Introduction
Concerns about environmental degradation and protection, together with increasing consumer awareness of food safety issues, have contributed to the development of a number of ‘sustainable’ or ‘eco’ farming approaches in recent decades. Organic farming, first developed in the 1940s, has found a booming market for its products and it is now considered to provide viable livelihoods in many circumstances and a realistic alternative to other more high input–high output approaches to agricultureReference Stockdale, Lampkin, Hovi, Keatinge, Lennartsson, Macdonald, Padel, Tattersall, Wolfe and Watson1. Across the world organic farming and processing has well-developed certification systems and, in many countries, the definition and practices of organic agriculture are defined in law (e.g. Regulation 834/2007 of the European Union). There is no single homogeneous and easily recognizable organic farming system. Organic farming systems are underpinned by a set of agreed global principles (Table 1), thereafter crops, livestock and their management on organic farms are regionally diverse and locally adapted.
Table 1. Principles of Organic Agriculture—International Federation of Organic Agriculture Movements, 2005 (http://www.ifoam.org/about_ifoam/principles/index.html).Footnote 1
1 In the full text, each principle is articulated through a statement followed by an explanation, which is not given here. They are given as ethical principles to inspire action and consequently should be taken as a whole. The principles of organic agriculture serve to inspire the organic movement in its full diversity and guide IFOAM's development of positions, programmes and standards.
The health of the soil, recognized by its active role in the linked processes of decomposition and nutrient supply, was proposed as the foundation of agriculture by the pioneers of the organic movementReference Howard2, Reference Balfour3. The organic farming movement has developed its principles and recommendations for farm management from an underpinning recognition of the biological, ecological conception of nature and the importance of the relationships and interactions between organisms—plant, animals and within the soil. In contrast, intensification of agricultural production is often marked by increased use of mechanical and manufactured inputs and increased specialization of production; these changes mean that regulation of the agro-ecosystem through biological processes is displacedReference Giller, Beare, Lavelle, Izac and Swift4. Hence in organic farming systems, use of manufactured fertilizers is prohibited (or at least significantly restricted), crops must be grown in rotation or as mixtures. Rotations/mixtures are designed with a strong awareness of their impact on soil structure. The cropping plan is also designed with regard to the fertility building and depleting role of the crops, with a focus on nutrient recycling to reduce the need for external inputReference Watson, Atkinson, Gosling, Jackson and Rayns5. Nutrients are dominantly added to the soil as organic (e.g. manures, compost, crop residues and legumes) or slow-release sources (e.g. rock phosphate). Consequently in organic farming systems a greater reliance is placed on chemical and biological processes within the soil to release nutrients in forms available for plant uptake. In this respect, while the processes controlling nutrient availability are the same in soils whether under organic or conventional management, nutrient availability in organically farmed soils is more dependent on soil processes than is the case in conventional agricultureReference Stockdale, Shepherd, Fortune and Cuttle6. It is also clear that the role of the soil in weed, disease and pest management may be significant for organic farming systemsReference Van Bruggen7, Reference Jackson8. Soils also play an important role in the regulation of broader environmental quality; for example, taking key roles in the regulation of water flow in watersheds, global emissions of greenhouse gases and degradation of wastes.
There is strong evidence that organic agriculture, particularly in temperate arable systems, is able to deliver positive impacts on biodiversityReference Bengtsson, Ahnstrom and Weibull9–Reference Hole, Perkins, Wilson, Alexander, Grice and Evans11, which offset the declines in farmland biodiversity that have been seen in these regions as a result of the intensification of farming systems and consequent homogenization of the landscapeReference Benton, Vickery and Wilson12, Reference Krebs, Wilson, Bradbury and Siriwardena13. A full range of evidence in all climates and farming systems has yet to be collected. The absence of synthetic fertilizers and pesticides, increased diversity of crop types in space and time, together with requirements in organic certification schemes for beneficial management for wildlife in non-cropped areas, are likely to contribute to the increases in biodiversity seen in organic systemsReference Hole, Perkins, Wilson, Alexander, Grice and Evans11.
In considering soil biological quality, it is important to take a broad view of ‘which organisms count?’ and in the first instance consider the whole food web and its interactions. For example it has been shown that the activity of soil fauna is responsible for 30–40% of the N released into plant-available forms in the soilReference Brussaard, Behan-Pelletier, Bignell, Brown, Didden, Folgarait, Fragoso, Freckman, Gupta, Hattori, Hawksworth, Klopatek, Lavelle, Malloch, Rusek, Söderström, Tiedje and Virginia14; mineralization is not purely a microbially driven process. Often agricultural systems are associated with simplified soil food webs compared to semi-natural systems; dominantly pastoral systems also have been shown to have qualitatively different ecological interactions below ground than dominantly arable systemsReference Van der Putten, De Ruiter, Bezemer, Harvey, Wassen and Wolters15. However, agricultural intensification need not necessarily have adverse consequences on below-ground biodiversityReference Giller, Beare, Lavelle, Izac and Swift4, Reference Wardle, Nicholoson, Bonner and Yeates16. In contrast, in a range of grassland systems, it has been shown that increased intensity of management tended to reduce the diversity of soil organisms within most functional groupsReference Mulder, De Zwart, Van Wijnen, Schouten and Breure17. This paper will therefore further investigate the evidence for the impact of organic farming systems on soil biological quality and consider the identification of appropriate biological indicators for use by organic farmers and their advisors.
In the following review, where differences between treatments are cited from previously published work, these refer only to significant differences reported in the original work. However, in many cases the published studies reviewed contain evidence of significant increases, significant decreases and no significant differences as a result of farming systems or treatments; the authors of this review have therefore, on many occasions, applied their expert judgment to assess the overall implications of a number of contrasting studies. In these cases, no formal meta-analysis has been carried out and hence no statistical significance is discussed.
Impact of Organic Farming on Soil Biological Quality
Pastoral systems
A large body of work carried out on soil biodiversity at an unimproved grassland site in the uplands of southern Scotland (320 m above sea level) showed that even soils with relatively low above-ground vegetation diversity had extremely high below-ground biodiversity and were able to process carbon inputs rapidlyReference Fitter, Gilligan, Hollingworth, Kleczkowski, Twyman and Pitchford18, this resulted in a soil ecosystem that was highly resistant to perturbations, including the application of lime, nitrogen fertilizer and biocides. Almost no work has been done to study the impact of differences between farming systems on soil biological quality in hill pastures. Given that differences between organic and conventional management in hill pasture systems are relatively small, large differences in soil biological quality are not expected. No significant differences were seen in bacterial diversity between improved and unimproved grassland despite differences in grazing intensity, fertilizer use and plant speciesReference McCaig, Glover and Prosser19; there was, however, some indication of an underlying difference in specific population components. Organic management, which is likely to reduce stocking density on unimproved grazing land, may have a negative impact on below-ground ecology in these areas due to reduced nutrient inputsReference Bardgett, Whittaker and Frankland20, Reference Bardgett, Leemans, Cook and Hobb21. Soil biota was studied along a fertility gradient in permanent pastures in the hills of New ZealandReference Parfitt, Yeates, Ross, Mackay and Budding22 with a range of plant species, stocking rates (6–16 ewe equivalents) and fertilizer applications (to a maximum of 90 kg N and 33 kg P ha−1). Bacteria and nematode populations showed an increase with increasing fertility; the same trends were found in both organic and conventional pastures and the farming systems were not distinguishableReference Parfitt, Yeates, Ross, Mackay and Budding22.
In lowland dairy systems, there are much larger differences between organic and conventional practices. Stocking density is often lower in organic systems. Conventional systems are generally associated with more intensive grassland management. Temperate organic dairy systems are dependent on grass–legume leys, rather than intensively fertilized predominantly rye-grass swards. There is some evidence of reduced numbers and activity of dung beetles where veterinary drugs are used regularly in lowland grassland systemsReference Hutton and Giller23; anecdotal evidence suggests that dung decomposes more slowly where wormers have been used. Impacts on earthworms are less clear; studies have shown both no significant differences in earthworm numbers and species diversityReference Foissner24, Reference Younie, Armstrong, Isart and Llerena25 and also reduced earthworm numbersReference Yeates, Bardgett, Cook, Hobbs, Bowling and Potter26 when comparing grassland management systems. In a comparison of grassland under conventional (c. 5-year grass–clover swards receiving NPK fertilizers) and organic management (>10-year grass–clover swards with a significant proportion of other grass species, slurry applied at one site) on three contrasting soil types (silt, loam and sand), strong interactions were shown between soil and farming system on soil biological quality. Bacterial and mite populations tended to increase under organic management, while fungal and total nematode populations were significantly increased under organic management at all sitesReference Yeates, Bardgett, Cook, Hobbs, Bowling and Potter26. Detailed analysis of nematode populations under conventional and organic management showed that fungal feeders were increased at all sites under organic management, whereas bacterial feeders, predatory and plant feeding species showed strong interactions with site and no clear effect of managementReference Yeates, Bardgett, Cook, Hobbs, Bowling and Potter26. Results from a gradient of grassland sites in The NetherlandsReference Mulder, De Zwart, Van Wijnen, Schouten and Breure17 showed higher diversity of bacterial and fungal feeding nematodes under organic than intensive grassland management systems—a gradient of practice related to management intensity including increasing livestock density, increasing use of mineral fertilizers and biocides and reducing use of farmyard manure was studied. A study of nematodes across a management intensity gradient in Germany and Switzerland also showed similar trendsReference Oehl, Sieverding, Ineichen, Mäder, Boller and Wiemken27. The highest nematode diversity was recorded on an organic farmReference Mulder, De Zwart, Van Wijnen, Schouten and Breure17. There was a strong relationship between higher bacterial populations and bacterial feeding nematodes, both increasing with intensity of management. Hyphal feeding nematodes show much lower resilience than bacterial feeders to increasing intensity of farming practices in all grassland systems with lower number of taxa and fewer individuals in generalReference Mulder, De Zwart, Van Wijnen, Schouten and Breure17. Arbuscular mycorrhizal fungi have shown greater spore density and infectivity under organic management (grass-clover swards) than at paired conventional sites (with higher rates of fertilizer use and lower proportions of cloverReference Eason, Scullion and Scott28). Arbuscular mycorrhizal fungi are likely to be increased as a result of increased plant diversity and decreasing P availability in organic systemsReference Gosling, Hodge, Goodlass and Bending29; conventional dairy pastures often have very high P availabilityReference Haygarth, Chapman, Jarvis and Smith30. Taken together the data collected in grassland systems suggest that decomposition pathways in low-intensity and/or organically managed grassland are likely to be more complex/diverse than under high-intensity conventional grassland, with consequent impacts on the higher trophic levels of the food web. However, there are few studies of the impact of organic management on predatory meso- and macrofauna in lowland grassland systems.
Rainfed arable cropping systems
Most studies comparing the effects of organic, integrated and conventional systems have been carried out in temperate rainfed arable systems. In these systems, there are large differences between organic and conventional management. All systems are permitted to use lime to maintain an optimum pH. However, there are marked differences in the use of mineral fertilizer, herbicides and pesticides. Organic livestock-based ley–arable systems use grass-clover leys and manures to maintain soil fertility; stockless organic farms use N fixing green manure crops at the heart of their rotationsReference Watson, Atkinson, Gosling, Jackson and Rayns5. Tillage intensity varies in both conventional and organic systems, though due to the prohibition of herbicides, zero-till systems are less common in organic systems.
Paired farm studies in New Zealand have shown greater microbial biomass in organic than conventional systemsReference Reganold, Palmer, Lockhart and Macgregor31, Reference Murata and Goh32. However, where organic management was compared with conventional systems using reduced tillage, no differences were found in the size of the microbial biomassReference Filser, Mebes, Winter, Lang and Kampichler33. Soil type (sand compared with clay) was shown to have a larger effect on the size of the microbial biomass than farming system in a comparison of 13 paired sitesReference Van Diepeningen, De Vos, Korthals and Van Bruggen34. Under field conditions in a long-term trial comparing a conventional system, an organic system based around animal production using manures, and a stockless organic system using N fixing cover cropsReference Drinkwater, Waggoner and Sarrantonio35, there were only very small differences between the size of the microbial biomass but significant differences between activity of the populationsReference Wander, Hedrick, Kaufman, Traina, Stinner, Kehrmeyer and White36. Larger microbial biomass populations and higher respiration rates have been measured in the grass–clover ley phase of organic rotationsReference Watson, Ritz, Younie and Franklin37. Increased microbial biomass in forage compared with arable rotations has also been found in conventional and integrated systemsReference Breland and Eltun38. There was no equivalent distinction between organic arable and forage rotation in the same trial; it was proposed that the higher returns of organic matter, as a result of the inclusion of ley and green manure crops in the organic arable rotation, offset the impact of increased tillageReference Breland and Eltun38. In a long-term comparison of farming systems under the same crop rotation in Switzerland, soil microbial biomass size and activity were shown to be more sensitive than the total soil organic carbon pool to differences in the quantity and quality of applied animal manureReference Flieβbach, Oberholzer, Gunst and Mäder39. Detailed observations of microbial population size, composition and dynamics and populations of other below-ground fauna made in a long-term multidisciplinary study under irrigation in a Mediterranean climateReference Bossio, Scow, Gunapala and Graham40–Reference Berkelmans, Ferris, Tenuta and Van Bruggen42 confirm the findings from temperate climates that the main factors leading to the increase in microbial populations and activity that are observed under organic management are the quantity and quality of the carbon inputs.
There is some indication that organically managed soils have a larger population of viable but non-culturable micro-organismsReference Shannon, Sen and Johnson43. There is also some indication of increased diversity of bacterial populations under organic managementReference Girvan, Bullimore, Pretty, Osborn and Ball44; however, a large number of factors varied between the sites studied. Soil properties that regulate microbial activity may also regulate microbial community compositionReference Cookson, Osman, Marschner, Abaye, Clark, Murphy, Stockdale and Watson45; management practices that modify soil pH and cycling of dissolved organic matter are most important in modifying microbial community structure and activity. Higher functional diversity coupled with higher microbial carbon efficiency have been measured under organic managementReference Flieβbach, Mäder, Insan and Rangger46. At the same site genotyping approaches have been used to show that the structural diversity of bacterial communities was influenced more by the application of animal manures than by conventional or organic management per se Reference Hartmann, Flieβbach, Oberholzer and Widmer47. This work was extended using lipid profiling to study microbial phenotypes to confirm that application of farmyard manure had the strongest influence on microbial community structureReference Esperschütz, Gattinger, Mäder, Schloter and Flieβbach48; in addition an influence of conventional versus organic management could be distinguished, whereas no direct impact of the immediately previous crop could be identified. Interaction between tillage and organic matter inputs within the constraints set by climate and soil texture rather than management system per se dominantly control the size and activity of the soil microbial biomass in arable systems.
Ergosterol (as an indicator of fungal biomass) was compared in soils from an organic, a conventional arable and conventional livestock farmReference Jensen, Elmholt and Labouriau49. The conventional livestock farm had greater ergosterol contents than the conventional arable farm. The biodynamic system that had a mixed cropping rotation, and intermediate inputs of organic matter had intermediate ergosterol contents. Spatial heterogeneity in ergosterol also increased with increasing pool size. However, in other cases few (and no consistent) differences in fungal biomass appear between organic and conventional systemsReference Shannon, Sen and Johnson43; indeed, the variation in fungal abundance within farming systems has been shown to be as great (and often greater) than differences between farming systemsReference Elmholt and Labouriau50. Higher arbuscular mycorrhizal colonization has been shown in organic than conventional paired cropping systemsReference Sattelmacher, Reinhard and Pomikalko51–Reference Bending, Turner, Rayns, Marx and Wood53. Using a paired farm approach it was shown that arbuscular mycorrhizal fungi in organic farms had a higher infectivity to roots than conventional systems (compared at the same inoculum levels)Reference Scullion, Eason and Scott54, infectivity also increased with time since conversion to organic management; the largest difference was seen on an inherently low P status soil. At the Rodale Research Institute in Pennsylvania, three farming systems (conventional, organic based around animal production using manures and stockless organic system using N fixing cover crops) showed similar levels of arbuscular mycorrhizal fungiReference Franke-Snyder, Douds, Galvez, Phillips, Wagoner, Drinkwater and Morton55; all plots also had very high levels of available P. A higher diversity of arbuscular mycorrhizal fungal spores under organic management regimes has also been shownReference Sattelmacher, Reinhard and Pomikalko51, Reference Oehl, Sieverding, Mäder, Dubois, Ineichen, Boller and Wiemkein56. Summarized evidence from 13 available studies showed greater root colonization, larger numbers of spores and greater diversity of arbuscular mycorrhizal fungi in organically managed soilsReference Eason, Scullion and Scott28. However, poor performance of arbuscular mycorrhizal fungi was also identified in some organic systemsReference Eason, Scullion and Scott28; the causes could not be identified because of differences in the details of management practices used in organic systems and contrasting land management at the sites before conversion.
Protozoans and nematodes are primary consumers of the soil microbial biomass and may be more sensitive indicators of the microbial dynamics than the measurements of the microbial biomass itselfReference Foissner57, Reference Bongers and Ferris58. No differences were shown in protozoan populations between organic and conventional farming systems in AustriaReference Hutton and Giller23. The nematode community structure has been shown to vary with fertilizer and crop protection systemsReference Neher and Olson59; different components of nematode biomass responded differently to different management practices. Overall nematode abundance has been shown to be higher under organic management than in comparable conventional systemsReference Hutton and Giller23, Reference Neher60. However, a larger effect of soil type (sand compared with clay) compared to farming system was found in The Netherlands on the size of the total nematode population in a comparison of 13 paired sitesReference Van Diepeningen, De Vos, Korthals and Van Bruggen34. It has been observed that organically managed arable land in a crop rotation maintained nematode species diversity and species type at a level more similar to low intensity grass than comparable conventional arable systemsReference Yeates, Bardgett, Cook, Hobbs, Bowling and Potter26.
Long-term system studies have found fundamental differences in soil food web structure between conventional and less intensive farming systems (The NetherlandsReference Brussaard61, USAReference Crossley, Coleman and Hendrix62 and SwedenReference Andren, Lindberg, Paustian and Rosswall63). Microbes, protozoa and nematodes have been shown to contribute more to the total amount of N mineralized in a lower-input system, while in the conventional system mites and enchytraeids made a larger contribution to mineralizationReference De Ruiter, Moore, Zwart, Bouwan, Hassink, Bloem, Devos, Marinissen, Didden, Lebbink and Brussaard64. Contribution to mineralization is a function of both species abundance and turnoverReference De Ruiter, Moore, Zwart, Bouwan, Hassink, Bloem, Devos, Marinissen, Didden, Lebbink and Brussaard64. It has been suggested that, as for grassland systems discussed above, under conventional arable cultivation, the bacterial community dominates the microbial component while, in less intensive systems, the fungal community is the dominant microbial component. Such differences influence nutrient cycling and have implications for the efficient use of nutrient inputs and leaching potentialReference De Ruiter, Neutel and Moore65, Reference Pankhurst, Doube, Gupta and Grace66. Long-term system studies in The Netherlands, USA and SwedenReference Brussaard61–Reference Andren, Lindberg, Paustian and Rosswall63 have also found that most soil faunal groups were more diverse or unchanged in less intensive farming systems (organic and integrated) than in conventional systems. In addition, no difference in collembolan population size or species abundance was evident between conventional systems using reduced tillage and organic farming systemsReference Filser, Mebes, Winter, Lang and Kampichler33. Many collembolan taxa have been shown to be ubiquitous in arable farming systemsReference Alvarez, Frampton and Goulson67, where the most important source of variation was local differences between management practices. However, in general, taxa responded differently to farming systems; it has been suggested that collembolan species showing an increase in organic farming systems are those that prefer increased humidity and hence higher weed populationsReference Alvarez, Frampton and Goulson67. Significantly higher carabid populations have also been reported in organic management regimesReference Mäder, Flieβbach, Dubois, Gunst, Fried and Niggli68. A meta-analysis of all the data collected on comparisons of carabids in organic and conventional systems in southern Germany and Switzerland showed that on average there were 34% more species found in organically managed winter wheatReference Doring and Kromp69; carabid species also responded to management systems differently, with some species showing increases and some decreases in organic systems. Identification of key species traits and requirements is needed if optimum management practices for any particular species are to be developed, e.g., Carabus auratus often shows increased populations in organic farming systems. However, this effect is not found on very sandy soils, and shows a strongly negative response to mechanical weeding in spring due to its long larval stageReference Doring and Kromp69. Earthworms are generally higher in organic than conventional systemsReference Reganold, Palmer, Lockhart and Macgregor31, Reference Mäder, Flieβbach, Dubois, Gunst, Fried and Niggli68. Within organic rotations earthworm numbers were found to be highest in the second year of grass–clover ley, the population declined through the tillage phase of the rotation with increased time after the ley phaseReference Watson, Younie, Armstrong, Olesen, Eltun, Gooding, Jensen and Kopke70. Increases in earthworm population have been strongly linked to farming systems with reduced cultivationReference Higginbotham, Leake, Jordan and Ogilvy71.
Beneficial effects of organic farming on the abundance and species richness of arable weeds are often reported, e.g., Roschewitz et al.Reference Roschewitz, Gabriel, Tscharntke and Carsten72. This clearly has benefits for plant species diversity and can therefore impact on above ground insect diversityReference Clough, Holzschuh, Gabriel, Purtauf, Kleijn, Kruess, Steffan-Dewenter and Tscharntke73. The presence of weeds can act as an important bridge for arbuscular mycorrhizal fungi in non-mycorrhizal cropsReference Kabir and Koide74. It is likely that the presence of increased weed populations may have broader impacts on the soil ecosystems. Selected biological indicators of soil quality have also been associated with potential weed-suppressive activity in soil. In reduced tillage systems, the proportion of water-stable soil aggregates was the greatest in soils with the highest organic matter and was found to be related to higher enzyme and weed-suppressive activityReference Kremer and Li75. Interactions between crops, weed and soil biological quality are complex and not much studied.
Lowland rice (paddy) systems
Little work has been carried out in paddy systems to compare biological soil quality between organic and conventionally managed systems. However, differences have been found in the ground arthropod community structure and insect pest regulatory mechanismsReference Hidaka76. No consistent structural differences were found in the abundance of plant eating and predatory arthropods in comparisons of organic and conventional rice paddiesReference Hossain, Choudhury, Hossain and Alam77. The same study also demonstrated that soils under organic management had lower bulk densities. Improved soil physical quality (including ease of cultivation) has been shown in organic rice systems and this has been linked to the larger returns of organic matter through rice straw and animal manure typically associated with organic management practicesReference Mendoza78. Given the very different soil processes operating under the reducing environment in rice paddies, more work is needed to establish whether these changes in soil physical quality and organic matter management have any measurable impact on soil biological quality.
Overall impacts on soil biological quality
Given our limited ability to apply robust taxonomic classification systems to below-ground groups, it is probably not surprising that a range of positive and negative effects on below-ground ecology are observed as a result of the application of contrasting management systems. The evidence collected until 1992 on the impacts of organic management on soil biodiversity showed uncertain results: ‘It is increasingly evident that generalisations like—conventional farming destroys life in the soil or Eco-farming stimulates soil life—are only partially supported by the data’Reference Hutton and Giller23. More recent reviews have largely shown positive impacts of organic farming systems on soil biological quality. A larger number of studies showing positive impacts of organic farming systems on below-ground species than studies showing no difference or negative impacts were reported in a 2005 reviewReference Fuller, Norton, Feber, Johnson, Chamberlain, Joys, Matthews, Stuart, Townsend, Manley, Wolfe, Macdonald and Firbank10. As part of a meta-analysis considering all aspects of biodiversity in organic farming systems in 2005, it was shown that despite the considerable heterogeneity amongst studies, soil organisms were generally more abundant in organic farming systemsReference Jackson8. Effects on bacterial biomass and activity were unclear, whereas positive impacts on earthworms, collembolan, mites and fungal populations were confirmed. For groups that can be resolved to the species level, e.g., collembola and carabids, differential effects of systems are found for different species.
Interactions between tillage and management of the carbon cycle (both the amount and quality of inputs) dominantly control soil biological quality within the constraints set by the particular climate/soil conditions at any site. Tillage intensity seems to have the most significant effect in reducing soil biological quality. Impacts of cropping management (particularly the amount and quality of organic matter returned to the soil) can moderate the impact of even quite severe tillage operations and seem to increase the resilience of below-ground ecosystems. Increased use of ley–arable rotations and green manures in organic farming systems tends to increase the amounts and diversity of organic matter inputs compared to conventional arable rotations. Consequently, both organic and reduced tillage systems have positive effects on soil biological quality, though significant variations are found within any defined farm management system. Much smaller differences in soil biological quality are seen in grassland systems, where differences in management between organic and conventional management are also often smaller. For grassland systems, balancing grazing intensity in space and time, together with the considered use of drainage, aeration, fertilizers, lime and organic inputs, all affect the impact of agricultural management on soil biological quality.
Using indicators of soil biological quality in organic farming systems
Consideration of the current evidence on the impact of organic farming systems on soil biological quality indicates that while organic farming practices generally have a positive impact on soil biological quality, differences between practices within farming systems have as great (or often greater) impact on soil biological activity than the farming system per se. Consequently, even within the constraints of organic farming practices, it is possible for farmers to make changes that will improve soil biological quality. It is, however, by no means clear that distinct indicators of soil biological quality will be needed for organic farming. Most of the measurements of soil biological quality and soil ecology discussed above have used the same methods for both organic and conventional systems. Although a greater reliance is placed on chemical and biological processes within the soil in organic farming systems to release nutrients in forms available for plant uptake, the processes controlling nutrient availability are the same in soils whether under organic or conventional managementReference Watson, Atkinson, Gosling, Jackson and Rayns5. There is much that can and should be learned from the literature on soil quality indicators for conventional farming systemsReference Idowu, Van Es, Abawi, Wolfe, Ball, Gugino, Moebius, Schindelbeck and Bilgili79, Reference Winding, Hund-Rinke and Rutgers80 in the search for appropriate indicators of biological quality for application within organic farming systems.
There is currently no reliable method to predict the impact of management on the soil microbial biomass and its whole range of activity due to the complex interaction of site and management factors (both directly and indirectly) and the ability of the soil microbial biomass itself to alter the soil habitat in response to management changesReference Stockdale and Brookes81. Changes in biological methods, including (but not exclusively) those based on molecular methods, now offer new ways of examining the size, diversity and activities of the groups within the soil population. This is an area of intense research activity and scientific excitement and provides major opportunities for developing new indicators of changes in soil relevant to specific activities and functions. However, in the context of monitoring soils and detecting trends or problems, caution is required in interpreting the large amount of data that can now be collectedReference Alabouvette, Backhouse, Steinberg, Donovan, Edel-hermann, Burgess, Schjønning, Elmholt and Christensen82–Reference Johnson, Lee and Scow84. Factors and management practices that increase resilience are also likely to vary for different below-ground organisms and may include management in both cropped and no-cropped habitats—for insect species the maintenance of a source of organisms able to re-invade may be critical (i.e., size, proximity and connectivity with an unaffected community). In some circumstances, management practices can also provide a reservoir population, e.g., using intercrops or tree saplings inoculated with appropriate mycorrhizal fungi. Where inoculation with mycorrhizal fungi and pseudomonads had been used to improve crop yield under organic management then a modification of the soil microbial structural diversity can be detected using denaturing gradient gel electrophoresisReference Srivastava, Roseti and Sharma85. Such analytical approaches have not yet been developed to allow definition of target states or ideal ranges so that their measurement could guide management, e.g., distinction between sites that would benefit from inoculation from those with appropriate existing microbial diversity. Even where the use of bio-logical inoculation is so far advanced, such as for rhizobia, the understanding of the soil and environmental factors necessary to characterize the specific requirements or limitations in the soil for establishing Rhizobium populations to ensure optimal nitrogen fixation following inoculation of legumes remains incompleteReference Slattery, Coventry and Slattery86. In this case a simple chemical measurement, pH, was found to be the best indicator of an aspect of soil biological quality, i.e., the survival and effectiveness of rhizobial strainsReference Evans87. A quest for indicators of soil biological quality should not immediately reject chemical and physical measurements.
In a search for appropriate indicators of soil biological quality it is appropriate to note the cautionary comment made by the late Ted ElliottReference Elliott, Schjønning, Elmholt and Christensen88:
The ideal bioindicator of soil health would be simply measured, work equally well in all environments and reliably reveal what problems existed where. For the reasons outlined …, we are more likely to develop bioindicators for which information is laboriously obtained, that are specific to a given ecosystem or environmental problem and only tell us that there is a problem and not show us what the problem is. Even with this gloomy forecast, it is unquestionable that we will continue to seek ways by which we can determine the health of ecosystems, or their components, such as soil.
In the literature on soil quality, almost entirely written by soil scientists rather than soil users, there is a strong tendency to develop lists of measurements that can be made on soils and then interpret them as indicators of soil quality, e.g., Karlen et al.Reference Karlen, Andrews and Doran89. In part, this tendency to make measurements reflects the training and mode of working of reductionist scientists. Consequently, a common approach, contained in much of the literature summarized in the consideration of the impact of organic farming systems on soil quality above, is to measure as many things as possible in contrasting systems and then use statistical approaches to identify those showing significant differences, so that these can be proposed as indicators, e.g., Xua et al.Reference Xua, Zhao, Liu and Argent90 This can lead to the identification of a good set of descriptor measurements which can be used to distinguish between systems and/or high and yield variants in a systemReference Rezaei, Gilkes and Andrews91. Some groups favor the development of an index that normalizes measured soil quality indicator data and generates a numeric value that can be used to compare various management practices or to assess management-induced changes over timeReference Andrews, Karlen and Cambardella92. However, there has been much less work showing the added value of using these approaches predictively and/or to guide management. In practice, these approaches will often lead to a sensible analysis of an issue or problem, given that soil scientists should have a good understanding of the relationships between soil properties and functions. However, we suggest that the stakeholders or land managers most concerned in a given situation should be engaged at an early stage of the process to define the outcomes or functions they require. The soil scientists should then, and only then, work alongside them to develop a set of measurements or observations that will provide information on these functions. In practice, the two approaches may often lead to the same set of measurements—but not always.
Where we are seeking to develop indicators that will guide changes in farming practice, then farmers must also be able to manipulate the indicator beneficially and such manipulation must be cost effective. Consequently, it is important not just to identify the most appropriate indices but also to ensure that these can be quantified with the necessary precision and that farmers and land managers can understand and relate to themReference Lal93. This requires an awareness of the constraints of a farming system, whether legislative, as for many organic farming systems, or physical, economic, etc. For example, the constraints of the organic principles to on-farm practice may mean that some indicators developed for conventional farming systems therefore have little/limited use in organic farming system since the actions which they are designed to trigger are not permitted in organic farming management. For example, while development of a rapid and reliable detection method for evaluating soil inoculum levels in naturally infested soils might trigger the selection of resistant or partly resistant cultivars (e.g., for Plasmodiophora brassicae Reference Wallenhamar and Arvidsson94) and hence be a useful screening method in organic as well as conventional systems, a screening method developed for use within the growing season to trigger a fungicide application would be of limited use to organic farmers.
Often authors of reviews on soil biological fertility argue that maintenance and enhancement of soil biological fertility is generally of benefit within agricultural systems, e.g., Doran and SmithReference Doran and Smith95, Beauchamp and HumeReference Beauchamp, Hume, Van Elsas, Trevors and Wellington96 and Clapperton et al.Reference Clapperton, Chan, Larney, Abbott and Murphy97. However their guidance as to monitoring and management of soil biological fertility at a farming system level is given only in very general way. For example: ‘Ideally agroecosystems should be managed to maintain the structural integrity of the [soil] habitat, increase SOM and optimise the C:N ratios in soil organic matter using cover crops and/or crop sequence to synchronise nutrient release and plant uptake’.Reference Clapperton, Chan, Larney, Abbott and Murphy97 But a farmer might well ask how many cover crops and which ones, where the right balance (economic as well as ecological) is between minimizing tillage and optimizing weed control … and many more pertinent questions. Interactions between practices, rather than the impact of any single practice, are often the focus of farm management decisions. In the development of indicators of soil quality, closer links to management practices are needed, so that indicators can support improved quality of soil management.
Conclusions
The legislative requirements placed on organic farming systems mean that many of the practices which are likely to maintain or enhance soil biological fertility are at the heart of this approach to farming. It is a requirement of organic farming systems that they recycle nutrients within the farming system, so that total returns of organic materials to the soil are often higher under organic management. In addition, organic farming systems develop diverse cropping patterns in space and time, hence increasing the diversity of residue quality input to the soil. Consequently, many organic farming systems have increased biological activity and increased below-ground biodiversity compared with conventional farming in the same region. However, within organic farming systems, weed management is largely achieved through tillage and perhaps the key remaining question for organic arable farming systems with regard to the enhancement of soil biological fertility is to what extent can minimum tillage approaches can be adopted?
There is no evidence that new distinct indicators are needed to measure biological soil quality in organic farming systems. For all farming systems, the key is to identify indicators that are suitably responsive to changes in practice and can be readily interpreted by the farmer. More work is needed, however, to test existing indicator frameworks (e.g., Idowu et al.Reference Idowu, Van Es, Abawi, Wolfe, Ball, Gugino, Moebius, Schindelbeck and Bilgili79) to guide management within organic farming systems, rather than simply to compare organic and conventional management.
Acknowledgements
We prepared the presentation on which this paper is based for the joint China–UK Soil Quality Workshop, Beijing, October 2007. The workshop was supported by the UK Biotechnology and Biological Sciences Research Council (BBSRC), Natural Science Fund of China (NSFC), Education Ministry of China, China Agricultural University (CAU) and China Academy of Science (CAS).
We also wish to acknowledge the sponsorship of English Nature, Countryside Council for Wales, Department for Environment, Food and Rural Affairs and Scottish Natural Heritage, which was provided to carry out a literature review in 2005–2006 on which some of this paper is based.
