Natural and deliberate disturbances may affect soil organisms either directly or indirectly. Consequently, the biological processes that these organisms facilitate are also influenced by soil disturbance. Indirect effects are common.
The inter-relationship between changes in physical, chemical and biological characteristics of soil is further illustrated in Abbott and Murphy (2003). When one factor is changed, there may be a consequential effect on other factors and the final outcome is that the habitat of soil organisms is changed in several different ways following every type of disturbance (Abbott and Abbott 1989).
For any pathway of change, there are a variety of influences on soil organisms. For example, an increase in soil pH with the addition of lime may increase the activity of one group of organisms and decrease the activity of another. This may have no overall effect on some microbial-mediated processes (e.g. mineralisation), but it may affect others (e.g. nodulation of a legume). Understanding these pathways assists in predicting the impact of land management (i.e. soil disturbances) on soil biological activities.
The type, magnitude and frequency of soil disturbance are all likely to influence the diversity of soil organisms. The maximum diversity of species depends on an interaction between the frequency or intensity of disturbance and the growth rate of organisms (Huston 1994). Based on Huston's Dynamic Equilibrium Model, it is expected that:
(i) in soil with a highly active community, maximum diversity of organisms is expected to occur when there are relatively frequent or major disturbances.
(ii) in soil with a moderately active community, maximum diversity of organisms is expected to occur when disturbances are of intermediate frequency or moderate intensity.
(iii) in soil with a low level of activity of organisms, maximum diversity is expected to occur when there is a low frequency or low intensity of disturbance.
The presence of soil organic matter significantly influences heterotrophic soil organisms. Based on Huston’s model, an interaction between disturbance frequency or intensity and the rate of growth of organisms in soil would be closely linked with the amount and kind of organic matter. The diversity of organisms is expected to be high in a soil containing large amounts of different kinds of organic matter, but only if there is also a high level of disturbance. Low levels of disturbance of the same soil would have a lower diversity of organisms. In contrast, a soil with low levels of organic matter would be expected to have greater diversity if it was disturbed frequently.
It is more difficult to measure soil organism diversity than plant diversity. Also, in soil, organisms can be present at low numbers and may not be active because of unfavourable conditions. Thus organisms in low abundance are only likely to appear in an assessment of soil biodiversity when soil conditions are changed. While the application of the Dynamic Equilibrium Model is complex for soil organisms and needs more experimental testing, the following general hypotheses are proposed:
• for soils with high levels of organic matter
at low levels of disturbance: some organisms become dominant.
at high levels of disturbance: more even growth of a range of organisms is possible because the disturbance prevents the fast-growing organisms from out-competing the slow-growing organisms.
• for soils with low levels of organic matter
at low levels of disturbance: growth of organisms on organic matter is restricted by low quantities of organic matter and maximum diversity occurs because there is insufficient resource to allow fast-growing organisms to grow rapidly.
at high levels of disturbance: the organic resource becomes further depleted by conditions that favour mineralisation and most organisms become inactive.
The following is a series of examples of how different types of soil disturbance could change the activities of soil organisms. The examples are grouped according to:
A. natural disturbances,
B. disturbances due to land management,
C. disturbances associated with dispersal of waste and industrial activities.
This list is merely a sample to illustrate the types of influences experienced by soil organisms when their environment is changed. Disturbance in the ecological literature generally refers to discrete events rather than to continuous processes such as drought, but the distinction is always not clear. In this context for soil organisms, disturbance is used in a very broad sense to mean any change in soil conditions. Changed soil conditions can have positive or negative influences on growth of organisms, depending on the organism being investigated, as well as on the frequency, type and severity of disturbance.
Examples of natural events that disturb the habitat of soil organisms include the following:
1. Wind and water erosion removes surface soil layers that contain the majority of soil organic matter and soil organisms. Therefore, the contribution of soil organisms to biological processes is reduced by soil loss due to erosion. The lost soil surface is not replaced quickly as soil formation processes are extremely slow. Therefore, the new soil surface is formed by soils that originated at a lower depth in the profile where fewer organisms were present. Restoration of biological processes would take a long time because the important reserve of organic matter would also have been removed.
2. Slow drainage of land following high rainfall can lead to waterlogging in natural and extensively managed ecosystems. Increased water content of a soil lowers oxygen concentration and may reduce the activity of aerobic microorganisms. Simultaneously, activity of anaerobic organisms increases, and processes such as mineralisation continue with different microorganisms dominating until the water subsides and aerobic conditions return.
3. Flood influences soil organisms through deposition of topsoil onto lower-lying areas. Depletion of organisms and organic matter from one area can lead to their enhancement elsewhere. Biologically and chemically fertile flood plains can result. Increased plant growth at the site of deposition increases the capacity of the land to allow soil organisms to proliferate. In contrast, soil erosion from the original location reduces abundance of soil organisms.
4. Tree-fall occurs from time to time in forests or other natural communities following tree death or severe disturbance during storms, wildfire, or lightning strike. Localised soil disturbance occurs around the roots of disturbed trees. This increases soil aeration and reduces bulk density allowing fungi that may have been present in a dormant or relatively inactive state to be re-activated and colonise the tree stump. An example of a fungus that may be stimulated in this way is Armillaria. This fungus forms an extensive underground network and has been estimated to be one of the largest of all living creatures (Smith et al. 1992).
5. Digging by small animals can continually alter small pockets of soil, increasing aeration and mineralisation of organic matter, which may increase root growth and stimulate release of root exudates. Animals can also be important in the dispersal of spores of fungi and bacteria in soil. Marsupials were found to have a range of spores of ectomycorrhizal fungi in their faecal pellets (Lamont et al. 1985).
6. Fire occurs periodically in many natural ecosystems. Nutrient input into the soil, especially phosphorus, can increase after fire (Autry and Fitzgerald 1993). The loss of leaf litter from the soil surface during a fire alters the form and availability of organic carbon and energy for heterotrophic soil organisms. Therefore, fire can have a long-term influence on the cycling of nutrients in soil, as well as short-term effects.
Fire has little direct effect on the organisms below the soil surface. Generally, soil is well insulated and heat, even from a wildfire, does not penetrate many millimetres below the soil surface. Although fire has little direct effect on soil organisms, it does have an indirect effect on microbial biomass and respiration (Autry and Fitzgerald 1993). In this study, there was an increase in the microbial carbon in the 0-5 cm layer of soil following the fire, and a decrease in microbial nitrogen. At the unburnt site, qCO2 was higher in the surface layer, but not below 5 cm. The change in the ratio of carbon and nitrogen in the microbial biomass could indicate a change in the dominance of species of soil organisms.
Other significant changes in microbial activity following fire are induced by the growth of new roots as plants re-sprout and seeds germinate.
7. Drought and seasonally dry periods lead to significant changes in activity of soil organisms. Many soil organisms are well adapted to drying. Survival strategies of larger soil animals such as earthworms include deep burrowing to moister regions of the profile. Earthworms may aestivate or form cocoons that contain young earthworms that are less susceptible to drying than adult earthworms. Bacteria and fungi have various physiological characteristics which enable their survival in dry soil; when soil is moistened, they re-activate extremely quickly.
8. Freezing and thawing. In environments that are exposed to cycles of freezing and thawing, soil organisms respond in a similar way to that described above for wetting and drying (Edwards and Cresser 1992). The organisms that occur in such environments are able to tolerate extremes in conditions and respond quickly when conditions become more favourable for their growth.
9. Succession in plant communities. A major influence on soil organisms is successional change in above ground plant communities. Changes in the structure of plant communities are matched by changes in the structure of communities of soil organisms. This occurs principally because the type of organic matter changes or because fungi alter the nutrient uptake characteristics of roots.
However, soil organisms also contribute to the structure of plant communities. An example of the extensive impact fungi can have on plant community structure is demonstrated by the fungus Phytophthora cinnamomi. The disease caused by this fungus has eliminated many species of plant from sections of forest because of its broad host range. In contrast, colonisation of roots by AM fungi may enhance plant species diversity in swards of turf (Grime et al. 1987).
In this study, the plants C. erythraea and H. pilosella did not colonise the turf when mycorrhizal fungi were absent, whereas A. hirsuta and R. acetosa colonised the turf to a greater extent in the absence of mycorrhizal fungi.
The following disturbances are examples of changes imposed by land management. These changes all alter the soil in ways that alter the habitat of soil organisms. Any one disturbance does not have the same effect on all organisms.
Cultivation has direct, physical effects on a soil by altering the distribution of aggregates, increasing aeration, altering the moisture characteristics of the soil and incorporating organic matter. Cultivation also alters the distribution of organisms throughout the soil profile. Thus, the physical effect of cultivation has a profound direct effect on the habitat of soil organisms. Secondary effects of cultivation include changes in nutrient cycling that result from an increase in mineralisation of organic matter. This occurs due to increased aeration and greater access to organic matter on the soil surface.
Cultivation has a wide range of influences on soil organisms. It depends on whether or not the soil environment is changed to suit the growth of organisms and whether cultivation has a direct physical impact on an organism (e.g. damage to earthworms). A difficulty in trying to determine the impact of cultivation on a soil organism is that more than one factor is usually altered simultaneously.
Direct effects of cultivation
Example 1: Rhizoctonia solani
R. solani is a major pathogen in agriculture. Disturbance of soil breaks up hyphae and restricts the ability of the pathogen to colonise roots and cause disease, especially in wheat (e.g. Wiseman et al 1996; Rovira 1986).
Example 2: Arbuscular mycorrhizal fungi
Cultivation can reduce the capacity of AM fungi to take up phosphorus. This can occur even if colonisation of the roots is not affected because the functioning of the network of hyphae in the soil is disrupted by cultivation (e.g. McGonigal and Miller 2000).
Indirect effects of cultivation
Example 1: Earthworms
Earthworms appear to be susceptible to physical damage by cultivation practices. However, an important effect of cultivation on earthworms is the increase in mineralisation of organic matter associated with cultivation and the corresponding reduction in organic matter as an important nitrogen supply for the earthworms (e.g. Friend and Chan 1995).
Example 2 Microbial biomass
Cultivation can reduce total microbial carbon compared with direct-drilling over a one year period (e.g. Lynch and Panting 1980)
Fertiliser application to natural ecosystems to improve tree productivity or to agricultural and horticultural land has a significant effect on the abundance and activity of soil organisms. The increase in chemical fertility increases microbial biomass because of higher inputs of organic matter into the soil. For example, in an alpine tundra the total microbial biomass nitrogen increased with application of nitrogen (Fisk and Schmidt 1996). Similar effects are observed with the addition of phosphorus fertiliser to many soils. Major changes also occur in the relative abundance of soil organisms following fertiliser addition. This is because the altered soil conditions suit some organisms but not others.
Application of phosphate can increase the abundance of heterotrophic fungi in the soil. Simultaneously, the abundance of beneficial mycorrhizal fungi in the soil may decrease, depending on the amount of phosphorus added.
Lime application increases the pH of a soil, making it more suitable for the activity of some organisms and less suitable for others. However, a changed pH alone should not be the sole cause of a change in the relative abundance of organisms with the addition of lime. Soil amendments of this kind initiate a chain reaction of events that involve the activity of many different types of soil organisms.
In a study of the nodulation of clover, a pasture soil contained several strains of bacteria that wer able to form nodules on clover (Almendras and Bottomley 1987). Addition of lime and phosphorus to the soil changed the relative abundance of the two dominant strains or rhizobia that were recorded in the nodules. Such a change in nodule occupancy could affect plant production if the rhizobia differed in their ability to fix nitrogen.
Organic soil amendments include manure, legume residues, green manure and compost. Soil organisms have different responses to the addition of organic matter depending on its chemical structure and state of degradation. Legume residues usually have a high concentration of nitrogen and when they are degraded there is excess nitrogen available to the requirements of the microorganisms that mineralise it. The excess is released into the soil and is available to plants unless other microorganisms gain access to it first. Increased plant productivity further stimulates microbial activity in the soil.
Organic soil amendments alter the relative abundance of soil animals, influencing the interactions between members of the soil community that depend on others as a food source. Application of both legume residues and manure increased the number of nematodes that ate fungi (fungivores) and bacteria (bacterivores) in a field study as well as in an artificially controlled experiment (microcosm). In contrast, in the microcosm environment, there was no effect of addition of manure on the number of fungivores (Bohlen and Edwards 1994).
Pesticide application to a soil can have substantial and unwanted effects on some soil organisms. Pesticides are intended to affect only the target organisms. For example, herbicides target specific groups of plants and insecticides target insect pests. However, some pesticides affect organisms that are not their intended target. The impact of insecticides on beneficial soil animals, including earthworms, can be high but the impact on other organisms may be less marked (Duah-Tentumi and Johnson 1986). Assessments of the effect of pesticide application on soil organisms collectively (e.g. number of bacteria or fungi) gives no indication of the effects on the individual members of the microbial community.
Generally, herbicides applied at the rate recommended have little measurable effect on the total biomass of soil organisms. Where such effects have been shown, they can be related to changes in plant species (e.g. removal of weeds) or plant productivity (increases or decreases). Again, individual organisms can be affected differently by different herbicides, without this being reflected by the total soil microbial biomass.
Fungicides are applied to soils and plants to eradicate fungal pathogens. However, they may also affect non-pathogenic fungi. The magnitude of their effects depends on the fungus and the fungicide. Increasing the rate or frequency of fungicide application can reduce total fungal biomass (Duah-Yentumi & Johnson 1986).
In this study, a decrease in the abundance of fungi led to an increase in the abundance of cellulolytic bacteria. In contrast, the anaerobic bacteria decreased in abundance with the fungal biomass. These investigations are very complex because the abundance of organisms changes with time. Samples taken at one time do not reflect the possible dynamics of microbial abundance following pesticide use.
Fungicides can also interfere with the formation of an effective symbiosis between legumes and root nodule bacteria. Development of this symbiosis involves many steps including the growth of the bacteria and plant, infection of the root cells and formation of the nodule. Some stages are more sensitive to fungicides and herbicides than others (Mårtensson 1992). For example, the herbicide glyphosate had no effect on the infection process, but did affect nodule formation.
Rotation of cultivated plant species has significant effects on soil organisms because it changes the type of organic matter and the plant species available for plant-soil organism interactions. In particular, the abundance of AM fungi in soil is considerably influenced by changes in plant species because:
• some plants form mycorrhizas and others do not,
• plants that form mycorrhizas become colonised to different extents,
• plants that form mycorrhizas have different root densities and therefore different capacities to alter the abundance of the fungi in roots and in the surrounding soil (Thompson 1991).
The rotation of plants within a farming system significantly amplifies the abundance of potential plant pathogens. Inclusion of legumes in agricultural rotations increases the abundance of their root nodule bacteria in soil if they are either already present or are added as an inoculant.
Some plants produce compounds with potentially detrimental effects on some soil organisms. Brassica species are used as a disease-break crop because they decrease the abundance of root pathogens. For example, canola or oilseed rape can be used as a soil ‘biofumigant’ (Kirkegaard and Sarwar 1998). The molecules produced by these plants to destroy soil pathogens may also have detrimental effects on more beneficial soil organisms, so the non-target effects to be considered.
In addition, during the decomposition of some forms of organic matter, certain soil organisms produce molecules that can be toxic to plants if present in high concentrations. Acetic acid is an example of such a toxin.
Stubble burning reduces the amount of organic matter that is incorporated into the soil. In doing so, it eliminates an important source of carbon for heterotrophic soil organisms. Although nutrients are released into the soil after stubble burning, these nutrients move through a different pathway to those released during the microbial degradation of organic matter and they may not be as available to soil microorganisms. Stubble burning releases a high proportion of the carbon directly into the atmosphere and nitrogen, phosphorus and other elements are converted to inorganic, non-usable forms. In contrast, decomposition of organic matter is usually a more gradual process, although it can occur rapidly when a soil is intensely cultivated. Microorganisms degrade the carbon molecules in stubble and some carbon is returned to the atmosphere through microbial respiration. Other elements are released gradually as organisms colonise the stubble. Stubble retention provides a source of carbon, energy and other compounds required for the growth of soil organisms that are not present in the ash of burned stubble.
Stubble retention. As mentioned above, retention of organic matter in agricultural and horticultural systems provides a source of nutrients for soil organisms. In an outstanding example of the effect of long-term retention of organic matter, 60 years of trash mulching under sugar cane in South Africa raised soil microbial biomass and activity considerably (Dominy et al. 2002). Unfortunately, few long-term studies of organic matter retention are available so it is difficult to assess the degree to which stubble retention benefits different soil types and agricultural systems.
Salinity is a major problem that is often caused by excessive clearing of land for agriculture or excessive irrigation. An increase in salinity is detrimental to most soil organisms. Although saline environments occur naturally throughout the world and there are some tolerant organisms, most soil organisms have a low tolerance of salinity. Processes such as nodulation by symbiotic organisms are particularly susceptible to salinity. Isolates of Frankia differ in their capacity to increase growth of Casuarina in saline soils (Reddell et al. 1986). Similarly, species of AM fungi differ in their ability to tolerate saline conditions.
The role of soil organisms in soils that have been remediated to overcome hydrological problems of raising water tables could be considerable. Re-establishment of biological nutrient cycling processes based on improving plant cover and inputs of organic matter into soil can help restore soil chemical as well as physical fertility.
Soil acidity increases with some agricultural practices and soil organisms differ in their ability to tolerate acidity. Therefore, increasing acidity can change the relative abundance of species of fungi and bacteria. The great diversity of heterotrophic soil organisms provides a buffer to effects of soil acidity on the total soil microbial biomass, even though individual organisms may be quite severely affected. For example, nitrifying bacteria are highly intolerant of acid soil conditions and this will affect the transformation of ammonium to nitrate. Some species of root nodule bacteria are more tolerant of acidity than others. Furthermore, there are even differences within one species in tolerance of acidity. This means more acid tolerant strains of rhizobia can be selected for inoculant use with legumes that are to be grown in more acidic soils.
Soil disturbance in a forest decreased the ability of arbuscular mycorrhizal fungi to form mycorrhizas because the permanent hyphal network was damaged (Jasper et al. 1992). In contrast, disturbance of a pasture soil had little effect on the ability of AM fungi to form mycorrhizas. This is because in the pasture, the very high density of roots increases the abundance of AM fungi in the soil, creating a surplus of infective hyphae. Also, AM fungi in the pasture were not dependent on a permanent hyphal network because they are adapted to re-establishing mycorrhizas and hyphae each year. This example shows that understanding the way soil organisms function provides a clear basis to predicting how different forms of disturbance affect soil organisms and soil biological processes.
Tree planting and tree harvesting disturb soil in a similar way to that already discussed under ‘natural disturbances’. The technique of phospholipid fatty acid (PLFA) analysis was used to demonstrate the effect of logging and burning on microbial community structure in a coniferous forest in Central Finland (Bååth et al. 1995). Bacterial PLFAs increased compared with fungal PLFAs when the forest was clear-felled, and increased further after burning. The change in proportion of bacteria to fungi reflects the changes in the quantity and type of organic matter present following each disturbance.
Vehicle use has both localised and wide-scale influences on soil organisms. The localised impact of vehicles is increased soil compaction, which reduces the bulk density of the soil and decreases aeration. These physical changes to the soil alter the habitat of soil animals resulting in less organic matter degradation. Soil compaction and associated changes also impede water infiltration and reduce the suitability of the soil environment for the activity of many organisms. The wider impact of vehicle use is the dispersal of soil organisms over a large area. This may be of little consequence to most soil organisms, but it may have more serious consequences for plant communities if vehicles spread spores of a plant pathogen such as Phytophthora cinnamomi (Shea 1975).
The disposal of wastes onto soil alters its physical and chemical characteristics in ways that may significantly influence the growth and survival of soil organisms.
Sewage sludge and manure have long been used as soil amendments, both to improve soil fertility and to dispose of wastes. There are many significant effects of the addition of these materials to soil. A major concern in highly industrial communities is the effect of heavy metals contained within the wastes. Microorganisms differ in their tolerance of heavy metals (Angle et al. 1993). Differences in tolerance occur both between species and among strains of the same species.
Acid rain occurs as a result of industrial activity and can lead to significant changes in abundance and activities of soil organisms. The main direct effect of acid rain occurs through the input of water with high acidity onto soil. But acid rain can also have indirect effects on the soil community by affecting the growth and survival of plant communities. Because plants have such a major impact on microbial diversity and activity, any alteration in their growth is likely to be reflected in soil communities.
Elevated levels of atmospheric CO2 can alter plant growth as well as that of organisms in the soil. This can lead to major changes in the cycling of carbon in ecosystems, including plant growth and succession. Nodule number and nitrogenase activity may both be increased by elevated concentrations of CO2 in the atmosphere (O’Neil 1994).
Accidental spills of toxic substances disturb local areas of soil. While these occurrences may decrease the activity of some organisms, they increase the activity of groups of organisms that are able to catabolise these toxic substances (Toccalino et al. 1993). Addition of nitrogen to the soil in this study increased the activity of organisms that degrade butane. Therefore, in this case, the breakdown of the contaminating substance (butane) was limited by nitrogen, rather than by the presence and abundance of bacteria with a capacity to degrade it.
Urban rubbish disposal sites increase the activity of organisms that can tolerate anaerobic conditions. The anaerobic conditions are due to the compaction of rubbish material and the associated reduction in oxygen concentration. The anaerobic decomposition of organic wastes at land-fill sites produces high levels of methane gas, which is a greenhouse gas. However, the current trend towards composting and recycling urban organic wastes in preference to using landfill will reduce methane production at these sites.
Wide-scale addition of compost to soil is increasing in industrial countries because there is an increasing awareness of the potential for reducing waste by composting. However, fully composted material contributes organic material that has already had the majority of the readily available carbon and nitrogen sources removed and incorporated into the microbial biomass. The dominant carbon molecules remaining are lignin and cellulose which degrade slowly. Therefore, in the short-term, fully composted material does not increase the availability of nutrients in the soil.
The use of certain types of organic material in compost such as composted grape marc can eliminate plant pathogens (Hadar and Gordecki 1991). In this study, the germination of sclerotia of a pathogenic fungus in peat and composted grape marc was compared. There was little germination in composted grape marc, but 70% germination in peat. No sclerotia survived at all in the composted grape marc.
• Soil organisms are diverse and are found in all environments, even those with extreme physical and chemical conditions.
• Soil organisms respond variously to disturbances caused by natural events, land management or land misuse. The responses depend on how the environment of the organisms is changed and how this affects the ability of the organisms to function.
• In spite of the wide range in tolerance of soil conditions by soil organisms, the availability of organic matter overrides the functioning of soil organisms. Therefore, disturbances that change the type or quantity of organic matter in the soil will have significant impacts on soil communities.
• Little is known about the effects of soil disturbance on many individual soil organisms because they cannot be isolated, identified or studied individually.
• Organisms such as earthworms, some plant pathogens and symbiotic bacteria and fungi have been studied in more detail in terms of their responses to disturbance than have most other organisms.