Tillage, habitat space and function of soil microbes
I.M. Young
*, K. Ritz
Soil-Plant Dynamics Unit, Scottish Crop Research Institute, Cellular and Environmental Physiology, Dundee, Scotland DD2 5DA, UK
Accepted 16 July 1999
Abstract
This review examines the effect of tillage on microbial habitat space, and the roles of microbes in in¯uencing N-transformation processes within a heterogeneous soil environment. Literature relating tillage to microbial processes is assessed critically focusing on (a) degrees of physical disruption and N-processes, (b) interactions between organisms and the soil pore network, and (c) the role of soil structure in mediating oxygen movement to sites of microbial activity in soil. Spatial heterogeneity is shown to be a key characteristic of soil structure and N-transformation processes, impacting on predator:prey relations, microbial habitable pore space, and the modelling of the soil system with respect to denitri®cation. The latter area is discussed with respect to the notion of how a functional appraisal of soil structure may be approached theoretically, at the aggregate and soil pro®le scale.#2000 Elsevier Science B.V. All rights reserved.
Keywords:Soil structure; Soil pore network; Spatial heterogeneity; Microbial activity; Nitrogen transformations; Tillage
1. Introduction
A large body of literature exists relating tillage practices to microbial activity and microbially mediated processes (e.g., Haban, 1986; Bowman et al., 1990; Shtina and Kirov, 1992; Franzluebbers et al., 1994, 1995; McGarty et al., 1995). Manipulation of soil structure is one of the principal means by which microbial dynamics can be controlled both at the small- and ®eld-scale (Elliott and Coleman, 1988).
This control arises through alterations in habitat space, water and substrate distribution, and the spatial arrangement of pore pathways. The primary effect of tillage is to physically disturb the soil pro®le. Microbial inhabitants of the soil will react differently to such disturbance. The speci®c effect will depend largely on the disturbance that occurs, or is `sensed', at the spatial scale to which the organisms are sensitive. For instance, an extensive network of fungal hyphae ramifying through the soil pro®le may be affected dramatically by a plough tearing apart hyphal con-nections, and disrupting ¯ow paths within the myce-lium. Bacterial colonies living in the centre of aggregates may, on the other hand, remain initially unaffected, as long as the zone of soil in which they inhabit remains largely intact. These intuitive
consid-*Corresponding author. Present address: Statistical and Infor-matics Modelling of Biological Systems, Abertay University, Kydel Building, Bell Street, Dundee, DD1 1HG. Tel.: 44-1382-308646; fax:44-1382-562426.
E-mail address: i.m.young@tay.ac.uk (I.M. Young).
erations focus on a number of important issues for the farmer; ranging from the scale of habitat space within which organisms live, to the ®nal effect tillage has on processes within the soil system.
Different tillage systems will disturb the physical framework of the soil to different degrees (Gantzer and Blake, 1978), affecting changes in organic matter levels, mineral concentrations and physical para-meters (Bowman et al., 1990). In this review we examine the role of soil structure, and changes in structure through tillage operations, in affecting some microbially mediated processes.
2. No-tillage versus conventional tillage
The two extremes of the physical disruption spec-trum are represented by comparisons of soil para-meters associated with conventional and reduced tillage systems. The latter is commonly referred to as no-tillage, no-till, or minimum tillage in the litera-ture, and connections have been made between no-till systems and `bene®cial' effects on soil micro-organ-isms (Elliott and Coleman, 1988).
Doran (1980, 1987) and Linn and Doran (1984a, b) present convincing scenarios of the effects of large-scale disruption of soil on the small-large-scale behaviour, existence and function of soil micro-organisms. In this work, these relations centre on the changes in soil
structure, and associated moisture regimes, in each tillage system. A general picture of the relation between microbial activity and soil moisture is described by Linn and Doran (1984a) and summarised in Fig. 1, and illustrates that the wetter, denser and cooler conditions typically associated with reduced tillage systems result in higher amounts of organic matter and greater microbial activity/biomass, princi-pally in the upper layers of the soil (Lynch and Panting, 1980; Blevins et al., 1983, 1984; Arshad et al., 1990; Dalal et al., 1991). Some knock-on effects are greater leaching of mineral-N (Carter and Rennie, 1982) and greater denitri®cation rates (Aulak et al., 1984). For instance, Doran (1987) found that, in seven no-tilled soils, microbial biomass and potentially mineralisable nitrogen averaged 54 and 37% higher, respectively, than those in the surface layer of ploughed soils. Deeper in the soil pro®les (7.5± 30 cm) differences between tillage treatments were negligible.
The body of work carried out in comparing no-till and conventional tillage, relating N-transformation processes to tillage systems, is compelling. At one scale, differences in physical parameters (bulk density, volumetric moisture content, etc.) are related to the presence of speci®c micro-organisms (Linn and Doran, 1984a), enzyme activity (Sequi et al., 1985; Doran, 1987; Pagliai and De Nobili, 1993), through to differences in CO2 and N2O production (Linn and
Doran, 1984b). A clear connection exists, and empha-sis is often placed on, the role of water and associated bulk density differences between tillage systems. However, there are interesting departures from the proposed scenarios, which only become apparent by comparing the body of work which Doran and co-workers have produced.
Linn and Doran (1984a) state that ``Populations of aerobic and anaerobic micro-organisms in the surface (0±75 mm) of no-till soils, were generally greater than those from conventionally tilled soil''. This is con-nected by the authors to differences in bulk densities, volumetric water contents and water-®lled pore space. The latter term actually refers to the degree of satura-tion of the pore space. Data from two separate years (1980 and 1981), at ®ve or more different locations in the United States, were examined. Despite the state-ment of Linn and Doran's (1984a) it is clear from the data presented that no signi®cant differences were observed in 1980, for total aerobic and anaerobic organisms, whilst large and signi®cant differences are seen in the physical parameters. This is supported by data from the same year, from the same locations (Doran, 1987), where signi®cant differences were observed for microbial biomass measurements. Sev-eral points are worth attention. Firstly, in 1980, although no differences were observed in total aerobes there were large and signi®cant differences in micro-bial biomass. Secondly, the observed link between soil physical parameters and microbial parameters, which is seen in 1981, is not seen in 1980. The question is why? It is clear that substrate quantity and quality play a leading role in modulating microbial activity. The quality of organic matter plays an important role in mediating the presence and functioning of micro-organisms over and above any observed physical differences. Arshad et al. (1990) found that no-till soil had greater amounts of carbohydrates, amino acids, aliphatic C and less aromatic C. Schulten et al. (1990) observed similar differences in organic matter quality between two such tillage systems. Given that no-till systems also have greater amounts of organic-C than conventional systems (Doran, 1987), it is probable that the quality of the organic matter as well as the quantity in no-till may have been suf®cient to provide the observed differences in microbial populations and activity, despite the simi-larity in microbial numbers seen in both tillage
systems. Another reason may be that the bulk physical parameters were not measured at a high enough resolution to account for the link between moisture and microbial activity. There is a growing awareness that the measurement of many soil parameters is scale-dependent (Starr et al., 1995). Whilst the overall moisture contents between tillage treatments may have been dissimilar, the distribution of moisture in the soil pro®les, at scales relevant to microbial popu-lations, may have been the same. We discuss this further below, in relation to modelling N-transforma-tion events.
3. Organism interactions
Elliott and Coleman (1988) point out that control of soil structure is one of the most effective ways to manipulate soil biota. In this section we will examine the predator:prey dynamics which may interact with N-transformation processes, brie¯y outlining the prin-ciples of predator±prey interactions and the impor-tance of microbial community structure.
3.1. Effect of tillage on soil structure
The habitat space in soils is essentially de®ned by the architecture of the soil pore network. The topo-graphy of this pore space in¯uences strongly the nature and extent of interactions between the myriad of organisms inhabiting the soil. In no-till soils bio-logical activity is characteristically higher than in tilled soils, resulting in the formation of more pores of biological origin, e.g., macropores due to earth-worm activity (Hendrix et al., 1987; Shipitalo and Protz, 1987; Drees et al., 1994).
lost, and thus they do not provide information about the global pore architecture. Nonetheless some infor-mation can be gleaned from such data in that there are obviously relationships between mean aggregate sizes and the way such structures are likely to pack together. Aggregate sizes have generally been found to be greater in no-till compared to tilled soils (Drees et al., 1994; Lal et al., 1994), although Vyn and
Raim-bault (1993) found no-till resulted in a lower propor-tion of aggregates <5 mm in diameter.
Thin sections provide the highest resolution infor-mation and maintain the spatial context of the pore network across all scales. Relatively few comparisons have been made between no-till and tilled soils using this approach. Boone et al. (1976) found no-till soils contained more pores <100mm. Shipitalo and Protz (1987) measured no-till soils having half the number of pores >200mm compared to tilled soils. Pagliai and De Nobili (1993) found greater porosity in tilled versus no-tilled soil, and large differences in pore morphology within these soils. In the surface 10 cm of soils, round pores were twice as abundant and elongated pores half as abundant in no-till soils com-pared to tilled. The tilled soils were also character-istically platy at their surface and heterogeneous below with numerous irregular pores and large com-pact aggregates separated by large planar pores. In contrast, no-till had a more homogeneous subangular blocky structure. Drees et al. (1994) found the con-verse of these observations, with no-till soils having a loose granular surface with strong platy structure separated by interconnected planar voids, and con-ventionally tilled samples showing loose packed aggregates. Shipitalo and Protz (1987) also found many horizontal planar pores in no-till soils. One of the problems of thin section work has been the lack of a rigorous framework for describing pore architecture in the context of biological interactions and processes, i.e., a general framework for integrating soil biological and physical processes. However, recent develop-ments have provided quite sophisticated methods of quantifying soil structural heterogeneity (Eggleston and Peirce, 1995; Crawford and Young, 1998) which offer some real possibilities of progress.
At a higher spatial resolution Foster (1994) found no distinction on the basis of ultrastructure between aggregates of conventionally tilled and reduced-tillage plots of some Australian soils, but there were differ-ences in no-till soils. These were mainly related to the apparent increase in access microbes had to organic matter in tilled soils (Foster, 1994).
3.2. Community structure
Whilst many studies have shown increases in total microbial biomass resulting from reduced or absence
of tillage (e.g., Doran, 1980, 1987; Lynch and Panting, 1980; McGill et al., 1986; Granastein et al., 1987; Buchanan and King, 1992), regular cultivation is also well known to have a major effect upon the composi-tional structure of soil microbial communities and their attendant function in relation to nutrient cycling. The seminal work carried out at Horseshoe Bend in Geor-gia, USA, demonstrates this clearly (e.g., summarised in Coleman et al., 1994), where it was found that many of the effects of tillage related speci®cally to the composition of decomposer communities. Saprophy-tic fungi appeared to play a major role in regulating the decomposition of (predominantly surface-deposited) residues in no-till systems, whilst bacteria dominated in tilled soils (Hendrix et al., 1986; Holland and Coleman, 1987; Beare et al., 1992). Fungi also appear to contribute more to the formation and stabilisation of aggregates in no-till compared to tilled soils (Beare et al., 1992). It is possible that these effects are mediated by the repeated disruption of mycelia during tillage; indeed this effect may also partly account for the apparent reduction in soil-borne fungal diseases which can be induced through tillage. Earthworms have been consistently shown to be more abundant in no-till soils (e.g., Atlanvinyte, 1964; Parmelee et al., 1990; Francis and Knight, 1993; Fraser, 1994).
3.3. Habitable pore space
Tillage clearly affects the size distribution and topography of pore networks, as described above, and thus will indirectly regulate organism interactions and their access to oxygen, substrate, and water.
The concept of `habitable pore space' suggests that there is a relation between the size of organisms and the zones of soils they are physically able to inhabit. This is conceptually straightforward for larger fauna, where physical exclusion from small pores is certain if exoskeletons are rigid; exclusion from large voids which would otherwise readily accommodate the animals only necessitates an appropriately small entrance, such as frustrated human cavers experience. However, more ¯exible bodies make a distinct size cut-off range more dif®cult to de®ne, and propagules, either in the form of juveniles, eggs or spores may permit colonisation to occur at lower size scales than would be intuitively considered. Amoebae are perhaps the ultimate in deformable organisms and it is not
clear how narrow a pseudopodium can become: if the nucleus ®ts, the amoeba will be able to pass through an ori®ce, in much the same way an octopus is limited by the dimensions of its most rigid component, its beak. Little is known about soil protistan ecology in relation to constraints imposed by physical structure.
Habitable pore space is most often calculated using water-release curves (e.g., Postma and van Veen, 1990; Hassink et al., 1993). The problem with this technique is that it assumes all pores are spherical, which is clearly never the case in real soils, and it essentially relates to the diameter of the largest water-®lled pore neck. Such a parameter is directly relevant to the consideration given above of whether organisms can gain access to large pores through `small entrances'. More direct measurements can be made using soil thin sections and image analysis (e.g., Darbyshire et al., 1989; Kampichler and Hauser, 1993; Crawford et al., 1993). The two methods do not necessarily give the same results (e.g., Bullock and Thomasson, 1979), for the reason alluded to above.
Coarse-textured soils have been demonstrated to promote the reproduction of the nematodeXiphinema index compared to ®ner textures (Sultan and Ferris, 1991). However, there are interactions with moisture status; under conditions of limited moisture, nematode reproduction can increase in ®ne textured soils (Har-ris, 1979), where there is a greater range of smaller pores consequently providing a greater moisture-hold-ing capacity. Hassink et al. (1993) have demonstrated a clear correlation between soil pore volume classes and nematode and bacterial biomass (Fig. 3). How-ever, this data is a rare instance of such correlation, and there are few such clear-cut examples in the literature. Grif®ths and Young (1994) demonstrated that reductions in pore space alone could not account for the large decrease in protozoan biomass measured when soils were compacted, and any differences they observed in soils of different structure was primarily related to differences in water regimes rather than the structure per se.
below. But many soil organisms also rely on water ®lms for their transmission through the soil, especially nematodes, protozoa and bacteria. Migration across a relatively large pore space merely lined with a thin ®lm of moisture would require a longer passage and utilisation of more energy compared to a direct route made permissible by the pore being ®lled with water. Filamentous fungi are rarely restricted by such factors since their hyphal growth form permits exploration of space with extraordinary ef®ciency, and they can translocate water within these conduits to permit bridging of air gaps several orders of magnitude greater than their diameter both in agar and soil systems (Ritz, 1995; Toyota et al., 1996). Chains of actinomycete ®laments may bridge in the same fash-ion, and roots obviously are able to do so at much larger spatial scales. The extent to which such biolo-gical structures may act as bridges to motile organ-isms, especially if water ®lms prevail, is unknown.
There is much discussion in the literature of the possible roles habitable pore space and physical pro-tection may play in mediating organism interactions (Elliott et al., 1980), especially predator:prey relation-ships (e.g., Alexander, 1981; Steinberg et al., 1987; Hattori, 1988; Heijnen and van Veen, 1991; Wright et al., 1993). The tenet is that organisms residing in pores of appropriate size will be protected from pre-dation by other organisms of larger dimension since the latter are denied physical access to their prey. This
concept is extended further with consideration of `physically protected organic matter' (Rovira and Greacen, 1957; Powlson, 1980), where the same prin-ciple applies, viz., substrate located in pores below a threshold size is unavailable to organisms since they cannot gain physical access to it. Nevertheless extra-cellular enzymes may be able to penetrate pores down to extremely small dimensions. This is subtly different from organic matter physically protected by pores becoming totally occluded through plugging with organic materials and ®ne clay particles (Adu and Oades, 1978; Foster, 1981; Elliott, 1986; Beare et al., 1994). Disturbance of the soil results in a redistribu-tion of the pore network, and the resultant architecture permits utilisation of newly exposed substrates and predation of freshly exposed organisms until a new equilibrium is attained, or further disturbance main-tains the dynamics of such processes. Tillage clearly plays a major role in generating such dynamics and all the attendant consequences such as increased respira-tion rates, mineralisarespira-tion/immobilisarespira-tion phenomena, population dynamics, etc.
Theoretical calculations of the extent to which such physical protection may operate have been made. Crawford et al. (1993) applied fractal descriptions of pore surface topology to calculate that approxi-mately half of the potential habitable area for a bacterium of 5mm diameter would be accessible to a predator of 30mm. Experimental evidence for the
protective microhabitat theory is more abundant. For example, Heijnen and van Veen (1991) reported that the number of cells of Rhizobium leguminosarum
surviving following inoculation into a loamy sand was strongly correlated to the water-®lled pore size distribution. Pores with necks <6mm positively affected the survival of the bacteria whereas pores with necks >6mm had a negative effect. It is clear that the water status of the soil when microbes are inocu-lated into it affects the resultant distribution of cells. In drier soils, cells will tend to be located in smaller pores. Postma et al. (1989) found that if a soil was relatively dry at the moment of introduction, the survival rate of introduced bacteria was higher than when cells were inoculated into wetter soils. This principal was used by Wright et al. (1993) to selec-tively introduce cells ofPseudomonas ¯uorescensinto known pore sizes, which were then subjected to grazing pressure by the ciliate protozoan Colpoda steinii, subsequently inoculated into the same soils. When the bacteria were predominantly located in the smaller pores (<6mm), the decline in viable cell concentration was less than that when located in larger pores. It is also clear that the water status of soils modulates the physical protection of prey, in that water ®lms regulate the mobility and activity of predators such as protozoa or nematodes. For example, Kuik-man et al. (1991) demonstrated that in soil micro-cosms maintained at three soil moisture levels, the activity of protozoa was severely restricted as pores of neck diameters >3mm were devoid of water.
One of the problems with the physical protection hypothesis with respect to predator:prey relations is that it assumes body sizes of predator and prey are signi®cantly different. Whilst this may be the predo-minant case for vertebrates and other animals, soil organisms can, as usual, provide exceptions. Bamforth (1985) reports that protozoan cells can occupy pores down to 2mm, and bacterial sized protists are known to occur in marine environments (Cynar et al., 1985). Soil protozoa have also been found to pass 0.4mm membrane ®lters (Grif®ths, personal communication). Furthermore, some microbes can circumvent the pro-blem of body size altogether, e.g., ciliates can generate water currents to wash prey cells out of niches (Hat-tori, 1994), and amoebal pseudopodia can penetrate pores to gain access to bacteria (Foster and Dormaar, 1991). A further problem is that although soil bacteria,
which can certainly have diameters as small as 0.4mm (BaÊaÊth, 1994), could in principal occupy pores of comparable dimension, most cells in soil are found in pores three times their diameter (Kilbertus, 1980), well within the range of many indigenous soil proto-zoa (Bamforth, 1985; Grif®ths and Ritz, 1988).
A key consequence of grazing of bacteria by pre-dators is that nutrient cycling is accelerated with consequences for the supply of nutrients to plants. The scenario of the C:N ratio of predator being lower than that of prey, with a resultant mineralisation of N is well rehearsed and studied (e.g., Elliott et al., 1979; Clarholm, 1985; Ingham et al., 1985; Coleman et al., 1988; Hassink et al., 1993; Grif®ths, 1994). Kuikman and co-workers (e.g., Kuikman and van Veen, 1989; Kuikman et al., 1989) have explored the concept in relation to habitable pore space and demonstrated that predation by protozoa in their experimental system led to an overall increase in plant nitrogen uptake, mea-sured using15N. The interaction between bacteria and protozoa was affected signi®cantly by the soil moist-ure regime (and hence propensity of the bacteria to be grazed). Similar conclusions were drawn by Hassink et al. (1993). Enhanced mineralisation due to grazing will also increase the possibility for leaching if plants are absent or their uptake of N is limited.
4. Gas movement in relation to micro-organisms and N-transformations
The transport of gases in soil is crucial to the survival and functioning of micro-organisms. As the supply of oxygen ¯owing into microbial habitats decreases below respiratory demand, aerobic activity will decrease and ultimately cease. In the presence of nitrate, denitri®cation will occur. The structure of the soil may act to speed or slow oxygen diffusion to habitat sites, depending on the connectivity and tor-tuosity of pore pathways. Tillage operations clearly affect these parameters and, perhaps more impor-tantly, control the spatial distributions of water-®lms, which are the crucial in controlling diffusion rates to and from active microbial populations.
is 104faster than through water (Marshall and Holmes, 1979, p. 271). Therefore, depending on the spatial arrangement of soil water-®lms, diffusion of O2to the
centre of a well aerated aggregate may be decreased signi®cantly.
The concept of neighbouring wet and dry patches in soil is not dif®cult to grasp at the ®eld scale. Every farmer knows this. At the microbial scale moisture patchiness, over very small scales (e.g., millimetres), can result in manifestly different N-transformations occurring side by side. Fig. 4 illustrates a situation where aerobic and anaerobic sites exist in close proxi-mity and are controlled by moisture ®lms slowing the rate of replenishment of O2 between and within
aggregates. The controlling factors in this spatial heterogeneity of soil moisture include aggregate/par-ticle size distributions and substrate composition and location. The effect of such situations on nitri®cation± denitri®cation processes is examined by Focht (1992) for structurally homogeneous soil.
Much has been made of the link between aggregate size distributions and the processes described above. Smith (1977) and Arah and Smith (1989) note that calculations of the size of aerobic zones, and thus the probability of speci®c N-transformation processes,
requires data of aggregate size distribution, which in turn is dependent on tillage practices (Adem et al., 1984). The link relies on the log-normal distribution of aggregates found in ®eld studies (Gardner, 1956) which provide a prediction of anaerobic fractions in soil, which are in turn linked to denitri®cation rates. However, there has been criticism of the approach adopted by Smith (1977), Arah and Smith (1989), and Arah and Vinten (1995), and other workers (Leffelaar, 1993; Sierra et al., 1995), mainly because they do not take account of soil structural heterogeneity (Rap-poldt, 1990). These approaches assume idealised spherical aggregates with properties that do not vary with size. For instance, bulk density is assumed to be constant across scales. Other authors have shown that bulk density can decrease with aggregate size (Gumbs and Warkentin, 1976; Young and Crawford, 1991), and soil aggregates are only rarely actually spherical. Further, there may be no strict relation between certain microbial parameters and aggregate size. Whilst Gupta and Germida (1988) found that micro-aggre-gates (<0.25 mm) had lower respiratory rates than macro-aggregates, the opposite relation was observed by Seech and Beauchamp (1988). The sensitivity of shape and density parameters to modelling
cation is not known. The variance in density alone may be expected to in¯uence any prediction in denitri®ca-tion rates signi®cantly, through associated changes in water content and gas ¯ow in aggregates. The ®ckle nature of microbial parameters with aggregate size further increases the risk of errors.
However, the models developed by such workers have gone a long way to incorporate heterogeneity in processes, and thus some of the criticisms levelled at them are too harsh. Arah and Smith (1989) examine the role of some soil `structural' attributes in in¯uen-cing denitri®cation rates in the ®eld. Taking log-normal aggregate size distributions they then input `structured' soils with mean aggregate sizes and asso-ciated standard deviations. They compare the relation between respiration rates and anaerobic fractions in a ®ne structured soil (mean radius of 0.2 cm and coef®-cient of variation [c.v.] of 100%) with coarse struc-tured soil (mean radius 1.0 cm and c.v. 100%). They conclude that where large aggregates are present a signi®cant percentage of the soil volume may remain anaerobic even when the aggregates are unsaturated and the mean aerobic respiration is low.
Nevertheless, Rappoldt's (1990) criticism of mod-els based on aggregate parameters is partly justi®able. He states that such models must account for a range of operational structures including macropore and smal-ler-scale aggregates. In soil science, the term aggre-gate is used continually to `quantify' and `describe' some structural parameters. In reality, distinct aggre-gates may be relatively rare features in a soil pro®le. Rather, soil is a complex interconnected framework, and the spatial context of aggregates (see above) is extremely relevant to the way soil functions. Many experimenters continue to search for operational struc-tural parameters which are ®rstly easy to `describe' and secondly intuitively linked to soil processes and tillage practices.
Rappoldt's view of a more appropriate concept of soil structure stems from a recognition that a model of structure at best should have a physical and visual similarity to the soil pro®le. Thus, in the case of Rappoldt's (1990), structure becomes spatial distances between cracks where the distribution of these dis-tances serves to parameterise the structure. An impor-tant point here is that Rappoldt's concept does not preclude the notion of distinct aggregates, whilst the concepts used by Smith (1977) and others preclude
structures that do not have distinct aggregates. This shift from number size distributions, which may or may not have been arti®cially created, to a more physically realistic structure which takes account of irregular geometry's is certainly attractive. In recent times it has allowed a range of soil structures to be directly related to gas and water transport (Crawford et al., 1993; Crawford, 1994), microbial dynamics (Kampichler and Hauser, 1993; Crawford et al., 1993) and to tillage practices (Young and Crawford, 1991, 1992).
This view of structure, then, allows for the signi®-cant spatial heterogeneity seen in both soil structure, oxygen uptake and denitri®cation rates seen at the ®eld scale. Measuring such `hotspots' of activity by averaging results may lead to considerable over- or under-estimates (Parkin et al., 1987). These hotspots in part arise from the different tillage practices which are adopted. Tillage will lead to a heterogeneous mixing of plant roots and other organic debris. The ®nal spatial distribution of organic material will dra-matically in¯uence subsequent biological activity. The ¯ow pathways from and to such organic `hot-spots' will, in turn, in¯uence the type of N-transfor-mation process which dominates (as seen in the minimum tillage section). Van Noordwijk et al. (1993) use the term `synlocation' to describe the spatial distribution of roots, biological activity and cracks in soil. They suggest that certain degrees of synlocation (i.e., resulting from certain tillage prac-tices) will increase N mineralisation. However, quan-titative evidence for this hypothesis has yet to be reported.
Rappoldt's (1990) analysis of oxygen consumption rates on a clayey soil demonstrate the juxtaposition of oxic and anoxic patches, sometimes within milli-metres of each other. These results indicate that local respiration rates may exceed bulk respiration by over a factor of 100. This variation is related to the location of potential anoxic zones to well-aerated cracks or biopores in soil, and again demonstrates the high degree of heterogeneity of microbial and N-transfor-mations which occur throughout the soil pro®le (Parkin et al., 1987).
water content per se which drives N-transformations. This is illustrated in Fig. 4(b), where it can be seen that isolated water-®lms may act to signi®cantly reduce oxygen into (and carbon dioxide ¯ow out of) a dry, but increasingly anoxic, zone. Microbial activity is cer-tainly in¯uenced by soil water content, but anoxic processes such as denitri®cation are not solely reliant on bulk water content. It is the spatial distribution of water-®lms, combined with the distribution of decom-posable organic matter, which has the ultimate control. This is what any physical disruption (tillage, root exploration, worm burrowing, etc.) is controlling at the small-scale, and this has the ®nal control over N-transformation rates. There may be a critical distribu-tion of water-®lms above which aerobic processes dominate. All that is required is for isolated water menisci to form in the manner shown in Fig. 4 and in a short time a relatively dry portion of soil will be anoxic.
5. Conclusions
We have shown that physically disturbing the soil pro®le can have profound effects on microbial dynamics of the soil system. A large body of literature supports the view that large-scale disruption of soil by tillage can have highly signi®cant effects on individual microbes, and on their functions (e.g., N-transforma-tion processes). The degree of disrupN-transforma-tion plays an important role in the ultimate transformation process. However, as we have again pointed out, knowledge of the changes brought about by the alteration in the soil structure is not enough to pinpoint the controlling mechanisms, even when allied to information con-cerning microbial species. Substrate quality and quan-tity play a major role in tillage±microbe±nitrogen relations. The ®ne-scale detail of soil has been shown to exert a profound in¯uence on the larger scale processes, being the source of signi®cant spatial and temporal heterogeneity of microbial-related pro-cesses in the soil pro®le. The heterogeneity of soil structure acts to increase this variability. A de®ning signature of soil-plant-microbial processes may well be this heterogeneity. How to measure, model and manipulate it is one of the keystones to sustaining agricultural productivity, allied to environmental health.
Acknowledgements
We are grateful to H. Rogasik, M. Joschko (Institut fuÈr Bodenforschung, ZALF, MuÈncheberg, Germany) and J. Brunotte (Institut fuÈr Betriebstechnik, FAL, Braunschweig-VoÈlkenrode, Germany) for the use of their CT images. The Scottish Crop Research Institute is funded by The Scottish Of®ce Agriculture Environ-ment and Fisheries DepartEnviron-ment.
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