Soil health in agricultural systems Hlth RoyalSoc 2008.pdf · but non-trivial task for the...

doi: 10.1098/rstb.2007.2178, 685-701363 2008 Phil. Trans. R. Soc. B

M.G Kibblewhite, K Ritz and M.J Swift Soil health in agricultural systems

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Soil health in agricultural systemsM. G. Kibblewhite1, K. Ritz1 and M. J. Swift2,3,*

1National Soil Resources Institute, School of Applied Sciences, Cranfield University,Cranfield MK43 0AL, UK

2Tropical Soil Biology and Fertility Institute of CIAT, PO Box 30677, Nairobi, Kenya3Department of Biological Sciences, University of Essex, Colchester CO4 3SQ, UK

Soil health is presented as an integrative property that reflects the capacity of soil to respond toagricultural intervention, so that it continues to support both the agricultural production and theprovision of other ecosystem services. The major challenge within sustainable soil management is toconserve ecosystem service delivery while optimizing agricultural yields. It is proposed that soil healthis dependent on themaintenance of four major functions: carbon transformations; nutrient cycles; soilstructure maintenance; and the regulation of pests and diseases. Each of these functions is manifestedas an aggregate of a variety of biological processes provided by a diversity of interacting soil organismsunder the influence of the abiotic soil environment. Analysis of current models of the soil communityunder the impact of agricultural interventions (particularly those entailing substitution of biologicalprocesses with fossil fuel-derived energy or inputs) confirms the highly integrative pattern ofinteractions within each of these functions and leads to the conclusion that measurement of individualgroups of organisms, processes or soil properties does not suffice to indicate the state of the soil health.A further conclusion is that quantifying the flowof energy and carbon between functions is an essentialbut non-trivial task for the assessment and management of soil health.

Keywords: soil health; agricultural impact; ecosystem services; biological processes and functions;indicators

1. INTRODUCTIONSoil health is a term which is widely used withindiscussions on sustainable agriculture to describe thegeneral condition or quality of the soil resource. Soilmanagement is fundamental to all agricultural systems,yet there is evidence for widespread degradation ofagricultural soils in the form of erosion, loss of organicmatter, contamination, compaction, increased salinityand other harms (European Commission 2002). Thisdegradation sometimes occurs rapidly and obviously,for example when poor soil management leads to gullyerosion. Often degradation is slower and more subtle,and may only impact on agricultural production andthe wider environment over years. For this reason,research has been directed to devising measures of thehealth of soil, which could be used to monitor itscondition and inform its management so thatdegradation is avoided. This has led to debate aroundthe question ‘What is soil health?’

There are two ways in which the concept of soilhealth (or the closely related concept of soil quality) hasbeen considered, which can be termed either ‘reduc-tionist’ or ‘integrated’. The former is based onestimation of soil condition using a set of independentindicators of specific soil properties—physical,chemical and biological. This approach has beenmuch discussed and well reviewed (e.g. Doran et al.1994; Doran & Jones 1996; Van-Camp et al. 2004).

This reductionist approach has much in common withconventional quality assessments in other fields, suchas materials science. The alternative, integrated,approach makes the assumption that the health of asoil is more than simply the sum of the contributionsfrom a set of specific components. It recognizes thepossibility that there are emergent properties resultingfrom the interaction between different processes andproperties. These aspects do not seem to have beenexplored to the same extent in recent literature (but seeHarris et al. 1996). In this paper, we have taken theview that while the reductionist approach is anaccessible and practical means of assessing soilcondition, progress in understanding the interactionsbetween management interventions and the capacity ofthe soil to respond depends on insights into itsfunctioning as an integrated subsystem of the agroeco-system. We thus focus on analysing the extent to whichsoil can be seen to be responding as a living system toagricultural intervention and the implications of this forsustainable agricultural practices.

Our definition of soil health is derived from a contextwhich we accept as an essential feature of sustainableagriculture, namely that agricultural production shouldnot prejudice other ecosystem services that humansrequire from agricultural landscapes. Thus, our work-ing definition is that ‘a healthy agricultural soil is onethat is capable of supporting the production of food andfibre, to a level and with a quality sufficient to meethuman requirements, together with continued deliveryof other ecosystem services that are essential formaintenance of the quality of life for humans and theconservation of biodiversity’.

Phil. Trans. R. Soc. B (2008) 363, 685–701

doi:10.1098/rstb.2007.2178

Published online 4 September 2007

One contribution of 15 to a Theme Issue ‘Sustainable agriculture II’.

*Author and address for correspondence: Via Carlo Conti Rossini115, Int 12, 00147 Roma, Italy ([email protected]).

685 This journal is q 2007 The Royal Society



We establish two contextual limits to the followingaccount. Firstly, we make no attempt to review bygiving examples and data from the vast amount ofinformation relating to the performance of specificcomponents, including specific biological populations,nutrients, physical conditions, etc. that contribute tosoil health (i.e. the reductionist approach), except in sofar as they shed light on an understanding of soil healthas a system property. Secondly, we do not addresssocio-economic dimensions in any detail. Farmers, andthe weight of factors that influence their decisions,always have a tangible presence in any agriculturalintervention. We recognize the reality that anyprinciples proposed for soil health must pass the testsnot only of scientific validity but also of practicality andrelevance, but we do not presume to evaluate them inthis account.

Wehave considered agricultural systems inwhich cropand financial yields are maximized by optimal inputs ofnutrients and other resources, whether artificial ororganic, which we call ‘industrial’; as well as those‘subsistence’ systems which seek to achieve optimumyields where there is only limited access to industriallyderived inputs, including fertilizers and power for tillage.

2. AN INTEGRATED CONCEPT OF SOIL HEALTH(a) Soil as a systemSoil is undeniably a very complex system. It may bedescribed as a multicomponent and multifunctionalsystem, with definable operating limits and a charac-teristic spatial configuration. Within a continuum ofpossibilities, there are recognizable soil types thatoriginate depending on variations in factors, such asparent material, climate and topography, which largelydetermine the dominant physical and chemical proper-ties. These have often been altered, however, byagricultural interventions, such as drainage, irrigation,use of lime to alter soil reaction and additions of plantnutrients. The agricultural soil system is a subsystem ofthe agroecosystem, and the majority of its internalfunctions interact in a variety of ways across a range ofspatial and temporal scales. As an example at thesubmillimetre scale, soil microbes modify soil structureby aggregating both mineral and organic constituentsvia production of extracellular compounds withadhesive properties. Such compounds are producedby bacteria and fungi as a feeding mechanism, to aidcolony coalescence, as protective coatings againstdesiccation and as a means of attaching to surfaces—the aggregation of soil constituents is an inevitableconsequence of such material being produced.However, there is an associated change in the localsoil structure and topology of the pore network which isthe microbial habitat that affects the distribution andavailability of water, delivery of substrate and gases tothe organisms and removal of metabolic products fromtheir vicinity, with subsequent consequences for themicrobial activity. Such microbial activity is fundamen-tally governed by the availability of fixed carbon(the major ‘currency’ of the soil system), which isamenable to manipulation via agronomic factors suchas crop type, and residue and other organic wastemanagement. Organic matter indubitably plays other

important roles in modulating soil functions, forexample via the provision of surface charges, expressedas the cation exchange capacity, or influencinghydrological properties such as wettability. However,while the chemistry (and physics) of the soil systemprovides the context, and indeed sets the limits, inwhich the biotic assemblages of soils operate, theunique and absolutely crucial feature of the biota is thatit is adaptive to changes in environmental circumstances,driven by processes of natural selection, in ways that theabiotic systems of the soil are not.

(b) Services, functions and assemblages of soilHumans depend on both natural and managed(including agricultural) ecosystems for a range ofwhat have been called ‘environmental (or ecosystem)goods and services’ (Daily 1997; Costanza et al. 1997;De Groot et al. 2002). These include the naturalprocesses that support the production of food and fibre,such as nutrient cycles and the biological control ofpests and diseases together with the regulation of waterflow and quality, and influence on the gaseouscomposition of the atmosphere with its implicationsfor the control of the global climate. In reality, thesegoods and services are functional outputs of biologicalprocesses. Soil is a living system and as such isdistinguished from weathered rock (regolith) mainlyby its biology. Nonetheless, it should be emphasizedthat these functions operate by complex interactionwith the abiotic physical and chemical environment ofsoil. Both natural and agricultural soils are the habitatfor many different organisms which collectivelycontribute to a variety of soil-based goods and services(Wall 2004). Figure 1 shows the relationships betweenthese and the soil-based biological processes thatdeliver them. In the third column, these processes areaggregated into four ecosystem functions, which wepropose collectively provide the basis for all the majorservices provided by soil, viz.

(i) Transformation of carbon through the decom-position of plant residues and other organicmatter, including soil organic matter, togetherwith the synthetic activities of the soil biota,including, and particularly, soil organic mattersynthesis. Decomposition in itself is not only anessential ecosystem function and driver ofnutrient cycles but also supports a detoxificationand waste disposal service. Soil organic mattercontributes to nutrient cycling and soil structuremaintenance. Sequestration of C in soil alsoplays some role in regulating the emission ofgreenhouse gases such as methane and carbondioxide.

(ii) Cycling of nutrients, for example nitrogen,phosphorus and sulphur, including regulationof nitrous oxide emissions.

(iii) Maintenance of the structure and fabric of thesoil by aggregation and particle transport, andformation of biostructures and pore networksacross many spatial scales. This function under-pins the maintenance of the soil habitat andregulation of the soil-water cycle and sustains afavourable rooting medium for plants.

686 M. G. Kibblewhite et al. Soil health in agricultural systems

Phil. Trans. R. Soc. B (2008)



(iv) Biological regulation of soil populations includ-ing organisms recognized as pests and diseasesof agriculturally important plants and animals aswell as humans.

The biological processes that contribute to theseaggregate functions, such as carbon transformation andnutrient cycling, are provided by assemblages ofinteracting organisms (sometimes termed ‘key functionalgroups’; Lavelle 1997; Swift et al. 2004), which aresubsets of the full soil community. The major functionalgroups of organisms contributing to the four aggregatesoil functions are given in the final column offigure 1.Wepropose that soil health is a direct expression of thecondition of these assemblages, which, in turn, dependson the physical and chemical condition of the soil habitat.

These assemblages do not, however, operate inisolation but are part of an interactive soil system. Themost fundamental integrating feature is that of thefeeding relationships between organisms. Soil food webmodels are based on grouping organisms into assem-blages with similar trophic roles (figure 2). Thesetrophic groupings subsume a high degree of taxonomicdiversity which also hides a significant extent ofvariation in functional behaviour. Nonetheless, thegeneral pattern described in figure 2 is one whichhas been mirrored in a wide range of models of‘detritus-based’ systems in the soil (e.g. Hunt et al.1987; De Ruiter et al. 1994; Wardle 1995).

The primary agents of decomposition are fungi andbacteria which, in their turn, provide a food source for

a variety of microbivorous predators occupying thelower row of the larger box in figure 2. A wide range ofexperimental studies have shown the importance ofthese organisms in regulating the rate of decom-position through the release of nutrients and bystimulating microbial population turnover throughtheir feeding activity (e.g. papers in Coleman &Hendrix (2000)). This path of decomposition maybe supplemented or diverted by the intervention oflarger detritivorous fauna, such as earthworms (shownin the diagram) and other macroarthropods (such astermites in tropical soils) which consume both organicmatter and microbes, often together with soil. Infigure 2, the rate of decomposition is shown as beingregulated by climate (particularly soil moisturecontent and temperature), soil conditions (pH andparticularly habitat structure) and resource quality(particularly in relation to organic matter and thecontent of nutrients, lignin and polyphenols; Swiftet al. 1979; Lavelle et al. 1997). Soil organic matter isnot only a synthetic product of the primary decom-position process but also a substrate for decompositionand mineralization by a subset of the decomposerorganisms. In figure 2, it is presented as two fractionsdiffering in their resistance to decomposition, i.e.active (sensu labile) and slow passive. These fractionsare also hypothesized to differ in their functional roles,with the former contributing more to nutrient cyclingand the latter to soil structural features.

Detritus-based food webs have been used forquantitative assessment of transfers of nutrients, energy

Food and fibre

Water quality and supply

Pollutant attenuation anddegradation

Non-agricultural pest anddisease control

Biodiversity conservation

Erosion control

Agricultural goods

1. C transformations

3. Soil structure maintenance

4. Biological population regulation

2. Nutrient cycling

Decomposers• fungi• bacteria• microbivores• detritivores

Nutrient transformers• decomposers• element transformers• N-fixers• mycorrhizae

Ecosystem engineers• megafauna• macrofauna• fungi• bacteria

Biocontrollers• predators• microbivores• hyperparasites

Non-agriculturalservices

Biologicalpopulationregulation

Biologicalpopulationregulation

Habitatprovision

AggregateEcosystem functions

FunctionalAssemblages

Atmospheric composition andclimate regulation

Nutrient capture and cycling

SOM dynamics

Soil structure maintenance

Biological population regulation


Decomposition

Nutrient cycling




Habitat provision

OM input decomposition

SOM dynamics

Nutrient cycling

Soil-baseddelivery processes

Soil-baseddelivery processes

Figure 1. Relationships between the activities of the soil biological community and a range of ecosystem goods and services thatsociety might expect from agricultural soils. OM, organic matter; SOM, soil organic matter.

Soil health in agricultural systems M. G. Kibblewhite et al. 687




or carbon between the designated compartments.However, they are not explicit with respect to otherecosystem functions. Figure 3 hypothesizes relation-ships between the four major ecosystem functionsidentified above. In this model the arrows representflows of energy from the plant and dead organic matterto and between the four different functions. Theconcept incorporates the activity of parasitic andmutualistic micro-organisms and root herbivores assources of flow directly from photosynthate and livingplant cells into the soil system, features not shown infigure 2. The model implies a high degree ofinterconnectedness between the functions. This isdue to the high frequency with which soil organismscontribute to more than one function, i.e. theassemblages of organisms involved in the differentfunctions overlap to a considerable degree. Thus, whilemany of the organism groups implicated in figure 3 arethe same as those that are explicitly shown in figure 2,the functional model does not map directly onto thetrophic model. For instance, many of the species offungi, bacteria and detritivores, such as earthwormsand termites, that participate in decomposition alsocontribute to soil structure modification and/ornutrient cycling. This makes the simple but importantpoint that decomposition of organic matter is not only akey ecosystem function in its own right but also themain source of energy for driving other functions suchas nutrient cycling and soil structure maintenance.

Figure 3 shows that the environmental service ofpest and disease control originates in an energy flowpath from plant photosynthate, rather than throughdead organic matter, although these two energy flowpaths converge at higher trophic levels. Predators and

hyperparasites that are important in regulatingherbivores and parasites may also feed on decom-posers including those that influence soil structuremodification and nutrient cycling (figure 3). Similarlythere is a direct link between these two major energyflow paths through the key roles in nutrient cyclingplayed by the root symbiotic mycorrhizal fungi andnitrogen-fixing bacteria.

This brief analysis of biotic interactions in soil-based ecosystem functions reveals two key points withrespect to the management of soil health. First, theoverlapping nature of the biotic relationships makes itclear that soil-based functions do indeed comprise ahighly integrated system, and that intervention whichdisturbs any one function will inevitably alter thedynamics of others. The degree of interrelatednessincreases at higher trophic levels, suggesting thatchanges in the biota of these trophic groups mayhave significant regulatory impacts on the organismsand the processes they perform at the lower levels.This is most obvious with respect to a service such aspest control and also applies to the other functions. Incontrast, a second conclusion is that organic matterdecomposition, which lies at the lowest trophic level,underpins and is crucial to all the other functions, soany ‘damage’ at this level is likely to have wideimplications. This particular connection is leastobvious with respect to pest control, but if it is correctthat energy from decomposition partially supportspopulations of animals that can also be consumers ofpests, then a decrease or diversion of energy flow fromdecomposition will also influence pest regulation.

The understanding of the mechanistic basis of soilhealth would be greatly enhanced by quantifying the

Activeorganic pool

Mineral pool

Plants

Climate

Management

Fungivorousmicroarthropods

Fungivorousnematodes Protozoa Bacterivorous

nematodes

Fungi Bacteria

Plant residue

ClimateResource qualitySoil conditions

Harvest

Loss

Slow-passiveorganic pool

Earthworms Enchytraeids Microarthropods Macroarthropods

Fertilizer

Figure 2. Major trophic relationships in the soil biological community of an agricultural soil under zero tillage (adapted withpermission from Hendrix et al. (1986)).





flows of energy to and between each of the fouraggregate functions and demonstrating how theseallocations change under different circumstances,particularly those of agricultural management. Thecomplexity of the functional interactions makes this amajor challenge. In order to do this, it would benecessary to build energy flow models for functionssuch as soil structural dynamics and biological controlof soil-borne pests and diseases (as discussed in §5)and then map them onto the established models ofnutrient cycling and soil organic matter dynamics toidentify the overlaps and convergences. This mightprove particularly valuable in identifying keystonespecies or functional groups which may be susceptibleto particular types of soil management. This type ofargument has been used to identify organisms such asthe Collembola as indicators of change in below-ground food webs (Edwards 2000).

(c) Soil as a habitatThe ecosystem services provided by soil are driven bysoil biological processes, but our concept of soil healthembraces not only the soil biota and themyriad of bioticinteractions that occur, but also the soil as a habitat(Young & Ritz 2005). The key concept here is that soilprovides a living space for the biota, which is defined bythe architecture of the pore networks. Indeed, it is theporous nature of soils that governs so much of theirfunction since the physical framework defines the spatialand temporal dynamics of gases, liquids, solutes,particulates and organisms within the matrix, andwithout such dynamics there would be no function.The walls of soil pore networks provide surfaces forcolonization, and their labyrinthine nature defines how,and to large extent where, organisms can move through

the total soil volume. The enormous range in pore sizesaffords physical protection mechanisms for prey fromtheir larger predators and organicmatter frommicrobialdecomposition. Hence the capacity of the soil biota todeliver ecosystem services may be compromised notonly by loss of diversity or impairment of function butalso by destruction of the habitat via changes in soilstructure and physical–chemical properties. Organismsaggregate the solid constituents of soil, and hencegenerate structure and associated pore networks. Thesemechanisms occur across orders of magnitude inscale and involve processes of adhesion, coating,enmeshment, particle alignment and gross movement(Tisdall&Oades 1983;Lavelle et al. 1997;Ritz&Young2004). Biotic activity can also degenerate structuralintegrity, primarily through the decomposition oforganic material that, while it may be a binding agent,also represents energy-rich substrate to a predominantlyC-limited biota. The community and the habitattherefore have a two-directional interactive relationship,which encompasses both feed-forward and feedbackinteractions between the biota and architecture of thesoil. Thesemechanisms lead to the concept that soilmaybe a self-organizing system (Young & Crawford 2004).The capacity for self-organization can be recognized asan essential component of soil health,which relies on thepresence of appropriate constituents and sources ofenergy to drive biological processes.

3. FACTORS CONTROLLING SOIL HEALTH(a) Soil typeParticular soil types form in response to the nature ofparent material, topography and environmentalfactors, such as climate and natural vegetation. Past

PPHerbivory Parasitism Mutualism

(Death)

SOM synthesis

Soil structuremaintenance

Nutrientcycling

(Death)

Plant growth

Decomposition

Biological populationregulation

Figure 3. Interconnectedness between the major ecosystem functions of soil. The arrows hypothesize two flows of energy fromthe plant to the major functions of the soil biota; either directly through the actions of herbivory, parasitism and mutualisticsymbiosis, or indirectly via heterotrophic carbon-transforming processes in the soil. Soil organic matter (SOM) synthesis ispictured as supported by energy flowing from the decomposition of plant residues and contributing energy in its turn directly(i.e. by virtue of its properties) to soil structure maintenance and indirectly, through its own decomposition, to nutrient cyclingand biological population regulation. See text for further explanation.





land management by humans can alter natural soilsconsiderably, for example by loss of surface horizonsdue to erosion, alteration of soil water regime viaartificial drainage, salinization due to poor irrigationpractices, loss of natural soil organic matter caused byarable production or contamination. Thus, land-useand management are the controlling factors for soilhealth. A set of fixed characteristics such as texture,stone content, etc. combine with climate to set anenvelope of possible soil habitat conditions, especiallythose relating to the soil water regime. Variable factorssuch as pH, bulk density and soil organic mattercontent, which are influenced by land-use and manage-ment, then determine the prevailing condition of thehabitat within the range for a particular soil. Thesefixed and variable abiotic factors interact with bioticones to determine the overall condition of the soilsystem and its associated health. Primary biologicalfactors will include the presence or absence of specificassemblages and types of organisms, the availability ofcarbon substrate and nutrients, and the concentrationsof toxic materials.

(b) Organisms and functionsThe relationships between community structure andfunction are inevitably complex and a prevalent themein contemporary soil ecology (e.g. Schulze & Mooney1994; Wardle 2002; Bardgett et al. 2005). They areunderwritten by the three principles of repertoire (i.e.the ‘toolkit’ of available functions), interaction andredundancy (Ritz 2005). Relationships between diver-sity and function have been postulated to follow anumber of forms (Swift et al. 1996; Gaston & Spicer1998), but rigorous experimental demonstration ofthese issues is relatively scarce, not least owing to thedifficulty in manipulating soil biodiversity as the solefactor (Ritz & Griffiths 2000). There is someexperimental evidence that there may be thresholdlevels of soil biodiversity below which functions decline(e.g. van der Heijden et al. 1998; Liiri et al. 2002;Setala & McLean 2004). However, in many instances,this is at experimentally prescribed unrealistically lowlevels of diversity that rarely prevail in nature. Manystudies demonstrate high levels of functional redun-dancy in soil communities (e.g. Setala et al. (2005) forreview). It can be argued that high biodiversity withintrophic groups is advantageous since the group is likelyto function more efficiently under a variety ofenvironmental circumstances, due to an inherentlywider potential. More diverse systems may be moreresilient to perturbation since if a proportion ofcomponents are removed or compromised in someway, others that prevail will be able to compensate.However, more diverse systems may be less efficientsince a greater proportion of available energy is used ingenerating and countering competitive interactionsbetween components, a situation which may beexacerbated by the similarity in functional propertiesand hence potential niche competition. All thesefactors are likely to influence the patterns of interactionbetween the soil-based functions illustrated in figure 3,and thence the status of soil health.

(c) Carbon and energyThe energy that drives soil systems is derived fromreduced carbon that is ultimately derived from netprimary productivity (figure 3). Carbon is the commoncurrency of the soil system, and its transfer withassociated energy flows is the main integrating factor.This suggests that the quantities and quality of differentorganic matter pools may be indicative of the state ofthe soil system, while the flows and allocations ofcarbon between assemblages of organisms may provideinformation about their relationships to ecosystemfunctions. However, as shown above, food web modelsas presently constructed do not explain how differentassemblages use carbon to support these functions.Existing models of soil carbon dynamics (Jenkinson &Rayner 1977; Parton 1996) assume the presence ofpools of carbon that turn over at different rates. Rapidand medium turnover fractions provide immediate andshort-term sources of carbon substrate for the soilbiota. More recalcitrant forms that turn over slowlyrepresent long-term reservoirs of energy that serve tosustain the system in the longer term, as well as providesome structural stability. These models are not,however, based on measurable carbon pools or thoseused by particular assemblages of organisms. Neitherare they explicit with respect to allocation to differentsoil functions. Consequently, their utility for assessingsoil health appears to be limited.

The limitations to current models may be dimin-ished by the answers to a range of research questionsthat emerge from the previous discussion: how mightthe allocation of soil carbon regulate functionaloutputs? What quantities and qualities of organicmatter are needed to support soil system performanceand are the levels and forms of soil organic carbonindicative of soil health? Are there minimum levels ofcarbon reserves below which long-term soil health iscompromised? Are there levels of readily decomposedorganic matter which if present continually mightindicate reduced carbon transformation and so a lackof soil health? How do the forms and flows of soilcarbon to and between different assemblages exertcontrol over the physical condition of the soil habitat,and can this condition be used to infer soil health? In §4we propose some principles for defining the soil systemand assessing its health, as a basis for directing theseand other research questions.

(d) NutrientsNutrients are a controlling input to the soil system andthe processes within it. Their levels and transform-ations are critical to soil health. After carbon, thecycling of nitrogen and phosphorus to, from and withinthe soil system most affects its dynamics and thedelivery of ecosystem services, including agriculturalproduction. Manipulation of nutrient supplies toincrease productive outputs from the soil system bythe addition of fertilizers has been one of the keystonesof agriculture for centuries. Nonetheless, knowledge islimited about the impacts of nutrient additions on thecondition of different assemblages of soil organismsand thence on their functions.

Generally, while it is considered that the availabilityof carbon substrate is normally the primary limiting





factor on microbial activity in soils, this is notnecessarily the case, and there is accumulating evidencethat soil microbes may frequently be N limited(Schimel et al. 2005). Where demand for nitrogen ishigher than its supply, the functional capacity of the soilsystem will be strongly influenced by N availability. Inundisturbed natural soil systems, inputs from theatmosphere are usually low and losses through leachingor gaseous emissions are also slight because biologicaldemand for mineral nitrogen is high and any that isrendered available is quickly assimilated. When the soilsystem is disturbed, for example by tillage, losses vialeaching or to the atmosphere are increased becausemixing of the soil leads to more rapid decomposition oforganic matter and the conversion rate of organicnitrogen to mineral forms may exceed the biologicaldemand, particularly where balancing of availablenitrogen to plant requirements is poorly managed.Moreover, nitrogen is removed in agricultural produce,often in considerable excess of that which can bereplaced by natural inputs. So without balancingadditional inputs of nitrogen, and particularly withoutdue consideration of the associated carbon (energy)requirements of the biomass, soil health declines inagricultural systems owing to progressive reductions inthe pool of nitrogen available to organisms supportingsoil functions and for plant growth. Similarly, thenatural pool of phosphorus in soil is reduced throughcropping and via other pathways such as erosion,causing a decline in soil health in the absence of anybalancing replacement that inherent mineralization(i.e. weathering) can deliver. Agricultural strategiesbased on additions of animal manures and the use ofmineral fertilizers counter losses of nitrogen,phosphorus and other nutrients with the aim ofrestoring and sustaining soil health. In well-managedsystems employing high levels of manufactured,processed or mechanized inputs, where these strategiesare implemented effectively, productivity is main-tained, but it may be compromised in subsistenceagriculture where nutrient additions are inadequate orabsent. In industrial agriculture, on the other hand,additions of nutrients beyond that which can be usedby the soil–plant system lead to their damaging leakagefrom the soil system into other environmental compart-ments via leaching and gaseous emissions. In this casethe soil system is polluted and unhealthy.

4. ASSESSING SOIL HEALTH(a) PrinciplesAssessment of soil health across agricultural systems,soil types and climatic zones presents major scientificand policy challenges. Given the multicomponentnature of soil systems, the breadth of goods, servicesand functions that they are called upon to provide, andtheir spatial variability, a complex debate is to beexpected about appropriate methods for soil assess-ment. Clearly, no single indicator will encompassall aspects of soil health, nor would it be feasible(or necessary) to measure all possible indicators.

Emergent proposals for soil assessment are linkedto the establishment of legal frameworks for theprotection of soil at national (e.g. Defra 2004) and

international levels. For example, the EuropeanCommission is implementing a Thematic Strategyfor Soil Protection in Europe (European Commission2002) which identifies erosion, declining organicmatter, contamination, compaction, salinization, lossin biodiversity, soil sealing, landslides and flooding asthe main threats to soil. In response, the ENVASSOproject (European Commission 2007) has beenestablished, which is an initiative to harmonize existingdatasets to form a European-wide reference to assesscurrent and future soil status. This and other initiativescan provide valuable information about the physicaland chemical state of soil, but a rationale is needed torelate this state to soil health. The problem is that anintegrative conceptual framework is lacking for identi-fying diagnostic indicators.

To reiterate, our definition of a healthy agriculturalsoil is essentially one that is capable of supporting bothan adequate production of food and fibre and also thecontinued delivery of other essential ecosystem ser-vices. Using concepts taken from operations manage-ment theory (Slack 1997), a healthy soil could thus bedescribed as one that presents a satisfactory systemperformance. A set of system performance curves canbe imagined describing the relationship betweenpotential rates of outputs from a soil system to ratesof inputs (Kibblewhite 2005). Such curves define thecurrent capacity of a soil to support required ecosystemservices, including agricultural production and corre-spond to the familiar form of response curves (figure 4).The ‘working range’ of the soil system is that overwhich there is no degradation of system performance interms of input-to-output conversion efficiency withincreasing outputs. Above this range, performancedeteriorates as indicated by falling efficiency, but aslong as the level of inputs do not exceed the workingrange greatly, no permanent damage occurs. However,if the loading is excessive, outputs fall as the soil systembecomes increasingly compromised and at some pointpermanent degradation results. The capacity of the soilsystem to deliver goods and services is defined by theextent of the working range and the input-to-outputconversion ratio at the upper limit of the working range.

Wor

king

rang

e

Output

Input

Limit of sustainablecapacity

Figure 4. Performance curve showing an idealized relation-ship between input(s) to the soil system and delivery of anoutput of an ecosystem service. The capacity of the system isthe output above which process performance deteriorates.





Thus, the ‘healthiness’ of a soil is indicated by its actualcapacity relative to that within a population of soils.Healthy soils will have more extended working rangesand higher conversion ratios compared with lesshealthy ones.

The soil system is an open one and its health isaffected by external environmental and anthropogenicpressures. The reaction of the soil system to thesepressures can be described in terms of resistance andresilience (Griffiths et al. 2000; Orwin & Wardle2004). Resistance is denoted by the magnitude of thechange in state for a given level of perturbation. Itfurther indicates a change in conversion ratio, forexample a reduction in the respiration rate arisingfrom compaction. Resilience describes the capacity ofthe system to return to its original state followingperturbation and reflects the ‘self-healing’ capacityof the soil system, a concept that maps onto that ofself-organization. Indeed, resilience may be a wayof measuring the capacity for self-organization insoils. Some formally demonstrated examples of soilresilience are where the soil structure rejuvenatesfollowing compaction (Griffiths et al. 2005), microbialbiomass reverts to antecedent concentrationsfollowing a drying cycle (Orwin & Wardle 2004) ordecomposition potential is restored following atemperature perturbation (Griffiths et al. 2004). Ifthe perturbation is within the capacity, the soil systemcan recover to its original condition, but if not, apermanent loss of soil health is expected. For example,in the latter study, while the grassland soil under studywas resilient to a heat perturbation, this was not thecase where the soils were subjected to copper(Griffiths et al. 2004).

(b) MeasurementThere are, however, practical difficulties which makeassessment of soil system health by measurement ofperformance curves and reactions to external pressuresrather problematic. First, there is difficulty in rigorouslydefining at least some of the ecosystem services otherthan food-and-fibre production. Second, soil systemsare multifunctional and able to deliver a variety ofcombinations and levels of services, so that fullevaluation of the system performance would requirevery extensive testing. Third, soil systems are opensystems and their performance is variable and interactivewith environmental factors, such as air temperature andprecipitation, which are not easily controlled. Fourth,soil system performance does not respond instan-taneously to altered conditions, and its assessment hasto be made over significant time periods. In truth, fieldassessment of whole soil system performance requireslong-term, complex and detailed experimentation whichcan pragmatically only be conducted at a restrictednumber of sites. While an alternative within-laboratoryassessment may provide useful information that helpsto understand better how the system operates underwell-controlled experimental conditions, it cannotprovide an assessment which is indicative of wholesystem performance in the field.

The condition of complex systems is often assessedusing diagnostic tests to support operational assetmanagement because whole system performance

assessment is either impossible or too costly. Wepropose that the same approach can be applied to soilsystems to indicate their healthiness. Diagnostic testsoffer a means to provide ongoing information about thecondition, connection and configuration of thosecomponents or component processes that are criticalto overall system performance.

We have identified critical processes in the soilsystem as transformations of carbon, cycling ofnutrients, maintenance of the structure and fabric ofthe soil, and biological regulation of soil populations.There are existing techniques for assessing theperformance of specific processes linked to thesefunctions, such as respiration rates following organicmatter addition, organic nitrogen mineralization ratesduring incubation, etc. While providing useful infor-mation about specific processes, these reflect thecurrent activity within soil rather than any intrinsiccapacity to support ecosystem services. An indicationof the health of the soil system as a whole requires amore integrative approach. Individual processes are notrelated solely in a linear fashion, but within a network ofinteractions leading to a nonlinear system withassociated feed-forward and feedback loops. Buildingon our conceptual model for the soil system as a livingand reactive system whose performance is interactivewith habitat condition, we propose that assessment ofsoil system health may be achieved using diagnostictests, for example, abiotic ones that are indicative of thestate of the habitat (i.e. physical and chemicalconditions such as bulk density, aggregate stability,pH, cation exchange capacity, etc.), and the levels ofkey energy and nutrient reservoirs (e.g. ratios of organicmatter fractions and nutrient balances); as well as bioticmeasures, such as those which are discussed below,which describe the community composition andpopulations of key functional groups of organisms(earthworms, N fixers, pest-control populations, etc.).

Although there are many similarities between all soilsystems, differences in soil forming factors over spaceand time have led to distinct soil populations withcharacteristic properties. Any scientific assessment ofsoil health has to be made with due regard to thesedifferent populations. Soils that are intrinsically veryfertile, for example because they are deep, well drainedand have a favourable texture and background nutrientcontent, may be in good or bad health, and in the lattercase may only be able to support delivery of ecosystemservices at levels below that of a less fertile soil that is inexcellent (healthy) condition. The question then arises‘What levels of such measures are indicative of soilhealth?’ The ‘agricultural equilibrium’ that agroeco-systems reach following conversion from naturalvegetation could theoretically be used as a baselinefor assessing the health of similar soils. It is difficulthowever, given its dynamic nature, to establish whatthat equilibrium should be for any given combinationof soil type, climate and agroecosystem design. Thus,relative comparisons of soil health have to be madebetween modified soil systems (derived from the sametype of soil) that are, or have been, subject to differentagricultural systems and/or practices. It seems unlikely,and is scientifically naive, that exact thresholds forindividual measures can be set objectively that define





where the impact of substitutions or other managementpractices lowers efficiency below an ecologically oreconomically acceptable level. However, an approachwould be to measure chosen indicators for soilsrepresentative of the whole population of a soil typeand evaluate changes, trends and ranges within thesepopulations. From this flows the conclusion that theconcept of soil health and related diagnostic testing ismost useful when applied to soil populations at thelandscape scale, when the concern is about the generalimpact of natural pressures or agricultural practices onpopulations of similar soils at a landscape or regionalscale. A more instrumental approach is needed at theindividual field level to support operational decisionmaking about nutrient additions, pesticide appli-cations, cultivation timing, etc. Nonetheless, assess-ment of soil health by analysis of changes, trends andranges using diagnostic tests for soil habitat conditionand biological community structure offers a powerfulmeans for evaluating the impacts of climate, land usechange and altered agronomic practices on the valuablenatural capital represented by soil.

(c) Biotic indicatorsWe have argued that soil health is fundamentallyunderwritten by the assemblages that carry out thevarious key processes. These assemblages are predom-inantly biological in origin, but actually involve aparticular configuration of the biology, physics andchemistry of the soil constituents. This configuration isundoubtedly complex and unlikely to be directlymeasurable, so surrogates must be sought. The statusof the soil biota may be a surrogate measure,notwithstanding there is a panoply of ways ofmeasuring soil community attributes (Kirk et al.2004; Leckie 2005). Community-level measurementscan be classified as those based on genotype, phenotypeand function (Ritz et al. 2004), which forms a logicalseries from the fundamental information required tocreate organisms and biological molecules, through itsphysical expression to its environmental manifestation.The genetic structure of the soil biomass, particularlyat the prokaryotic level, is remarkably complex(Curtis & Stoan 2005). To date, there is little evidencethat the soil genome relates particularly to theenvironmental circumstances from which it is derived,although the biogeography of soil microbial commu-nities is not well researched. Community-level geneticprofiles tend to show great variation both within andbetween soils under both similar and disparateecosystems (e.g. Grayston et al. 2004; Fierer & Jackson2006). At a whole-community microbial level, whileeverything might not be literally everywhere, extremegenetic complexity is apparently universal and geneticprofiling has yet to be proven as a useful diagnostic ofsoil health. The much-vaunted belief that the gene isthe appropriate level to measure the state of the system(e.g. reviews by Insam 2001; Torsvik & Ovreas 2002;Kirk et al. 2004; O’Donnell 2005) may be misguided,distorted by a strong contemporary focus on (pre-dominantly organismal) genomics in biology. Inparticular, it may be an inappropriate paradigm forsoil communities due to their extraordinary diversity.The potential for the phenotypic state of the soil

community to be an effective indicator of biotic status isapparently greater. This makes ecological sense, sincethe phenotype, by definition, reflects the manner inwhich the environment interacts with the complex soilgenome and impacts upon the expressed biota—an‘environmental sieve’ through which the soil genomepasses and is manifest as the attendant phenotype.There is increasing evidence that soil microbialphenotypic profiles, such as those based on mem-brane-lipid composition, are generally coherent andconsistent, for example between different soil–land-usecombinations, under different management practicesor in soils exposed to pollutants (e.g. Kelly et al. 2003;Grayston et al. 2004; Abaye et al. 2005; Bossio et al.2005). Functional profiling is a looser concept, notleast because there are such a variety of functions thatcan be defined and measured. The so-called ‘commu-nity-level physiological profiling’ (CLPP) concept,which measures the ability of the soil community tometabolize a prescribed range of diverse carbonsources, shows potential, particularly when basedupon the use of carbon substrates added directly tosoil (Degens & Harris 1997; Campbell et al. 2003).This is because the suite of substrates employed can beprescribed according to a variety of ecologicallypertinent factors such as synergy with C inputs thatthe system normally encounters (or not), energeticstatus, molecular complexity and so forth. Coherentstudies applied at appropriate spatial and temporalscales to truly test these issues of genotype versusphenotype versus functional profiling as interpretablebiotic indicators of soil health are lacking. What is quiteclear is that any measure of soil health must bemultivariate—single properties will not adequatelyencompass or integrate the features or issues thatunderwrite soil health.

5. IMPACTS OF AGRICULTURAL PRACTICE ONSOIL HEALTHTo maximize yields of food and fibre, a variety ofagricultural management processes are imposed on theecosystem, including artificial inputs such as chemicalsand tillage. These practices and inputs supplement oreven ‘substitute’ for biological functions that are seenas inadequate or inefficient for achieving required levelsof production. This distorts the natural balance of theecosystem and may compromise the output of otherenvironmental services. The loss of non-productiveservices may affect farmers directly but often has effectswhich are distant in space and time. For example,nutrient leakage from the soil–plant system may lead todegradation of surface and ground waters and pollutedrinking water supplies, while fine seed bed prep-aration on some land may increase the risk of soilerosion and sediment transfer to streams, or lead tosurface capping, rapid surface water runoff andincreased flood risk. In these and other cases, thecosts of remediation or lost services are not borneby the farmer but elsewhere in the economy(Environment Agency 2002). Achievement of sustain-able development requires that such externalities arecontained, and new legal frameworks are beingconstructed that attach economic value to natural





functions (i.e. by recognizing them as services),particularly those that relate to the water cycle, throughlegislation, incentives, trading mechanisms, etc. (e.g.European Commission 2005). Thus, one essentialcomponent of sustainable agriculture is (as embeddedin our definition of soil health) to balance theecosystem functions in such a way as to secure thetarget of agricultural production without compromis-ing other ecosystem functions with respect to bothpresent and future needs. In this section we examinethe impacts of agricultural practice on the soil healthsystem as described above, as a basis for deriving someprinciples for managing soil for sustainable soil health.

All agricultural soils have been altered from theirnatural state by human interventions which are aimedat maximizing production functions and which, tosome degree, always result in a loss of other ecosystemfunctions. After clearing the natural vegetation toestablish agricultural fields, all the major soil propertieswhereby we describe its health are changed, largelynegatively. After a period of continuous cultivation theyreach a new, dynamic, equilibrium. This has been mostsubstantially documented in terms of the decline in soilorganic matter content over the years immediatelyfollowing clearing and the initiation of cultivation (e.g.papers in Leigh & Johnston (1994)). If there are noadditions of nutrients to replace those lost by releaseduring the transition to a new equilibrium andsubsequently in crop offtake, the capacity of the soilecosystem to deliver production and other servicesdeclines, and according to our proposed definition sodoes the health of the soil. Furthermore, the loss of ionexchange capacity which is concomitant with a declinein soil organic matter reduces the capacity of the soilsystem to retain nutrients that would otherwise beleached to groundwater.

The soil food web may also be substantiallychanged. In the Brazilian Amazon, large areas offorest have been converted to cattle pasture. Studies ofchange in the soil fauna showed that many of the mainspecies of macrofauna present in the forest soils arenot found in the pastures. In particular, the earth-worm community changed from one commonlycharacterized by about six endemic species to onedominated by the opportunistic exotic species,Pontoscolex corethrurus. This is a species which, incontrast to many of the native worms, produces highlycompact casts which have the effect of decreasing soilmacroporosity, resulting in a surface layer whichquickly becomes saturated and develops anaerobicconditions in the rainy season, which in turnstimulates methane emission and denitrification.Subsequent plant growth is also inhibited by theunfavourable soil physical conditions. Experimentsshowed that inoculation with a diverse group of thenative soil macrofauna resulted in the ‘re-engineering’of this soil to reproduce a friable soil structure(Chauvel et al. 1999; Barros et al. 2004).

The agricultural management practised in the yearsimmediately subsequent to clearing may serve to eitherexacerbate or ameliorate the processes of change put inplace during the conversion phase. The intensity ofagricultural intervention varies enormously acrossdifferent farming systems, and may be expected to

have both quantitatively and qualitatively differentimpacts on the soil health system. Different soils indifferent climatic and topographic situations may bemore or less resilient to the introduction of agriculture.Flat alluvial soils in areas without extremes of climateare less likely to degrade quickly compared with shallowsoils on steep slopes where rainfall may be intense.

The form and extent of substitution is a potentialhazard to soil health, with the three most frequentpractices being industrial pesticides (substituting forbiological pest control), mechanical tillage (substi-tuting for biological regulation of soil structure) andinorganic fertilizers (substituting for organically andbiologically driven nutrient cycles). In view of the highdegree of interconnectedness between functionsdescribed earlier, the use of energy and/or chemicalproducts to replace, bypass or modify any particularbiological function can be expected also to havesignificant consequences for other functions that havenot been targeted.

The effects of intensive mechanical tillage on soilfood webs provide a most instructive insight into theimpacts of agricultural intervention on the integratedfunctioning and health of the soil system. The adoptionfirst of animal-drawn and then of fossil fuel-driventillage was one of the most significant steps in thehistory of agricultural intensification, enabling hugesavings in human labour and increased efficiency,through improved timing in other agriculturaloperations, as well as the guarantee of a well-preparedseed bed. However, over the past two decades or so,there has been a substantial reversion to reduced tillagepractices in many parts of the world, particularly inNorth and South America (Landers et al. 2001). Themain perceived benefits driving the adoption ofreduced or even zero tillage regimes were improvedwater and soil conservation, consequent on improvedsoil protection from the retained crop residues as wellas reduced costs in terms of fuel (Van Doren &Allmaras 1978).

A number of major and long-term studiescomparing soil food webs under intensive and reducedor zero tillage conditions have been made since themid-1980s. Wardle (1995) reviewed and analysed morethan 100 papers reporting on these studies and was ableto derive a number of generalizations with respect tothe impacts of tillage on the soil food web and a varietyof processes mediated by the soil biota. The mostobvious effect is a relationship between the size of theorganism and the inhibitory effect of tillage (figure 5).This is indeed not unexpected, since mechanical tillagedisrupts the spatial integrity of the soil fabric,particularly at meso- and macrofaunal scales. Tosome extent, tillage is intended to substitute forbiological ploughing and it is well known that earth-worms are killed during this process. In no-till,however, the enhanced activity of the macrofaunalengineers in soil structure modification ‘re-substitutes’for the withdrawal of intensive tillage. The origin ofchanges to the water regime under no-tillage, such asreduced runoff, increased infiltration and storage, aresignificantly physical in origin but the results ofthe food web studies show that enhanced activity ofthe macrofaunal ecosystem engineers also plays a





substantial part. The effects of the changes pictured infigure 5 are, however, by no means confined to soilstructure modification.

In the food web of Hendrix et al. (1986) for ano-tillage system at Horseshoe Bend in Georgia, USA(figure 2), the dominant path of organic matterdecomposition was that leading from the fungi to theearthworms, a pattern very similar to that typicallyfound in forest ecosystems. In contrast, under conven-tional tillage bacteria assumed greater importance asprimary decomposers, and in the higher trophic levelssmaller fauna with shorter generation times, such asenchytraeid worms, largely replaced the earthwormsand other macrofauna. The explanation given byHendrix et al. (1986) for these effects is that duringthe process of ploughing such crop residues as areretained are both broken up and redistributed throughthe plough layer. This provides a greater surface areafor microbial colonization as well as enhanced aerationand stimulates faster and more complete decom-position. This dispersed pattern of small ‘resourceislands’ compared with the layering of residues at thesurface in no-till systems also favours bacteria overfungi, which have a greater capacity to temporarilyimmobilize nitrogen.Mechanical tillage also results in adisruption of the spatial organization of the soil,rendering previously physically protected organicmatter available to microbial decomposition, andpreviously inaccessible prey to predation, with aconcomitant acceleration of nutrient cycling. As aconsequence, increased N mineralization and higherrates of soil carbon loss are regularly found underintensive as compared with reduced or zero tillage.

Fungi also tend to predominate in reduced tillagesystems, since there is less frequent physical disruptionof their mycelia. Fungi are often overlooked asecosystem engineers but they contribute to structuralgenesis via many mechanisms (Ritz & Young 2004),and fungally mediated translocation of C and Nbetween residue layers and soil horizons can besubstantial (Frey et al. 2000, 2003). Long-term studiesof soil organic matter dynamics have shown howprogressive decline in soil carbon from the initiationof continuous intensive cropping in the mid-West of theUnited States over 60 years ago may be halted and evenreversed by reduced tillage (Paustian et al. 2000).These effects have been shown to be not only due togreater retention of carbon but also due to improvedaggregate formation (Six et al. 1999).

Thus, with respect to three of our four keyenvironmental services, carbon transformation, nutri-ent cycling and soil structure modification, intensivemechanical tillage shows a significant negative effect,which can, however, be reversed under many circum-stances without loss, and in many cases with gains, ofcrop production. Reduced tillage is usually associatedwith increased weed development and the retention ofresidues can also stimulate diseases that are retained inthem (e.g. the root-rot and stem-infecting fungusRhizoctonia) or pests and diseases that respond to theincreased moisture (such as slugs, and fungal rots suchas Pythium species). This has lead to increased use ofherbicides in many such systems, sometimes alsoassociated with other pesticide. Wardle’s (1995) reviewrevealed two interesting features in this respect. First,that the impacts of herbicides on the soil food web, and

Width of organism (mm)

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0.001 0.002 0.004 0.008 0.016 0.032 0.064 0.128 0.256 0.512 1.020 2.050 4.10 8.190%soilC

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n of

inde

x V

BacteriaC N

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Figure 5. Differences in soil communities (shown in relation to their body size), carbon and nitrogen in mechanized versusno-tillage agriculture averaged for 106 studies across a variety of site conditions (adapted with permission from Wardle 1995).The index V is a measure of the abundance or mass of organisms under mechanized as compared with no-tillage; a value of zeroimplies equal abundance in each treatment, negative values indicate inhibition by mechanized tillage to a maximum of K1, i.e.the state in which the organisms only occur under no-till (see original paper for further details).





thence on their functions, was usually very slight; andsecond, that the presence of weeds frequently enhancedboth carbon and nutrient dynamics by providingadditional organic inputs.

The most significant lesson that the widespread anddetailed studies of the effects of tillage contribute to ourunderstanding of soil health is that the single practice ofploughing has multiple, and largely negative, impactson the soil biota, the processes they mediate and theenvironmental functions that they contribute. Further-more, these impacts are highly interactive between thefunctions, supporting the concept proposed in figure 3.The positive side of this story is that the response of thesoil biota to a removal of this disturbance is one ofintegrated reconfiguration, revealing the resilience ofthe system, and that the capacity for self-organizationhas not been lost. These generalizations must clearly bequalified by the differences in detail that occur underthe varying circumstance of soil type, climate andmanagement intensity.

The same broad lesson emerges from considerationof the impact of pesticides and fertilizers, so these willbe described only briefly. While there have been manystudies of the ecological impacts of pesticides onabove-ground ecology and soil macro- and mesofauna,rather less information is available on their impacts, orindeed those of other practices, on soil microbialecology. All pesticides, whether applied directly ortargeted at the above-ground parts of the plant or thepests themselves, are liable to end up in the soil and incontact with soil organisms. The impacts of a widerange of pesticides on specific groups of soil organ-isms, soil food webs and, to a more limited extent,biological processes in soil have been extensivelydocumented (Edwards 1993). Predictably, the effectsare highly variable, dependent on the type and amountof pesticide, soil environment and biotic groupsstudied. Generally speaking, however, the impactsare similar to those of tillage in that the impacts withthe most far-reaching effects are often those at thehigher trophic levels. Thus, the impact is not restrictedto the target but has disruptive effects on the biologicalregulatory capacity of the soil community withdamaging consequences for all soil functions(Edwards & Bohlen 1995; Edwards 2002). Thesame concerns thus exist with respect to the impactof pesticides on soil health as exist for their usegenerally, i.e. not only that indiscriminate use can havedangerous consequences for human health andimpacts on environmental functions, but also thatthe whole basis of pesticide use can be economicallyinefficient if the non-target impacts are weighedagainst the targeted success.

The impacts of industrially produced fertilizer onthe soil health system and ecosystem functions relatefirstly to their effect on primary productivity. Theeffects of excessive quantities are on process rates ratherthan any direct toxic effects. A very important indirectimpact is the fact that high fertilizer input use iscommonly associated with reduction in the quantity oforganic matter input.

The presence of high concentrations of ammoniuminhibits nitrogen fixation and stimulates nitrification.High levels of some nitrogenous fertilizers can lead to

acidification in some soils and consequent effects onthe soil biota. Excess nitrate may leach from the soiland contaminate sources of drinking water and/orchange the nutrient balance in aquatic ecosystems.These excesses also fuel denitrification and theproduction of nitrous oxide. The combination ofthese effects has been documented extensively andhas led to the conclusion that the global nitrogen cycleis significantly out of balance, and that agriculture isone of the main contributors (Vitousek et al. 1997;Wood et al. 2000). In terms of soil health at a more locallevel, the effect is a substrate-driven loss of internalcontrols and the opening up of cycle function.

These direct effects of inorganic fertilizers on thenutrient cycling function are exacerbated by thereduction in organic matter inputs which oftenaccompanies high rates of fertilizer use. Althoughfertilizers are highly effective in increasing cropproduction, integrative practices of combining themwith organic inputs are commonly abandoned in theinterests of efficiency, and above-ground residues areoften removed or burned. Inorganic fertilizers havebeen shown to increase the rate of decomposition of‘low-quality’ organic inputs and soil organic matter(Vanlauwe et al. 1994, 2001; Recous et al. 1995). Thiseffect is usually attributed to the enhancement ofmicrobial decomposer activity previously limited bylow nutrient concentrations in the organic resources. Itshould be noted, however, that the results of experi-ments on this effect are equivocal: although a majorityof results indicate the above effect, in a significantminority added inorganic nitrogen has either a neutralor even an inhibitory effect on the decomposition oflow-N plant materials (Hobbie 2005). This is probablyindicative of the interaction with secondary rate-limiting factors, but makes the point that the additionof a single ‘simple’ source of nitrogen can have complexinteractive effects on carbon transformations in the soil.The commonly observed overall effect of continuousinorganic fertilization with diminished input ofcarbon and energy is continuing decline in soil organicmatter content.

Finally, it should be noted that although each of thethree substitutive practices have been consideredseparately, they are commonly used in concert.Comparative studies of soil food webs and functionsin such multiple substitution systems and low sub-stitution integrated agriculture confirm the improvedsoil health in the latter (Brussaard 1994).

6. TOWARDS AGRICULTURAL MANAGEMENTFOR SUSTAINABLE SOIL HEALTHThe conclusions arising from this paper are derivedfrom the premise that soil is the site of a vital range ofecosystem functions which provide humans with arange of essential services. In natural ecosystems, thesefunctions and services are driven by the energygenerated by carbon transformations carried out bythe soil biological community acting in a highlyinteractive and integrated fashion.

Conventionally, the practice of agriculture may beseen as providing only a single service, namely arable orlivestock food production. Primary and secondary





production depends on soil-based ecosystem functionssuch as nutrient cycling, maintenance of soil structureand biotic population regulation. Society may alsorequire that other services, such as the supply ofgood quality water, protection of human health andreduction of greenhouse gas emissions, be maintainedat acceptable levels. This demand is already beingstrongly voiced in many developed economies. A majortarget of sustainable agriculture must be to ensure thatthe full range of ecosystem services is conserved forfuture generations: agricultural soils must thus retain amultifunctional capacity. We use soil health as a term todescribe the capacity of soil to deliver a range ofdifferent ecosystem functions and services.

Agricultural interventions, such as the use ofpesticides, powered tillage and the use of inorganicsources of nutrients, impact upon the biologicalcommunities of soil, damage their habitats anddisrupt their functions to varying extents. The linkbetween disturbance, targeted biota and effect onfunction is far from linear owing to the high level ofinteraction between organisms and functions. Themain integrating feature in the soil community isenergy flow. The majority of the soil organismsdepend directly or indirectly via one or more trophiclevels on the processes of organic matter decom-position for their source of energy and carbon. Anydisruption of this energy generating system may thusresult in changes in the flow of energy and carbon tothe different functions. Assessment of the relativeenergy allocation to different functions remains to becomputed but may prove difficult owing to thesecond integrating feature of the soil health system,that of the probability of participation in more thanone function by the same organisms. Althoughdistinct ‘functional assemblages’ of organisms respon-sible for the different functions have been recognized(figure 1), a significant proportion of the soil biotamay contribute to more than one function. Forexample, a substantial proportion of the organismsparticipating in functions such as nutrient cycling andsoil structure maintenance are also primary orsecondary agents of decomposition; while earthwormsand termites can clearly be identified as major‘ecosystem engineers’ with respect to their role insoil structure maintenance, they also contributesignificantly to nutrient cycling. At the trophic levelsof microbivores and predators, the crossover infunction is even more evident as is apparent fromfood web diagrams (figures 2 and 3). A third majorintegrative feature is that of the relationship betweenorganism and habitat. The activities of soil organismsare influenced by the condition of their habitat in thesoil, but at the same time continuously modify it. Anyshift in one function is thus likely to influence othersby habitat change.

These generalizations hide a huge amount of thevariation possible in the functioning of the soilcommunity and the lack of clear evidence for thepatterns of energy flow within the communities and theparticipation of particular species or taxonomic groupsin different functions. Elucidation of these issuesremains a major research challenge; nonetheless theoverwhelming conclusion from this analysis is that soil

health in its functional sense should be seen, andmanaged, not as a set of individual soil characteristicsbut as an integral property of the ecosystem.

An integrative approach is also essential for assess-ment of soil health. It is not feasible to assess soil healthdirectly on the basis of its delivery of differentecosystem services. Furthermore, soil health is relatedto functional capacity rather than actual serviceoutputs. As argued above, an effective approachappears to be using a set of diagnostic tests for soilsystem performance, chosen to be indicative of habitatcondition, i.e. physical (e.g. bulk density) and chemical(e.g. pH, salinity), of energetic reservoirs (e.g. soilorganic matter content) and key organisms andcommunity structure (e.g. earthworms and phenotypicprofiling). Nevertheless, we consider that this essen-tially reductionist method for diagnosing soil healthfalls short of that required to properly assess thecondition of the integrated and complex soil system.While it offers the only current means to attemptdiagnosis, the development of more integrative bio-logical methods is a research priority. It is necessary toassess soil health by comparison of diagnostic test datafor relevant populations of soils at the landscape scale,covering combinations of soil type and land manage-ment classes (e.g. arable and grassland). At present,there are no agreed distinct thresholds above or belowwhich the soil can be said to be healthy or not in adefinitive sense.

The integrated nature and high diversity of the soilhealth system may contribute a significant degree ofresilience under conditions of disturbance, particularlyat lower (largely microbial) trophic levels. Nonetheless,the conversion of natural vegetation to agriculturalland results in major changes in both physicalorganization and community structure in the soil,including species loss and changes in dominanceamong the surviving biota. This then becomes theresource with which agriculture must work and anytargets should realistically be set in relation to thepotential equilibria in agricultural systems rather thanthe natural systems from which they are derived, as hassometimes been advocated. More importantly, it isclear that subsequent agricultural practices may alsoimpair soil health through significant impacts on thecomposition and structure of the soil biologicalcommunity and consequently on soil-based ecosystemfunctions and services. Damage to ecosystem functionscan arise both owing to an inadequate supply ofresources (carbon, energy, nutrients or water) andthrough the impact of intensive substitutive practicessuch as continuous mechanical tillage, the use ofpesticides and excessive amounts of fertilizers. Theseinterventions may also impact on soil functions bydestroying or changing the habitat of the soil organismsand their capacity to repair it.

Sustainable management of soil health requires thesetting of criteria for acceptable levels of soil-basedecosystem functions and in particular the balancebetween the food production functions and otherssupporting soil conservation, water flow and quality,crop, livestock and human health control, and green-house gas emissions. The established principles forestablishing and maintaining soil fertility are familiar.





These include inputs of organic matter to meet demandfor carbon and energy supply to the soil biota, balancedwith the nutrient demand of the crops and thedevelopment of integrated (i.e. organic plus inorganic)nutrient management systems where inorganic fertil-izers are used in precise dosage in combination withequally carefully designed practices of organic mattermanagement that conserve nutrients and levels of soilorganic matter. These principles are consistent withthose needed to support soil health, and so capacity todeliver a range of ecosystem services, in the context ofthe integrated description of the soil system that wehave proposed. In addition, however, the maintenanceof continuous vegetative cover and in particular rootingsystems as advocated in some integrated farmingpractices (Tilman et al. 2002; Sanchez et al. 2004)will also promote a healthy soil, via an associatedcontinuous feed of carbon substrate below ground. Ingeneral, intensive mechanical tillage and pesticide useshould be kept to a minimum.

Sustainable management of soil will nonethelessalways be related to particular circumstances. Thepriorities in industrial agriculture, to reduce and refinethe input management system, are clearly differentfrom those of subsistence farmers where the key tosustainable management is to increase inputs. In Africagenerally, and more sporadically through much of thetropical regions, production is inadequate, resourceslimited and food sufficiency and agricultural profit-ability are lacking. The key issue here is to findmanagement practices that will ‘lift’ the systems andcan be implemented within the limited resource base(including cash) that is available, and are alsosustainable in the long term. In sharp contrast is thecase of industrial agriculture where productivity andreturns are high (although the latter is often distortedby subsidies) and where the realization of unacceptableimpacts on the environment and human health has ledto the search for more sustainable practices thatnonetheless do not compromise productivity or profit-ability. In both cases, a healthy soil is central to thesustainable solution.

Sustainable solutions with regard to soil health willdepend on the willingness of society to pay for itsmaintenance, which in its turn depends on the valueaccorded to the various functions and services itsupports. To date, it appears that both the measure-ment and economic evaluation of soil-based ecosystemfunctions have not been made. Industrial societies,through the agency of governmental policies, haveincreasingly shown themselves willing to pay the costsfor establishing limits to polluting effects (e.g. onnitrate levels in groundwater) or in encouraging actionsto enhance ecosystem functions (e.g. for carbonsequestration). Few would now disagree with theassertion that a practice which results in substantialaccumulations of heavy metals, pesticides or nitrates isundesirable, and be prepared to pay for it to be avoidedor alleviated, even when the effects of these accumu-lations on human health or agricultural production areunclear. Legislation has placed limits on such effects inmany countries. The same widespread consensus inrelation to soil degradation by erosion, organic matterloss and physical damage is emerging only now.

The effect is to alter the mix and levels of ecosystemservices required from soil and the definition of ‘healthysoil’. An example is temperate arable soil systems.Where these have been managed with intensivesubstitution over extended periods, their organiccarbon levels have declined. High levels of agriculturalproductivity can, however, be maintained in most soiltypes through appropriate substitutive practices. Onthe other hand, this loss of organic carbon has reducedtheir capacity to absorb and retain pollutants, repre-senting a loss of ecosystem service capacity. Thus, soilthat has been assumed to remain healthy from a cropproduction perspective is increasingly recognized to beunhealthy in the context of greater valuation ofenvironmental service provision.

For farmers in the developing regions of the worldwho are starting from a very low resource base, accessto inorganic fertilizers is essential to ‘kick-starting’their degraded systems, as are pesticides underfrequent conditions of acute pest or disease problems.The economic circumstances of these farmers,however, render such inputs unobtainable and a widevariety of alternative practices have been developedusing variations in cropping and farming system designas an alternative to industrially produced inputs.These ‘organic’ practices, enforced by necessity, maycontribute to improved soil health and sustainablepractice but are generally insufficient in terms ofproduction. Wherever inputs are affordable, they mustclearly be used to enhance production, but the risk toother ecosystem services and soil health can beminimized by maintaining the integrated nature oftheir farming systems.

Despite the great variety of biophysical and socio-economic circumstances that need to be accommo-dated, a working hypothesis for sustainable agriculturemay be advanced that ‘agriculture can be productivelyand profitably practised without impairment of soilhealth’. A more cautious assertion that recognizes thereality behind such a target is that ‘some degree oftrade-off between the optimization of one ecosystemfunction (in this case food or fibre production) andothers (e.g. water quality, carbon sequestration) isacceptable and indeed inevitable in any managedlandscape’. Irrespective of which of these approachesbecomes dominant, the emergence of a globallyacceptable concept of sustainable agriculture willrequire the convergence of the excess-resource andinadequate-resource trajectories of change on adiversity of practices rather than any single homogen-ized approach such as has characterized agriculturaldevelopment over the past 50 years.

As in any broad review, our concepts and ideas are thoseformulated over a long time and in dialogue with many valuedcolleagues and peers. We especially acknowledge JohnCrawford, Jim Harris, Iain Young and numerous colleaguesin TSBF and NSRI (sensu lato in both cases) for collaborationand stimulating discussions.

REFERENCESAbaye, D. A., Lawlor, K., Hirsch, P. R. & Brookes, P. C. 2005

Changes in the microbial community of an arable soilcaused by long-term metal contamination. Eur. J. Soil Sci.56, 93–102. (doi:10.1111/j.1365-2389.2004.00648.x)




http://dx.doi.org/doi:10.1111/j.1365-2389.2004.00648.x


Bardgett, R. D., Usher, M. B. & Hopkins, D. W. (eds) 2005Biological diversity and function in soils. Cambridge, UK:Cambridge University Press.

Barros, M. E., Grimaldi, M., Sarrazin, M., Chauvel, A.,Mitja, D., Desjardins, D. & Lavelle, P. 2004 Soil physicaldegradation and changes in macrofaunal communities inCentral Amazonia. Appl. Soil Ecol. 26, 157–168. (doi:10.1016/j.apsoil.2003.10.012)

Bossio, D. A. et al. 2005 Soil microbial community responseto land use change in an agricultural landscape of WesternKenya. Microb. Ecol. 49, 50–62. (doi:10.1007/s00248-003-0209-6)

Brussaard, L. (ed.) 1994 Soil ecology of conventional andintegrated farming systems.Agric. Ecosyst. Environ. 51, 1–267.

Campbell, C. D., Chapman, S. J., Cameron, C. M.,Davidson, M. S. & Potts, J. M. 2003 A rapid microtiterplate method to measure carbon dioxide evolved fromcarbon substrate amendments so as to determine thephysiological profiles of soil microbial communities byusing whole soil. Appl. Environ. Microbiol. 69, 3593–3599.(doi:10.1128/AEM.69.6.3593-3599.2003)

Chauvel, A., Grimaldi, M., Barros, M. E., Blanchart, E.,Sarrazin, M. & Lavelle, P. 1999 Pasture degradation by anAmazonian earthworm. Nature 389, 32–33. (doi:10.1038/17946)

Coleman, D. C. & Hendrix, P. F. 2000 Invertebratesas webmasters in ecosystems. Wallingford, UK: CABInternational.

Costanza, R. et al. 1997 The value of the world’s ecosystemservices and natural capital.Nature 387, 253–260. (doi:10.1038/387253a0)

Curtis, T. P. & Stoan, W. T. 2005 Exploring microbialdiversity—a vast below. Science 309, 1331–1333. (doi:10.1126/science.1118176)

Daily, G. (ed.) 1997 Nature’s services: societal dependence onnatural ecosystems. Washington, DC: Island Press.

Defra 2004 The First Soil Action Plan for England. London,UK: Department of Environment, Food and Rural Affairs.

De Groot, R. S., Wilson, M. & Boumans, R. M. J. 2002A typology for the classification, description and valuationof ecosystem functions, goods and services. Ecol. Econ. 41,393–408. (doi:10.1016/S0921-8009(02)00089-7)

De Ruiter, P. C. et al. 1994 Simulation and dynamics ofnitrogen mineralisation in the below-ground food webs oftwo arable farming systems. Agric. Ecosyst. Environ. 51,199–208. (doi:10.1016/0167-8809(94)90044-2)

Degens, B. P. & Harris, J. A. 1997 Development of aphysiological approach to measuring the catabolic diver-sity of soil microbial communities. Soil Biol. Biochem. 29,1309–1320. (doi:10.1016/S0038-0717(97)00076-X)

Doran, J. W. & Jones, A. J. (eds) 1996Methods for assessing soilquality, vol. 49. SSSA special publication. Madison, WI:ASA.

Doran, J. W., Coleman, D. C., Bezdicek, D. F. & Stewart,B. A. (eds) 1994 Defining soil quality for a sustainableenvironment, vol. 35. SSSA special publication. Madison,WI: ASA.

Edwards, C. A. 1993 The impact of pesticides on theenvironment. New York, NY: Chapman and Hall.

Edwards, C. A. 2000 Soil invertebrate controls and microbialinteractions in nutrient and organic matter dynamics innatural and agroecosystems. In Invertebrates as webmastersin ecosystems (eds D. C. Coleman & P. E. Hendrix),pp. 141–159. Wallingford, UK: CAB International.

Edwards, C. A. 2002 Assessing the effects of environmentalpollutants on soil organisms, communities, processes andecosystems. Eur. J. Soil Biol. 38, 225–231. (doi:10.1016/S1164-5563(02)01150-0)

Edwards, C. A. & Bohlen, P. J. 1995 The effects ofcontaminants on the structure and function of soilcommunities. Acta Zool. Fenn. 196, 284–289.

Environment Agency 2002 Agriculture and natural resources:benefits, costs and potential solutions. Bristol, UK: Environ-ment Agency.

European Commission 2002 Communication of 16 April2002 from the Commission to the Council, the EuropeanParliament, the Economic and Social Committee and theCommittee of the Regions: towards a thematic strategy forsoil protection [COM (2002) 179 final]. Brussels,Belgium: European Commission.

European Commission 2005 The common agriculturalpolicy 2003 review. Luxembourg, Europe: EuropeanCommunities.

European Commission 2007 Directorate General forResearch—Sustainable Development, Global Change andEcosystems. Catalogue of projects funded during the SixthFramework, pp. 362–363. Brussels, Belgium: EuropeanCommission.

Fierer, N. & Jackson, R. B. 2006 The diversity andbiogeography of soil bacterial communities. Proc. NatlAcad. Sci. USA 103, 626–631. (doi:10.1073/pnas.0507535103)

Frey, S. D., Elliott, E. T., Paustian, K. & Peterson, G. A. 2000Fungal translocation as a mechanism for soil nitrogeninputs to surface residue decomposition in a no-tillageagroecosystem. Soil Biol. Biochem. 32, 689–698. (doi:10.1016/S0038-0717(99)00205-9)

Frey, S. D., Six, J. & Elliott, E. T. 2003 Reciprocal transfer ofcarbon and nitrogen by decomposer fungi at the soil-litterinterface. Soil Biol. Biochem. 35, 1001–1004. (doi:10.1016/S0038-0717(03)00155-X)

Gaston, K. J. & Spicer, J. I. 1998 Biodiversity: an introduction.Oxford, UK: Blackwell Scientific.

Grayston, S. J. et al. 2004 Assessing shifts in microbialcommunity structure across a range of grasslands ofdiffering management intensity using CLPP, PLFA andcommunity DNA techniques. Appl. Soil Ecol. 25, 63–84.(doi:10.1016/S0929-1393(03)00098-2)

Griffiths, B. S. et al. 2000 Ecosystem response of pasture soilcommunities to fumigation-induced microbial diversityreductions: an examination of the biodiversity–ecosystemfunction relationship. Oikos 90, 279–294. (doi:10.1034/j.1600-0706.2000.900208.x)

Griffiths, B. S., Kuan, H. L., Ritz, K., Glover, L. A., McCaig,A. E. & Fenwick, C. 2004 The relationship betweenmicrobial community structure and functional stability,tested experimentally in an upland pasture soil. Microb.Ecol. 47, 104–113. (doi:10.1007/s00248-002-2043-7)

Griffiths, B. S., Hallett, P. D., Kuan, H. L., Pitkin, Y. &Aitken, M. N. 2005 Biological and physical resilience ofsoil amended with heavy metal-contaminated sewagesludge. Eur. J. Soil Sci. 56, 197–205. (doi:10.1111/j.1365-2389.2004.00667.x)

Harris, R. F., Karlen, D. L. &Mulla, D. J. 1996 A conceptualframework for assessment and management of soil qualityand health. In Methods for assessing soil quality, vol. 49 (edsJ. W. Doran & A. J. Jones). SSSA special publication,pp. 61–82. Madison, WI: ASA.

Hendrix, P. H., Parmelee, R. W., Crossley, D. A., Coleman,D. C., Odum, E. P. & Groffman, P. M. 1986 Detritus foodwebs in conventional and no-tillage agroecosystems.BioScience 36, 374–380. (doi:10.2307/1310259)

Hobbie, S. E. 2005 Contrasting effects of substrate andfertilizer nitrogen on the early stages of litter decom-position. Ecosystems 8, 644–656. (doi:10.1007/s10021-003-0110-7)




http://dx.doi.org/doi:10.1016/j.apsoil.2003.10.012

http://dx.doi.org/doi:10.1016/j.apsoil.2003.10.012

http://dx.doi.org/doi:10.1007/s00248-003-0209-6


http://dx.doi.org/doi:10.1128/AEM.69.6.3593-3599.2003

http://dx.doi.org/doi:10.1038/17946


http://dx.doi.org/doi:10.1038/387253a0

http://dx.doi.org/doi:10.1038/387253a0

http://dx.doi.org/doi:10.1126/science.1118176


http://dx.doi.org/doi:10.1016/S0921-8009(02)00089-7

http://dx.doi.org/doi:10.1016/0167-8809(94)90044-2

http://dx.doi.org/doi:10.1016/S0038-0717(97)00076-X



http://dx.doi.org/doi:10.1073/pnas.0507535103

http://dx.doi.org/doi:10.1073/pnas.0507535103















Hunt, H. W., Coleman, D. C., Ingham, E. R., Elliott, E. T.,Moore, J. C., Rose, S. L., Reid, C. P. P. & Morley, C. R.1987 The detrital food web in a shortgrass prairie. Biol.Fertil. Soils 3, 57–78. (doi:10.1007/BF00260580)

Insam, H. 2001 Developments in soil microbiology since themid 1960s.Geoderma 100, 389–402. (doi:10.1016/S0016-7061(01)00029-5)

Jenkinson, D. S. & Rayner, J. H. 1977 The turnover of soilorganic material in some of the Rothamsted classicalexperiments. Soil Sci. 123, 298–305. (doi:10.1097/00010694-197705000-00005)

Kelly, J. J., Haggblom, M. M. & Tate, R. L. 2003 Effects ofheavy metal contamination and remediation on soilmicrobial communities in the vicinity of a zinc smelteras indicated by analysis of microbial communityphospholipid fatty acid profiles. Biol. Fertil. Soils 38,65–71. (doi:10.1007/s00374-003-0642-1)

Kibblewhite, M. G. 2005 Soil quality assessment and manage-ment. InGrassland: a global resource (ed.D. A.McGilloway),pp. 219–226. Wageningen, The Netherlands: WageningenAcademic Publishers.

Kirk, J. L., Beaudette, L. A., Hart, M., Moutoglis, P.,Khironomos, J. N., Lee, H. & Trevors, J. T. 2004Methodsof studying soil microbial diversity. J. Microbiol. Meth. 58,169–188. (doi:10.1016/j.mimet.2004.04.006)

Landers, J. N., DeC Barros, G. S.-A., Manfrinato, W. A.,Weiss, J. S. & Rocha, M. T. 2001 Environmental benefitsof zero-tillage in Brazilian agriculture—a first approxi-mation. In Conservation agriculture—a worldwide challenge,vol. 1 (eds L. GarciaTorres, L. Benites & A. MartinezVilela), pp. 317–326. Cordoba, Italy: XUL.

Lavelle, P. 1997 Faunal activities and soil processes: adaptivestrategies that determine ecosystem function. Adv. Ecol.Res. 27, 93–132.

Lavelle, P., Bignell, D., Lepage, M., Wolters, V., Roger, P.,Ineson, P., Heal, O.W. &Dhillion, S. 1997 Soil function ina changing world: the role of invertebrate ecosystemengineers. Eur. J. Soil Biol. 33, 159–193.

Leckie, S. E. 2005Methods of microbial community profilingand their application to forest soils. Forest Ecol. Manage.220, 88–106. (doi:10.1016/j.foreco.2005.08.007)

Leigh, R. A. & Johnston, A. E. 1994 Long-term experiments inagricultural and ecological sciences. Wallingford, UK: CABInternational.

Liiri, M., Setala, H., Haimi, J., Pennanen, T. & Fritze, H.2002 Relationship between soil microarthropod speciesdiversity and plant growth does not change when thesystem is disturbed. Oikos 96, 137–149. (doi:10.1034/j.1600-0706.2002.960115.x)

O’Donnell, A. G. 2005 Twenty years of molecular analysisof bacterial communities in soils and what have welearned about function? In Biological diversity and functionin soils (eds R. D. Bardgett, M. B. Usher & D. W.Hopkins), pp. 44–56. Cambridge, UK: CambridgeUniversity Press.

Orwin, K. H. & Wardle, D. A. 2004 New indices forquantifying the resistance and resilience of soil biotato exogenous disturbances. Soil Biol. Biochem. 36,1907–1912. (doi:10.1016/j.soilbio.2004.04.036)

Parton, W. J. 1996 The CENTURY model. In Evaluation ofsoil organic models (eds D. S. Powlson, P. Smith & J. U.Smith), pp. 283–293. Berlin, Germany: Springer.

Paustian, K., Six, J., Elliott, E. T. & Hunt, H. W. 2000Management options for reducing CO2 emissions fromagricultural soils. Biogeochemistry 48, 147–163. (doi:10.1023/A:1006271331703)

Recous, S., Robin, D., Darwis, D. & Mary, B. 1995 Soilinorganic nitrogen availability: effect on maize residuedecomposition. Soil Biol. Biochem. 27, 1529–1538.(doi:10.1016/0038-0717(95)00096-W)

Ritz, K. 2005 Underview: origins and consequences ofbelowground biodiversity. In Biological diversity andfunction in soils (eds R. D. Bardgett, M. B. Usher &D. W. Hopkins), pp. 381–401. Cambridge, UK:Cambridge University Press.

Ritz, K. & Griffiths, B. S. 2000 Implications of soilbiodiversity for sustainable organic matter management.In Sustainable management of soil organic matter (eds R. M.Rees, C. A. Watson, B. C. Ball & C. D. Campbell),pp. 343–356. Wallingford, UK: CAB International.

Ritz, K. & Young, I. M. 2004 Interactions between soilstructure and fungi. Mycologist 18, 52–59. (doi:10.1017/S0269915X04002010)

Ritz, K., McHugh, M. & Harris, J. A. 2004 Biologicaldiversity and function in soils: contemporary perspectivesand implications in relation to the formulation of effectiveindicators. In Agricultural soil erosion and soil biodiversity:developing indicators for policy analyses (ed. R. Francaviglia),pp. 563–572. Paris, France: OECD.

Sanchez, J. E., Harwood, R. R., Willson, T. C., Kizilkaya, K.,Smeenk, J., Parker, E., Paul, E. A., Knezek, B. D. &Robertson, G. P. 2004 Managing carbon and nitrogen forproductivity and environmental quality. Agron. J. 96,769–775.

Schimel, J. P., Bennett, J. & Fierer, N. 2005 Microbialcommunity composition and soil nitrogen cycling: is therereally a connection? In Biological diversity and function insoils (eds R. D. Bardgett, M. B. Usher & D. W. Hopkins),pp. 172–188. Cambridge, UK: Cambridge UniversityPress.

Schulze, E.-D. & Mooney, H. A. 1994 Biodiversity andecosystem function. Berlin, Germany: Springer.

Setala, H. & McLean, M. A. 2004 Decomposition rate oforganic substrates in relation to the species diversity of soilsaprophytic fungi. Oecologia 139, 98–107. (doi:10.1007/s00442-003-1478-y)

Setala, H., Berg, M. P. & Jones, T. H. 2005 Trophic structureand functional redundancy in soil communities. InBiological diversity and function in soils (eds R. D. Bardgett,M. B. Usher & D. W. Hopkins), pp. 236–249. Cambridge,UK: Cambridge University Press.

Six, J., Elliott, E. T. & Paustian, K. 1999 Aggregate and SOMdynamics under conventional and no-tillage systems. SoilSci. Soc. Am. J. 63, 1350–1358.

Slack, N. 1997 The Blackwell encyclopaedic dictionary ofoperations management. Oxford, UK: Blackwell.

Swift, M. J., Heal, O. W. & Anderson, J. M. 1979Decomposition in terrestrial ecosystems. Oxford, UK: Black-well Scientific.

Swift, M. J., Vandermeer, J., Ramakrishnan, P. S., Anderson,J. M., Ong, C. K. & Hawkins, B. A. 1996 Biodiversity andagroecosystem function. In Functional roles of biodiversity: aglobal perspective (eds H. A. Mooney, J. H. Cushman,E. Medina, O. E. Sala & E.-D. Schulze), pp. 261–298.Chichester, UK: Wiley.

Swift, M. J., Izac, A.-M. N. & Van Noorwidjk, M. N. 2004Biodiversity and ecosystem services in agricultural land-scapes—are we asking the right questions? Agric. Ecosyst.Environ. 104, 113–134. (doi:10.1016/j.agee.2004.01.013)

Tilman, D., Cassman, K. G., Matson, P. A., Naylor, R. &Polasky, S. 2002 Agricultural sustainability and intensiveproduction processes.Nature 418, 671–677. (doi:10.1038/nature01014)

Tisdall, J. M. & Oades, J. M. 1983 Organic matter and water-stable aggregates in soils. J. Soil Sci. 33, 141–163. (doi:10.1111/j.1365-2389.1982.tb01755.x)

Torsvik, V. & Ovreas, L. 2002 Microbial diversity andfunction in soil: from genes to ecosystems. Curr.Opin. Microbiol. 5, 240–245. (doi:10.1016/S1369-5274(02)00324-7)




http://dx.doi.org/doi:10.1007/BF00260580



http://dx.doi.org/doi:10.1097/00010694-197705000-00005

http://dx.doi.org/doi:10.1097/00010694-197705000-00005


http://dx.doi.org/doi:10.1016/j.mimet.2004.04.006

http://dx.doi.org/doi:10.1016/j.foreco.2005.08.007



http://dx.doi.org/doi:10.1016/j.soilbio.2004.04.036

http://dx.doi.org/doi:10.1023/A:1006271331703

http://dx.doi.org/doi:10.1023/A:1006271331703

http://dx.doi.org/doi:10.1016/0038-0717(95)00096-W

http://dx.doi.org/doi:10.1017/S0269915X04002010

http://dx.doi.org/doi:10.1017/S0269915X04002010

http://dx.doi.org/doi:10.1007/s00442-003-1478-y

http://dx.doi.org/doi:10.1007/s00442-003-1478-y

http://dx.doi.org/doi:10.1016/j.agee.2004.01.013

http://dx.doi.org/doi:10.1038/nature01014

http://dx.doi.org/doi:10.1038/nature01014

http://dx.doi.org/doi:10.1111/j.1365-2389.1982.tb01755.x

http://dx.doi.org/doi:10.1111/j.1365-2389.1982.tb01755.x




van der Heijden, M. G. A., Klironomos, J. N., Ursic, M.,Moutoglis, P., Streitwolf-Engel, R., Bollr, T.,Wiemken, A.& Sanders, I. R. 1998 Mycorrhizal fungal diversitydetermines plant biodiversity, ecosystem variability andproductivity. Nature 396, 69–72. (doi:10.1038/23932)

Van Doren, D. M. & Allmaras, R. R. 1978 Effect of residuemanagement practices on the soil physical environment,microclimate and plant growth. In Crop residue manage-ment systems, vol. 31 (ed. W. R. Oschwald), ASA specialpublication, pp. 49–84. Madison, WI: American Societyof Agronomy.

Van-Camp, L., Bujarrabal, B., Gentile, A. R., Jones, R. J. A.,Montanarella, L., Olazabal, C. & Selvaradjou, S.-K. 2004Reports of the technical working groups established underthe thematic strategy for soil protection, vol. 5 Moni-toring. EUR 21319 EN/5, pp. 653–718. Luxembourg,Europe: European Communities.

Vanlauwe, B., Dendooven, L. & Merckx, R. 1994 Residuefractionation and decomposition: the significance of theactive fraction. Plant Soil 183, 221–231. (doi:10.1007/BF00011437)

Vanlauwe, B., Wendt, J. & Diels, J. 2001 Combining organicmatter and fertiliser for the maintenance and improve-ment of soil fertility. In Sustaining soil fertility in West Africa

(eds G. Tian, F. Ishida & J. D. H. Keatinge), pp. 247–279.Madison, WI: American Society of Agronomy.

Vitousek, P. M., Aber, J. D., Howarth, R. W., Likens, G. E.,Matson, P. A., Schindler, D. W., Schlesinger, W. H. &Tilman,D.G. 1997Human alteration of the global nitrogencycle: sources and consequences. Ecol. Appl. 7, 737–750.

Wall, D. H. 2004 Sustaining biodiversity and ecosystem servicesin soils and sediments. SCOPE 64. Washington, DC: IslandPress.

Wardle, D. A. 1995 Impacts of disturbance on detritus foodwebs in agro-ecosystems of contrasting tillage and weedmanagement practices. Adv. Ecol. Res. 26, 105–185.

Wardle, D. A. 2002 Communities and ecosystems: linkingaboveground and belowground components. Princeton, NJ:Princeton University Press.

Wood, S., Sebastian, K. & Scherr, S. J. 2000 Pilot analysisof global ecosystems: agroecosystem. Washington, DC:IFPRI/WRI.

Young, I. M. & Crawford, J. W. 2004 Interactions and self-organization in the soil-microbe complex. Science 304,1634–1637. (doi:10.1126/science.1097394)

Young, I. M. & Ritz, K. 2005 The habitat of soil microbes. InBiological diversity and function in soils (eds R. D. Bardgett,M. B. Usher & D. W. Hopkins), pp. 31–43. Cambridge,UK: Cambridge University Press.









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