to recom-
Received 13 March 2012; Accepted 08 October 2012 mend policy [4]. A better understanding of soil organ-
isms, their distributions, interactions and functions in
1877-3435/$ – see front matter, # 2012 Elsevier B.V. All rights soils and how they translate into ecosystem services is
reserved. therefore essential to guide action [7]. A necessary first
http://dx.doi.org/10.1016/j.cosust.2012.10.009 step is a better knowledge on spatial and temporal distri-
bution of soil biodiversity and how this relates to soil

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Please cite this article in press as: Pulleman M, et al.: Soil biodiversity, biological indicators and soil ecosystem services—an overview of European approaches, Curr Opin Environ Sustain (2012),
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COSUST-266; NO. OF PAGES 10

2 Terrestrial systems

Figure 1

Soil-based
Agricultural goods delivery processes
Food and fibre Nutrient capture and cycling

OM input decomposition Aggregate Functional

Ecosystem functions Assemblages
SOM dynamics
1. C transformations Decomposers
Soil structure maintenance • fungi
• bacteria
Biological population regulation • microbivores
• detritivores

Non-agricultural Soil-based
2. Nutrient cycling Nutrient transformers
services delivery processes
• decomposers
Water quality and supply Soil structure maintenance • element transformers
• N-fixers
Nutrient cycling • mycorrhizae

Erosion control Soil structure maintenance 3. Soil structure Ecosystem engineers

maintenance • megafauna
• macrofauna
Atmospheric composition SOM dynamics • fungi
and climate regulation • bacteria
Pollutant attenuation and Decomposition
4. Biological population Biocontrollers
degradation
regulation • predators
Nutrient cycling • microbivores
• hyperparasites
Non-agricultural pest and Biological population regulation
disease control

Biodiversity conservation Habitat provision

Biological population regulation

Current Opinion in Environmental Sustainability

The relationships between functional assemblages of soil organisms, aggregate ecosystem functions and ecosystem services. Ecosystem services
represent aggregations of functional outputs of biological processes that are of direct benefit to the society.
Kibblewhite et al., 2008 [3].

management and habitat quality. A crucial second step is sustainable management of soil biodiversity and soil
to better communicate the implications for ecosystem ecosystem services.
services, such that soil biodiversity conservation is taken
into account in decision making. In the face of those Soil biodiversity
needs, monitoring of biological soil parameters has been Soil biota comprise the organisms that spend all or part of
initiated in several countries and data are becoming their life cycle belowground. Soil organisms range from
increasingly available. This paper combines a literature the myriad of invisible microbes, such as bacteria, fungi
review on soil biodiversity and biological soil indicators, and protozoa, to the macro-fauna, for example earth-
with examples of monitoring programmes across Europe. worms, ants and termites (http://www.fao.org/ag/AGL/
We aim to address the following objectives: agll/soilbiod/). Larger animals such as moles and voles
are considered soil fauna, but rarely included in soil
1. To provide a brief overview of current knowledge and biodiversity assessments because of their small numbers.
developments related to soil biodiversity characteriz- And although plants belong to the soil biota their role is
ation. beyond the scope of this review. It is however recognized
2. To discuss the development of biological soil that plant root exudates and plant residues form the major
indicators and monitoring systems, based on European source of carbon and energy for heterotrophic soil biota.
experiences. For an illustrated overview of different soil organisms,
3. To discuss needs and opportunities for data integra- their functions and important threats we refer to the
tion and stakeholder involvement, to advance the European Atlas of Soil Biodiversity [9].

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Please cite this article in press as: Pulleman M, et al.: Soil biodiversity, biological indicators and soil ecosystem services—an overview of European approaches, Curr Opin Environ Sustain (2012),
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Soil biodiversity, biological indicators and soil ecosystem services Pulleman et al. 3

One of the most complete definitions of soil biodiver- Box 1 Examples from different broad functional groups that have
frequently been used as biological soil indicators: Earthworms
sity is derived from the CBD definition of biodiversity:
(photograph: R.G. de Goede.
Soil biodiversity comprises ‘the variation in soil life,
from genes to communities, and the ecological com-
plexes of which they are part, that is from soil micro-
habitats to landscapes’ [4]. This variation is generally
described in terms of three interrelated attributes of
biodiversity: composition, structure and function [10].
We then consider soil biodiversity as the quantity,
variety and structure of all forms of life in soils, as well
as related functions [11]. Soil organisms have tradition-
ally been classified according to their taxonomic pos-
ition, throphic interactions and body size class [12,13].
Taxonomic identification can be problematic because a
vast amount of soil organisms has not yet been ident-
ified, especially in the microbial community. Moreover,
Earthworms: These invertebrates belong to the functional group of
technical and labor constraints may apply as a result of ecosystem engineers [3,4]. By producing soil structures such as
the huge diversity of certain groups, such as microor- burrows and excrements they strongly modify the habitat for other
ganisms, nematodes and mites. Relations between soil soil organisms, including plant roots. Earthworms can play a
biodiversity and ecosystem functions, however, tend to particularly large role in litter transformation and incorporation as well
as soil structure formation [22]. Earthworms are used as bioindica-
depend more on structural and functional diversity than
tors in contaminated soils because of their sensitivity to soil
on species richness or taxonomic parameters per se pollutants (e.g. heavy metals and organic contaminants) [28]. They
[14,15,44]. This phenomenon is partly explained by also respond strongly to agricultural practices (e.g. tillage, crop
the high level of functional redundancy within species- rotations, pesticides application, organic matter inputs)
rich soil communities [15]. As an exception, so-called [22,28,32,37,44,53]. Species (e.g. approximately 100 in France)
are classified into three ecological groups (anecics, endogeics and
‘keystone species’ have been identified for their unique epigeics) that provide different functions and show different
role in specialized soil processes [16]. Examples are sensitivity to soil disturbances or chemical contamination
fungal species that are capable of decomposing recal- [28,53,32,54]. Epigeic earthworms live at the soil surface and feed
citrant organic compounds [17], symbiotic micro organ- on plant litter. Anecics create permanent vertical or subvertical
burrows and feed at the soil surface. Those two groups are
isms involved in atmospheric N fixation or P uptake by
negatively affected by soil tillage. Endogeics feed on mineral soil
plants [18] or bioturbators like earthworm species (Box enriched in soil organic matter, and therefore benefit from organic
1). matter incorporation either through tillage or the activities of epigeics
or anecic earthworms [55]. Anecic and endogeic earthworms play a
Considering the complex of biotic interactions in the soil, key role in the formation and maintenance of soil structure, enhance
water infiltration and remediation of soil pollutants and reduce soil
in conjunction with the abiotic environment, it is essential erosion [30,37]. Total abundance or biomass of earthworms are
to determine soil processes and functions using a com- commonly used as indicators (Table 2). Nevertheless the functional
prehensive as possible characterization of soil biodiver- group diversity may be a better proxy for habitat quality and soil
sity. Like ecosystems in general, soils are hierarchical functions [11,28,53]. An important advantage of earthworms as
indicators is that taxonomic identification is relatively easy. Earth-
systems with internal processes operating at each level of
worms can be observed with the naked eye and are commonly
organization and interacting across levels. Hierarchy known, and are therefore suitable for communication purposes with
theory suggests that higher levels facilitate or constrain stakeholders. However, their spatial variability in the field can be
the behavior of lower levels. An extensive discussion on high, which makes representative sampling a laborious task.
the hierarchical relations between habitat characteristics,
soil organisms and implications for ecosystem functions is
provided by Lavelle [19]. The microbial world
represents the major part of the soil community in terms
of total biomass and is largely responsible for organic organo-mineral soil material. As they can modify the soil
matter decomposition, nutrient transformations and habitat in terms of physical structure and availability of
degradation of toxic compounds (Box 3). The soil micro resources to other soil organisms, those soil animals have
and mesofauna regulate the activities of the microbial been characterized as ‘ecosystem engineers’ [19] (Box
community, mainly through predation, thereby releasing 1). Soil organisms with larger body sizes, including the
nutrients [20]. The soil macrofauna, in turn, can possess a ecosystem engineers, have frequently been found to be
strong effect on the distribution and activities of those more sensitive to anthropogenic disturbances than smal-
smaller groups of soil organisms. For instance, the soil ler organisms [21–23]. Hierarchical theory suggests that
macrofauna comprises ecological groups that have the the disappearance of soil ecosystem engineers can have
ability to dig in the soil profile, create burrows, nests strong impacts at lower levels of organization, including
and galleries while mixing, ingesting and/or excreting biological regulation by smaller soil fauna.

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Please cite this article in press as: Pulleman M, et al.: Soil biodiversity, biological indicators and soil ecosystem services—an overview of European approaches, Curr Opin Environ Sustain (2012),
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COSUST-266; NO. OF PAGES 10

4 Terrestrial systems

Accordingly, Kibblewhite et al. [3] and Turbé et al. [4] multiple levels of organization (organism, population,
classified soil organisms into functional assemblages that community, ecosystem) and at multiple spatial scales
act at different spatio-temporal scales, and are associated (e.g. from plot to farm to landscape) [10,19]. Different
with different functional domains [19] (Figure 1). A organisms from the three functional groups or hierarchical
distinction is made between: levels described in the previous section have frequently
been used as biological soil indicators (see Boxes 1–3 for
1. ‘Decomposers’ and ‘nutrient transformers’ [3] examples). Other organism groups that have commonly
(grouped as ‘chemical engineers’ by Turbé et al. been measured in monitoring programmes are micro-
[4]), that is soil microorganisms (Box 3); arthropods, for example collembola (springtails) and acari
2. ‘Biocontrollers’ [3] (or ‘biological regulators’ [4]), that (mites) [31,34] and other mesofauna, for example enchy-
is small invertebrates, such as nematodes (Box 2), traeids (potworms) [31] (Table 2). In addition to the
springtails and mites, which act as herbivores or organisms themselves, soil structures created by soil
predate on other invertebrates or micro-organisms; biota, especially biogenic soil aggregates formed by eco-
3. ‘Ecosystem engineers’, that is soil macrofauna such as
termites, earthworms (Box 1), or ants.
Box 2 Examples from different broad functional groups that have
It should be noted that this broad classification does frequently been used as biological soil indicators: Nematodes. The
provide a generalization as multiple functions can be picture represents a nematode curling through the soil pore space
(photograph: K. Ritz).
performed by different functional assemblages and over-
lap in functions occurs across all levels (e.g. microbes can
contribute to soil aggregate formation [24]). Furthermore,
the functional assemblages do not operate in isolation.
This implies that an intervention that affects one function
will inevitably alter other functions [3,19] (Figure 1).

Biological soil indicators

The concept of indicators is widely used in environmental
monitoring, mainly in relation to anthropogenic disturb-
ances. Indicators are measurable surrogates for environ-
mental end points that are in themselves too complex to
assess. Such indicators, either biological, physical or chemi-
cal, give information about the state and trends as well as
the seriousness of the situation, and should support
environmental decision making [2,4,10]. The soil com- Nematodes are biological regulators and represent one of the most
munity provides many potentially interesting indicators for numerous and speciose groups in soils. Soil nematodes are
environmental monitoring in response to a range of stresses trophically diverse and include economically important plant para-
or disturbances [3,25–27,28]. According to Gerhardt [29], sites. They show a high and diverse sensitivity to pollutants and
because of their trophic diversity nematode assemblages do not only
we define biological indicators as (characteristics of) organ-
reflect their own fate, but also the condition of the bacterial, fungal
isms whose response, in terms of presence/absence, abun- and protozoan communities. These characteristics make them
dance, activity, morphology, physiology or behavior, gives potentially interesting bio-indicators for soil health and soil dis-
information on the condition of a habitat or ecosystem. turbances [56]. Although nematodes can easily be sampled and
They are useful in situations where the environmental end extracted from soil, their identification is time consuming and
requires expert knowledge. Previous studies demonstrate that the
point is difficult to measure directly, or where the environ- small subunit ribosomal DNA (SSU rDNA) gene harbors enough
mental stressor is easy to measure but difficult to interpret phylogenetic signal to distinguish between nematode families,
in terms of ecological significance [29]. Biological soil genera and often species [57]. A robust and affordable quantitative
indicators have been applied in environmental risk assess- PCR-based nematode detection tool for agricultural and scientific
purposes, and comparable tools for the assessment of the
ment and monitoring of responses to land use (e.g. [30,31]),
ecological condition of soils, are being developed [58]. Briefly this
agricultural management (e.g. [28,30,31,32,33]) and soil works as follows: after nematodes extraction from soil the nematode
contamination (e.g. [26,28]). The parameters measured community is lysed and after DNA purification the lysate is used to
include different soil organisms selected for their sensi- quantitatively characterize nematode assemblages. The difference in
tivity to soil management or environmental pressures, and/ DNA contents of various life stages is limited and different
distributions of the life stages barely interfere with quantitative
or for their relevance for soil functions (such as organic community analyses. Verification in recent field studies suggests that
matter decomposition, N mineralization or soil structure Q-PCR based analysis of nematode assemblages is a reliable
formation) or for soil quality or soil health in general [3,25]. alternative for microscopic analysis. The availability of an affordable
and user-friendly tool might facilitate and stimulate the use of this
ecological informative group of soil inhabitants.
The hierarchical organization of the soil community and
ecosystems suggest that soil biodiversity be monitored at

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Please cite this article in press as: Pulleman M, et al.: Soil biodiversity, biological indicators and soil ecosystem services—an overview of European approaches, Curr Opin Environ Sustain (2012),
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COSUST-266; NO. OF PAGES 10

Soil biodiversity, biological indicators and soil ecosystem services Pulleman et al. 5

Box 3 Examples from different broad functional groups that have Table 1
frequently been used as biological soil indicators: Microorganisms.
The picture on the left side represents bacterial cells. The picture on Seven criteria for the selection of biological soil indicators
the right shows fungal hyphae in soil (blue stained) as observed in a 1. Meaningful – Indicators must relate to important ecological
soil thin section (photograph: K. Ritz). functions
2. Standardized – Parameters should be standardized to ensure
comparability of data
3. Measurable and cost efficient – Parameters should be
assessable not only by experts, in order to ensure that
the indicators will be used in practice and can be routinely
collected
4. Policy relevance – Indicators should be sensitive to changes
at policy-relevant spatio-temporal scales, and allow for
comparisons with a baseline situation to capture progress
towards policy targets
5. Spatio-temporal coverage – Indicators should be validated
in a wide range of conditions and should be amenable to
aggregation or disaggregation at different spatial scales, from
ecosystem to national and international levels
6. Understandability – Indicators should be simple and easily
understood
7. Accuracy – The value of the indicators should be precise
and robust reflecting the changes they monitor

Source: Turbé et al. [4]

[36] and Turbé et al. [4] (Table 1). No single indicator

will comply with all these criteria. In practice, focus is on
the development of sets of complementary indicators,
including both biotic and abiotic parameters. However,
Microorganisms: Chemical engineers decompose organic matter
despite the fact that a multitude of indicators estimating
and transform nutrients. Soil microorganisms dominate this some aspect of soil biodiversity exists, no reference set of
functional group [3,4]. They indicate environmental changes by standardized indicators is available. This issue, as well as
modifications in (i) quantity/biomass, (ii) structure and/or (iii) promising avenues for progress on indicator development
activity [36,38]. Until now the impact of microbial biomass versus
and application, are discussed in the remainder of this
community structure on ecosystem processes and function is
uncertain [38,59,60,62]. Levels of functional redundancy among paper.
microorganisms depend largely on function and environment
considered [15,16,61]. Disconnections between factors driving
microbial community structure and those driving its function further Examples of European approaches
complicate indicator selection [62]. To comprehensively assess
Since the late 1980s biological parameters have been
soil microbial diversity it is recommended to include indicators of
each parameter group: quantity, structure and activity [11]. assessed in an increasing number of studies, ranging from
However, the number of studies and monitoring networks using long-term agricultural field trials [20,21,32,37] to regional
indicators of all three groups is limited (Table 2). Different methods or national monitoring programmes (e.g. [30,31,36,38]).
[41] are used to describe and quantify microbial diversity at the Currently there are over 15 European countries that have
genotype, phenotype or metabolic level, and thousands of
microbial species can occur in just a few grams of soil. To achieve
collected soil biological parameters as part of a large scale
progress in the area of microbial indicators it is important to work monitoring programme [4]. Some examples are provided
on the definition and identification of microbial functional groups in Table 2. Ideally this would provide the foundation for
and their response to environmental changes [61]. Beside integrated assessments of soil biodiversity across a wide
molecular approaches new conceptual models and experimenta-
range of situations in Europe. However, the information
tion are needed to link microbial diversity to ecosystem functions.
The development of concepts describing the relationship between has been collected for different objectives and using a
the stoichiometry of soil microorganisms (e.g. the C, N and P variety of methods, and few indicators have consistently
status) and nutrient cycling is promising [39]. been used in national-scale monitoring [31,36]. Recent
attempts to develop standardized indicator sets that
comply with the criteria listed in Table 1 are briefly
reviewed here.

system engineers, have been identified, quantified and Frameworks for selecting biological indicators for national
proposed as indicators [22,35]. soil monitoring have been devised in, for example, France
[28], the Netherlands [31] and the UK [36]. These
Criteria for the selection of indicators that are suitable for frameworks adopted a similar approach; a wide range
monitoring purposes have been summarized by Ritz et al. of candidate indicators were assembled and tested for

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Please cite this article in press as: Pulleman M, et al.: Soil biodiversity, biological indicators and soil ecosystem services—an overview of European approaches, Curr Opin Environ Sustain (2012),
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6 Terrestrial systems

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Table 2

Examples of European national or regional soil biodiversity monitoring networks, their geographical coverage and types of indicators measured

Country Programme Geographical coverage Starting year Indicators

Soil fauna Microbial parameters
Netherlands DSQN-BISQ (Dutch Soil Quality Nationwide, 1997 Micro-arthropods (collembola Quantity: Bacterial and
Network – Biological Indicator approx. 400 sites and mites), earthworms, fungal biomass
of Soil Quality) enchythraeids and nematodes Activity: Potential C and
N mineralization, anaerobic
mineralization, thymidine and
leucine incorporation rates
Structure: Functional bacterial
diversity (Biolog-ECO-plates),
bacterial structural
diversity (DGGE)
France RMQS-BioDiv (Reseau de Nationwide, 109 sites 2006 Earthworms, micro-arthropods Structure: B-ARISA, F-ARISA
Mesures de la Quality des (collembola and mites), nematodes,
Sols de France) total macrofauna
France BioIndicator Programme Pilot, 47 sites differing 2009 Nematodes, micro-arthropods Activity: Enzymatic activities
in land use, (collembola and mites), earthworms, Structure: B-ARISA,
agricultural practices or total macrofauna, bioaccumulation F-ARISA, PLFA, TTGE
contamination origin in snails, biomarkers in earthworms
(methalotionein)
UK Countryside Survey- SQID Nationwide, 256 sites 2000 Micro-arthropods (collembola Structure: Bacterial 16S tRFLP,
(Scoping biological indicators and mites), nematodes fungal ITS tRFLP, archaea amoA,
of soil quality) PLFA, culturable bacteria
Germany Several programmes organized Almost nationwide 2000 Earthworms, micro-arthropods Activity: Basal respiration, substrate-
in regions, data collated in two (collembola and mites), induced respiration
databases (UBA & EDAPHO-BASE) enchytraeids, myriapods
Switzerland NABO; Nationalen Almost nationwide, 2004 Quantity: Microbial biomass
Bodenbeobachtung Schweiz 69 sites (fumigation-extraction),
Activity: Basal respiration,
substrate-induced respiration
Structure: B-ARISA, F-ARISA,
fungal and bacterial TRFLp
Ireland Cre-Bio Survey Nationwide, 2006 Micro-arthropods (collembola
61 sites and acari), nematodes,
www.sciencedirect.com

earthworms

Source: Turbé et al. [4] and unpublished data from the ECOFINDERS project
COSUST-266; NO. OF PAGES 10

Soil biodiversity, biological indicators and soil ecosystem services Pulleman et al. 7

their suitability to be used in systematic soil biodiversity The abovementioned projects showed that different bio-
assessment. Selected indicators had to comply with logical parameters were (more) discriminative to different
requirements such as (i) pertinence to predefined soil types of disturbances, for example soil cultivation versus
functions, including agricultural production, environmen- heavily contaminated soils [28]. Comparison of data
tal interactions and habitat support, (ii) applicability to between consecutive samplings over multiple years indi-
the range of ecosystems under consideration, (iii) ability cated that species composition tends to be relatively
to discriminate between soil types and (iv) technical, stable, but abundances and biomasses were more vari-
practical and financial criteria [36]. Ritz et al. [36] and able, depending for example on weather conditions and
Rutgers et al. [33] used a systematic approach of stake- crop rotations [11,28,31]. In order to interpret the
holder consultation taking into account a diversity of end- results, there is a strong need to define reference values
user requirements and priorities. It was concluded, how- for certain combinations of land use, soil type and climatic
ever, that further work is needed to confirm the sensitivity conditions. Such references do not yet exist at a European
of the indicators, their ability to discriminate between scale, although density ranges for different groups of
soil-land use combinations and their ecological interpret- organisms have been published for a selection of soil
ation [36]. and land use types in the Netherlands [31] and France
[42]. Among the objectives of the ongoing FP7 project
One example of such work is the ongoing (2006–2012) Ecofinders are the standardization of methodologies for
French national BioIndicator programme [28]. Using the assessment of biological soil indicators, and charac-
homogeneous procedures, 47 biological parameters were terization of normal operating ranges for soil biodiversity
assessed in a large number of sites differing in land use, according to climatic zones, soil and land uses types [43].
agricultural management, contamination type and pollu- The increasing availability of ISO standards [39–41] for
tion levels. Those included microorganisms, fauna and sampling procedures and analyses is an important step
flora at the community level (e.g. abundance, biomass, towards homogenization of procedures, but further work
species and functional composition and ecological traits) is still required [11].
as well as the organism level (e.g. gene expression) (Table
2). Their potential to be used as a bioindicator for national Another important challenge for biological soil indicators
scale monitoring was validated based on their sensitivity is to capture the spatio-temporal scales over which
to different environmental conditions and disturbances, environmental changes occur. Depending on life history
and their accessibility and applicability by experts and traits and dispersal characteristics, certain groups of soil
non-specialist stakeholders. organisms can respond slowly to land use or management
changes [32,44]. Those observations emphasize the
In parallel with national initiatives, European research need for sampling designs with wide spatiotemporal
projects have been initiated to promote standardization of coverage [3,11,32]. Long-term field experiments remain
biological soil indicators, mainly through Framework important to enhance our understanding of biotic
Programmes (FP) [4]. Among those, the FP6 project responses with time after changes in management or land
ENVASSO (Environmental Assessment of Soil Monitor- use occur, as well as the underlying mechanisms
ing) was the first attempt to develop a harmonized system [32,37,44].
for soil biodiversity monitoring across Europe. Standar-
dized indicator sets were defined and organized into Linking biological soil indicators and
different priority levels [11]. ‘Level I’ indicators included ecosystem services for decision support
organisms, corresponding with the functional classifi- The rationale behind soil monitoring and the use of
cation of Kibblewhite et al. [3], as well as ecological biological indicators is to assess trends in the state of soil
functions: resources as a habitat for soil organisms, as well as their
capacity to support human well-being. Monitoring should
(1) abundance, biomass and species diversity of earth- further provide information to decision makers on what
worms (or enchytraeids if no earthworms are present, needs to be done to halt or revert negative trends. The
for example in soils with low pH); decision support function of the indicators therefore
(2) abundance and species diversity of collembola; implies that they facilitate communication with a variety
(3) microbial respiration of end users such as policy makers and land managers.
Interpretation of the data in terms of ecosystem services,
Depending on local objectives and available resources, defined as the beneficial flows arising from natural capital
the key indicators could be complemented with ‘level II’ stocks and fulfilling human needs [5], is a first step. It has
or ‘level III’ indicators [11]. Procedures and protocols, been shown that pragmatic choices enable quantification
based on ISO standards [39–41], have been tested in pilot of soil quality through the performance of multiple
sites in France, Ireland, Portugal and Hungary to assess ecosystem services, based on data derived from monitor-
the efficiency and sensitivity of the indicators across ing of biotic and abiotic soil properties [31,33,45,46].
European land-use categories [11]. Velasquez et al. [46] and Ruiz et al. [45] showed how

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8 Terrestrial systems

synthetic indicators of soil quality can be developed sal distances, as well as their lifetimes and sensitivity to
through the evaluation of different soil ecosystem ser- habitat disturbances with consequences for multiple,
vices. These compound indicators are derived from interconnected soil functions [21,23]. Mulder et al.
physical, chemical and biological soil parameters using [12] showed how mining of databases of abiotic and
multivariate analyses. These approaches allow for biotic soil variables can be used to explore general
monitoring of change through time and variation between relationships between habitat characteristics, the (trait)
sites or farms, without relying on expert opinion. Values structure of the soil community and ecosystem function-
need to be calibrated and validated with respect to the ing. Ecological concepts such as allometry, that is size-
regional or national context of the study, but the meth- abundance relationships amongst organisms in the soil
odology used to derive these indices can be applied community, and stoichiometry, that is the biotic relation-
everywhere [45,46]. Through a system of reference values ships of plants and soil organisms in terms of chemical
for certain soil and land use types performances can be compositions (e.g. nutrient-to-carbon ratios) were
compared on a relative scale [31,33]. explored. Such ecological concepts provide opportunities
to develop mechanistic models of invertebrate responses
Stakeholder involvement and weighting of trade-offs to environmental changes. Detritus-based food web mod-
between multiple ecosystem services is central to the eling has already been used successfully for quantification
identification and prioritization of ecosystem services by of nutrient and carbon flows based on soil biodiversity
different end users [33,47]. The abovementioned assessments [20,52]. A next step is to develop these
approaches [31,33,45,46] are examples of communi- models for predicting multiple functions and services
cation tools that can be applied in awareness raising [3,50], provided that hierarchical organization of the soil
and multi-stakeholder processes and have already be community into functional assemblages and intercon-
implemented in practical situations [28,33]. When nectedness of soil ecosystem functions are taken into
spatially presented, derived models can demonstrate that account.
different options in land-use planning and management
result in highly different impacts on soil biodiversity, Conclusions
including differences in functional attributes [12,48]. To support policy and decision making towards the
For proper quantification of ecosystem services indicators sustainable management of soils across Europe, there is
should be fitted to so called ‘utility’ functions which a need for the monitoring and communication of bio-
transform the specific units of the indicator to a uniform logical soil indicators that are linked to soil functions and
scale for ecosystem service performance [49]. This is not ecosystem services. No single indicator is universally
straightforward because ecosystem services act on differ- applicable and different indicators, including biotic as
ent spatial and temporal scales. For a detailed overview of well as abiotic parameters, are needed for different func-
current thinking on, and approaches for, the classification tions and environmental conditions. Functional assem-
and quantification of soil ecosystem services we refer to blages of soil organisms have been distinguished and their
Dominati et al. [5]. hierarchical organization should be reflected in soil bio-
diversity assessments and biological soil indicator sets.
Finally, until now, interpretation of biological soil The development of sets of complementary indicators
indicators in terms of ecosystem services has largely been requires validation across a wide range of environmental
based on expert judgements [33,36]. A more robust and conditions using standardized methods to produce accu-
quantitative approach relies on empirical testing and rate and consistent results. Despite considerable progress
development of models. Datasets derived from soil bio- and several initiatives contributing to indicator selection
diversity monitoring provide potentially important and homogenization of methods, major scientific and
sources of information. One promising avenue for linking practical issues remain to be addressed. Those include
anthropogenic disturbances, soil biodiversity and ecosys- (i) adequate funding to allow sufficient spatiotemporal
tem services is based on ecological traits, that is the coverage in soil monitoring systems; (ii) definition of
morphological, physiological, behavioral or life-history reference values for different combinations of land use,
attributes of organisms. Identifying traits that determine soil type and climate; (iii) obtaining a better predictive
the response of soil organisms to (changing) environmen- understanding of the relationships between anthropo-
tal conditions, and/or can be linked to effects on ecosys- genic disturbances, soil biodiversity and ecosystem ser-
tem functions has several advantages. Those include a vices. Detailed assessments in long-term trials or
better mechanistic understanding of the relationships and observatories (LTO’s) across Europe remain important.
possible generalizations across eco-regions, independent Additionally, integration of datasets across national bor-
of taxonomy [28,50,51]. Information on trait values of ders offers data mining opportunities to develop ecologi-
soil organisms being accumulated in databases can be cal concepts and modeling of ecosystem services.
connected with the occurrence of a species as an indicator Promising avenues include approaches based on the
[28]. For example, the body size of organisms strongly analysis of ecological traits, and studying the extent to
determines their spatial aggregation patterns and disper- which driving forces behind the partitioning of energy in

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Soil biodiversity, biological indicators and soil ecosystem services Pulleman et al. 9

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