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The cost of soil degradation in England and Wales Appendix K: Soil biota Introduction The structure and processes of terrestrial ecosystems are profoundly dependant upon a functioning soil biota. The biota is responsible for processing carbon, nutrient cycling, structural genesis and maintenance, pathogenicity and symbionts. It drives many above ground processes. However, in the majority of studies the soil biota reflects the pressures and changes in the rest of the ecosystem arising from human activity, and in only a few cases studies so far, drive or facilitate such changes 1. Consistent relationships between soil biodiversity and specific soil functions have yet to be demonstrated2, suggesting that more species do not necessarily provide more services – most likely due to a high degree of functional redundancy. There have been no single species – exclusive single function relationships found. Intense cultivation impacts heavily on the invertebrate population, especially earthworms, and decreases fungal biomass. Both of these will result in decreases in aggregate stability, increased susceptibility to erosion – but these losses are captured in the general effects of cultivation – i.e. this is the mechanism by which losses due to decrease in soil integrity are mediated. There are few terrestrial ecosystem services which are not dependant on soil biodiversity – either wholly or in part (Figure 1). Multiple services are provided by single species of soil organisms, which makes it almost impossible to disentangle the effects of a particular species on a particular function3. What is more, the delivery of the supporting service underly the delivery of the other services, so that these other services are dependant on the activities of soil biota, without necessarily exhibiting a strong relationship with any one group. Figure 1. Ecosystem services - those in bold are in whole or part dependant on soil biodiversity 1 Harris, J. (2009). Soil Microbial Communities and Restoration Ecology: Facilitators or Followers? Science 31 July 2009: Vol. 325 no. 5940 pp. 573-574 2 Turbe et al (2010) Soil biodiversity: functions, threats and tools for policy makers. Bio Intelligence Service IRD and NIOO, Report for European Commission (DG Environment). 3 Turbe et al (2010) Soil biodiversity: functions, threats and tools for policy makers. Bio Intelligence Service IRD and NIOO, Report for European Commission (DG Environment). Draft report Page 1 Cranfield University The cost of soil degradation in England and Wales The Function of the soil biota Turbe et al (2010)4 have outlined the principal functions of the soil biota in three principal categories, chemical engineers, biological regulators and ecosystem engineers. Decomposition – chemical engineers The soil biota is responsible for the decomposition of organic matter into small molecules which form the nutrient supply for further plant growth. This is carried out by a number of groups, but fungi and bacteria are the most important in this regard. Regulation – biological regulators Ranging from bacteria to small invertebrates, biological regulators act as predators and pathogens of plants and other organisms, affecting the distribution and activities of these organisms. They are extremely important in regulating population size, and the composition of plant communities, and dampen wild oscillations in populations of soil organisms and vegetation. Ecosystem engineers Small invertebrates, from earthworms to ants, and small mammals structure soils and produce the complexity found in soil environments. Fungi also structure soils by binding together mineral particles with their hyphae, and many bacteria produce gums which aids this process. The effect of ecosystem engineers are manifold, from producing pore structure allowing the free movement of liquids and gases, to isolating organisms and organic matter which regulates the availability of resources to other organisms. Factors affecting the soil biological system Abiotic factors A number of interacting factors affect the composition and activity of the soil biota. These include temperature, moisture, pH, salinity, and oxygen availability. Climate regulates the physiology of organisms, within their range of adaptation although many form resistant structures such as cysts to avoid periods of drought or low temperatures. The effect of pH is profound in controlling the composition and activity of the soil biota, by regulating the activity of enzymes, internal physiological states and the availability of nutrients – outside optimum ranges availability of some elements become so low or non-existent to the point of starving the biota – other elements, especially metals become so available that they begin to exert toxic effects. Biotic factors Plants can strongly influence the soil biota due to the latter’s dependence of these primary producers for their energy and carbon needs – and this is most clearly seen in the vicinity of plant roots in the “rhizosphere” which is the volume immediately surrounding them. Similar plants can be significantly dependant on the soil biota – the composition of plant assemblages may be regulated by pathogens and the presence of absence of key symbionts such as N-fixing bacteria and mycorrhizae. Services provided by soil biodiversity Soil organic matter cycling and fertility The soil biota processes organic matter arising from plants (as root exudates and above ground litter) animals and other organisms. This releases nutrients, builds structure and provides a buffer against fluctuations in food supply and environmental conditions. Soil structural formation and maintenance The formation of soil structure is driven by plant rooting and the activities of ecosystem engineers – this provides pore spaces and stability of soil structures, particularly aggregates. However, this 4 Turbe et al (2010) Soil biodiversity: functions, threats and tools for policy makers. Bio Intelligence Service IRD and NIOO, Report for European Commission (DG Environment). Draft report Page 2 Cranfield University The cost of soil degradation in England and Wales structure is constantly being turned over, and with out continued inputs and activities of the soil biota structure quickly degrades and collapses, increasing susceptibility to eroding forces, particularly wind and water. Similar compaction caused by grazing and trafficking can only be revered by the activities of the soil biota – absence of key groups, such as earthworms may make soil structural degradation irreversible. Regulation of carbon flux and feedback to climate Regulation of carbon fluxes has a key role to play in climate feedbacks. Immobilisation of carbon or its mineralisation (and therefore release into the atmosphere) is dependant upon the interactions between biota, structure and chemistry of the soil (Figure 2). C storage C Soil biota Regulated by •Structure •Chemistry •C input quality & quantity •Community phenotype C loss Figure 2 Control of C storage and loss is regulated by key biotic and abiotic factors, and mediated by the soil biota. Regulation of the water cycle The water relations in the soil are profoundly affected by the soil biota (Figure 3). Microbes, notably fungi affect water repellency, and after dry spells can impede the penetration of water into the soil surface. Plant water uptake and evaporation is affected by the relationships between plant roots and mycorrhizas, and the activities of roots feeding organism, the latter can hamper water uptake. Generally ecosystem engineers, such as earthworms generate pore spaces, drainage channels, which are stabilised in conjunction with the activities of fungi producing mycelia, and gums and mucilages generated by bacteria. Figure 3. The relationship between soil biota and soil properties with respect to water (redrawn from Bardgett et al 20015) 5 R. D. Bardgett, J. M. Anderson, V. Behan-Pelletier, L. Brussaard, D. C. Coleman, C. Ettema, A. Moldenke, J. P. Schimel and D. H. Wall (2001) The Influence of Soil Biodiversity on Hydrological Pathways and the Transfer of Materials between Terrestrial and Aquatic Ecosystems Ecosystems 4, 421 – 429. Draft report Page 3 Cranfield University The cost of soil degradation in England and Wales Decontamination and bioremediation Many groups of micro-organism are capable of producing molecules and structures capable of decomposing quite recalcitrant poly-aromatic, cross linked and polymerised compounds such as lignin. This allows the soil biota to degrade the complex materials produced over the course of seasonal cycles in response to litter fall. This also allows these groups to attack recalcitrant xenobiotics compounds produced by human activitiy, such as plastics and contaminants. Pest control There are several mechanisms by which soil biota can suppress pest organism. Mycorrhizas can prevent the infection of plant roots by pathogens. Some fungi will trap pest nematodes and digest them. Bacterial species produce endotoxins that, when ingested by insects result in death - Bacillus thuringiensis is a good example of this. Economic valuation Attempts to provide a monetary valuation of soil biodiversity are scarce, principally because of the difficulty in disentangling the effects solely attributable to a single species or group of species on a particular identifiable service or function – this is due to the complex interactions between soil organism and the abiotic environment and the emergent properties arising out of this complexity. Soils cannot exist without a living biota providing all of the supporting services and therefore there is a danger of double-accounting in considering the biota separately as this underlying service is manifest through the other services. This notwithstanding Pimental et al6 did attempt to provide an estimate of the value of ecosystem services delivered by the soil biota (Table 1). Table 1. Total economic benefit of services provided by soil biodiversity (modified from Pimentel et al, 19977) Service/Activity World economic benefits (x US dollars 109 per year adjusted to 2010 prices) 1030 34 122 164 217 271 244 8 2090 Organic matter cycling/waste recycling Soil formation Nutrient cycling Bioremediation Pest control Fertility/pollination Wild food Biotechnology industry Total This translates approximately (assuming only 70% of the terrestrial surface is covered by significant soil stocks) to £600GBP ha-1 at current exchange rates, and accounting for inflation since 1997. This total is realised through the variety of services experienced by society, and the cost of degradation of soil biota is therefore accounted for in the individual services described elsewhere in this report. Potential relationships between decreasing biodiversity and decline in service provision There are a number of potential relationships between biodiversity and ecosystem functions and therefore ecosystem service delivery (Figure 4). The simplest relationship would be linear – an increase in biodiversity leads to a steady increase in function. An idiosyncratic relationship occurs when the addition of further species results in an unpredictable change in a function or service through competition or predation. Redundancy occurs when beyond a certain diversity no further 6 7 Pimental, D. et al (1997) Economic and environmental benefits of biodiversity. Bioscience 47, 747 – 757. Pimental, D. et al (1997) Economic and environmental benefits of biodiversity. Bioscience 47, 747 – 757. Draft report Page 4 Cranfield University The cost of soil degradation in England and Wales functions are added to the system, as multiple organisms carry out a variety of functions – furthermore the inflection point, when this has been demonstrated in terrestrial plant communities for example, tends to be at a very low number, usually around 8 to 10 species. Since biotic communities in soil are highly diverse it is difficult to imagine a scenario where this low number would be found. Function or process rate Redundant Linear Idiosyncratic Species richness Figure 4. Relationships between species richness and ecosystem process rate or function (redrawn from Nielsen et al, 2010) Nielsen et al (2011)8 reviewed studies relating functions related to carbon cycling and biodiversity. In studies where the system was constrained to have fewer than 10 species, there were generally more positive relationships between increase in soil biodiversity and C cycling (Table 2). However, in those studies where more (arguably more realistically) than 10 species were involved the relationships were for more equivocal, with as many neutral relationships as positive ones, and more negative relationships than in the studies with fewer than 10 species. Table 2. Summary of studies where species richness of soil biological groups has been manipulated and aspects of C-cycling determined and proportions of negative, neutral or positive relationships detected with 10 or fewer species or more than 10 species (redrawn from Nielsen et al 20119). Negative Relationships in % Neutral Positive 4 7 13 4 28 0 0 8 25 7 0 0 15 50 14 100 100 77 25 79 11 13 31 2 57 18 8 13 0 12 18 46 52 50 44 64 46 35 50 44 No. Studies Communities with < 10 Species Decomposition Respiration Biomass Other Total Communities with > 10 Species Decomposition Respiration Biomass Other Total Further analysis of those studies exhibiting positive relationships between species richness and C cycling showed that in those studies with fewer than 10 species, the relationships were mainly idiosyncratic, whereas those with more than 10 species exhibited either redundancy or more often 8 Nielsen, U.N., Ayres, E., Wall, D.H. & Bardgett, R.D. (2011) Soil biodiversity and carbon cycling: a synthesis of studies examining diversity-function relationships. European Journal of Soil Science, 62, 105-116 9 Nielsen, U.N., Ayres, E., Wall, D.H. & Bardgett, R.D. (2011) Soil biodiversity and carbon cycling: a synthesis of studies examining diversity-function relationships. European Journal of Soil Science, 62, 105-116 Draft report Page 5 Cranfield University The cost of soil degradation in England and Wales unknown relationships – demonstrating the inherent difficulty in defending a simple “more diversity brings increasing function” (Table 3). Table 3. Summary of the type of positive relationships between soil species richness and Ccycling with 10 or fewer species or more than 10 species (redrawn from Nielsen et al 201110). No. Studies Communities with < 10 Species Decomposition 4 Respiration 7 Biomass 10 Other 1 Total 22 Communities with > 10 Species Decomposition 5 Respiration 6 Biomass 11 Other 1 Total 23 Linear Redundant Idiosyncratic Unknown 0 1 0 0 1 0 1 0 0 1 4 5 9 1 19 0 0 1 0 1 0 0 0 0 0 0 2 3 0 5 2 0 1 0 3 3 4 7 1 15 It is unlikely that any environmental disturbance would depress species richness to these levels without the wholesale loss of the soil itself – as occurs during major erosion events. Susceptibility of the soil biota to physical disturbance Generally as the size of soil organisms decrease, then their susceptibility to physical disturbance tends to decrease. In this sense relatively large organisms such as earthworms are readily killed by cultivation, and civil engineering operations. Fungi, because of their large mycelia structure and the lack of cross-cell walls in certain species are also susceptible. Bacteria are relatively unaffected by the direct effects of cultivation but are impacted by consequent changes in soil conditions. For example, opencast coal operations to form soil stores at the outset of working mine sites leads to the immediate loss of earthworms and fungi, but the consequent development of anaerobic conditions in soil stores leads to the majority of the soil biomass. Impact of human activity Humanity’s spread and demand for increasing food supply, has lead to a large part of the Earth’s terrestrial ecosystems becoming converted, dominated by humans 11, through a number of mechanisms: Cultivation Monoculture Fertilisers Pesticides Direct effects of physical disturbance have been described above, but there are other activities which may impact on soil biota– such as the pressures on edible fungi through foraging in forests. This may lead to loss of those symbionts required for the establishment of fastidious plant species. Implications of the loss of soil biota It is difficult to imagine situations where biota is lost first, resulting in degradation to the rest of the system, except in a few particular circumstances. The introduction of the New Zealand flatworm has led to a loss in aggregate stability in UK pasture soils, which could result in increased susceptibility to erosion. The elimination of earthworm populations can reduce the water infiltration rate in soil by up 10 Nielsen, U.N., Ayres, E., Wall, D.H. & Bardgett, R.D. (2011) Soil biodiversity and carbon cycling: a synthesis of studies examining diversity-function relationships. European Journal of Soil Science, 62, 105-116 11 Ellis, E.C., and Ramnkutty, N. (2008) Putting people in the map: anthropogenic biomes of the world. Frontiers in Ecology and Environment 6, 439 – 447. Draft report Page 6 Cranfield University The cost of soil degradation in England and Wales to 93%12. Senepati et al (1999)13 demonstrated a four to five fold increase in plant yield when earthworms were re-introduced to tea plantations. There are a number of putative mechanism whereby we could follow the loss of particular groups and their consequences for ecosystem functions and therefore ecosystem service flows in the functional groups of the soil biota, however these are heavily interrelated and co-dependant (Table 4). Table 4. Examples of how losses in biodiversity might impact ecosystem service flows Functional group Chemical engineers Biological regulators Example Functional loss Service loss Restorative action Fungi Yield decline; increased flood risk Yield decrease, increased erosivity Retain/add organic matter, decrease cultivation Reduce cultivation, minimise nutrient addition Ecosystem engineers Earthworms Decline in aggregate stability, loss of stable organic matter Increased susceptibility to pathogens, nutrient uptake compromised Decline in porosity, increase in compaction and erosivity Decline in yield, loss of soil, increased run-off, increased cultivation costs Decrease cultivation; add organic matter, increased herbicide use Mycorrhizae Influence of soil type There is indubitable difference in susceptibility brought about by different soil types. This may be due to the soil biota having a different “starting point” in different soils, but also some inherent properties will produce a buffering or amplification of the effects of direct disturbance and indirect pressures. For example, finer textured soils are more susceptible to physical pressures and the development of anaerobiosis as a result of the loss of structure. This means that careful matching of land use to soil type must be achieved to minimise loss in soil function and associated costs (Figure 5). Figure 5. mismatch of land use and soil type will lead to increased degradation and costs, loss in function and hence ecosystem service. 12 Clements, R.O. (1982) Some consequences of large and frequent pesticide applications to grassland. Third Australian Conference on Grassland Invertebrate Ecology, Adelaide: South Australia Government Printer. 13 Senapati, B.K., Lavelle, P., Giri, S., Pashanasi, B., Alegre, J. Decaëns, T., Jiménez, J.J., Albrecht, A., Blanchart,E., Mahieux, M., Rousseaux, L., Thomas, R., Panigrahi, P.K. and Venkatachalan, M. (1999) In-soil technologies for tropical ecosystems. In Earthworm management in tropical agroecosystems, eds P.Lavelle, L. Brussaard and P.F. Hendrix, pp. 199-237. CAB International, Wallingford. Draft report Page 7 Cranfield University The cost of soil degradation in England and Wales Conclusion Soil biota losses will be greatest where intense cultivation, inorganic fertiliser, biocide use, and contamination are greatest – but these costs are probably already captured in the costs for erosivity, flood risk, compaction and yield losses already calculated, e.g. arable, intensive grassland and contaminated sites. Invasive species will change the composition of the soil biota, with potential knock-on effects for soil biodiversity and the functions above. It is currently impossible to ascribe even qualitative relationships between soil biodiversity loss and loss in service values (Turbe et al, 2010). We must also recognise that many aspects of soil biodiversity are central to the fundamental operation of ecosystems, and economic valuation may not be helpful - and in a number of respects is dangerous. The soil biota represents critical stocks in ecosystems and is not substitutable. Draft report Page 8 Cranfield University