Department for Environment Food and Rural Affairs Research project final report Project title Review of current knowledge on the impacts of climate change on

soil processes functions and biota Sub-Project D of Defra Project SP1601 Soil Functions Quality and

Degradation ndash Studies in Support of the Implementation of Soil Policy Defra project code SP1601 Contractor organisations

SKM Enviros Lancaster University Cranfield University Rothamsted Research

Report authors Richard Bardgett (rbardgettlancasteracuk ) Jim Harris Lynda

Deeks Andy Whitmore Project start date October 2009 Project end date March 2010

Page 1

Review of current knowledge on the impacts of climate change on soil processes functions and biota

Sub-Project D of Defra Project SP1601 Soil Functions Quality and Degradation ndash Studies in Support of the Implementation of Soil Policy

1 Introduction

The soil biota operates at a critical nexus in the functioning of the Earth system The highly complex and dynamic soil food web reflects the spatial-temporal variability of the soil physical and chemical environment and it mediates magnifies and buffers flows of energy and materials in the soil system (Wardle 2002 Bardgett 2005 Harris 2009) Of particular relevance to this section soil biota play a key role in regulating carbon dynamics in terrestrial ecosystems with potential global consequences for land-atmosphere exchanges of carbon and carbon cycle feedbacks that could amplify climate change (Bardgett et al 2008) Indeed it has been estimated that soils contain some 80 of the Earthrsquos terrestrial carbon stock and there is considerable concern that global warming will increase this liberation of carbon dioxide from soil to atmosphere due to enhanced microbial breakdown of soil organic matter (Jenkinson et al 1991 Cox et al 2000 Davidson and Janssens 2006) Such acceleration in carbon loss could significantly exacerbate the soil carbon cycle feedback if predicted climate change scenarios are correct (Cox et al 2000 Friedlingstein et al 2006)

Information on the factors that regulate soil biodiversity and the processes that it drives is relatively scarce However it is becoming evident that patterning of soil biota and the functions it drives occurs across a range of temporal and spatial scales Large-scale patterns of soil biodiversity and processes that occur across regional scales relate primarily to dispersal and to higher order climatic factors which determine rates of primary productivity and resource availability and also the activity of decomposer organisms Patterning at smaller spatial scales for example within grassland or forests or agricultural fields appears to relate mostly to patterns of resource availability and heterogeneity created by litter animal wastes roots and other organic materials and patterns of root carbon flow and disturbance Soil biological communities are also very susceptible to disturbance especially those caused by human interventions which very often lead to significant loss of soil species (Bardgett 2005)

With regards the function of the soil biotic community biotic interactions including trophic interactions between organisms that live in soil and those that occur between soil biota and the plant community play a significant role Whilst microbial processes of nutrient mineralisation are of central importance for plant nutrient supply there is much evidence to indicate that trophic interactions between microbes and their animal predators strongly influence rates of nutrient supply to plants thereby influencing plant productivity Trophic cascades involving top predators that feed on microbial-feeding fauna can also influence microbial communities and processes of decomposition and nutrient supply Evidence is also accumulating of important non-nutritional effects of animal-microbial interactions on plant growth in that animals indirectly influence root growth by influencing bacterial production of plant growth-promoting hormones Other types of biotic interactions that influence ecosystem form and function include mutualistic associations with plants such as mycorrhizal fungi and N fixers and the interactions between soil-dwelling plant pathogens such as fungal pathogens and herbivores and plants (Wardle et al 2004) All these biotic interactions together with impacts of soil organisms on the biophysical nature of decomposing material and the soil environment collectively act as important drivers of ecosystem processes of decomposition nutrient supply and plant productivity

Studies that have explored how variations in the diversity and composition of the soil community influence ecosystem processes mostly point to the important role of individual species and functional traits suggesting that to predict the consequences of species loss on ecosystem processes first requires an understanding of how individual species contribute to multiple species interactions Also in cases where diversity effects on decomposition processes have been found they tend to occur at the lower end of the diversity gradient (Liiri et al 2002 Setaumllauml and McLean 2004 Tiunov and Scheu 2005) pointing to a high degree of functional redundancy within soil communities (Liiri et al 2002 Setaumllauml and McLean 2004) However it is also evident that some species are more redundant than others and some are functionally irreplaceable (Laakso and Setaumllauml 1999ab) It is also important to recognize that the role of soil biota relative to abiotic factors that drive ecosystem processes varies

Page 2

greatly across ecosystems and that relationships are complicated further by the fact that the complexity of soil communities also varies greatly across ecosystems indeed it has been suggested (but not explicitly tested) that decomposition processes may be especially susceptible to changes in soil diversity in species poor soils (Wall 2007)

Another important point is that plant and soil communities are mutually dependant on one another and that feedback between plant and soil communities acts as an important driver of ecosystem structure and function (Wardle et al 2004 Bardgett and Wardle 2010) Plants provide C and other nutrients to the decomposer community but plant roots also act as a host for many soil organisms such as herbivores pathogens and symbionts In turn soil biota influence plant communities indirectly by recycling dead plant material and making nutrients available for plant use and directly through the action of the root-associated organisms which selectively influence the growth of plant species thereby affecting plant productivity and community structure The nature and significance of these interactions between plants and soil biota appears to be highly context dependent and involve a wide range of multi-trophic interactions (Bardgett and Wardle 2010) Moreover there is now much available evidence that feedback between plant and soil communities is instrumental in determining the way that ecosystems respond to global change including climate change (Bardgett and Wardle 2010) Hence to understand the consequences of global change phenomena for ecosystems requires explicit consideration of linkages between above-ground and below-ground biota

Soil structure and function is critically dependent upon its biotic component It follows that ecosystem goods and services which flow from terrestrial ecosystems are to a greater or lesser extent dependent upon that same biota ie the basis for all ldquonatural capitalrdquo Robinson et al (2009) recently set out to develop a comprehensive definition of soil natural capital based on mass energy and organisationentropy In their schema soil water temperature and structure are seen as valuable stocks along with the more traditionally recognised stocks such as organic matter content and mineralogy The current UK National Ecosystem Assessment explicitly recognises the role that soils and their biota play in underpinning and providing ecosystem goods and services

Bradley et al (2005) conjectured that the impact of climate change on soils is complex because a multiple of factors impact on soil processes function and biota causing changes over a time scale that ranges from hours to millennia From their scoping study they defined a division between direct impacts on soil (eg the effects of increased rainfall on soil water content) and indirect impacts (eg changes in litter inputs from plants impacting on soil organic matter as a result of changing plant productivity driven by climate change) Their work considered these two forms of impact in relation to the five core functions of soil identified in the UK Soil Action Plan food and fibre soil air and water interactions soil biodiversity soil in the landscape and cultural heritage and soils in mineral extraction construction and the built environment) within the context of generic climate changes envisaged under the UKCIP02 scenarios

bull Increasing summer temperature

bull Increasing winter temperature

bull More extreme high temperature

bull Less extreme low temperature

bull Higher winter rainfall

bull Less summer rainfall

bull More intense downpours

bull Sea level rise and increased coastal flood risk

bull More winter storms

Bradley et al (2005) identified that the main impacts of climate change will be in relation to soil moisture and soil temperature Soil water is a key driver of most soil processes and determines the use that soil can be put to Climate change will directly affect soil water through precipitation and temperature effects on evaporation and evapotranspiration and indirectly affect water through changes in plant growth and species The main soil forming processes affected by soil water include organic matter turnover soil structural formation weathering podzolisation clay translocation and gleying However because of the many different interacting influences on soil water it is difficult to

Page 3

predict the effect of climate change on soil water at regional or local level As with soil moisture soil temperature is also an important driver of soil processes potentially increasing heterotrophic activity in soil and the rate of decomposition of organic matter the rate of nutrient cycling and the chemical weathering of minerals Climate change will directly impact on soil temperature through rising air temperatures but will indirectly affect soils through changing plant productivity and community structure (Bardgett et al 2008)

The main changes in soil forming processes and properties as influenced by the UKCIP02 predicted climate change scenarios were suggested to relate to soil organic matter soil structure soil fauna and microflora acidification and nutrient status and soil erosion The review of Bradley et al (2005) revealed that there was uncertainty as to how climate change would impact on soil organic matter decomposition however the general opinion was that organic matter decomposition would likely exceed levels gained from increased plant growth resulting in a net loss of carbon A decline in soil organic matter would impact on soil structure resulting in a decrease in soil aggregate stability increased susceptibility to compaction lower infiltration rates increased run-off and increased susceptibility to erosion Drier climatic conditions would also result in greater frequency and size of crack formation in soils with high clay content particularly those with smectitic mineralogy Temperature and water are likely to result in changes in ecosystems and migration of vegetation zones which may seriously affect soil flora and fauna that can not adapt or migrate at an equivalent rate Significant increases of rain will lead to increases in leaching loss of nutrients and increasing acidification depending on the buffering pools existing in soil Both temperature and precipitation changes will impact on the rate of soil erosion by water and wind either through increased vulnerability of the soil properties or through changes in vegetation cover

In the review by Bradley et al (2005) most of the available information at the time only enabled a qualitative or semi-qualitative interpretation of the likely impact of climate change on soils Subsequently more data has become available and these are discussed in Section 3 of this report However the main effects identified by Bradley et al 2005 of climate change on the five core functions identified in the UK Soil Action Plan are summarised in Table 1

Table 1 Main climate change affects on soil function identified by Bradley et al (2005)

Soil function Impact of UKCIP02 climate change scenarios

Food and fibre bull Soil wetness water-logging and flooding are all predicted to increase in winter ndashincreasing the potential for soil sealing soil erosion poaching compaction and land use change

bull Warmer temperatures will increase the potential for growing a wider range of crops and increased amount of land under arable production ndash could lead to increased erosion and carbon loss

bull Less available work days in autumn winter and spring ndash result in damage to soil structure and problems from soil erosion nutrient and pesticide losses and N2O fluxes

bull Unpredictable springs ndash spraying for pests eg wheat bulb fly (Alternaria) will be more risky if the soil is still wet when access to the land is required ie increase risk of soil compaction spring N application vulnerable to risk of run-off

bull Higher spring temperatures will bring forward the start of the season

bull Drier and warmer summers ndash less wet weather diseases easier to combine but seed-beds very dry which will impact on the timing of germination of both weed and crop seed

bull Autumn conditions will start off dry but with an earlier onset of wetter conditions ndash increase urgency to get crops established before the onset of heavy rainfall dry conditions may make soil too hard and dry to cultivate efficiently after harvest may cause a shift to spring drilling on more difficult heavy soils The shift to spring drilling will leave the soil surface bare over wintre

Page 4

Soil function Impact of UKCIP02 climate change scenarios

increasing the risk of soil erosion Therefore in the long term soil resources will be reduced and food production will be affected

bull Generally warmer temperature may increase the risk of parasite infections if climate change helps that part of the parasite life cycle outside the body

Soil air and water interactions

bull Warming will decrease soil organic matter increase CO2 emissions increase litter decomposition and N mineralisation rate which may increase N leaching rate

bull In the long term carbon stock may become insensitive to temperature increases This is based on the assumption that soil physico-chemical ldquostabilisationrdquo reaction may respond more to warming than microbial decompositionrespiration reactions In turn warming may increase the rate of physico-chemical processes that transfer organic carbon to more stable carbon pools As a result total soil carbon loss may be very small and even may increase

bull Elevated CO2 will increase above-ground and below ground biomass Increasing the total carbon flux to the soil The effects of CO2 to soil C may be positive in the short term but reverse in the long term

bull Higher seasonal fluctuations in soil water increase the risk of changes to soil chemistry eg more leaching soil acidification gradually lower soil CEC and therefore buffering capacity

bull Drying out of peaty soils may convert peatlands from CO2 sinks to CO2 source

bull Drier summers will lead to the accumulation of nutrients and pollutants in the soil which will be flushed out when significant rainfall occurs for example during the autumn

bull Soil with a high water content promote methanogenic activity and reduces methanotrophic activity by reducing the size of oxidised zones

bull Waterlogged upland soils may become CH4 sources

Soil biodiversity As will be discussed later in this chapter very few UK projects have investigated climate impacts on soil biodiversity

Soil in the landscape and cultural heritage

Very few UK studies

bull Heritage sites will suffer from an increased rate of chemical-flooding risk on certain structures and fabrics

bull Increased soil water could increase biological attack and other decay (salt mobilisation)

bull Artefacts may be exposed through the process of soil erosion (wind and water) and begin to deteriorate

bull Changes to the vegetation supported will alter the look of the historic landscape

bull Lower water table will affect the preservation of archaeological remains Drier soils will increase damage to artefacts through increased oxidation and exposure due to soil erosion eg increased risk of wind erosion to peat soils as they dry out

Page 5

Soil function Impact of UKCIP02 climate change scenarios

bull If intensive arable cultivation shifts from the south east to the north buried archaeological sites currently not at risk from arable damage could become so

Soils in mineral extraction construction and the built environment

bull Increased winter rainfall especially extreme events could impact on land stability increased risk of land slides

bull increased risk of subsidence due to intermittent rainfall leading to an increased soil moisture deficit and soil shrinkage

bull High intensity rainfall events may overwhelm drainage systems and increase the risk of downstream flooding

bull Land may become unsuitable for development

bull Increased droughtiness will increase shrink-swell causing disturbance to building foundations and the need to underpinrepair

bull Increased temperature may exacerbate chemical attack to foundations

bull Increased temperatures may increase the risk to engineered structures based on clay caps ndash increasing leaching and release of landfill gases

bull Increase flooding and erosion will increase the risk of loss of contaminants from brownfield land

bull Land to be used for temporary flood drainage must be underlain by soils with suitable infiltration capacity and hydraulic conductivity and must not be erodible

bull Higher temperatures will also encourage volatilisation of some organic pollutants and mercury on contaminated sites

The seven key recommendations made by Bradley et al (2005) in relation to research requirements were

1 More research specifically aimed at soil functions under climate change Incorporating climate change on soil in all relevant research With research being updated to the latest climate change predictions or at least an assessment of possible changes

2 Further investigation of the interactions between climate change and pollutant deposition and exposure particularly critical loads and their exceedance for agricultural land and woodland in relation to issues of acidificationrecovery and eutrophication

3 Future research into soil functions under climate change should attempt to deal with uncertainties in climate predictions and soil process model formulation and parameterisation of soil processes Model development for organic and woodland soils needs to be promoted including the collection of data required for parameterisation and verification

4 Studies integrating the impact of land use changes and socio-economic factors should be encouraged since these may be as important as the impacts of climate change on soil functions

5 Further targeted research is recommended to investigate the effects of CO2 combined with changes in the temperature regime on soil function directly or indirectly and interactions with changes in temperature and rainfall

6 More research is warranted on the ability of soils to hold and buffer pollutants in the face of climate change particularly on lsquobrownfieldrsquo soils as well as in the urban built environment

Page 6

7 Improved estimates of non-CO2 GHG balance (primarily N2O and CH4) of forest soils including predictions of the impacts of climate change and the effects of forest management extension to broadleaf woodland and deforestation activities is important

2 Climate change scenarios

UKCIP09 climate change predictions as based on medium emissions scenarios for 2080 predict that England and Wales will get warmer with summers showing a slightly greater (on average 4degC) increase in temperature than winters (on average 3degC Table 2) While temperatures are predicted to rise the annual amount of precipitation is not expected to change However the distribution of rainfall throughout the year is predicted to change Summer precipitation is predicted to decrease across England and Wales (Table 2) on average by -24 to -18 while winter precipitation is predicted to increase by between 14 and 23 Also there is expected to be an increased frequency of extreme weather occurrences such as heat waves dry spells heavy rain and flooding as well as rises in sea level Central estimates are for heavy rain days (rainfall greater than 25 mm) over most of the lowland UK to increase by a factor of between 2 and 35 in winter and 1 to 2 in summer by the 2080s under the medium emissions scenario (UKCP09)

Table 2 UKCIP09 central climate change predictions based on medium emission scenarios for 2080 (low and high probabilities given in brackets)

Administrative regions

Winter mean temperature (degC)

Summer mean temperature (degC)

Annual winter mean precipitation ()

Annual summer mean precipitation ()

Wales 28 (1642) 35 (1958) 19 (442) -20 (-435) North East England 26 (1441) 37 (2058) 14 (232) -18 (-361)

East of England 30 (1647) 36 (1959) 20 (444) -21 (-456) South West England 28 (1643) 39 (2164) 23 (654) -24 (-506)

South East England 30 (1647) 39 (2065) 22 (451) -23 (-487)

West Midlands 29 (1644) 37 (2061) 17 (338) -20 (-446) East Midlands 30 (1646) 35 (1858) 19 (341) -20 (-446) Yorkshire and Humber 30 (1646) 33 (1754) 15 (233) -23 (-440)

North West England 26 (1440) 37 (2059) 16 (334) -22 (-430)

Mean 29 36 18 -21

The south west of England is predicted to experience the greatest increase in summer temperatures as well as the highest predicted increase in winter mean precipitation and lowest summer mean precipitation of all regions in England and Wales (Table 2) while the east of England south east England and Yorkshire and Humber are predicted to have some of the mildest winter temperatures The north east of England is predicted to experience a less extreme change in winter and summer precipitation

The predictions made by UKCP09 are supported by resent observed trends in UK climate reported by Jenkins et al (2009) Global average temperatures have risen by nearly 02degCdecade over the past 25 years In central England temperatures have risen by about a degree Celsius since the 1970s Annual mean precipitation in England and Wales has not changed significantly although summers do appear to be drier and winters wetter Over the past 45 years there has been an increase in heavy winter rainfall events Severe windstorms around the UK have become more frequent in the past few decades

Page 7

UKCP09 predictions are broadly consistent with UKCIP02 predictions Comparisons of UKCIP02 and UKCP09 by Jenkins et al (2009) suggest mean temperature projections are generally greater and summer reduction in rainfall is not as great using UKCP09 The range of increase in winter rainfall is broadly similar with a different geographical pattern Decreases in cloud cover in summer are also broadly in agreement Therefore observations made by Bradley et al (2005) with regard to impact of climate change on soil function are still valid Bradley et al (2005) defined both direct and indirect impacts of climate change on soil functions and these are summarised in Section 1 Table 1 Subsequently there has been more attention paid to the impact of climate change on soil biota and its impact on soil processes and functions This new information is summarised in Table 3

Table 3 Potential implications of predicted climate change on soil biota

Climate change Implications for soil biota

Warmer springs bull Changes in timings of seasonal events may cause loss of synchrony between species and the availability of food (Hopkins et al 2007 Newton et al 2008)

Warmer and drier summers

bull Reduced soil moisture content may limit plant production without additional irrigation

bull Drier soils may affect the mobility of soil fauna such as nematodes and earthworms (Bardgett 2005 Eggleton et al 2009)

bull Changes to habitat may favour drought tolerant soil biota soil may experience a shift in species which may impact on the over all function of the soil depending on redundancy in the system (Castro et al 2010)

bull Summer droughts may cause stress in some soil microbial communities and result in changes in fungal diversity impacting on functional diversity (Toberman et al 2008)

bull Drier conditions and higher temperatures may accelerate decomposition of organic material through increased oxygen availability and increased microbial activity However additional input of leaf litter from increased production may offset net loss of carbon from the soil profile (Dawson and Smith 2007)

bull Decreased loss of methane due to increased oxygen availability impacting on methanogens (McNamara et al 2006)

bull May cause shift in vegetation patterns with subsequent implications for soil biota (Pentildeuelas et al 2007)

Warmer and wetter winters

bull Increase the likely survival of soil pests and diseases (Newton et al 2008)

bull Inward migration of soil biota from warmer areas

bull Water logging will reduce the availability of oxygen in the soil profile affecting both soil fauna and soil flora (Sowerby et al 2008)

bull Soil compaction will impede root penetration and may restrict soil fauna movement within the soil profile (Whally et al 1995)

bull May cause shift in vegetation patterns with subsequent implications for soil biota (Pentildeuelas et al 2007)

Extreme events bull Drying of the top soil followed by sudden rewetting encourages flushes of microbial activity and nutrient loss from soil (Sowerby et al 2008 Gordon et al 2008)

Increased CO2 bull Increased transfer of C through root system into the soil stimulating

Page 8

Climate change Implications for soil biota

microbial abundance and activity (Castro et al 2010)

bull Increased transfer of C to the soil stimulating mycorrhizal fungi which may stimulate nutrient transfer (Tyliankis et al 2008)

bull Stimulation of microbial biomass can lead to microbial immobilization of N thereby enforcing plant N limitation (de Graaff et al 2007)

bull May cause shift in vegetation patterns with subsequent implications for soil biota

Section 3 Potential impacts of climate change on soil processes function and biota

Carbon and nutrient cycling

Climate change has both direct and indirect effects on soil organisms and the processes that they drive often with consequences for the return greenhouse gases to the atmosphere Direct effects include the influence of temperature changing precipitation and extreme climatic events on soil organisms and the processes that they drive whereas indirect effects result from climate-driven changes in plant productivity and species composition which alter soil physicochemical conditions the supply of carbon to soil and the structure and activity of microbial communities involved in decomposition processes and carbon release from soil (Bardgett et al 2008)

One of the most commonly discussed contributions of soil organisms to climate change is their role in soil organic matter decomposition and the idea that warming will accelerate rates of heterotrophic microbial activity thereby increasing the transfer of carbon dioxide from soil to the atmosphere and exports of dissolved organic carbon by hydrologic leaching (Jenkinson et al 1991 Davidson and Janssens 2006) The concern here is that because rates of soil respiration are more sensitive than is primary production to temperature (Jenkinson et al 1991 Schimel et al 1994) it is thought that climate warming will increase the net transfer of carbon from soil to atmosphere thus creating a positive feedback on climate change (Cox et al 2000) Although it is well known that temperature is an important determinant of rates of organic matter decomposition the nature of the relationship between temperature and microbial respiration is far from clear (Davidson and Janssens 2006) There are several reasons for this uncertainty but key factors include potential for variations in organic matter quality to influence the temperature sensitivity of microbial decomposition (Fang et al 2005 Conen et al 2006 Davidson and Janssens 2006) and for environmental constraints such as physical and chemical protection of organic matter to decrease substrate availability for microbial attack and thereby dampen microbial responses to warming (Davidson and Janssens 2006) Also there is uncertainty about how reactive different microbial and faunal groups and species are to temperature change with several studies showing that soil microbial and animal communities are insensitive to small increases in temperature (eg Kandeler et al 1998 Bardgett et al 1999 Wardle 2002) whereas others show that soil organisms and the carbon cycling processes that they drive are responsive to temperature change For instance the abundance of enchytraeid worms which dominate the fauna of acid peat soils have been shown to be strongly related to temperature and it is has been suggested that climate warming could increase their abundance leading to enhanced carbon mineralization and carbon loss from soil (Briones et al 1998 Cole et al 2002ab) Also a recent analysis by Gange et al (2007) related temporal shifts in autumnal fruiting patterns of macrofungi in southern England to shifts in climate and found that the average first fruiting date of 315 species is now earlier while last fruiting date is now later than was the case 56 years ago Their study also found that many species are now fruiting twice a year indicative of increased mycelial activity and possibly greater decomposition rates in ecosystems

Increases in the frequency of extreme weather events with climate change such as droughting and freezing may have an even greater effect on soil organisms and their activities than will overall changes in temperature and precipitation It is well know for example that droughting and freezing have substantial direct effects on microbial physiology and the composition of the soil microbial community with important consequences for ecosystem-level carbon dynamics (Schimel et al 2007) For example increased drought and drying in wetlands and peatlands which will lower the water

Page 9

table and introduce oxygen into previously anaerobic soil will create a more favorable environment for microbial activity (Freeman et al 2004) potentially enhancing the activity of enzymes (eg phenol oxidases) which play a pivotal role in the breakdown of recalcitrant organic matter (Freeman et al 2004) Because peatlands and wetlands represent amongst the largest stocks of terrestrial carbon globally (Ward et al 2007) such enhanced breakdown of recalcitrant organic matter under drying could have major implications for the global carbon cycle (Freeman et al 2004) Before leaving this topic it is important to note that methanogenic pathways are also affected by increased oxygen availability associated with drought in that methane emissions are reduced by toxic effects of oxygen on methanogens (Roulet and Moore 1995 Freeman et al 2002) Also drought can have marked effects on nitrous oxide emission from soils a potent greenhouse gas that is increasing in atmospheric concentrations at the rate of 02ndash03 per year (Houghton et al 1996) However responses depend on the severity of drought in that modest summer drought is likely to have limited effect on soil nitrous oxide emissions whereas more extreme drought can greatly increase them (Dowrick et al 1999)

The majority of studies to date that have explored effects of climate change on biological systems and soil organisms have considered single factors such as elevated atmospheric carbon dioxide concentration warming and drought However there is much potential for interactions between these factors to have additive or antagonistic effects on soil organisms and the activities that they drive (Mikkelsen et al 2008 Bardgett et al 2008 Tylianakis et al 2008) Very little is known about the influence of multiple and interacting climate drivers on soil organisms and their activities although some studies do point to strong non-additive belowground effects of these drivers with feedback consequences for carbon exchange For instance microbial decomposition of peat was found to be significantly greater when subject to both elevated temperature and atmospheric carbon dioxide than when these factors were each elevated singly (Fenner et al 2007ab) thereby potentially causing an even stronger feedback on carbon loss from soil as dissolved organic carbon in drainage water and respiration Added to this complexity is our knowledge that other organisms and trophic groups that influence soil microbes directly such as microbial-feeding fauna will also respond to multiple climate change factors (Wardle 2002 Bardgett 2005 Tylianakis et al 2008) This complexity further hampers our ability to predict effects of multiple climate change drivers on soil biological communities and carbon exchange feedbacks

In addition to multiple climate change drivers soil organisms and their activities are also affected substantially by other global change phenomena such as nitrogen deposition invasion of new species and land use change Perhaps the strongest driver is land use change (cf Sala et al 2000) and it is widely documented that changes in the intensity of land use or the conversion of natural vegetation to agriculture or forestry can have substantial and often strongly negative and irreversible effects on soil biological communities and their activities (Brussaard et al 1997 Wardle 2002 Bardgett 2005) One pattern that commonly emerges in the context of land use change is that intensification of farming including increased tillage fertilizer use and grazing is typically associated with an increased role of the bacterial-based energy channel relative to the fungal-based channel (Wardle 2002 Bardgett 2005 Bardgett and Wardle 2010) which is away from what would typically found in more stable late successional ecosystems with large fungalbacterial ratios (Harris 2009) As discussed above this increased bacterial role is associated with faster leakier nutrient cycling and more losses of nutrients and carbon in water and greenhouse gases to the atmosphere (Wardle et al 2004 van der Heijden et al 2008) In contrast low intensity management systems often encourage fungal-based soil food webs that are more similar to those of natural systems and tend to be associated with more efficient nutrient cycling (Bardgett and McAlister 1999 Gordon et al 2008) and enhanced soil carbon sequestration (De Deyn et al 2008) Although not tested global change drivers may alter the balance of communities in favour bacterial populations thereby accelerating rates of nutrient and carbon mineralization with implications for carbon sequestration and C loss to the atmosphere

Soil biological communities are also strongly affected by nitrogen enrichment which is of high relevance because anthropogenic activities have substantially increased global rates of nitrogen fixation and deposition (Schlesinger 2009) For instance it is well known that nitrogen enrichment can have direct and differential impacts on extracellular enzymes involved in decomposition processes This typically involves stimulation of the synthesis of cellulases which degrade labile high cellulose litter but suppression of the synthesis of ligninolytic enzymes by white rot fungi which decompose recalcitrant high lignin litter (Carreiro et al 2000 Waldrop et al 2004 Allison et al 2008) Also

Page 10

nitrogen enrichment is known to influence the abundance and diversity of different components of the soil microbial community including saprophytic fungi (Donnison et al 2000 Allison et al 2008) mycorrhizal fungi (Egerton-Warburton and Allen 2000 Frey et al 2004) and soil fauna (Scheu and Schaeffer 1998 Ettema et al 1999) which are also affected by climate change and are well known to have substantial effects on decomposition processes and ecosystem-level carbon exchange A recent meta-analysis on this topic revealed that soil microbial biomass declined 15 on average under nitrogen fertilization but that declines in abundance of microbes and fungi were more evident in studies of longer durations and with higher total amounts of nitrogen added (Treseder 2008) Moreover that study showed negative responses of microbial biomass to nitrogen fertilization to be significantly correlated with declines in soil carbon dioxide emissions indicating that moderate declines in microbial biomass under nitrogen fertilization may also have consequences for carbon fluxes However another meta-analysis of 109 studies across the globe revealed that nitrogen enrichment had no significant effect on net ecosystem carbon dioxide exchange in non-forest natural ecosystems but did increase methane and nitrous oxide emissions by 97 and 216 respectively (Liu and Greaver 2009) It was suggested therefore that any potential positive effects of nitrogen enrichment on the global terrestrial carbon sink should be offset by the stimulation of methane and nitrous oxide emissions which are more potent greenhouse gases than is carbon dioxide (Liu and Greaver 2009) Importantly nitrogen deposition and other global changes can also influence soil microbes and decomposition processes indirectly through altering vegetation composition and productivity and by alleviating progressive nitrogen limitation of plant growth which typically occurs under elevated atmospheric carbon dioxide (Finzi et al 2002 Luo et al 2004 de Graaff et al 2006)

The likely effect of drought during summers is well-appreciated but much less is known about the impacts of warmer wetter winters for which plants appear to have fewer adaptations to cope (Whitmore and Whalley 2009) Waterlogging becomes more likely with increased rainfall but at the same time root respiration is likely to increase in response to warmer temperatures There is thus a considerably raised risk of waterlogging of UK soils during the future winter months No additional impact of drought has been found on cereal yields following winter waterlogging and reasonable diversity and resistance to waterlogging has been found in UK cereal varieties (Dickin and Wright 2009 Dickin et al 2008) However soil-dwelling organisms may be at risk some earthworms for example are more intolerant of waterlogging than others (Chuang and Chen 2009) Earthworms are relatively well studied other species less so and in general macrofauna diversity is greatly reduced in flooded grasslands (Plum 2005) with opportunists becoming more abundant Microbes and plants compete for resources in waterlogged soils For example Blom (1999) reported that plants out-competed nitrifiers for ammonium in waterlogged soil It is not clear to what extent plants and microbes compete for oxygen

In general very little is known about the combined effects of global changes on soil biological communities and their activities but they clearly have the potential to amplify suppress or perhaps even neutralize climate change driven effects on soil microbes and their feedback to carbon exchange (Bardgett et al 2008) A recent synthesis by Tylianakis et al (2008) of data from 688 published studies on the effects of global change on biotic interactions in terrestrial ecosystems (including those that occur in the decomposer food web) highlighted that there is substantial variability among studies in both the magnitude and direction of effects of any given global change driver on any given type of biotic interaction Further that analysis highlighted that the unanticipated effects of multiple drivers acting simultaneously create major challenges in predicting future responses to global environmental change Experimental studies that simultaneously vary two or more global change drivers within the same experiment therefore have considerable promise for improving our understanding of how interactions involving soil communities and their effects on ecosystem-level processes may respond to current global change scenarios

Soil structural integrity and dynamics

The architecture of soil the ways in which particles are arranged in space so forming a stable connected pore space determines the habitat of soil dwelling organisms including plants This soil physical environment is mutable however Soil is hard or dusty but transmits gases readily when dry when wet it becomes soft and plastic and gas ingress becomes much reduced These two extremes are expected to become more prevalent with the changes in climate expected for the UK drier

Page 11

summers and wetter winters The presence of plants indirectly exacerbates the effects of climate change by extracting water in summer and oxygen for root respiration in the winter There is a greater risk of compaction with wetter more plastic soils with late-harvested crops such as potatoes or sugar beet and establishment afterwards Working day access to land may be reduced or more variable leading to damage to soil through inappropriate management (Section B Degradation) Drought may affect soil stability and structure and possibly encourage wind erosion Cecillon et al (2010) examined sites along a latitudinal mountain spatial climate gradient for aggregation and aggregate stability and showed that erodibility was linked to climate and therefore susceptible to change under a shifting climatic regime Other studies have shown effects on organisms associated with the genesis of aggregate structure For instance Eggleton et al (2009) demonstrated in southern England pasture woodland hat earthworm community structure was dependant on soil temperature and water This faunal group has long been established as being of critical importance in no and minimal-till systems both organic and inorganic with potential for declines in aggregate stability as a result of climate change linked to declines in earthworm abundance and shifts in earthworm community structure There are also emerging models linking earthworm population dynamics and soil structural components (Blanchart et al 2009) which offer the possibility of modelling a biotic and abiotic component simultaneously under different climate change scenarios with consequences for hydrology erodibility and trophic level effects

Kohler et al (2009) found that increased CO2 concentrations led to a significantly higher percentage of stable aggregates growing under Lectuca sativa in drought conditions and this was linked to increases in soil microbial biomass and inoculation with a vesicular arbuscular mycorrhizal fungus and plant-growth-promoting rhizobacterium Other workers (Rillig et al 2001) had found a similar effect of elevated carbon dioxide and increased water supply by irrigation on increased aggregate stability due to arbuscular mycorrhizal fungi in soils under Sorghum

Earlier work suggested that climate change would not affect accessibility to land unless winter rainfall increased by 15 (Rounsevell and Brignall 1994) Since this is now what is expected it may be necessary to re-calculate workable days for England based on up-to-date climate change scenarios Neither the direct effect of climate change on soil stability via wet-dry cycles nor its indirect effect via the soil fauna is certain and as Horn and Smucker (2005) have noted that changes in aggregate stability and soil structure can be undesirable if the soil becomes difficult to manage We need to better understand the processes underlying soil structure in order to predict direct soil response to climate change and we need to better understand the wider impact of climate change on soil ecosystems if we are to understand and predict the indirect effects of the soil fauna on soil

Warmer wetter winters may lead to increased competition for oxygen among more strongly respiring organisms in wetter soils into which oxygen penetration is slower Drier summers will lead to soils into which root penetration becomes restricted Both effects are likely to impact on the ability of plants to acquire nutrients and on biogeochemical cycles in general Research on waterlogging appears to have concluded in the 1980s that UK cereals could compensate provided waterlogging did not occur during establishment or repetitively (eg Belford et al 1985) While this may have been true of the conditions prevailing at the time the same may not be true for our future climate The effect that plant root extraction of oxygen has on soil fauna and microflora and vice versa appears to be poorly researched especially in the context of our expected climate change

In summary stability of soil is likely to be impacted by the increasing intensity of wet-dry cycles with climate change but note that an increase is not necessarily desirable if the soil becomes less workable Stepniewska and Stepniewska (2009) have stressed the need for a moderate stable redox above 300 mV Soil fauna and community structure is also likely to be impacted by a change in climate with effects on soil stability that are unclear It is also likely that with wetter winters the number of days when soil is safely accessible by heavy farm machinery without causing damage may become more variable and therefore unpredictable

Page 12

4 Methodologies for investigating the impacts of climate change on soil

Experiments on climate change drivers have been carried out over a variety of spatial and temporal scales ranging from short term laboratory incubation studies to ecosystem-level and long-term manipulations of climatic factors (Wullschleger and Strahl 2010) The main approaches for studying climate change include (1) the use of environmental gradients (temperature and water) and reciprocal transplants (2) in situ field manipulation experiments including Free-Air CO2 Enrichment (FACE) experiments for manipulation of atmospheric CO2 and field-scale manipulations of temperature and precipitation (3) controlled environment facilities such as the Ecotron controlled environment facilities at Imperial College Silwood Park UK and Montpellier France and (4) highly artificial often laboratory based microcosm experiments that have little relevance to real systems These approaches in the order listed above follow a spectrum of decreasing realism but increasing mechanistic control We discuss these approaches in turn

Environmental gradients (temperature and water) and reciprocal transplants

Climatic gradients for instance in annual precipitation and temperature that cross continents countries and elevation gradients are commonly used to determine impacts of climatic variation on soil biota and processes While useful for establishing general patterns such approaches leave significant questions about other factors that could explain differences in soil biota along climatic gradients such as soil fertility and mineralogy To overcome this problem an associated approach is the use of transplant experiments whereby intact soil-vegetation turves (or varying size) are transplanted at different places along climatic gradients so that effects of movement to another climate on soil biota can be assessed This approach for example was used by Briones et al (19971998) who transplanted peat soils from high to lower altitudes at Great Dunn Fell Cumbria to simulate climate warming and that this increased the density of enchytraeid worms the dominant fauna of these peat soils leading to enhanced decomposition and DOC concentrations in soil leachates The same system was also used by Tipping et al (1999) to show that warming and drying can accelerate the production of dissolved organic matter in organic soil horizons Such approaches are valuable in that they provide information on the response of soil biota and processes to real changes in climate but they are limited by the lack of control of environmental variables along transects and potential effects of disturbance from moving soil cores from one site to another

The further experimentation moves away from surveys and experiments in the field the less likely they are to represent real world systems This is not necessarily an issue when detailed and specific mechanisms are being explored but become increasingly problematic when large scale predictions are asserted from them

In situ field manipulation experiments

Many studies have used various field-based manipulations of climate including elevated carbon dioxide in the previously mentioned FACE experiments (eg Norby et al 2004 Jackson et al 2009) drought using rainfall roofs (eg Beier et al 2004) and artificial warming using heating cables (eg Grime et al 2008) passive night time warming roofs (eg Beier et al 2004) and infra-red lamps (Zhang et al 2005) Such experiments have contributed significantly to our understanding of the effects of different climate change drivers on vegetation soil biota and soil processes as detailed in the previous section However as stated previously most studies of this kind have explored effects of single climate factors whereas there is much potential for interactions between multiple factors to have additive or antagonistic effects on soil organisms and the activities that they drive (Bardgett et al 2008) Therefore future experiments which manipulate multiple climate change and other site factors are needed to better understand the effects of climate change on soil biota

As an example of in situ field manipulations Zhang et al (2005) artificially heated soils under tall grass prairie using infra-red heaters to simulate an increase in daily soil temperatures of 18 ndash 27oC and studied two clipping regimes clipped and unclipped In the heated treatments they found changes in the soil microbial community structure as determined using phospholipid fatty acid analysis (PLFA) in the unclipped plots with a shift to fungal dominance but not in the clipped

Page 2

greatly across ecosystems and that relationships are complicated further by the fact that the complexity of soil communities also varies greatly across ecosystems indeed it has been suggested (but not explicitly tested) that decomposition processes may be especially susceptible to changes in soil diversity in species poor soils (Wall 2007)

Another important point is that plant and soil communities are mutually dependant on one another and that feedback between plant and soil communities acts as an important driver of ecosystem structure and function (Wardle et al 2004 Bardgett and Wardle 2010) Plants provide C and other nutrients to the decomposer community but plant roots also act as a host for many soil organisms such as herbivores pathogens and symbionts In turn soil biota influence plant communities indirectly by recycling dead plant material and making nutrients available for plant use and directly through the action of the root-associated organisms which selectively influence the growth of plant species thereby affecting plant productivity and community structure The nature and significance of these interactions between plants and soil biota appears to be highly context dependent and involve a wide range of multi-trophic interactions (Bardgett and Wardle 2010) Moreover there is now much available evidence that feedback between plant and soil communities is instrumental in determining the way that ecosystems respond to global change including climate change (Bardgett and Wardle 2010) Hence to understand the consequences of global change phenomena for ecosystems requires explicit consideration of linkages between above-ground and below-ground biota

Soil structure and function is critically dependent upon its biotic component It follows that ecosystem goods and services which flow from terrestrial ecosystems are to a greater or lesser extent dependent upon that same biota ie the basis for all ldquonatural capitalrdquo Robinson et al (2009) recently set out to develop a comprehensive definition of soil natural capital based on mass energy and organisationentropy In their schema soil water temperature and structure are seen as valuable stocks along with the more traditionally recognised stocks such as organic matter content and mineralogy The current UK National Ecosystem Assessment explicitly recognises the role that soils and their biota play in underpinning and providing ecosystem goods and services

Bradley et al (2005) conjectured that the impact of climate change on soils is complex because a multiple of factors impact on soil processes function and biota causing changes over a time scale that ranges from hours to millennia From their scoping study they defined a division between direct impacts on soil (eg the effects of increased rainfall on soil water content) and indirect impacts (eg changes in litter inputs from plants impacting on soil organic matter as a result of changing plant productivity driven by climate change) Their work considered these two forms of impact in relation to the five core functions of soil identified in the UK Soil Action Plan food and fibre soil air and water interactions soil biodiversity soil in the landscape and cultural heritage and soils in mineral extraction construction and the built environment) within the context of generic climate changes envisaged under the UKCIP02 scenarios

bull Increasing summer temperature

bull Increasing winter temperature

bull More extreme high temperature

bull Less extreme low temperature

bull Higher winter rainfall

bull Less summer rainfall

bull More intense downpours

bull Sea level rise and increased coastal flood risk

bull More winter storms

Bradley et al (2005) identified that the main impacts of climate change will be in relation to soil moisture and soil temperature Soil water is a key driver of most soil processes and determines the use that soil can be put to Climate change will directly affect soil water through precipitation and temperature effects on evaporation and evapotranspiration and indirectly affect water through changes in plant growth and species The main soil forming processes affected by soil water include organic matter turnover soil structural formation weathering podzolisation clay translocation and gleying However because of the many different interacting influences on soil water it is difficult to

Page 3

predict the effect of climate change on soil water at regional or local level As with soil moisture soil temperature is also an important driver of soil processes potentially increasing heterotrophic activity in soil and the rate of decomposition of organic matter the rate of nutrient cycling and the chemical weathering of minerals Climate change will directly impact on soil temperature through rising air temperatures but will indirectly affect soils through changing plant productivity and community structure (Bardgett et al 2008)

The main changes in soil forming processes and properties as influenced by the UKCIP02 predicted climate change scenarios were suggested to relate to soil organic matter soil structure soil fauna and microflora acidification and nutrient status and soil erosion The review of Bradley et al (2005) revealed that there was uncertainty as to how climate change would impact on soil organic matter decomposition however the general opinion was that organic matter decomposition would likely exceed levels gained from increased plant growth resulting in a net loss of carbon A decline in soil organic matter would impact on soil structure resulting in a decrease in soil aggregate stability increased susceptibility to compaction lower infiltration rates increased run-off and increased susceptibility to erosion Drier climatic conditions would also result in greater frequency and size of crack formation in soils with high clay content particularly those with smectitic mineralogy Temperature and water are likely to result in changes in ecosystems and migration of vegetation zones which may seriously affect soil flora and fauna that can not adapt or migrate at an equivalent rate Significant increases of rain will lead to increases in leaching loss of nutrients and increasing acidification depending on the buffering pools existing in soil Both temperature and precipitation changes will impact on the rate of soil erosion by water and wind either through increased vulnerability of the soil properties or through changes in vegetation cover

In the review by Bradley et al (2005) most of the available information at the time only enabled a qualitative or semi-qualitative interpretation of the likely impact of climate change on soils Subsequently more data has become available and these are discussed in Section 3 of this report However the main effects identified by Bradley et al 2005 of climate change on the five core functions identified in the UK Soil Action Plan are summarised in Table 1

Table 1 Main climate change affects on soil function identified by Bradley et al (2005)

Soil function Impact of UKCIP02 climate change scenarios

Food and fibre bull Soil wetness water-logging and flooding are all predicted to increase in winter ndashincreasing the potential for soil sealing soil erosion poaching compaction and land use change

bull Warmer temperatures will increase the potential for growing a wider range of crops and increased amount of land under arable production ndash could lead to increased erosion and carbon loss

bull Less available work days in autumn winter and spring ndash result in damage to soil structure and problems from soil erosion nutrient and pesticide losses and N2O fluxes

bull Unpredictable springs ndash spraying for pests eg wheat bulb fly (Alternaria) will be more risky if the soil is still wet when access to the land is required ie increase risk of soil compaction spring N application vulnerable to risk of run-off

bull Higher spring temperatures will bring forward the start of the season

bull Drier and warmer summers ndash less wet weather diseases easier to combine but seed-beds very dry which will impact on the timing of germination of both weed and crop seed

bull Autumn conditions will start off dry but with an earlier onset of wetter conditions ndash increase urgency to get crops established before the onset of heavy rainfall dry conditions may make soil too hard and dry to cultivate efficiently after harvest may cause a shift to spring drilling on more difficult heavy soils The shift to spring drilling will leave the soil surface bare over wintre

Page 4

Soil function Impact of UKCIP02 climate change scenarios

increasing the risk of soil erosion Therefore in the long term soil resources will be reduced and food production will be affected

bull Generally warmer temperature may increase the risk of parasite infections if climate change helps that part of the parasite life cycle outside the body

Soil air and water interactions

bull Warming will decrease soil organic matter increase CO2 emissions increase litter decomposition and N mineralisation rate which may increase N leaching rate

bull In the long term carbon stock may become insensitive to temperature increases This is based on the assumption that soil physico-chemical ldquostabilisationrdquo reaction may respond more to warming than microbial decompositionrespiration reactions In turn warming may increase the rate of physico-chemical processes that transfer organic carbon to more stable carbon pools As a result total soil carbon loss may be very small and even may increase

bull Elevated CO2 will increase above-ground and below ground biomass Increasing the total carbon flux to the soil The effects of CO2 to soil C may be positive in the short term but reverse in the long term

bull Higher seasonal fluctuations in soil water increase the risk of changes to soil chemistry eg more leaching soil acidification gradually lower soil CEC and therefore buffering capacity

bull Drying out of peaty soils may convert peatlands from CO2 sinks to CO2 source

bull Drier summers will lead to the accumulation of nutrients and pollutants in the soil which will be flushed out when significant rainfall occurs for example during the autumn

bull Soil with a high water content promote methanogenic activity and reduces methanotrophic activity by reducing the size of oxidised zones

bull Waterlogged upland soils may become CH4 sources

Soil biodiversity As will be discussed later in this chapter very few UK projects have investigated climate impacts on soil biodiversity

Soil in the landscape and cultural heritage

Very few UK studies

bull Heritage sites will suffer from an increased rate of chemical-flooding risk on certain structures and fabrics

bull Increased soil water could increase biological attack and other decay (salt mobilisation)

bull Artefacts may be exposed through the process of soil erosion (wind and water) and begin to deteriorate

bull Changes to the vegetation supported will alter the look of the historic landscape

bull Lower water table will affect the preservation of archaeological remains Drier soils will increase damage to artefacts through increased oxidation and exposure due to soil erosion eg increased risk of wind erosion to peat soils as they dry out

Page 5

Soil function Impact of UKCIP02 climate change scenarios

bull If intensive arable cultivation shifts from the south east to the north buried archaeological sites currently not at risk from arable damage could become so

Soils in mineral extraction construction and the built environment

bull Increased winter rainfall especially extreme events could impact on land stability increased risk of land slides

bull increased risk of subsidence due to intermittent rainfall leading to an increased soil moisture deficit and soil shrinkage

bull High intensity rainfall events may overwhelm drainage systems and increase the risk of downstream flooding

bull Land may become unsuitable for development

bull Increased droughtiness will increase shrink-swell causing disturbance to building foundations and the need to underpinrepair

bull Increased temperature may exacerbate chemical attack to foundations

bull Increased temperatures may increase the risk to engineered structures based on clay caps ndash increasing leaching and release of landfill gases

bull Increase flooding and erosion will increase the risk of loss of contaminants from brownfield land

bull Land to be used for temporary flood drainage must be underlain by soils with suitable infiltration capacity and hydraulic conductivity and must not be erodible

bull Higher temperatures will also encourage volatilisation of some organic pollutants and mercury on contaminated sites

The seven key recommendations made by Bradley et al (2005) in relation to research requirements were

1 More research specifically aimed at soil functions under climate change Incorporating climate change on soil in all relevant research With research being updated to the latest climate change predictions or at least an assessment of possible changes

2 Further investigation of the interactions between climate change and pollutant deposition and exposure particularly critical loads and their exceedance for agricultural land and woodland in relation to issues of acidificationrecovery and eutrophication

3 Future research into soil functions under climate change should attempt to deal with uncertainties in climate predictions and soil process model formulation and parameterisation of soil processes Model development for organic and woodland soils needs to be promoted including the collection of data required for parameterisation and verification

4 Studies integrating the impact of land use changes and socio-economic factors should be encouraged since these may be as important as the impacts of climate change on soil functions

5 Further targeted research is recommended to investigate the effects of CO2 combined with changes in the temperature regime on soil function directly or indirectly and interactions with changes in temperature and rainfall

6 More research is warranted on the ability of soils to hold and buffer pollutants in the face of climate change particularly on lsquobrownfieldrsquo soils as well as in the urban built environment

Page 6

7 Improved estimates of non-CO2 GHG balance (primarily N2O and CH4) of forest soils including predictions of the impacts of climate change and the effects of forest management extension to broadleaf woodland and deforestation activities is important

2 Climate change scenarios

UKCIP09 climate change predictions as based on medium emissions scenarios for 2080 predict that England and Wales will get warmer with summers showing a slightly greater (on average 4degC) increase in temperature than winters (on average 3degC Table 2) While temperatures are predicted to rise the annual amount of precipitation is not expected to change However the distribution of rainfall throughout the year is predicted to change Summer precipitation is predicted to decrease across England and Wales (Table 2) on average by -24 to -18 while winter precipitation is predicted to increase by between 14 and 23 Also there is expected to be an increased frequency of extreme weather occurrences such as heat waves dry spells heavy rain and flooding as well as rises in sea level Central estimates are for heavy rain days (rainfall greater than 25 mm) over most of the lowland UK to increase by a factor of between 2 and 35 in winter and 1 to 2 in summer by the 2080s under the medium emissions scenario (UKCP09)

Table 2 UKCIP09 central climate change predictions based on medium emission scenarios for 2080 (low and high probabilities given in brackets)

Administrative regions

Winter mean temperature (degC)

Summer mean temperature (degC)

Annual winter mean precipitation ()

Annual summer mean precipitation ()

Wales 28 (1642) 35 (1958) 19 (442) -20 (-435) North East England 26 (1441) 37 (2058) 14 (232) -18 (-361)

East of England 30 (1647) 36 (1959) 20 (444) -21 (-456) South West England 28 (1643) 39 (2164) 23 (654) -24 (-506)

South East England 30 (1647) 39 (2065) 22 (451) -23 (-487)

West Midlands 29 (1644) 37 (2061) 17 (338) -20 (-446) East Midlands 30 (1646) 35 (1858) 19 (341) -20 (-446) Yorkshire and Humber 30 (1646) 33 (1754) 15 (233) -23 (-440)

North West England 26 (1440) 37 (2059) 16 (334) -22 (-430)

Mean 29 36 18 -21

The south west of England is predicted to experience the greatest increase in summer temperatures as well as the highest predicted increase in winter mean precipitation and lowest summer mean precipitation of all regions in England and Wales (Table 2) while the east of England south east England and Yorkshire and Humber are predicted to have some of the mildest winter temperatures The north east of England is predicted to experience a less extreme change in winter and summer precipitation

The predictions made by UKCP09 are supported by resent observed trends in UK climate reported by Jenkins et al (2009) Global average temperatures have risen by nearly 02degCdecade over the past 25 years In central England temperatures have risen by about a degree Celsius since the 1970s Annual mean precipitation in England and Wales has not changed significantly although summers do appear to be drier and winters wetter Over the past 45 years there has been an increase in heavy winter rainfall events Severe windstorms around the UK have become more frequent in the past few decades

Page 7

UKCP09 predictions are broadly consistent with UKCIP02 predictions Comparisons of UKCIP02 and UKCP09 by Jenkins et al (2009) suggest mean temperature projections are generally greater and summer reduction in rainfall is not as great using UKCP09 The range of increase in winter rainfall is broadly similar with a different geographical pattern Decreases in cloud cover in summer are also broadly in agreement Therefore observations made by Bradley et al (2005) with regard to impact of climate change on soil function are still valid Bradley et al (2005) defined both direct and indirect impacts of climate change on soil functions and these are summarised in Section 1 Table 1 Subsequently there has been more attention paid to the impact of climate change on soil biota and its impact on soil processes and functions This new information is summarised in Table 3

Table 3 Potential implications of predicted climate change on soil biota

Climate change Implications for soil biota

Warmer springs bull Changes in timings of seasonal events may cause loss of synchrony between species and the availability of food (Hopkins et al 2007 Newton et al 2008)

Warmer and drier summers

bull Reduced soil moisture content may limit plant production without additional irrigation

bull Drier soils may affect the mobility of soil fauna such as nematodes and earthworms (Bardgett 2005 Eggleton et al 2009)

bull Changes to habitat may favour drought tolerant soil biota soil may experience a shift in species which may impact on the over all function of the soil depending on redundancy in the system (Castro et al 2010)

bull Summer droughts may cause stress in some soil microbial communities and result in changes in fungal diversity impacting on functional diversity (Toberman et al 2008)

bull Drier conditions and higher temperatures may accelerate decomposition of organic material through increased oxygen availability and increased microbial activity However additional input of leaf litter from increased production may offset net loss of carbon from the soil profile (Dawson and Smith 2007)

bull Decreased loss of methane due to increased oxygen availability impacting on methanogens (McNamara et al 2006)

bull May cause shift in vegetation patterns with subsequent implications for soil biota (Pentildeuelas et al 2007)

Warmer and wetter winters

bull Increase the likely survival of soil pests and diseases (Newton et al 2008)

bull Inward migration of soil biota from warmer areas

bull Water logging will reduce the availability of oxygen in the soil profile affecting both soil fauna and soil flora (Sowerby et al 2008)

bull Soil compaction will impede root penetration and may restrict soil fauna movement within the soil profile (Whally et al 1995)

bull May cause shift in vegetation patterns with subsequent implications for soil biota (Pentildeuelas et al 2007)

Extreme events bull Drying of the top soil followed by sudden rewetting encourages flushes of microbial activity and nutrient loss from soil (Sowerby et al 2008 Gordon et al 2008)

Increased CO2 bull Increased transfer of C through root system into the soil stimulating

Page 8

Climate change Implications for soil biota

microbial abundance and activity (Castro et al 2010)

bull Increased transfer of C to the soil stimulating mycorrhizal fungi which may stimulate nutrient transfer (Tyliankis et al 2008)

bull Stimulation of microbial biomass can lead to microbial immobilization of N thereby enforcing plant N limitation (de Graaff et al 2007)

bull May cause shift in vegetation patterns with subsequent implications for soil biota

Section 3 Potential impacts of climate change on soil processes function and biota

Carbon and nutrient cycling

Climate change has both direct and indirect effects on soil organisms and the processes that they drive often with consequences for the return greenhouse gases to the atmosphere Direct effects include the influence of temperature changing precipitation and extreme climatic events on soil organisms and the processes that they drive whereas indirect effects result from climate-driven changes in plant productivity and species composition which alter soil physicochemical conditions the supply of carbon to soil and the structure and activity of microbial communities involved in decomposition processes and carbon release from soil (Bardgett et al 2008)

One of the most commonly discussed contributions of soil organisms to climate change is their role in soil organic matter decomposition and the idea that warming will accelerate rates of heterotrophic microbial activity thereby increasing the transfer of carbon dioxide from soil to the atmosphere and exports of dissolved organic carbon by hydrologic leaching (Jenkinson et al 1991 Davidson and Janssens 2006) The concern here is that because rates of soil respiration are more sensitive than is primary production to temperature (Jenkinson et al 1991 Schimel et al 1994) it is thought that climate warming will increase the net transfer of carbon from soil to atmosphere thus creating a positive feedback on climate change (Cox et al 2000) Although it is well known that temperature is an important determinant of rates of organic matter decomposition the nature of the relationship between temperature and microbial respiration is far from clear (Davidson and Janssens 2006) There are several reasons for this uncertainty but key factors include potential for variations in organic matter quality to influence the temperature sensitivity of microbial decomposition (Fang et al 2005 Conen et al 2006 Davidson and Janssens 2006) and for environmental constraints such as physical and chemical protection of organic matter to decrease substrate availability for microbial attack and thereby dampen microbial responses to warming (Davidson and Janssens 2006) Also there is uncertainty about how reactive different microbial and faunal groups and species are to temperature change with several studies showing that soil microbial and animal communities are insensitive to small increases in temperature (eg Kandeler et al 1998 Bardgett et al 1999 Wardle 2002) whereas others show that soil organisms and the carbon cycling processes that they drive are responsive to temperature change For instance the abundance of enchytraeid worms which dominate the fauna of acid peat soils have been shown to be strongly related to temperature and it is has been suggested that climate warming could increase their abundance leading to enhanced carbon mineralization and carbon loss from soil (Briones et al 1998 Cole et al 2002ab) Also a recent analysis by Gange et al (2007) related temporal shifts in autumnal fruiting patterns of macrofungi in southern England to shifts in climate and found that the average first fruiting date of 315 species is now earlier while last fruiting date is now later than was the case 56 years ago Their study also found that many species are now fruiting twice a year indicative of increased mycelial activity and possibly greater decomposition rates in ecosystems

Increases in the frequency of extreme weather events with climate change such as droughting and freezing may have an even greater effect on soil organisms and their activities than will overall changes in temperature and precipitation It is well know for example that droughting and freezing have substantial direct effects on microbial physiology and the composition of the soil microbial community with important consequences for ecosystem-level carbon dynamics (Schimel et al 2007) For example increased drought and drying in wetlands and peatlands which will lower the water

Page 9

table and introduce oxygen into previously anaerobic soil will create a more favorable environment for microbial activity (Freeman et al 2004) potentially enhancing the activity of enzymes (eg phenol oxidases) which play a pivotal role in the breakdown of recalcitrant organic matter (Freeman et al 2004) Because peatlands and wetlands represent amongst the largest stocks of terrestrial carbon globally (Ward et al 2007) such enhanced breakdown of recalcitrant organic matter under drying could have major implications for the global carbon cycle (Freeman et al 2004) Before leaving this topic it is important to note that methanogenic pathways are also affected by increased oxygen availability associated with drought in that methane emissions are reduced by toxic effects of oxygen on methanogens (Roulet and Moore 1995 Freeman et al 2002) Also drought can have marked effects on nitrous oxide emission from soils a potent greenhouse gas that is increasing in atmospheric concentrations at the rate of 02ndash03 per year (Houghton et al 1996) However responses depend on the severity of drought in that modest summer drought is likely to have limited effect on soil nitrous oxide emissions whereas more extreme drought can greatly increase them (Dowrick et al 1999)

The majority of studies to date that have explored effects of climate change on biological systems and soil organisms have considered single factors such as elevated atmospheric carbon dioxide concentration warming and drought However there is much potential for interactions between these factors to have additive or antagonistic effects on soil organisms and the activities that they drive (Mikkelsen et al 2008 Bardgett et al 2008 Tylianakis et al 2008) Very little is known about the influence of multiple and interacting climate drivers on soil organisms and their activities although some studies do point to strong non-additive belowground effects of these drivers with feedback consequences for carbon exchange For instance microbial decomposition of peat was found to be significantly greater when subject to both elevated temperature and atmospheric carbon dioxide than when these factors were each elevated singly (Fenner et al 2007ab) thereby potentially causing an even stronger feedback on carbon loss from soil as dissolved organic carbon in drainage water and respiration Added to this complexity is our knowledge that other organisms and trophic groups that influence soil microbes directly such as microbial-feeding fauna will also respond to multiple climate change factors (Wardle 2002 Bardgett 2005 Tylianakis et al 2008) This complexity further hampers our ability to predict effects of multiple climate change drivers on soil biological communities and carbon exchange feedbacks

In addition to multiple climate change drivers soil organisms and their activities are also affected substantially by other global change phenomena such as nitrogen deposition invasion of new species and land use change Perhaps the strongest driver is land use change (cf Sala et al 2000) and it is widely documented that changes in the intensity of land use or the conversion of natural vegetation to agriculture or forestry can have substantial and often strongly negative and irreversible effects on soil biological communities and their activities (Brussaard et al 1997 Wardle 2002 Bardgett 2005) One pattern that commonly emerges in the context of land use change is that intensification of farming including increased tillage fertilizer use and grazing is typically associated with an increased role of the bacterial-based energy channel relative to the fungal-based channel (Wardle 2002 Bardgett 2005 Bardgett and Wardle 2010) which is away from what would typically found in more stable late successional ecosystems with large fungalbacterial ratios (Harris 2009) As discussed above this increased bacterial role is associated with faster leakier nutrient cycling and more losses of nutrients and carbon in water and greenhouse gases to the atmosphere (Wardle et al 2004 van der Heijden et al 2008) In contrast low intensity management systems often encourage fungal-based soil food webs that are more similar to those of natural systems and tend to be associated with more efficient nutrient cycling (Bardgett and McAlister 1999 Gordon et al 2008) and enhanced soil carbon sequestration (De Deyn et al 2008) Although not tested global change drivers may alter the balance of communities in favour bacterial populations thereby accelerating rates of nutrient and carbon mineralization with implications for carbon sequestration and C loss to the atmosphere

Soil biological communities are also strongly affected by nitrogen enrichment which is of high relevance because anthropogenic activities have substantially increased global rates of nitrogen fixation and deposition (Schlesinger 2009) For instance it is well known that nitrogen enrichment can have direct and differential impacts on extracellular enzymes involved in decomposition processes This typically involves stimulation of the synthesis of cellulases which degrade labile high cellulose litter but suppression of the synthesis of ligninolytic enzymes by white rot fungi which decompose recalcitrant high lignin litter (Carreiro et al 2000 Waldrop et al 2004 Allison et al 2008) Also

Page 10

nitrogen enrichment is known to influence the abundance and diversity of different components of the soil microbial community including saprophytic fungi (Donnison et al 2000 Allison et al 2008) mycorrhizal fungi (Egerton-Warburton and Allen 2000 Frey et al 2004) and soil fauna (Scheu and Schaeffer 1998 Ettema et al 1999) which are also affected by climate change and are well known to have substantial effects on decomposition processes and ecosystem-level carbon exchange A recent meta-analysis on this topic revealed that soil microbial biomass declined 15 on average under nitrogen fertilization but that declines in abundance of microbes and fungi were more evident in studies of longer durations and with higher total amounts of nitrogen added (Treseder 2008) Moreover that study showed negative responses of microbial biomass to nitrogen fertilization to be significantly correlated with declines in soil carbon dioxide emissions indicating that moderate declines in microbial biomass under nitrogen fertilization may also have consequences for carbon fluxes However another meta-analysis of 109 studies across the globe revealed that nitrogen enrichment had no significant effect on net ecosystem carbon dioxide exchange in non-forest natural ecosystems but did increase methane and nitrous oxide emissions by 97 and 216 respectively (Liu and Greaver 2009) It was suggested therefore that any potential positive effects of nitrogen enrichment on the global terrestrial carbon sink should be offset by the stimulation of methane and nitrous oxide emissions which are more potent greenhouse gases than is carbon dioxide (Liu and Greaver 2009) Importantly nitrogen deposition and other global changes can also influence soil microbes and decomposition processes indirectly through altering vegetation composition and productivity and by alleviating progressive nitrogen limitation of plant growth which typically occurs under elevated atmospheric carbon dioxide (Finzi et al 2002 Luo et al 2004 de Graaff et al 2006)

The likely effect of drought during summers is well-appreciated but much less is known about the impacts of warmer wetter winters for which plants appear to have fewer adaptations to cope (Whitmore and Whalley 2009) Waterlogging becomes more likely with increased rainfall but at the same time root respiration is likely to increase in response to warmer temperatures There is thus a considerably raised risk of waterlogging of UK soils during the future winter months No additional impact of drought has been found on cereal yields following winter waterlogging and reasonable diversity and resistance to waterlogging has been found in UK cereal varieties (Dickin and Wright 2009 Dickin et al 2008) However soil-dwelling organisms may be at risk some earthworms for example are more intolerant of waterlogging than others (Chuang and Chen 2009) Earthworms are relatively well studied other species less so and in general macrofauna diversity is greatly reduced in flooded grasslands (Plum 2005) with opportunists becoming more abundant Microbes and plants compete for resources in waterlogged soils For example Blom (1999) reported that plants out-competed nitrifiers for ammonium in waterlogged soil It is not clear to what extent plants and microbes compete for oxygen

In general very little is known about the combined effects of global changes on soil biological communities and their activities but they clearly have the potential to amplify suppress or perhaps even neutralize climate change driven effects on soil microbes and their feedback to carbon exchange (Bardgett et al 2008) A recent synthesis by Tylianakis et al (2008) of data from 688 published studies on the effects of global change on biotic interactions in terrestrial ecosystems (including those that occur in the decomposer food web) highlighted that there is substantial variability among studies in both the magnitude and direction of effects of any given global change driver on any given type of biotic interaction Further that analysis highlighted that the unanticipated effects of multiple drivers acting simultaneously create major challenges in predicting future responses to global environmental change Experimental studies that simultaneously vary two or more global change drivers within the same experiment therefore have considerable promise for improving our understanding of how interactions involving soil communities and their effects on ecosystem-level processes may respond to current global change scenarios

Soil structural integrity and dynamics

The architecture of soil the ways in which particles are arranged in space so forming a stable connected pore space determines the habitat of soil dwelling organisms including plants This soil physical environment is mutable however Soil is hard or dusty but transmits gases readily when dry when wet it becomes soft and plastic and gas ingress becomes much reduced These two extremes are expected to become more prevalent with the changes in climate expected for the UK drier

Page 11

summers and wetter winters The presence of plants indirectly exacerbates the effects of climate change by extracting water in summer and oxygen for root respiration in the winter There is a greater risk of compaction with wetter more plastic soils with late-harvested crops such as potatoes or sugar beet and establishment afterwards Working day access to land may be reduced or more variable leading to damage to soil through inappropriate management (Section B Degradation) Drought may affect soil stability and structure and possibly encourage wind erosion Cecillon et al (2010) examined sites along a latitudinal mountain spatial climate gradient for aggregation and aggregate stability and showed that erodibility was linked to climate and therefore susceptible to change under a shifting climatic regime Other studies have shown effects on organisms associated with the genesis of aggregate structure For instance Eggleton et al (2009) demonstrated in southern England pasture woodland hat earthworm community structure was dependant on soil temperature and water This faunal group has long been established as being of critical importance in no and minimal-till systems both organic and inorganic with potential for declines in aggregate stability as a result of climate change linked to declines in earthworm abundance and shifts in earthworm community structure There are also emerging models linking earthworm population dynamics and soil structural components (Blanchart et al 2009) which offer the possibility of modelling a biotic and abiotic component simultaneously under different climate change scenarios with consequences for hydrology erodibility and trophic level effects

Kohler et al (2009) found that increased CO2 concentrations led to a significantly higher percentage of stable aggregates growing under Lectuca sativa in drought conditions and this was linked to increases in soil microbial biomass and inoculation with a vesicular arbuscular mycorrhizal fungus and plant-growth-promoting rhizobacterium Other workers (Rillig et al 2001) had found a similar effect of elevated carbon dioxide and increased water supply by irrigation on increased aggregate stability due to arbuscular mycorrhizal fungi in soils under Sorghum

Earlier work suggested that climate change would not affect accessibility to land unless winter rainfall increased by 15 (Rounsevell and Brignall 1994) Since this is now what is expected it may be necessary to re-calculate workable days for England based on up-to-date climate change scenarios Neither the direct effect of climate change on soil stability via wet-dry cycles nor its indirect effect via the soil fauna is certain and as Horn and Smucker (2005) have noted that changes in aggregate stability and soil structure can be undesirable if the soil becomes difficult to manage We need to better understand the processes underlying soil structure in order to predict direct soil response to climate change and we need to better understand the wider impact of climate change on soil ecosystems if we are to understand and predict the indirect effects of the soil fauna on soil

Warmer wetter winters may lead to increased competition for oxygen among more strongly respiring organisms in wetter soils into which oxygen penetration is slower Drier summers will lead to soils into which root penetration becomes restricted Both effects are likely to impact on the ability of plants to acquire nutrients and on biogeochemical cycles in general Research on waterlogging appears to have concluded in the 1980s that UK cereals could compensate provided waterlogging did not occur during establishment or repetitively (eg Belford et al 1985) While this may have been true of the conditions prevailing at the time the same may not be true for our future climate The effect that plant root extraction of oxygen has on soil fauna and microflora and vice versa appears to be poorly researched especially in the context of our expected climate change

In summary stability of soil is likely to be impacted by the increasing intensity of wet-dry cycles with climate change but note that an increase is not necessarily desirable if the soil becomes less workable Stepniewska and Stepniewska (2009) have stressed the need for a moderate stable redox above 300 mV Soil fauna and community structure is also likely to be impacted by a change in climate with effects on soil stability that are unclear It is also likely that with wetter winters the number of days when soil is safely accessible by heavy farm machinery without causing damage may become more variable and therefore unpredictable

Page 12

4 Methodologies for investigating the impacts of climate change on soil

Experiments on climate change drivers have been carried out over a variety of spatial and temporal scales ranging from short term laboratory incubation studies to ecosystem-level and long-term manipulations of climatic factors (Wullschleger and Strahl 2010) The main approaches for studying climate change include (1) the use of environmental gradients (temperature and water) and reciprocal transplants (2) in situ field manipulation experiments including Free-Air CO2 Enrichment (FACE) experiments for manipulation of atmospheric CO2 and field-scale manipulations of temperature and precipitation (3) controlled environment facilities such as the Ecotron controlled environment facilities at Imperial College Silwood Park UK and Montpellier France and (4) highly artificial often laboratory based microcosm experiments that have little relevance to real systems These approaches in the order listed above follow a spectrum of decreasing realism but increasing mechanistic control We discuss these approaches in turn

Environmental gradients (temperature and water) and reciprocal transplants

Climatic gradients for instance in annual precipitation and temperature that cross continents countries and elevation gradients are commonly used to determine impacts of climatic variation on soil biota and processes While useful for establishing general patterns such approaches leave significant questions about other factors that could explain differences in soil biota along climatic gradients such as soil fertility and mineralogy To overcome this problem an associated approach is the use of transplant experiments whereby intact soil-vegetation turves (or varying size) are transplanted at different places along climatic gradients so that effects of movement to another climate on soil biota can be assessed This approach for example was used by Briones et al (19971998) who transplanted peat soils from high to lower altitudes at Great Dunn Fell Cumbria to simulate climate warming and that this increased the density of enchytraeid worms the dominant fauna of these peat soils leading to enhanced decomposition and DOC concentrations in soil leachates The same system was also used by Tipping et al (1999) to show that warming and drying can accelerate the production of dissolved organic matter in organic soil horizons Such approaches are valuable in that they provide information on the response of soil biota and processes to real changes in climate but they are limited by the lack of control of environmental variables along transects and potential effects of disturbance from moving soil cores from one site to another

The further experimentation moves away from surveys and experiments in the field the less likely they are to represent real world systems This is not necessarily an issue when detailed and specific mechanisms are being explored but become increasingly problematic when large scale predictions are asserted from them

In situ field manipulation experiments

Many studies have used various field-based manipulations of climate including elevated carbon dioxide in the previously mentioned FACE experiments (eg Norby et al 2004 Jackson et al 2009) drought using rainfall roofs (eg Beier et al 2004) and artificial warming using heating cables (eg Grime et al 2008) passive night time warming roofs (eg Beier et al 2004) and infra-red lamps (Zhang et al 2005) Such experiments have contributed significantly to our understanding of the effects of different climate change drivers on vegetation soil biota and soil processes as detailed in the previous section However as stated previously most studies of this kind have explored effects of single climate factors whereas there is much potential for interactions between multiple factors to have additive or antagonistic effects on soil organisms and the activities that they drive (Bardgett et al 2008) Therefore future experiments which manipulate multiple climate change and other site factors are needed to better understand the effects of climate change on soil biota

As an example of in situ field manipulations Zhang et al (2005) artificially heated soils under tall grass prairie using infra-red heaters to simulate an increase in daily soil temperatures of 18 ndash 27oC and studied two clipping regimes clipped and unclipped In the heated treatments they found changes in the soil microbial community structure as determined using phospholipid fatty acid analysis (PLFA) in the unclipped plots with a shift to fungal dominance but not in the clipped

Page 3

predict the effect of climate change on soil water at regional or local level As with soil moisture soil temperature is also an important driver of soil processes potentially increasing heterotrophic activity in soil and the rate of decomposition of organic matter the rate of nutrient cycling and the chemical weathering of minerals Climate change will directly impact on soil temperature through rising air temperatures but will indirectly affect soils through changing plant productivity and community structure (Bardgett et al 2008)

The main changes in soil forming processes and properties as influenced by the UKCIP02 predicted climate change scenarios were suggested to relate to soil organic matter soil structure soil fauna and microflora acidification and nutrient status and soil erosion The review of Bradley et al (2005) revealed that there was uncertainty as to how climate change would impact on soil organic matter decomposition however the general opinion was that organic matter decomposition would likely exceed levels gained from increased plant growth resulting in a net loss of carbon A decline in soil organic matter would impact on soil structure resulting in a decrease in soil aggregate stability increased susceptibility to compaction lower infiltration rates increased run-off and increased susceptibility to erosion Drier climatic conditions would also result in greater frequency and size of crack formation in soils with high clay content particularly those with smectitic mineralogy Temperature and water are likely to result in changes in ecosystems and migration of vegetation zones which may seriously affect soil flora and fauna that can not adapt or migrate at an equivalent rate Significant increases of rain will lead to increases in leaching loss of nutrients and increasing acidification depending on the buffering pools existing in soil Both temperature and precipitation changes will impact on the rate of soil erosion by water and wind either through increased vulnerability of the soil properties or through changes in vegetation cover

In the review by Bradley et al (2005) most of the available information at the time only enabled a qualitative or semi-qualitative interpretation of the likely impact of climate change on soils Subsequently more data has become available and these are discussed in Section 3 of this report However the main effects identified by Bradley et al 2005 of climate change on the five core functions identified in the UK Soil Action Plan are summarised in Table 1

Table 1 Main climate change affects on soil function identified by Bradley et al (2005)

Soil function Impact of UKCIP02 climate change scenarios

Food and fibre bull Soil wetness water-logging and flooding are all predicted to increase in winter ndashincreasing the potential for soil sealing soil erosion poaching compaction and land use change

bull Warmer temperatures will increase the potential for growing a wider range of crops and increased amount of land under arable production ndash could lead to increased erosion and carbon loss

bull Less available work days in autumn winter and spring ndash result in damage to soil structure and problems from soil erosion nutrient and pesticide losses and N2O fluxes

bull Unpredictable springs ndash spraying for pests eg wheat bulb fly (Alternaria) will be more risky if the soil is still wet when access to the land is required ie increase risk of soil compaction spring N application vulnerable to risk of run-off

bull Higher spring temperatures will bring forward the start of the season

bull Drier and warmer summers ndash less wet weather diseases easier to combine but seed-beds very dry which will impact on the timing of germination of both weed and crop seed

bull Autumn conditions will start off dry but with an earlier onset of wetter conditions ndash increase urgency to get crops established before the onset of heavy rainfall dry conditions may make soil too hard and dry to cultivate efficiently after harvest may cause a shift to spring drilling on more difficult heavy soils The shift to spring drilling will leave the soil surface bare over wintre

Page 4

Soil function Impact of UKCIP02 climate change scenarios

increasing the risk of soil erosion Therefore in the long term soil resources will be reduced and food production will be affected

bull Generally warmer temperature may increase the risk of parasite infections if climate change helps that part of the parasite life cycle outside the body

Soil air and water interactions

bull Warming will decrease soil organic matter increase CO2 emissions increase litter decomposition and N mineralisation rate which may increase N leaching rate

bull In the long term carbon stock may become insensitive to temperature increases This is based on the assumption that soil physico-chemical ldquostabilisationrdquo reaction may respond more to warming than microbial decompositionrespiration reactions In turn warming may increase the rate of physico-chemical processes that transfer organic carbon to more stable carbon pools As a result total soil carbon loss may be very small and even may increase

bull Elevated CO2 will increase above-ground and below ground biomass Increasing the total carbon flux to the soil The effects of CO2 to soil C may be positive in the short term but reverse in the long term

bull Higher seasonal fluctuations in soil water increase the risk of changes to soil chemistry eg more leaching soil acidification gradually lower soil CEC and therefore buffering capacity

bull Drying out of peaty soils may convert peatlands from CO2 sinks to CO2 source

bull Drier summers will lead to the accumulation of nutrients and pollutants in the soil which will be flushed out when significant rainfall occurs for example during the autumn

bull Soil with a high water content promote methanogenic activity and reduces methanotrophic activity by reducing the size of oxidised zones

bull Waterlogged upland soils may become CH4 sources

Soil biodiversity As will be discussed later in this chapter very few UK projects have investigated climate impacts on soil biodiversity

Soil in the landscape and cultural heritage

Very few UK studies

bull Heritage sites will suffer from an increased rate of chemical-flooding risk on certain structures and fabrics

bull Increased soil water could increase biological attack and other decay (salt mobilisation)

bull Artefacts may be exposed through the process of soil erosion (wind and water) and begin to deteriorate

bull Changes to the vegetation supported will alter the look of the historic landscape

bull Lower water table will affect the preservation of archaeological remains Drier soils will increase damage to artefacts through increased oxidation and exposure due to soil erosion eg increased risk of wind erosion to peat soils as they dry out

Page 5

Soil function Impact of UKCIP02 climate change scenarios

bull If intensive arable cultivation shifts from the south east to the north buried archaeological sites currently not at risk from arable damage could become so

Soils in mineral extraction construction and the built environment

bull Increased winter rainfall especially extreme events could impact on land stability increased risk of land slides

bull increased risk of subsidence due to intermittent rainfall leading to an increased soil moisture deficit and soil shrinkage

bull High intensity rainfall events may overwhelm drainage systems and increase the risk of downstream flooding

bull Land may become unsuitable for development

bull Increased droughtiness will increase shrink-swell causing disturbance to building foundations and the need to underpinrepair

bull Increased temperature may exacerbate chemical attack to foundations

bull Increased temperatures may increase the risk to engineered structures based on clay caps ndash increasing leaching and release of landfill gases

bull Increase flooding and erosion will increase the risk of loss of contaminants from brownfield land

bull Land to be used for temporary flood drainage must be underlain by soils with suitable infiltration capacity and hydraulic conductivity and must not be erodible

bull Higher temperatures will also encourage volatilisation of some organic pollutants and mercury on contaminated sites

The seven key recommendations made by Bradley et al (2005) in relation to research requirements were

1 More research specifically aimed at soil functions under climate change Incorporating climate change on soil in all relevant research With research being updated to the latest climate change predictions or at least an assessment of possible changes

2 Further investigation of the interactions between climate change and pollutant deposition and exposure particularly critical loads and their exceedance for agricultural land and woodland in relation to issues of acidificationrecovery and eutrophication

3 Future research into soil functions under climate change should attempt to deal with uncertainties in climate predictions and soil process model formulation and parameterisation of soil processes Model development for organic and woodland soils needs to be promoted including the collection of data required for parameterisation and verification

4 Studies integrating the impact of land use changes and socio-economic factors should be encouraged since these may be as important as the impacts of climate change on soil functions

5 Further targeted research is recommended to investigate the effects of CO2 combined with changes in the temperature regime on soil function directly or indirectly and interactions with changes in temperature and rainfall

6 More research is warranted on the ability of soils to hold and buffer pollutants in the face of climate change particularly on lsquobrownfieldrsquo soils as well as in the urban built environment

Page 6

7 Improved estimates of non-CO2 GHG balance (primarily N2O and CH4) of forest soils including predictions of the impacts of climate change and the effects of forest management extension to broadleaf woodland and deforestation activities is important

2 Climate change scenarios

UKCIP09 climate change predictions as based on medium emissions scenarios for 2080 predict that England and Wales will get warmer with summers showing a slightly greater (on average 4degC) increase in temperature than winters (on average 3degC Table 2) While temperatures are predicted to rise the annual amount of precipitation is not expected to change However the distribution of rainfall throughout the year is predicted to change Summer precipitation is predicted to decrease across England and Wales (Table 2) on average by -24 to -18 while winter precipitation is predicted to increase by between 14 and 23 Also there is expected to be an increased frequency of extreme weather occurrences such as heat waves dry spells heavy rain and flooding as well as rises in sea level Central estimates are for heavy rain days (rainfall greater than 25 mm) over most of the lowland UK to increase by a factor of between 2 and 35 in winter and 1 to 2 in summer by the 2080s under the medium emissions scenario (UKCP09)

Table 2 UKCIP09 central climate change predictions based on medium emission scenarios for 2080 (low and high probabilities given in brackets)

Administrative regions

Winter mean temperature (degC)

Summer mean temperature (degC)

Annual winter mean precipitation ()

Annual summer mean precipitation ()

Wales 28 (1642) 35 (1958) 19 (442) -20 (-435) North East England 26 (1441) 37 (2058) 14 (232) -18 (-361)

East of England 30 (1647) 36 (1959) 20 (444) -21 (-456) South West England 28 (1643) 39 (2164) 23 (654) -24 (-506)

South East England 30 (1647) 39 (2065) 22 (451) -23 (-487)

West Midlands 29 (1644) 37 (2061) 17 (338) -20 (-446) East Midlands 30 (1646) 35 (1858) 19 (341) -20 (-446) Yorkshire and Humber 30 (1646) 33 (1754) 15 (233) -23 (-440)

North West England 26 (1440) 37 (2059) 16 (334) -22 (-430)

Mean 29 36 18 -21

The south west of England is predicted to experience the greatest increase in summer temperatures as well as the highest predicted increase in winter mean precipitation and lowest summer mean precipitation of all regions in England and Wales (Table 2) while the east of England south east England and Yorkshire and Humber are predicted to have some of the mildest winter temperatures The north east of England is predicted to experience a less extreme change in winter and summer precipitation

The predictions made by UKCP09 are supported by resent observed trends in UK climate reported by Jenkins et al (2009) Global average temperatures have risen by nearly 02degCdecade over the past 25 years In central England temperatures have risen by about a degree Celsius since the 1970s Annual mean precipitation in England and Wales has not changed significantly although summers do appear to be drier and winters wetter Over the past 45 years there has been an increase in heavy winter rainfall events Severe windstorms around the UK have become more frequent in the past few decades

Page 7

UKCP09 predictions are broadly consistent with UKCIP02 predictions Comparisons of UKCIP02 and UKCP09 by Jenkins et al (2009) suggest mean temperature projections are generally greater and summer reduction in rainfall is not as great using UKCP09 The range of increase in winter rainfall is broadly similar with a different geographical pattern Decreases in cloud cover in summer are also broadly in agreement Therefore observations made by Bradley et al (2005) with regard to impact of climate change on soil function are still valid Bradley et al (2005) defined both direct and indirect impacts of climate change on soil functions and these are summarised in Section 1 Table 1 Subsequently there has been more attention paid to the impact of climate change on soil biota and its impact on soil processes and functions This new information is summarised in Table 3

Table 3 Potential implications of predicted climate change on soil biota

Climate change Implications for soil biota

Warmer springs bull Changes in timings of seasonal events may cause loss of synchrony between species and the availability of food (Hopkins et al 2007 Newton et al 2008)

Warmer and drier summers

bull Reduced soil moisture content may limit plant production without additional irrigation

bull Drier soils may affect the mobility of soil fauna such as nematodes and earthworms (Bardgett 2005 Eggleton et al 2009)

bull Changes to habitat may favour drought tolerant soil biota soil may experience a shift in species which may impact on the over all function of the soil depending on redundancy in the system (Castro et al 2010)

bull Summer droughts may cause stress in some soil microbial communities and result in changes in fungal diversity impacting on functional diversity (Toberman et al 2008)

bull Drier conditions and higher temperatures may accelerate decomposition of organic material through increased oxygen availability and increased microbial activity However additional input of leaf litter from increased production may offset net loss of carbon from the soil profile (Dawson and Smith 2007)

bull Decreased loss of methane due to increased oxygen availability impacting on methanogens (McNamara et al 2006)

bull May cause shift in vegetation patterns with subsequent implications for soil biota (Pentildeuelas et al 2007)

Warmer and wetter winters

bull Increase the likely survival of soil pests and diseases (Newton et al 2008)

bull Inward migration of soil biota from warmer areas

bull Water logging will reduce the availability of oxygen in the soil profile affecting both soil fauna and soil flora (Sowerby et al 2008)

bull Soil compaction will impede root penetration and may restrict soil fauna movement within the soil profile (Whally et al 1995)

bull May cause shift in vegetation patterns with subsequent implications for soil biota (Pentildeuelas et al 2007)

Extreme events bull Drying of the top soil followed by sudden rewetting encourages flushes of microbial activity and nutrient loss from soil (Sowerby et al 2008 Gordon et al 2008)

Increased CO2 bull Increased transfer of C through root system into the soil stimulating

Page 8

Climate change Implications for soil biota

microbial abundance and activity (Castro et al 2010)

bull Increased transfer of C to the soil stimulating mycorrhizal fungi which may stimulate nutrient transfer (Tyliankis et al 2008)

bull Stimulation of microbial biomass can lead to microbial immobilization of N thereby enforcing plant N limitation (de Graaff et al 2007)

bull May cause shift in vegetation patterns with subsequent implications for soil biota

Section 3 Potential impacts of climate change on soil processes function and biota

Carbon and nutrient cycling

Climate change has both direct and indirect effects on soil organisms and the processes that they drive often with consequences for the return greenhouse gases to the atmosphere Direct effects include the influence of temperature changing precipitation and extreme climatic events on soil organisms and the processes that they drive whereas indirect effects result from climate-driven changes in plant productivity and species composition which alter soil physicochemical conditions the supply of carbon to soil and the structure and activity of microbial communities involved in decomposition processes and carbon release from soil (Bardgett et al 2008)

One of the most commonly discussed contributions of soil organisms to climate change is their role in soil organic matter decomposition and the idea that warming will accelerate rates of heterotrophic microbial activity thereby increasing the transfer of carbon dioxide from soil to the atmosphere and exports of dissolved organic carbon by hydrologic leaching (Jenkinson et al 1991 Davidson and Janssens 2006) The concern here is that because rates of soil respiration are more sensitive than is primary production to temperature (Jenkinson et al 1991 Schimel et al 1994) it is thought that climate warming will increase the net transfer of carbon from soil to atmosphere thus creating a positive feedback on climate change (Cox et al 2000) Although it is well known that temperature is an important determinant of rates of organic matter decomposition the nature of the relationship between temperature and microbial respiration is far from clear (Davidson and Janssens 2006) There are several reasons for this uncertainty but key factors include potential for variations in organic matter quality to influence the temperature sensitivity of microbial decomposition (Fang et al 2005 Conen et al 2006 Davidson and Janssens 2006) and for environmental constraints such as physical and chemical protection of organic matter to decrease substrate availability for microbial attack and thereby dampen microbial responses to warming (Davidson and Janssens 2006) Also there is uncertainty about how reactive different microbial and faunal groups and species are to temperature change with several studies showing that soil microbial and animal communities are insensitive to small increases in temperature (eg Kandeler et al 1998 Bardgett et al 1999 Wardle 2002) whereas others show that soil organisms and the carbon cycling processes that they drive are responsive to temperature change For instance the abundance of enchytraeid worms which dominate the fauna of acid peat soils have been shown to be strongly related to temperature and it is has been suggested that climate warming could increase their abundance leading to enhanced carbon mineralization and carbon loss from soil (Briones et al 1998 Cole et al 2002ab) Also a recent analysis by Gange et al (2007) related temporal shifts in autumnal fruiting patterns of macrofungi in southern England to shifts in climate and found that the average first fruiting date of 315 species is now earlier while last fruiting date is now later than was the case 56 years ago Their study also found that many species are now fruiting twice a year indicative of increased mycelial activity and possibly greater decomposition rates in ecosystems

Increases in the frequency of extreme weather events with climate change such as droughting and freezing may have an even greater effect on soil organisms and their activities than will overall changes in temperature and precipitation It is well know for example that droughting and freezing have substantial direct effects on microbial physiology and the composition of the soil microbial community with important consequences for ecosystem-level carbon dynamics (Schimel et al 2007) For example increased drought and drying in wetlands and peatlands which will lower the water

Page 9

table and introduce oxygen into previously anaerobic soil will create a more favorable environment for microbial activity (Freeman et al 2004) potentially enhancing the activity of enzymes (eg phenol oxidases) which play a pivotal role in the breakdown of recalcitrant organic matter (Freeman et al 2004) Because peatlands and wetlands represent amongst the largest stocks of terrestrial carbon globally (Ward et al 2007) such enhanced breakdown of recalcitrant organic matter under drying could have major implications for the global carbon cycle (Freeman et al 2004) Before leaving this topic it is important to note that methanogenic pathways are also affected by increased oxygen availability associated with drought in that methane emissions are reduced by toxic effects of oxygen on methanogens (Roulet and Moore 1995 Freeman et al 2002) Also drought can have marked effects on nitrous oxide emission from soils a potent greenhouse gas that is increasing in atmospheric concentrations at the rate of 02ndash03 per year (Houghton et al 1996) However responses depend on the severity of drought in that modest summer drought is likely to have limited effect on soil nitrous oxide emissions whereas more extreme drought can greatly increase them (Dowrick et al 1999)

The majority of studies to date that have explored effects of climate change on biological systems and soil organisms have considered single factors such as elevated atmospheric carbon dioxide concentration warming and drought However there is much potential for interactions between these factors to have additive or antagonistic effects on soil organisms and the activities that they drive (Mikkelsen et al 2008 Bardgett et al 2008 Tylianakis et al 2008) Very little is known about the influence of multiple and interacting climate drivers on soil organisms and their activities although some studies do point to strong non-additive belowground effects of these drivers with feedback consequences for carbon exchange For instance microbial decomposition of peat was found to be significantly greater when subject to both elevated temperature and atmospheric carbon dioxide than when these factors were each elevated singly (Fenner et al 2007ab) thereby potentially causing an even stronger feedback on carbon loss from soil as dissolved organic carbon in drainage water and respiration Added to this complexity is our knowledge that other organisms and trophic groups that influence soil microbes directly such as microbial-feeding fauna will also respond to multiple climate change factors (Wardle 2002 Bardgett 2005 Tylianakis et al 2008) This complexity further hampers our ability to predict effects of multiple climate change drivers on soil biological communities and carbon exchange feedbacks

In addition to multiple climate change drivers soil organisms and their activities are also affected substantially by other global change phenomena such as nitrogen deposition invasion of new species and land use change Perhaps the strongest driver is land use change (cf Sala et al 2000) and it is widely documented that changes in the intensity of land use or the conversion of natural vegetation to agriculture or forestry can have substantial and often strongly negative and irreversible effects on soil biological communities and their activities (Brussaard et al 1997 Wardle 2002 Bardgett 2005) One pattern that commonly emerges in the context of land use change is that intensification of farming including increased tillage fertilizer use and grazing is typically associated with an increased role of the bacterial-based energy channel relative to the fungal-based channel (Wardle 2002 Bardgett 2005 Bardgett and Wardle 2010) which is away from what would typically found in more stable late successional ecosystems with large fungalbacterial ratios (Harris 2009) As discussed above this increased bacterial role is associated with faster leakier nutrient cycling and more losses of nutrients and carbon in water and greenhouse gases to the atmosphere (Wardle et al 2004 van der Heijden et al 2008) In contrast low intensity management systems often encourage fungal-based soil food webs that are more similar to those of natural systems and tend to be associated with more efficient nutrient cycling (Bardgett and McAlister 1999 Gordon et al 2008) and enhanced soil carbon sequestration (De Deyn et al 2008) Although not tested global change drivers may alter the balance of communities in favour bacterial populations thereby accelerating rates of nutrient and carbon mineralization with implications for carbon sequestration and C loss to the atmosphere

Soil biological communities are also strongly affected by nitrogen enrichment which is of high relevance because anthropogenic activities have substantially increased global rates of nitrogen fixation and deposition (Schlesinger 2009) For instance it is well known that nitrogen enrichment can have direct and differential impacts on extracellular enzymes involved in decomposition processes This typically involves stimulation of the synthesis of cellulases which degrade labile high cellulose litter but suppression of the synthesis of ligninolytic enzymes by white rot fungi which decompose recalcitrant high lignin litter (Carreiro et al 2000 Waldrop et al 2004 Allison et al 2008) Also

Page 10

nitrogen enrichment is known to influence the abundance and diversity of different components of the soil microbial community including saprophytic fungi (Donnison et al 2000 Allison et al 2008) mycorrhizal fungi (Egerton-Warburton and Allen 2000 Frey et al 2004) and soil fauna (Scheu and Schaeffer 1998 Ettema et al 1999) which are also affected by climate change and are well known to have substantial effects on decomposition processes and ecosystem-level carbon exchange A recent meta-analysis on this topic revealed that soil microbial biomass declined 15 on average under nitrogen fertilization but that declines in abundance of microbes and fungi were more evident in studies of longer durations and with higher total amounts of nitrogen added (Treseder 2008) Moreover that study showed negative responses of microbial biomass to nitrogen fertilization to be significantly correlated with declines in soil carbon dioxide emissions indicating that moderate declines in microbial biomass under nitrogen fertilization may also have consequences for carbon fluxes However another meta-analysis of 109 studies across the globe revealed that nitrogen enrichment had no significant effect on net ecosystem carbon dioxide exchange in non-forest natural ecosystems but did increase methane and nitrous oxide emissions by 97 and 216 respectively (Liu and Greaver 2009) It was suggested therefore that any potential positive effects of nitrogen enrichment on the global terrestrial carbon sink should be offset by the stimulation of methane and nitrous oxide emissions which are more potent greenhouse gases than is carbon dioxide (Liu and Greaver 2009) Importantly nitrogen deposition and other global changes can also influence soil microbes and decomposition processes indirectly through altering vegetation composition and productivity and by alleviating progressive nitrogen limitation of plant growth which typically occurs under elevated atmospheric carbon dioxide (Finzi et al 2002 Luo et al 2004 de Graaff et al 2006)

The likely effect of drought during summers is well-appreciated but much less is known about the impacts of warmer wetter winters for which plants appear to have fewer adaptations to cope (Whitmore and Whalley 2009) Waterlogging becomes more likely with increased rainfall but at the same time root respiration is likely to increase in response to warmer temperatures There is thus a considerably raised risk of waterlogging of UK soils during the future winter months No additional impact of drought has been found on cereal yields following winter waterlogging and reasonable diversity and resistance to waterlogging has been found in UK cereal varieties (Dickin and Wright 2009 Dickin et al 2008) However soil-dwelling organisms may be at risk some earthworms for example are more intolerant of waterlogging than others (Chuang and Chen 2009) Earthworms are relatively well studied other species less so and in general macrofauna diversity is greatly reduced in flooded grasslands (Plum 2005) with opportunists becoming more abundant Microbes and plants compete for resources in waterlogged soils For example Blom (1999) reported that plants out-competed nitrifiers for ammonium in waterlogged soil It is not clear to what extent plants and microbes compete for oxygen

In general very little is known about the combined effects of global changes on soil biological communities and their activities but they clearly have the potential to amplify suppress or perhaps even neutralize climate change driven effects on soil microbes and their feedback to carbon exchange (Bardgett et al 2008) A recent synthesis by Tylianakis et al (2008) of data from 688 published studies on the effects of global change on biotic interactions in terrestrial ecosystems (including those that occur in the decomposer food web) highlighted that there is substantial variability among studies in both the magnitude and direction of effects of any given global change driver on any given type of biotic interaction Further that analysis highlighted that the unanticipated effects of multiple drivers acting simultaneously create major challenges in predicting future responses to global environmental change Experimental studies that simultaneously vary two or more global change drivers within the same experiment therefore have considerable promise for improving our understanding of how interactions involving soil communities and their effects on ecosystem-level processes may respond to current global change scenarios

Soil structural integrity and dynamics

The architecture of soil the ways in which particles are arranged in space so forming a stable connected pore space determines the habitat of soil dwelling organisms including plants This soil physical environment is mutable however Soil is hard or dusty but transmits gases readily when dry when wet it becomes soft and plastic and gas ingress becomes much reduced These two extremes are expected to become more prevalent with the changes in climate expected for the UK drier

Page 11

summers and wetter winters The presence of plants indirectly exacerbates the effects of climate change by extracting water in summer and oxygen for root respiration in the winter There is a greater risk of compaction with wetter more plastic soils with late-harvested crops such as potatoes or sugar beet and establishment afterwards Working day access to land may be reduced or more variable leading to damage to soil through inappropriate management (Section B Degradation) Drought may affect soil stability and structure and possibly encourage wind erosion Cecillon et al (2010) examined sites along a latitudinal mountain spatial climate gradient for aggregation and aggregate stability and showed that erodibility was linked to climate and therefore susceptible to change under a shifting climatic regime Other studies have shown effects on organisms associated with the genesis of aggregate structure For instance Eggleton et al (2009) demonstrated in southern England pasture woodland hat earthworm community structure was dependant on soil temperature and water This faunal group has long been established as being of critical importance in no and minimal-till systems both organic and inorganic with potential for declines in aggregate stability as a result of climate change linked to declines in earthworm abundance and shifts in earthworm community structure There are also emerging models linking earthworm population dynamics and soil structural components (Blanchart et al 2009) which offer the possibility of modelling a biotic and abiotic component simultaneously under different climate change scenarios with consequences for hydrology erodibility and trophic level effects

Kohler et al (2009) found that increased CO2 concentrations led to a significantly higher percentage of stable aggregates growing under Lectuca sativa in drought conditions and this was linked to increases in soil microbial biomass and inoculation with a vesicular arbuscular mycorrhizal fungus and plant-growth-promoting rhizobacterium Other workers (Rillig et al 2001) had found a similar effect of elevated carbon dioxide and increased water supply by irrigation on increased aggregate stability due to arbuscular mycorrhizal fungi in soils under Sorghum

Earlier work suggested that climate change would not affect accessibility to land unless winter rainfall increased by 15 (Rounsevell and Brignall 1994) Since this is now what is expected it may be necessary to re-calculate workable days for England based on up-to-date climate change scenarios Neither the direct effect of climate change on soil stability via wet-dry cycles nor its indirect effect via the soil fauna is certain and as Horn and Smucker (2005) have noted that changes in aggregate stability and soil structure can be undesirable if the soil becomes difficult to manage We need to better understand the processes underlying soil structure in order to predict direct soil response to climate change and we need to better understand the wider impact of climate change on soil ecosystems if we are to understand and predict the indirect effects of the soil fauna on soil

Warmer wetter winters may lead to increased competition for oxygen among more strongly respiring organisms in wetter soils into which oxygen penetration is slower Drier summers will lead to soils into which root penetration becomes restricted Both effects are likely to impact on the ability of plants to acquire nutrients and on biogeochemical cycles in general Research on waterlogging appears to have concluded in the 1980s that UK cereals could compensate provided waterlogging did not occur during establishment or repetitively (eg Belford et al 1985) While this may have been true of the conditions prevailing at the time the same may not be true for our future climate The effect that plant root extraction of oxygen has on soil fauna and microflora and vice versa appears to be poorly researched especially in the context of our expected climate change

In summary stability of soil is likely to be impacted by the increasing intensity of wet-dry cycles with climate change but note that an increase is not necessarily desirable if the soil becomes less workable Stepniewska and Stepniewska (2009) have stressed the need for a moderate stable redox above 300 mV Soil fauna and community structure is also likely to be impacted by a change in climate with effects on soil stability that are unclear It is also likely that with wetter winters the number of days when soil is safely accessible by heavy farm machinery without causing damage may become more variable and therefore unpredictable

Page 12

4 Methodologies for investigating the impacts of climate change on soil

Experiments on climate change drivers have been carried out over a variety of spatial and temporal scales ranging from short term laboratory incubation studies to ecosystem-level and long-term manipulations of climatic factors (Wullschleger and Strahl 2010) The main approaches for studying climate change include (1) the use of environmental gradients (temperature and water) and reciprocal transplants (2) in situ field manipulation experiments including Free-Air CO2 Enrichment (FACE) experiments for manipulation of atmospheric CO2 and field-scale manipulations of temperature and precipitation (3) controlled environment facilities such as the Ecotron controlled environment facilities at Imperial College Silwood Park UK and Montpellier France and (4) highly artificial often laboratory based microcosm experiments that have little relevance to real systems These approaches in the order listed above follow a spectrum of decreasing realism but increasing mechanistic control We discuss these approaches in turn

Environmental gradients (temperature and water) and reciprocal transplants

Climatic gradients for instance in annual precipitation and temperature that cross continents countries and elevation gradients are commonly used to determine impacts of climatic variation on soil biota and processes While useful for establishing general patterns such approaches leave significant questions about other factors that could explain differences in soil biota along climatic gradients such as soil fertility and mineralogy To overcome this problem an associated approach is the use of transplant experiments whereby intact soil-vegetation turves (or varying size) are transplanted at different places along climatic gradients so that effects of movement to another climate on soil biota can be assessed This approach for example was used by Briones et al (19971998) who transplanted peat soils from high to lower altitudes at Great Dunn Fell Cumbria to simulate climate warming and that this increased the density of enchytraeid worms the dominant fauna of these peat soils leading to enhanced decomposition and DOC concentrations in soil leachates The same system was also used by Tipping et al (1999) to show that warming and drying can accelerate the production of dissolved organic matter in organic soil horizons Such approaches are valuable in that they provide information on the response of soil biota and processes to real changes in climate but they are limited by the lack of control of environmental variables along transects and potential effects of disturbance from moving soil cores from one site to another

The further experimentation moves away from surveys and experiments in the field the less likely they are to represent real world systems This is not necessarily an issue when detailed and specific mechanisms are being explored but become increasingly problematic when large scale predictions are asserted from them

In situ field manipulation experiments

Many studies have used various field-based manipulations of climate including elevated carbon dioxide in the previously mentioned FACE experiments (eg Norby et al 2004 Jackson et al 2009) drought using rainfall roofs (eg Beier et al 2004) and artificial warming using heating cables (eg Grime et al 2008) passive night time warming roofs (eg Beier et al 2004) and infra-red lamps (Zhang et al 2005) Such experiments have contributed significantly to our understanding of the effects of different climate change drivers on vegetation soil biota and soil processes as detailed in the previous section However as stated previously most studies of this kind have explored effects of single climate factors whereas there is much potential for interactions between multiple factors to have additive or antagonistic effects on soil organisms and the activities that they drive (Bardgett et al 2008) Therefore future experiments which manipulate multiple climate change and other site factors are needed to better understand the effects of climate change on soil biota

As an example of in situ field manipulations Zhang et al (2005) artificially heated soils under tall grass prairie using infra-red heaters to simulate an increase in daily soil temperatures of 18 ndash 27oC and studied two clipping regimes clipped and unclipped In the heated treatments they found changes in the soil microbial community structure as determined using phospholipid fatty acid analysis (PLFA) in the unclipped plots with a shift to fungal dominance but not in the clipped

Page 4

Soil function Impact of UKCIP02 climate change scenarios

increasing the risk of soil erosion Therefore in the long term soil resources will be reduced and food production will be affected

bull Generally warmer temperature may increase the risk of parasite infections if climate change helps that part of the parasite life cycle outside the body

Soil air and water interactions

bull Warming will decrease soil organic matter increase CO2 emissions increase litter decomposition and N mineralisation rate which may increase N leaching rate

bull In the long term carbon stock may become insensitive to temperature increases This is based on the assumption that soil physico-chemical ldquostabilisationrdquo reaction may respond more to warming than microbial decompositionrespiration reactions In turn warming may increase the rate of physico-chemical processes that transfer organic carbon to more stable carbon pools As a result total soil carbon loss may be very small and even may increase

bull Elevated CO2 will increase above-ground and below ground biomass Increasing the total carbon flux to the soil The effects of CO2 to soil C may be positive in the short term but reverse in the long term

bull Higher seasonal fluctuations in soil water increase the risk of changes to soil chemistry eg more leaching soil acidification gradually lower soil CEC and therefore buffering capacity

bull Drying out of peaty soils may convert peatlands from CO2 sinks to CO2 source

bull Drier summers will lead to the accumulation of nutrients and pollutants in the soil which will be flushed out when significant rainfall occurs for example during the autumn

bull Soil with a high water content promote methanogenic activity and reduces methanotrophic activity by reducing the size of oxidised zones

bull Waterlogged upland soils may become CH4 sources

Soil biodiversity As will be discussed later in this chapter very few UK projects have investigated climate impacts on soil biodiversity

Soil in the landscape and cultural heritage

Very few UK studies

bull Heritage sites will suffer from an increased rate of chemical-flooding risk on certain structures and fabrics

bull Increased soil water could increase biological attack and other decay (salt mobilisation)

bull Artefacts may be exposed through the process of soil erosion (wind and water) and begin to deteriorate

bull Changes to the vegetation supported will alter the look of the historic landscape

bull Lower water table will affect the preservation of archaeological remains Drier soils will increase damage to artefacts through increased oxidation and exposure due to soil erosion eg increased risk of wind erosion to peat soils as they dry out

Page 5

Soil function Impact of UKCIP02 climate change scenarios

bull If intensive arable cultivation shifts from the south east to the north buried archaeological sites currently not at risk from arable damage could become so

Soils in mineral extraction construction and the built environment

bull Increased winter rainfall especially extreme events could impact on land stability increased risk of land slides

bull increased risk of subsidence due to intermittent rainfall leading to an increased soil moisture deficit and soil shrinkage

bull High intensity rainfall events may overwhelm drainage systems and increase the risk of downstream flooding

bull Land may become unsuitable for development

bull Increased droughtiness will increase shrink-swell causing disturbance to building foundations and the need to underpinrepair

bull Increased temperature may exacerbate chemical attack to foundations

bull Increased temperatures may increase the risk to engineered structures based on clay caps ndash increasing leaching and release of landfill gases

bull Increase flooding and erosion will increase the risk of loss of contaminants from brownfield land

bull Land to be used for temporary flood drainage must be underlain by soils with suitable infiltration capacity and hydraulic conductivity and must not be erodible

bull Higher temperatures will also encourage volatilisation of some organic pollutants and mercury on contaminated sites

The seven key recommendations made by Bradley et al (2005) in relation to research requirements were

1 More research specifically aimed at soil functions under climate change Incorporating climate change on soil in all relevant research With research being updated to the latest climate change predictions or at least an assessment of possible changes

2 Further investigation of the interactions between climate change and pollutant deposition and exposure particularly critical loads and their exceedance for agricultural land and woodland in relation to issues of acidificationrecovery and eutrophication

3 Future research into soil functions under climate change should attempt to deal with uncertainties in climate predictions and soil process model formulation and parameterisation of soil processes Model development for organic and woodland soils needs to be promoted including the collection of data required for parameterisation and verification

4 Studies integrating the impact of land use changes and socio-economic factors should be encouraged since these may be as important as the impacts of climate change on soil functions

5 Further targeted research is recommended to investigate the effects of CO2 combined with changes in the temperature regime on soil function directly or indirectly and interactions with changes in temperature and rainfall

6 More research is warranted on the ability of soils to hold and buffer pollutants in the face of climate change particularly on lsquobrownfieldrsquo soils as well as in the urban built environment

Page 6

7 Improved estimates of non-CO2 GHG balance (primarily N2O and CH4) of forest soils including predictions of the impacts of climate change and the effects of forest management extension to broadleaf woodland and deforestation activities is important

2 Climate change scenarios

UKCIP09 climate change predictions as based on medium emissions scenarios for 2080 predict that England and Wales will get warmer with summers showing a slightly greater (on average 4degC) increase in temperature than winters (on average 3degC Table 2) While temperatures are predicted to rise the annual amount of precipitation is not expected to change However the distribution of rainfall throughout the year is predicted to change Summer precipitation is predicted to decrease across England and Wales (Table 2) on average by -24 to -18 while winter precipitation is predicted to increase by between 14 and 23 Also there is expected to be an increased frequency of extreme weather occurrences such as heat waves dry spells heavy rain and flooding as well as rises in sea level Central estimates are for heavy rain days (rainfall greater than 25 mm) over most of the lowland UK to increase by a factor of between 2 and 35 in winter and 1 to 2 in summer by the 2080s under the medium emissions scenario (UKCP09)

Table 2 UKCIP09 central climate change predictions based on medium emission scenarios for 2080 (low and high probabilities given in brackets)

Administrative regions

Winter mean temperature (degC)

Summer mean temperature (degC)

Annual winter mean precipitation ()

Annual summer mean precipitation ()

Wales 28 (1642) 35 (1958) 19 (442) -20 (-435) North East England 26 (1441) 37 (2058) 14 (232) -18 (-361)

East of England 30 (1647) 36 (1959) 20 (444) -21 (-456) South West England 28 (1643) 39 (2164) 23 (654) -24 (-506)

South East England 30 (1647) 39 (2065) 22 (451) -23 (-487)

West Midlands 29 (1644) 37 (2061) 17 (338) -20 (-446) East Midlands 30 (1646) 35 (1858) 19 (341) -20 (-446) Yorkshire and Humber 30 (1646) 33 (1754) 15 (233) -23 (-440)

North West England 26 (1440) 37 (2059) 16 (334) -22 (-430)

Mean 29 36 18 -21

The south west of England is predicted to experience the greatest increase in summer temperatures as well as the highest predicted increase in winter mean precipitation and lowest summer mean precipitation of all regions in England and Wales (Table 2) while the east of England south east England and Yorkshire and Humber are predicted to have some of the mildest winter temperatures The north east of England is predicted to experience a less extreme change in winter and summer precipitation

The predictions made by UKCP09 are supported by resent observed trends in UK climate reported by Jenkins et al (2009) Global average temperatures have risen by nearly 02degCdecade over the past 25 years In central England temperatures have risen by about a degree Celsius since the 1970s Annual mean precipitation in England and Wales has not changed significantly although summers do appear to be drier and winters wetter Over the past 45 years there has been an increase in heavy winter rainfall events Severe windstorms around the UK have become more frequent in the past few decades

Page 7

UKCP09 predictions are broadly consistent with UKCIP02 predictions Comparisons of UKCIP02 and UKCP09 by Jenkins et al (2009) suggest mean temperature projections are generally greater and summer reduction in rainfall is not as great using UKCP09 The range of increase in winter rainfall is broadly similar with a different geographical pattern Decreases in cloud cover in summer are also broadly in agreement Therefore observations made by Bradley et al (2005) with regard to impact of climate change on soil function are still valid Bradley et al (2005) defined both direct and indirect impacts of climate change on soil functions and these are summarised in Section 1 Table 1 Subsequently there has been more attention paid to the impact of climate change on soil biota and its impact on soil processes and functions This new information is summarised in Table 3

Table 3 Potential implications of predicted climate change on soil biota

Climate change Implications for soil biota

Warmer springs bull Changes in timings of seasonal events may cause loss of synchrony between species and the availability of food (Hopkins et al 2007 Newton et al 2008)

Warmer and drier summers

bull Reduced soil moisture content may limit plant production without additional irrigation

bull Drier soils may affect the mobility of soil fauna such as nematodes and earthworms (Bardgett 2005 Eggleton et al 2009)

bull Changes to habitat may favour drought tolerant soil biota soil may experience a shift in species which may impact on the over all function of the soil depending on redundancy in the system (Castro et al 2010)

bull Summer droughts may cause stress in some soil microbial communities and result in changes in fungal diversity impacting on functional diversity (Toberman et al 2008)

bull Drier conditions and higher temperatures may accelerate decomposition of organic material through increased oxygen availability and increased microbial activity However additional input of leaf litter from increased production may offset net loss of carbon from the soil profile (Dawson and Smith 2007)

bull Decreased loss of methane due to increased oxygen availability impacting on methanogens (McNamara et al 2006)

bull May cause shift in vegetation patterns with subsequent implications for soil biota (Pentildeuelas et al 2007)

Warmer and wetter winters

bull Increase the likely survival of soil pests and diseases (Newton et al 2008)

bull Inward migration of soil biota from warmer areas

bull Water logging will reduce the availability of oxygen in the soil profile affecting both soil fauna and soil flora (Sowerby et al 2008)

bull Soil compaction will impede root penetration and may restrict soil fauna movement within the soil profile (Whally et al 1995)

bull May cause shift in vegetation patterns with subsequent implications for soil biota (Pentildeuelas et al 2007)

Extreme events bull Drying of the top soil followed by sudden rewetting encourages flushes of microbial activity and nutrient loss from soil (Sowerby et al 2008 Gordon et al 2008)

Increased CO2 bull Increased transfer of C through root system into the soil stimulating

Page 8

Climate change Implications for soil biota

microbial abundance and activity (Castro et al 2010)

bull Increased transfer of C to the soil stimulating mycorrhizal fungi which may stimulate nutrient transfer (Tyliankis et al 2008)

bull Stimulation of microbial biomass can lead to microbial immobilization of N thereby enforcing plant N limitation (de Graaff et al 2007)

bull May cause shift in vegetation patterns with subsequent implications for soil biota

Section 3 Potential impacts of climate change on soil processes function and biota

Carbon and nutrient cycling

Climate change has both direct and indirect effects on soil organisms and the processes that they drive often with consequences for the return greenhouse gases to the atmosphere Direct effects include the influence of temperature changing precipitation and extreme climatic events on soil organisms and the processes that they drive whereas indirect effects result from climate-driven changes in plant productivity and species composition which alter soil physicochemical conditions the supply of carbon to soil and the structure and activity of microbial communities involved in decomposition processes and carbon release from soil (Bardgett et al 2008)

One of the most commonly discussed contributions of soil organisms to climate change is their role in soil organic matter decomposition and the idea that warming will accelerate rates of heterotrophic microbial activity thereby increasing the transfer of carbon dioxide from soil to the atmosphere and exports of dissolved organic carbon by hydrologic leaching (Jenkinson et al 1991 Davidson and Janssens 2006) The concern here is that because rates of soil respiration are more sensitive than is primary production to temperature (Jenkinson et al 1991 Schimel et al 1994) it is thought that climate warming will increase the net transfer of carbon from soil to atmosphere thus creating a positive feedback on climate change (Cox et al 2000) Although it is well known that temperature is an important determinant of rates of organic matter decomposition the nature of the relationship between temperature and microbial respiration is far from clear (Davidson and Janssens 2006) There are several reasons for this uncertainty but key factors include potential for variations in organic matter quality to influence the temperature sensitivity of microbial decomposition (Fang et al 2005 Conen et al 2006 Davidson and Janssens 2006) and for environmental constraints such as physical and chemical protection of organic matter to decrease substrate availability for microbial attack and thereby dampen microbial responses to warming (Davidson and Janssens 2006) Also there is uncertainty about how reactive different microbial and faunal groups and species are to temperature change with several studies showing that soil microbial and animal communities are insensitive to small increases in temperature (eg Kandeler et al 1998 Bardgett et al 1999 Wardle 2002) whereas others show that soil organisms and the carbon cycling processes that they drive are responsive to temperature change For instance the abundance of enchytraeid worms which dominate the fauna of acid peat soils have been shown to be strongly related to temperature and it is has been suggested that climate warming could increase their abundance leading to enhanced carbon mineralization and carbon loss from soil (Briones et al 1998 Cole et al 2002ab) Also a recent analysis by Gange et al (2007) related temporal shifts in autumnal fruiting patterns of macrofungi in southern England to shifts in climate and found that the average first fruiting date of 315 species is now earlier while last fruiting date is now later than was the case 56 years ago Their study also found that many species are now fruiting twice a year indicative of increased mycelial activity and possibly greater decomposition rates in ecosystems

Increases in the frequency of extreme weather events with climate change such as droughting and freezing may have an even greater effect on soil organisms and their activities than will overall changes in temperature and precipitation It is well know for example that droughting and freezing have substantial direct effects on microbial physiology and the composition of the soil microbial community with important consequences for ecosystem-level carbon dynamics (Schimel et al 2007) For example increased drought and drying in wetlands and peatlands which will lower the water

Page 9

table and introduce oxygen into previously anaerobic soil will create a more favorable environment for microbial activity (Freeman et al 2004) potentially enhancing the activity of enzymes (eg phenol oxidases) which play a pivotal role in the breakdown of recalcitrant organic matter (Freeman et al 2004) Because peatlands and wetlands represent amongst the largest stocks of terrestrial carbon globally (Ward et al 2007) such enhanced breakdown of recalcitrant organic matter under drying could have major implications for the global carbon cycle (Freeman et al 2004) Before leaving this topic it is important to note that methanogenic pathways are also affected by increased oxygen availability associated with drought in that methane emissions are reduced by toxic effects of oxygen on methanogens (Roulet and Moore 1995 Freeman et al 2002) Also drought can have marked effects on nitrous oxide emission from soils a potent greenhouse gas that is increasing in atmospheric concentrations at the rate of 02ndash03 per year (Houghton et al 1996) However responses depend on the severity of drought in that modest summer drought is likely to have limited effect on soil nitrous oxide emissions whereas more extreme drought can greatly increase them (Dowrick et al 1999)

The majority of studies to date that have explored effects of climate change on biological systems and soil organisms have considered single factors such as elevated atmospheric carbon dioxide concentration warming and drought However there is much potential for interactions between these factors to have additive or antagonistic effects on soil organisms and the activities that they drive (Mikkelsen et al 2008 Bardgett et al 2008 Tylianakis et al 2008) Very little is known about the influence of multiple and interacting climate drivers on soil organisms and their activities although some studies do point to strong non-additive belowground effects of these drivers with feedback consequences for carbon exchange For instance microbial decomposition of peat was found to be significantly greater when subject to both elevated temperature and atmospheric carbon dioxide than when these factors were each elevated singly (Fenner et al 2007ab) thereby potentially causing an even stronger feedback on carbon loss from soil as dissolved organic carbon in drainage water and respiration Added to this complexity is our knowledge that other organisms and trophic groups that influence soil microbes directly such as microbial-feeding fauna will also respond to multiple climate change factors (Wardle 2002 Bardgett 2005 Tylianakis et al 2008) This complexity further hampers our ability to predict effects of multiple climate change drivers on soil biological communities and carbon exchange feedbacks

In addition to multiple climate change drivers soil organisms and their activities are also affected substantially by other global change phenomena such as nitrogen deposition invasion of new species and land use change Perhaps the strongest driver is land use change (cf Sala et al 2000) and it is widely documented that changes in the intensity of land use or the conversion of natural vegetation to agriculture or forestry can have substantial and often strongly negative and irreversible effects on soil biological communities and their activities (Brussaard et al 1997 Wardle 2002 Bardgett 2005) One pattern that commonly emerges in the context of land use change is that intensification of farming including increased tillage fertilizer use and grazing is typically associated with an increased role of the bacterial-based energy channel relative to the fungal-based channel (Wardle 2002 Bardgett 2005 Bardgett and Wardle 2010) which is away from what would typically found in more stable late successional ecosystems with large fungalbacterial ratios (Harris 2009) As discussed above this increased bacterial role is associated with faster leakier nutrient cycling and more losses of nutrients and carbon in water and greenhouse gases to the atmosphere (Wardle et al 2004 van der Heijden et al 2008) In contrast low intensity management systems often encourage fungal-based soil food webs that are more similar to those of natural systems and tend to be associated with more efficient nutrient cycling (Bardgett and McAlister 1999 Gordon et al 2008) and enhanced soil carbon sequestration (De Deyn et al 2008) Although not tested global change drivers may alter the balance of communities in favour bacterial populations thereby accelerating rates of nutrient and carbon mineralization with implications for carbon sequestration and C loss to the atmosphere

Soil biological communities are also strongly affected by nitrogen enrichment which is of high relevance because anthropogenic activities have substantially increased global rates of nitrogen fixation and deposition (Schlesinger 2009) For instance it is well known that nitrogen enrichment can have direct and differential impacts on extracellular enzymes involved in decomposition processes This typically involves stimulation of the synthesis of cellulases which degrade labile high cellulose litter but suppression of the synthesis of ligninolytic enzymes by white rot fungi which decompose recalcitrant high lignin litter (Carreiro et al 2000 Waldrop et al 2004 Allison et al 2008) Also

Page 10

nitrogen enrichment is known to influence the abundance and diversity of different components of the soil microbial community including saprophytic fungi (Donnison et al 2000 Allison et al 2008) mycorrhizal fungi (Egerton-Warburton and Allen 2000 Frey et al 2004) and soil fauna (Scheu and Schaeffer 1998 Ettema et al 1999) which are also affected by climate change and are well known to have substantial effects on decomposition processes and ecosystem-level carbon exchange A recent meta-analysis on this topic revealed that soil microbial biomass declined 15 on average under nitrogen fertilization but that declines in abundance of microbes and fungi were more evident in studies of longer durations and with higher total amounts of nitrogen added (Treseder 2008) Moreover that study showed negative responses of microbial biomass to nitrogen fertilization to be significantly correlated with declines in soil carbon dioxide emissions indicating that moderate declines in microbial biomass under nitrogen fertilization may also have consequences for carbon fluxes However another meta-analysis of 109 studies across the globe revealed that nitrogen enrichment had no significant effect on net ecosystem carbon dioxide exchange in non-forest natural ecosystems but did increase methane and nitrous oxide emissions by 97 and 216 respectively (Liu and Greaver 2009) It was suggested therefore that any potential positive effects of nitrogen enrichment on the global terrestrial carbon sink should be offset by the stimulation of methane and nitrous oxide emissions which are more potent greenhouse gases than is carbon dioxide (Liu and Greaver 2009) Importantly nitrogen deposition and other global changes can also influence soil microbes and decomposition processes indirectly through altering vegetation composition and productivity and by alleviating progressive nitrogen limitation of plant growth which typically occurs under elevated atmospheric carbon dioxide (Finzi et al 2002 Luo et al 2004 de Graaff et al 2006)

The likely effect of drought during summers is well-appreciated but much less is known about the impacts of warmer wetter winters for which plants appear to have fewer adaptations to cope (Whitmore and Whalley 2009) Waterlogging becomes more likely with increased rainfall but at the same time root respiration is likely to increase in response to warmer temperatures There is thus a considerably raised risk of waterlogging of UK soils during the future winter months No additional impact of drought has been found on cereal yields following winter waterlogging and reasonable diversity and resistance to waterlogging has been found in UK cereal varieties (Dickin and Wright 2009 Dickin et al 2008) However soil-dwelling organisms may be at risk some earthworms for example are more intolerant of waterlogging than others (Chuang and Chen 2009) Earthworms are relatively well studied other species less so and in general macrofauna diversity is greatly reduced in flooded grasslands (Plum 2005) with opportunists becoming more abundant Microbes and plants compete for resources in waterlogged soils For example Blom (1999) reported that plants out-competed nitrifiers for ammonium in waterlogged soil It is not clear to what extent plants and microbes compete for oxygen

In general very little is known about the combined effects of global changes on soil biological communities and their activities but they clearly have the potential to amplify suppress or perhaps even neutralize climate change driven effects on soil microbes and their feedback to carbon exchange (Bardgett et al 2008) A recent synthesis by Tylianakis et al (2008) of data from 688 published studies on the effects of global change on biotic interactions in terrestrial ecosystems (including those that occur in the decomposer food web) highlighted that there is substantial variability among studies in both the magnitude and direction of effects of any given global change driver on any given type of biotic interaction Further that analysis highlighted that the unanticipated effects of multiple drivers acting simultaneously create major challenges in predicting future responses to global environmental change Experimental studies that simultaneously vary two or more global change drivers within the same experiment therefore have considerable promise for improving our understanding of how interactions involving soil communities and their effects on ecosystem-level processes may respond to current global change scenarios

Soil structural integrity and dynamics

The architecture of soil the ways in which particles are arranged in space so forming a stable connected pore space determines the habitat of soil dwelling organisms including plants This soil physical environment is mutable however Soil is hard or dusty but transmits gases readily when dry when wet it becomes soft and plastic and gas ingress becomes much reduced These two extremes are expected to become more prevalent with the changes in climate expected for the UK drier

Page 11

summers and wetter winters The presence of plants indirectly exacerbates the effects of climate change by extracting water in summer and oxygen for root respiration in the winter There is a greater risk of compaction with wetter more plastic soils with late-harvested crops such as potatoes or sugar beet and establishment afterwards Working day access to land may be reduced or more variable leading to damage to soil through inappropriate management (Section B Degradation) Drought may affect soil stability and structure and possibly encourage wind erosion Cecillon et al (2010) examined sites along a latitudinal mountain spatial climate gradient for aggregation and aggregate stability and showed that erodibility was linked to climate and therefore susceptible to change under a shifting climatic regime Other studies have shown effects on organisms associated with the genesis of aggregate structure For instance Eggleton et al (2009) demonstrated in southern England pasture woodland hat earthworm community structure was dependant on soil temperature and water This faunal group has long been established as being of critical importance in no and minimal-till systems both organic and inorganic with potential for declines in aggregate stability as a result of climate change linked to declines in earthworm abundance and shifts in earthworm community structure There are also emerging models linking earthworm population dynamics and soil structural components (Blanchart et al 2009) which offer the possibility of modelling a biotic and abiotic component simultaneously under different climate change scenarios with consequences for hydrology erodibility and trophic level effects

Kohler et al (2009) found that increased CO2 concentrations led to a significantly higher percentage of stable aggregates growing under Lectuca sativa in drought conditions and this was linked to increases in soil microbial biomass and inoculation with a vesicular arbuscular mycorrhizal fungus and plant-growth-promoting rhizobacterium Other workers (Rillig et al 2001) had found a similar effect of elevated carbon dioxide and increased water supply by irrigation on increased aggregate stability due to arbuscular mycorrhizal fungi in soils under Sorghum

Earlier work suggested that climate change would not affect accessibility to land unless winter rainfall increased by 15 (Rounsevell and Brignall 1994) Since this is now what is expected it may be necessary to re-calculate workable days for England based on up-to-date climate change scenarios Neither the direct effect of climate change on soil stability via wet-dry cycles nor its indirect effect via the soil fauna is certain and as Horn and Smucker (2005) have noted that changes in aggregate stability and soil structure can be undesirable if the soil becomes difficult to manage We need to better understand the processes underlying soil structure in order to predict direct soil response to climate change and we need to better understand the wider impact of climate change on soil ecosystems if we are to understand and predict the indirect effects of the soil fauna on soil

Warmer wetter winters may lead to increased competition for oxygen among more strongly respiring organisms in wetter soils into which oxygen penetration is slower Drier summers will lead to soils into which root penetration becomes restricted Both effects are likely to impact on the ability of plants to acquire nutrients and on biogeochemical cycles in general Research on waterlogging appears to have concluded in the 1980s that UK cereals could compensate provided waterlogging did not occur during establishment or repetitively (eg Belford et al 1985) While this may have been true of the conditions prevailing at the time the same may not be true for our future climate The effect that plant root extraction of oxygen has on soil fauna and microflora and vice versa appears to be poorly researched especially in the context of our expected climate change

In summary stability of soil is likely to be impacted by the increasing intensity of wet-dry cycles with climate change but note that an increase is not necessarily desirable if the soil becomes less workable Stepniewska and Stepniewska (2009) have stressed the need for a moderate stable redox above 300 mV Soil fauna and community structure is also likely to be impacted by a change in climate with effects on soil stability that are unclear It is also likely that with wetter winters the number of days when soil is safely accessible by heavy farm machinery without causing damage may become more variable and therefore unpredictable

Page 12

4 Methodologies for investigating the impacts of climate change on soil

Experiments on climate change drivers have been carried out over a variety of spatial and temporal scales ranging from short term laboratory incubation studies to ecosystem-level and long-term manipulations of climatic factors (Wullschleger and Strahl 2010) The main approaches for studying climate change include (1) the use of environmental gradients (temperature and water) and reciprocal transplants (2) in situ field manipulation experiments including Free-Air CO2 Enrichment (FACE) experiments for manipulation of atmospheric CO2 and field-scale manipulations of temperature and precipitation (3) controlled environment facilities such as the Ecotron controlled environment facilities at Imperial College Silwood Park UK and Montpellier France and (4) highly artificial often laboratory based microcosm experiments that have little relevance to real systems These approaches in the order listed above follow a spectrum of decreasing realism but increasing mechanistic control We discuss these approaches in turn

Environmental gradients (temperature and water) and reciprocal transplants

Climatic gradients for instance in annual precipitation and temperature that cross continents countries and elevation gradients are commonly used to determine impacts of climatic variation on soil biota and processes While useful for establishing general patterns such approaches leave significant questions about other factors that could explain differences in soil biota along climatic gradients such as soil fertility and mineralogy To overcome this problem an associated approach is the use of transplant experiments whereby intact soil-vegetation turves (or varying size) are transplanted at different places along climatic gradients so that effects of movement to another climate on soil biota can be assessed This approach for example was used by Briones et al (19971998) who transplanted peat soils from high to lower altitudes at Great Dunn Fell Cumbria to simulate climate warming and that this increased the density of enchytraeid worms the dominant fauna of these peat soils leading to enhanced decomposition and DOC concentrations in soil leachates The same system was also used by Tipping et al (1999) to show that warming and drying can accelerate the production of dissolved organic matter in organic soil horizons Such approaches are valuable in that they provide information on the response of soil biota and processes to real changes in climate but they are limited by the lack of control of environmental variables along transects and potential effects of disturbance from moving soil cores from one site to another

The further experimentation moves away from surveys and experiments in the field the less likely they are to represent real world systems This is not necessarily an issue when detailed and specific mechanisms are being explored but become increasingly problematic when large scale predictions are asserted from them

In situ field manipulation experiments

Many studies have used various field-based manipulations of climate including elevated carbon dioxide in the previously mentioned FACE experiments (eg Norby et al 2004 Jackson et al 2009) drought using rainfall roofs (eg Beier et al 2004) and artificial warming using heating cables (eg Grime et al 2008) passive night time warming roofs (eg Beier et al 2004) and infra-red lamps (Zhang et al 2005) Such experiments have contributed significantly to our understanding of the effects of different climate change drivers on vegetation soil biota and soil processes as detailed in the previous section However as stated previously most studies of this kind have explored effects of single climate factors whereas there is much potential for interactions between multiple factors to have additive or antagonistic effects on soil organisms and the activities that they drive (Bardgett et al 2008) Therefore future experiments which manipulate multiple climate change and other site factors are needed to better understand the effects of climate change on soil biota

As an example of in situ field manipulations Zhang et al (2005) artificially heated soils under tall grass prairie using infra-red heaters to simulate an increase in daily soil temperatures of 18 ndash 27oC and studied two clipping regimes clipped and unclipped In the heated treatments they found changes in the soil microbial community structure as determined using phospholipid fatty acid analysis (PLFA) in the unclipped plots with a shift to fungal dominance but not in the clipped

Page 5

Soil function Impact of UKCIP02 climate change scenarios

bull If intensive arable cultivation shifts from the south east to the north buried archaeological sites currently not at risk from arable damage could become so

Soils in mineral extraction construction and the built environment

bull Increased winter rainfall especially extreme events could impact on land stability increased risk of land slides

bull increased risk of subsidence due to intermittent rainfall leading to an increased soil moisture deficit and soil shrinkage

bull High intensity rainfall events may overwhelm drainage systems and increase the risk of downstream flooding

bull Land may become unsuitable for development

bull Increased droughtiness will increase shrink-swell causing disturbance to building foundations and the need to underpinrepair

bull Increased temperature may exacerbate chemical attack to foundations

bull Increased temperatures may increase the risk to engineered structures based on clay caps ndash increasing leaching and release of landfill gases

bull Increase flooding and erosion will increase the risk of loss of contaminants from brownfield land

bull Land to be used for temporary flood drainage must be underlain by soils with suitable infiltration capacity and hydraulic conductivity and must not be erodible

bull Higher temperatures will also encourage volatilisation of some organic pollutants and mercury on contaminated sites

The seven key recommendations made by Bradley et al (2005) in relation to research requirements were

1 More research specifically aimed at soil functions under climate change Incorporating climate change on soil in all relevant research With research being updated to the latest climate change predictions or at least an assessment of possible changes

2 Further investigation of the interactions between climate change and pollutant deposition and exposure particularly critical loads and their exceedance for agricultural land and woodland in relation to issues of acidificationrecovery and eutrophication

3 Future research into soil functions under climate change should attempt to deal with uncertainties in climate predictions and soil process model formulation and parameterisation of soil processes Model development for organic and woodland soils needs to be promoted including the collection of data required for parameterisation and verification

4 Studies integrating the impact of land use changes and socio-economic factors should be encouraged since these may be as important as the impacts of climate change on soil functions

5 Further targeted research is recommended to investigate the effects of CO2 combined with changes in the temperature regime on soil function directly or indirectly and interactions with changes in temperature and rainfall

6 More research is warranted on the ability of soils to hold and buffer pollutants in the face of climate change particularly on lsquobrownfieldrsquo soils as well as in the urban built environment

Page 6

7 Improved estimates of non-CO2 GHG balance (primarily N2O and CH4) of forest soils including predictions of the impacts of climate change and the effects of forest management extension to broadleaf woodland and deforestation activities is important

2 Climate change scenarios

UKCIP09 climate change predictions as based on medium emissions scenarios for 2080 predict that England and Wales will get warmer with summers showing a slightly greater (on average 4degC) increase in temperature than winters (on average 3degC Table 2) While temperatures are predicted to rise the annual amount of precipitation is not expected to change However the distribution of rainfall throughout the year is predicted to change Summer precipitation is predicted to decrease across England and Wales (Table 2) on average by -24 to -18 while winter precipitation is predicted to increase by between 14 and 23 Also there is expected to be an increased frequency of extreme weather occurrences such as heat waves dry spells heavy rain and flooding as well as rises in sea level Central estimates are for heavy rain days (rainfall greater than 25 mm) over most of the lowland UK to increase by a factor of between 2 and 35 in winter and 1 to 2 in summer by the 2080s under the medium emissions scenario (UKCP09)

Table 2 UKCIP09 central climate change predictions based on medium emission scenarios for 2080 (low and high probabilities given in brackets)

Administrative regions

Winter mean temperature (degC)

Summer mean temperature (degC)

Annual winter mean precipitation ()

Annual summer mean precipitation ()

Wales 28 (1642) 35 (1958) 19 (442) -20 (-435) North East England 26 (1441) 37 (2058) 14 (232) -18 (-361)

East of England 30 (1647) 36 (1959) 20 (444) -21 (-456) South West England 28 (1643) 39 (2164) 23 (654) -24 (-506)

South East England 30 (1647) 39 (2065) 22 (451) -23 (-487)

West Midlands 29 (1644) 37 (2061) 17 (338) -20 (-446) East Midlands 30 (1646) 35 (1858) 19 (341) -20 (-446) Yorkshire and Humber 30 (1646) 33 (1754) 15 (233) -23 (-440)

North West England 26 (1440) 37 (2059) 16 (334) -22 (-430)

Mean 29 36 18 -21

The south west of England is predicted to experience the greatest increase in summer temperatures as well as the highest predicted increase in winter mean precipitation and lowest summer mean precipitation of all regions in England and Wales (Table 2) while the east of England south east England and Yorkshire and Humber are predicted to have some of the mildest winter temperatures The north east of England is predicted to experience a less extreme change in winter and summer precipitation

The predictions made by UKCP09 are supported by resent observed trends in UK climate reported by Jenkins et al (2009) Global average temperatures have risen by nearly 02degCdecade over the past 25 years In central England temperatures have risen by about a degree Celsius since the 1970s Annual mean precipitation in England and Wales has not changed significantly although summers do appear to be drier and winters wetter Over the past 45 years there has been an increase in heavy winter rainfall events Severe windstorms around the UK have become more frequent in the past few decades

Page 7

UKCP09 predictions are broadly consistent with UKCIP02 predictions Comparisons of UKCIP02 and UKCP09 by Jenkins et al (2009) suggest mean temperature projections are generally greater and summer reduction in rainfall is not as great using UKCP09 The range of increase in winter rainfall is broadly similar with a different geographical pattern Decreases in cloud cover in summer are also broadly in agreement Therefore observations made by Bradley et al (2005) with regard to impact of climate change on soil function are still valid Bradley et al (2005) defined both direct and indirect impacts of climate change on soil functions and these are summarised in Section 1 Table 1 Subsequently there has been more attention paid to the impact of climate change on soil biota and its impact on soil processes and functions This new information is summarised in Table 3

Table 3 Potential implications of predicted climate change on soil biota

Climate change Implications for soil biota

Warmer springs bull Changes in timings of seasonal events may cause loss of synchrony between species and the availability of food (Hopkins et al 2007 Newton et al 2008)

Warmer and drier summers

bull Reduced soil moisture content may limit plant production without additional irrigation

bull Drier soils may affect the mobility of soil fauna such as nematodes and earthworms (Bardgett 2005 Eggleton et al 2009)

bull Changes to habitat may favour drought tolerant soil biota soil may experience a shift in species which may impact on the over all function of the soil depending on redundancy in the system (Castro et al 2010)

bull Summer droughts may cause stress in some soil microbial communities and result in changes in fungal diversity impacting on functional diversity (Toberman et al 2008)

bull Drier conditions and higher temperatures may accelerate decomposition of organic material through increased oxygen availability and increased microbial activity However additional input of leaf litter from increased production may offset net loss of carbon from the soil profile (Dawson and Smith 2007)

bull Decreased loss of methane due to increased oxygen availability impacting on methanogens (McNamara et al 2006)

bull May cause shift in vegetation patterns with subsequent implications for soil biota (Pentildeuelas et al 2007)

Warmer and wetter winters

bull Increase the likely survival of soil pests and diseases (Newton et al 2008)

bull Inward migration of soil biota from warmer areas

bull Water logging will reduce the availability of oxygen in the soil profile affecting both soil fauna and soil flora (Sowerby et al 2008)

bull Soil compaction will impede root penetration and may restrict soil fauna movement within the soil profile (Whally et al 1995)

bull May cause shift in vegetation patterns with subsequent implications for soil biota (Pentildeuelas et al 2007)

Extreme events bull Drying of the top soil followed by sudden rewetting encourages flushes of microbial activity and nutrient loss from soil (Sowerby et al 2008 Gordon et al 2008)

Increased CO2 bull Increased transfer of C through root system into the soil stimulating

Page 8

Climate change Implications for soil biota

microbial abundance and activity (Castro et al 2010)

bull Increased transfer of C to the soil stimulating mycorrhizal fungi which may stimulate nutrient transfer (Tyliankis et al 2008)

bull Stimulation of microbial biomass can lead to microbial immobilization of N thereby enforcing plant N limitation (de Graaff et al 2007)

bull May cause shift in vegetation patterns with subsequent implications for soil biota

Section 3 Potential impacts of climate change on soil processes function and biota

Carbon and nutrient cycling

Climate change has both direct and indirect effects on soil organisms and the processes that they drive often with consequences for the return greenhouse gases to the atmosphere Direct effects include the influence of temperature changing precipitation and extreme climatic events on soil organisms and the processes that they drive whereas indirect effects result from climate-driven changes in plant productivity and species composition which alter soil physicochemical conditions the supply of carbon to soil and the structure and activity of microbial communities involved in decomposition processes and carbon release from soil (Bardgett et al 2008)

One of the most commonly discussed contributions of soil organisms to climate change is their role in soil organic matter decomposition and the idea that warming will accelerate rates of heterotrophic microbial activity thereby increasing the transfer of carbon dioxide from soil to the atmosphere and exports of dissolved organic carbon by hydrologic leaching (Jenkinson et al 1991 Davidson and Janssens 2006) The concern here is that because rates of soil respiration are more sensitive than is primary production to temperature (Jenkinson et al 1991 Schimel et al 1994) it is thought that climate warming will increase the net transfer of carbon from soil to atmosphere thus creating a positive feedback on climate change (Cox et al 2000) Although it is well known that temperature is an important determinant of rates of organic matter decomposition the nature of the relationship between temperature and microbial respiration is far from clear (Davidson and Janssens 2006) There are several reasons for this uncertainty but key factors include potential for variations in organic matter quality to influence the temperature sensitivity of microbial decomposition (Fang et al 2005 Conen et al 2006 Davidson and Janssens 2006) and for environmental constraints such as physical and chemical protection of organic matter to decrease substrate availability for microbial attack and thereby dampen microbial responses to warming (Davidson and Janssens 2006) Also there is uncertainty about how reactive different microbial and faunal groups and species are to temperature change with several studies showing that soil microbial and animal communities are insensitive to small increases in temperature (eg Kandeler et al 1998 Bardgett et al 1999 Wardle 2002) whereas others show that soil organisms and the carbon cycling processes that they drive are responsive to temperature change For instance the abundance of enchytraeid worms which dominate the fauna of acid peat soils have been shown to be strongly related to temperature and it is has been suggested that climate warming could increase their abundance leading to enhanced carbon mineralization and carbon loss from soil (Briones et al 1998 Cole et al 2002ab) Also a recent analysis by Gange et al (2007) related temporal shifts in autumnal fruiting patterns of macrofungi in southern England to shifts in climate and found that the average first fruiting date of 315 species is now earlier while last fruiting date is now later than was the case 56 years ago Their study also found that many species are now fruiting twice a year indicative of increased mycelial activity and possibly greater decomposition rates in ecosystems

Increases in the frequency of extreme weather events with climate change such as droughting and freezing may have an even greater effect on soil organisms and their activities than will overall changes in temperature and precipitation It is well know for example that droughting and freezing have substantial direct effects on microbial physiology and the composition of the soil microbial community with important consequences for ecosystem-level carbon dynamics (Schimel et al 2007) For example increased drought and drying in wetlands and peatlands which will lower the water

Page 9

table and introduce oxygen into previously anaerobic soil will create a more favorable environment for microbial activity (Freeman et al 2004) potentially enhancing the activity of enzymes (eg phenol oxidases) which play a pivotal role in the breakdown of recalcitrant organic matter (Freeman et al 2004) Because peatlands and wetlands represent amongst the largest stocks of terrestrial carbon globally (Ward et al 2007) such enhanced breakdown of recalcitrant organic matter under drying could have major implications for the global carbon cycle (Freeman et al 2004) Before leaving this topic it is important to note that methanogenic pathways are also affected by increased oxygen availability associated with drought in that methane emissions are reduced by toxic effects of oxygen on methanogens (Roulet and Moore 1995 Freeman et al 2002) Also drought can have marked effects on nitrous oxide emission from soils a potent greenhouse gas that is increasing in atmospheric concentrations at the rate of 02ndash03 per year (Houghton et al 1996) However responses depend on the severity of drought in that modest summer drought is likely to have limited effect on soil nitrous oxide emissions whereas more extreme drought can greatly increase them (Dowrick et al 1999)

The majority of studies to date that have explored effects of climate change on biological systems and soil organisms have considered single factors such as elevated atmospheric carbon dioxide concentration warming and drought However there is much potential for interactions between these factors to have additive or antagonistic effects on soil organisms and the activities that they drive (Mikkelsen et al 2008 Bardgett et al 2008 Tylianakis et al 2008) Very little is known about the influence of multiple and interacting climate drivers on soil organisms and their activities although some studies do point to strong non-additive belowground effects of these drivers with feedback consequences for carbon exchange For instance microbial decomposition of peat was found to be significantly greater when subject to both elevated temperature and atmospheric carbon dioxide than when these factors were each elevated singly (Fenner et al 2007ab) thereby potentially causing an even stronger feedback on carbon loss from soil as dissolved organic carbon in drainage water and respiration Added to this complexity is our knowledge that other organisms and trophic groups that influence soil microbes directly such as microbial-feeding fauna will also respond to multiple climate change factors (Wardle 2002 Bardgett 2005 Tylianakis et al 2008) This complexity further hampers our ability to predict effects of multiple climate change drivers on soil biological communities and carbon exchange feedbacks

In addition to multiple climate change drivers soil organisms and their activities are also affected substantially by other global change phenomena such as nitrogen deposition invasion of new species and land use change Perhaps the strongest driver is land use change (cf Sala et al 2000) and it is widely documented that changes in the intensity of land use or the conversion of natural vegetation to agriculture or forestry can have substantial and often strongly negative and irreversible effects on soil biological communities and their activities (Brussaard et al 1997 Wardle 2002 Bardgett 2005) One pattern that commonly emerges in the context of land use change is that intensification of farming including increased tillage fertilizer use and grazing is typically associated with an increased role of the bacterial-based energy channel relative to the fungal-based channel (Wardle 2002 Bardgett 2005 Bardgett and Wardle 2010) which is away from what would typically found in more stable late successional ecosystems with large fungalbacterial ratios (Harris 2009) As discussed above this increased bacterial role is associated with faster leakier nutrient cycling and more losses of nutrients and carbon in water and greenhouse gases to the atmosphere (Wardle et al 2004 van der Heijden et al 2008) In contrast low intensity management systems often encourage fungal-based soil food webs that are more similar to those of natural systems and tend to be associated with more efficient nutrient cycling (Bardgett and McAlister 1999 Gordon et al 2008) and enhanced soil carbon sequestration (De Deyn et al 2008) Although not tested global change drivers may alter the balance of communities in favour bacterial populations thereby accelerating rates of nutrient and carbon mineralization with implications for carbon sequestration and C loss to the atmosphere

Soil biological communities are also strongly affected by nitrogen enrichment which is of high relevance because anthropogenic activities have substantially increased global rates of nitrogen fixation and deposition (Schlesinger 2009) For instance it is well known that nitrogen enrichment can have direct and differential impacts on extracellular enzymes involved in decomposition processes This typically involves stimulation of the synthesis of cellulases which degrade labile high cellulose litter but suppression of the synthesis of ligninolytic enzymes by white rot fungi which decompose recalcitrant high lignin litter (Carreiro et al 2000 Waldrop et al 2004 Allison et al 2008) Also

Page 10

nitrogen enrichment is known to influence the abundance and diversity of different components of the soil microbial community including saprophytic fungi (Donnison et al 2000 Allison et al 2008) mycorrhizal fungi (Egerton-Warburton and Allen 2000 Frey et al 2004) and soil fauna (Scheu and Schaeffer 1998 Ettema et al 1999) which are also affected by climate change and are well known to have substantial effects on decomposition processes and ecosystem-level carbon exchange A recent meta-analysis on this topic revealed that soil microbial biomass declined 15 on average under nitrogen fertilization but that declines in abundance of microbes and fungi were more evident in studies of longer durations and with higher total amounts of nitrogen added (Treseder 2008) Moreover that study showed negative responses of microbial biomass to nitrogen fertilization to be significantly correlated with declines in soil carbon dioxide emissions indicating that moderate declines in microbial biomass under nitrogen fertilization may also have consequences for carbon fluxes However another meta-analysis of 109 studies across the globe revealed that nitrogen enrichment had no significant effect on net ecosystem carbon dioxide exchange in non-forest natural ecosystems but did increase methane and nitrous oxide emissions by 97 and 216 respectively (Liu and Greaver 2009) It was suggested therefore that any potential positive effects of nitrogen enrichment on the global terrestrial carbon sink should be offset by the stimulation of methane and nitrous oxide emissions which are more potent greenhouse gases than is carbon dioxide (Liu and Greaver 2009) Importantly nitrogen deposition and other global changes can also influence soil microbes and decomposition processes indirectly through altering vegetation composition and productivity and by alleviating progressive nitrogen limitation of plant growth which typically occurs under elevated atmospheric carbon dioxide (Finzi et al 2002 Luo et al 2004 de Graaff et al 2006)

The likely effect of drought during summers is well-appreciated but much less is known about the impacts of warmer wetter winters for which plants appear to have fewer adaptations to cope (Whitmore and Whalley 2009) Waterlogging becomes more likely with increased rainfall but at the same time root respiration is likely to increase in response to warmer temperatures There is thus a considerably raised risk of waterlogging of UK soils during the future winter months No additional impact of drought has been found on cereal yields following winter waterlogging and reasonable diversity and resistance to waterlogging has been found in UK cereal varieties (Dickin and Wright 2009 Dickin et al 2008) However soil-dwelling organisms may be at risk some earthworms for example are more intolerant of waterlogging than others (Chuang and Chen 2009) Earthworms are relatively well studied other species less so and in general macrofauna diversity is greatly reduced in flooded grasslands (Plum 2005) with opportunists becoming more abundant Microbes and plants compete for resources in waterlogged soils For example Blom (1999) reported that plants out-competed nitrifiers for ammonium in waterlogged soil It is not clear to what extent plants and microbes compete for oxygen

In general very little is known about the combined effects of global changes on soil biological communities and their activities but they clearly have the potential to amplify suppress or perhaps even neutralize climate change driven effects on soil microbes and their feedback to carbon exchange (Bardgett et al 2008) A recent synthesis by Tylianakis et al (2008) of data from 688 published studies on the effects of global change on biotic interactions in terrestrial ecosystems (including those that occur in the decomposer food web) highlighted that there is substantial variability among studies in both the magnitude and direction of effects of any given global change driver on any given type of biotic interaction Further that analysis highlighted that the unanticipated effects of multiple drivers acting simultaneously create major challenges in predicting future responses to global environmental change Experimental studies that simultaneously vary two or more global change drivers within the same experiment therefore have considerable promise for improving our understanding of how interactions involving soil communities and their effects on ecosystem-level processes may respond to current global change scenarios

Soil structural integrity and dynamics

The architecture of soil the ways in which particles are arranged in space so forming a stable connected pore space determines the habitat of soil dwelling organisms including plants This soil physical environment is mutable however Soil is hard or dusty but transmits gases readily when dry when wet it becomes soft and plastic and gas ingress becomes much reduced These two extremes are expected to become more prevalent with the changes in climate expected for the UK drier

Page 11

summers and wetter winters The presence of plants indirectly exacerbates the effects of climate change by extracting water in summer and oxygen for root respiration in the winter There is a greater risk of compaction with wetter more plastic soils with late-harvested crops such as potatoes or sugar beet and establishment afterwards Working day access to land may be reduced or more variable leading to damage to soil through inappropriate management (Section B Degradation) Drought may affect soil stability and structure and possibly encourage wind erosion Cecillon et al (2010) examined sites along a latitudinal mountain spatial climate gradient for aggregation and aggregate stability and showed that erodibility was linked to climate and therefore susceptible to change under a shifting climatic regime Other studies have shown effects on organisms associated with the genesis of aggregate structure For instance Eggleton et al (2009) demonstrated in southern England pasture woodland hat earthworm community structure was dependant on soil temperature and water This faunal group has long been established as being of critical importance in no and minimal-till systems both organic and inorganic with potential for declines in aggregate stability as a result of climate change linked to declines in earthworm abundance and shifts in earthworm community structure There are also emerging models linking earthworm population dynamics and soil structural components (Blanchart et al 2009) which offer the possibility of modelling a biotic and abiotic component simultaneously under different climate change scenarios with consequences for hydrology erodibility and trophic level effects

Kohler et al (2009) found that increased CO2 concentrations led to a significantly higher percentage of stable aggregates growing under Lectuca sativa in drought conditions and this was linked to increases in soil microbial biomass and inoculation with a vesicular arbuscular mycorrhizal fungus and plant-growth-promoting rhizobacterium Other workers (Rillig et al 2001) had found a similar effect of elevated carbon dioxide and increased water supply by irrigation on increased aggregate stability due to arbuscular mycorrhizal fungi in soils under Sorghum

Earlier work suggested that climate change would not affect accessibility to land unless winter rainfall increased by 15 (Rounsevell and Brignall 1994) Since this is now what is expected it may be necessary to re-calculate workable days for England based on up-to-date climate change scenarios Neither the direct effect of climate change on soil stability via wet-dry cycles nor its indirect effect via the soil fauna is certain and as Horn and Smucker (2005) have noted that changes in aggregate stability and soil structure can be undesirable if the soil becomes difficult to manage We need to better understand the processes underlying soil structure in order to predict direct soil response to climate change and we need to better understand the wider impact of climate change on soil ecosystems if we are to understand and predict the indirect effects of the soil fauna on soil

Warmer wetter winters may lead to increased competition for oxygen among more strongly respiring organisms in wetter soils into which oxygen penetration is slower Drier summers will lead to soils into which root penetration becomes restricted Both effects are likely to impact on the ability of plants to acquire nutrients and on biogeochemical cycles in general Research on waterlogging appears to have concluded in the 1980s that UK cereals could compensate provided waterlogging did not occur during establishment or repetitively (eg Belford et al 1985) While this may have been true of the conditions prevailing at the time the same may not be true for our future climate The effect that plant root extraction of oxygen has on soil fauna and microflora and vice versa appears to be poorly researched especially in the context of our expected climate change

In summary stability of soil is likely to be impacted by the increasing intensity of wet-dry cycles with climate change but note that an increase is not necessarily desirable if the soil becomes less workable Stepniewska and Stepniewska (2009) have stressed the need for a moderate stable redox above 300 mV Soil fauna and community structure is also likely to be impacted by a change in climate with effects on soil stability that are unclear It is also likely that with wetter winters the number of days when soil is safely accessible by heavy farm machinery without causing damage may become more variable and therefore unpredictable

Page 12

4 Methodologies for investigating the impacts of climate change on soil

Experiments on climate change drivers have been carried out over a variety of spatial and temporal scales ranging from short term laboratory incubation studies to ecosystem-level and long-term manipulations of climatic factors (Wullschleger and Strahl 2010) The main approaches for studying climate change include (1) the use of environmental gradients (temperature and water) and reciprocal transplants (2) in situ field manipulation experiments including Free-Air CO2 Enrichment (FACE) experiments for manipulation of atmospheric CO2 and field-scale manipulations of temperature and precipitation (3) controlled environment facilities such as the Ecotron controlled environment facilities at Imperial College Silwood Park UK and Montpellier France and (4) highly artificial often laboratory based microcosm experiments that have little relevance to real systems These approaches in the order listed above follow a spectrum of decreasing realism but increasing mechanistic control We discuss these approaches in turn

Environmental gradients (temperature and water) and reciprocal transplants

Climatic gradients for instance in annual precipitation and temperature that cross continents countries and elevation gradients are commonly used to determine impacts of climatic variation on soil biota and processes While useful for establishing general patterns such approaches leave significant questions about other factors that could explain differences in soil biota along climatic gradients such as soil fertility and mineralogy To overcome this problem an associated approach is the use of transplant experiments whereby intact soil-vegetation turves (or varying size) are transplanted at different places along climatic gradients so that effects of movement to another climate on soil biota can be assessed This approach for example was used by Briones et al (19971998) who transplanted peat soils from high to lower altitudes at Great Dunn Fell Cumbria to simulate climate warming and that this increased the density of enchytraeid worms the dominant fauna of these peat soils leading to enhanced decomposition and DOC concentrations in soil leachates The same system was also used by Tipping et al (1999) to show that warming and drying can accelerate the production of dissolved organic matter in organic soil horizons Such approaches are valuable in that they provide information on the response of soil biota and processes to real changes in climate but they are limited by the lack of control of environmental variables along transects and potential effects of disturbance from moving soil cores from one site to another

The further experimentation moves away from surveys and experiments in the field the less likely they are to represent real world systems This is not necessarily an issue when detailed and specific mechanisms are being explored but become increasingly problematic when large scale predictions are asserted from them

In situ field manipulation experiments

Many studies have used various field-based manipulations of climate including elevated carbon dioxide in the previously mentioned FACE experiments (eg Norby et al 2004 Jackson et al 2009) drought using rainfall roofs (eg Beier et al 2004) and artificial warming using heating cables (eg Grime et al 2008) passive night time warming roofs (eg Beier et al 2004) and infra-red lamps (Zhang et al 2005) Such experiments have contributed significantly to our understanding of the effects of different climate change drivers on vegetation soil biota and soil processes as detailed in the previous section However as stated previously most studies of this kind have explored effects of single climate factors whereas there is much potential for interactions between multiple factors to have additive or antagonistic effects on soil organisms and the activities that they drive (Bardgett et al 2008) Therefore future experiments which manipulate multiple climate change and other site factors are needed to better understand the effects of climate change on soil biota

As an example of in situ field manipulations Zhang et al (2005) artificially heated soils under tall grass prairie using infra-red heaters to simulate an increase in daily soil temperatures of 18 ndash 27oC and studied two clipping regimes clipped and unclipped In the heated treatments they found changes in the soil microbial community structure as determined using phospholipid fatty acid analysis (PLFA) in the unclipped plots with a shift to fungal dominance but not in the clipped

Page 6

7 Improved estimates of non-CO2 GHG balance (primarily N2O and CH4) of forest soils including predictions of the impacts of climate change and the effects of forest management extension to broadleaf woodland and deforestation activities is important

2 Climate change scenarios

UKCIP09 climate change predictions as based on medium emissions scenarios for 2080 predict that England and Wales will get warmer with summers showing a slightly greater (on average 4degC) increase in temperature than winters (on average 3degC Table 2) While temperatures are predicted to rise the annual amount of precipitation is not expected to change However the distribution of rainfall throughout the year is predicted to change Summer precipitation is predicted to decrease across England and Wales (Table 2) on average by -24 to -18 while winter precipitation is predicted to increase by between 14 and 23 Also there is expected to be an increased frequency of extreme weather occurrences such as heat waves dry spells heavy rain and flooding as well as rises in sea level Central estimates are for heavy rain days (rainfall greater than 25 mm) over most of the lowland UK to increase by a factor of between 2 and 35 in winter and 1 to 2 in summer by the 2080s under the medium emissions scenario (UKCP09)

Table 2 UKCIP09 central climate change predictions based on medium emission scenarios for 2080 (low and high probabilities given in brackets)

Administrative regions

Winter mean temperature (degC)

Summer mean temperature (degC)

Annual winter mean precipitation ()

Annual summer mean precipitation ()

Wales 28 (1642) 35 (1958) 19 (442) -20 (-435) North East England 26 (1441) 37 (2058) 14 (232) -18 (-361)

East of England 30 (1647) 36 (1959) 20 (444) -21 (-456) South West England 28 (1643) 39 (2164) 23 (654) -24 (-506)

South East England 30 (1647) 39 (2065) 22 (451) -23 (-487)

West Midlands 29 (1644) 37 (2061) 17 (338) -20 (-446) East Midlands 30 (1646) 35 (1858) 19 (341) -20 (-446) Yorkshire and Humber 30 (1646) 33 (1754) 15 (233) -23 (-440)

North West England 26 (1440) 37 (2059) 16 (334) -22 (-430)

Mean 29 36 18 -21

The south west of England is predicted to experience the greatest increase in summer temperatures as well as the highest predicted increase in winter mean precipitation and lowest summer mean precipitation of all regions in England and Wales (Table 2) while the east of England south east England and Yorkshire and Humber are predicted to have some of the mildest winter temperatures The north east of England is predicted to experience a less extreme change in winter and summer precipitation

The predictions made by UKCP09 are supported by resent observed trends in UK climate reported by Jenkins et al (2009) Global average temperatures have risen by nearly 02degCdecade over the past 25 years In central England temperatures have risen by about a degree Celsius since the 1970s Annual mean precipitation in England and Wales has not changed significantly although summers do appear to be drier and winters wetter Over the past 45 years there has been an increase in heavy winter rainfall events Severe windstorms around the UK have become more frequent in the past few decades

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UKCP09 predictions are broadly consistent with UKCIP02 predictions Comparisons of UKCIP02 and UKCP09 by Jenkins et al (2009) suggest mean temperature projections are generally greater and summer reduction in rainfall is not as great using UKCP09 The range of increase in winter rainfall is broadly similar with a different geographical pattern Decreases in cloud cover in summer are also broadly in agreement Therefore observations made by Bradley et al (2005) with regard to impact of climate change on soil function are still valid Bradley et al (2005) defined both direct and indirect impacts of climate change on soil functions and these are summarised in Section 1 Table 1 Subsequently there has been more attention paid to the impact of climate change on soil biota and its impact on soil processes and functions This new information is summarised in Table 3

Table 3 Potential implications of predicted climate change on soil biota

Climate change Implications for soil biota

Warmer springs bull Changes in timings of seasonal events may cause loss of synchrony between species and the availability of food (Hopkins et al 2007 Newton et al 2008)

Warmer and drier summers

bull Reduced soil moisture content may limit plant production without additional irrigation

bull Drier soils may affect the mobility of soil fauna such as nematodes and earthworms (Bardgett 2005 Eggleton et al 2009)

bull Changes to habitat may favour drought tolerant soil biota soil may experience a shift in species which may impact on the over all function of the soil depending on redundancy in the system (Castro et al 2010)

bull Summer droughts may cause stress in some soil microbial communities and result in changes in fungal diversity impacting on functional diversity (Toberman et al 2008)

bull Drier conditions and higher temperatures may accelerate decomposition of organic material through increased oxygen availability and increased microbial activity However additional input of leaf litter from increased production may offset net loss of carbon from the soil profile (Dawson and Smith 2007)

bull Decreased loss of methane due to increased oxygen availability impacting on methanogens (McNamara et al 2006)

bull May cause shift in vegetation patterns with subsequent implications for soil biota (Pentildeuelas et al 2007)

Warmer and wetter winters

bull Increase the likely survival of soil pests and diseases (Newton et al 2008)

bull Inward migration of soil biota from warmer areas

bull Water logging will reduce the availability of oxygen in the soil profile affecting both soil fauna and soil flora (Sowerby et al 2008)

bull Soil compaction will impede root penetration and may restrict soil fauna movement within the soil profile (Whally et al 1995)

bull May cause shift in vegetation patterns with subsequent implications for soil biota (Pentildeuelas et al 2007)

Extreme events bull Drying of the top soil followed by sudden rewetting encourages flushes of microbial activity and nutrient loss from soil (Sowerby et al 2008 Gordon et al 2008)

Increased CO2 bull Increased transfer of C through root system into the soil stimulating

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Climate change Implications for soil biota

microbial abundance and activity (Castro et al 2010)

bull Increased transfer of C to the soil stimulating mycorrhizal fungi which may stimulate nutrient transfer (Tyliankis et al 2008)

bull Stimulation of microbial biomass can lead to microbial immobilization of N thereby enforcing plant N limitation (de Graaff et al 2007)

bull May cause shift in vegetation patterns with subsequent implications for soil biota

Section 3 Potential impacts of climate change on soil processes function and biota

Carbon and nutrient cycling

Climate change has both direct and indirect effects on soil organisms and the processes that they drive often with consequences for the return greenhouse gases to the atmosphere Direct effects include the influence of temperature changing precipitation and extreme climatic events on soil organisms and the processes that they drive whereas indirect effects result from climate-driven changes in plant productivity and species composition which alter soil physicochemical conditions the supply of carbon to soil and the structure and activity of microbial communities involved in decomposition processes and carbon release from soil (Bardgett et al 2008)

One of the most commonly discussed contributions of soil organisms to climate change is their role in soil organic matter decomposition and the idea that warming will accelerate rates of heterotrophic microbial activity thereby increasing the transfer of carbon dioxide from soil to the atmosphere and exports of dissolved organic carbon by hydrologic leaching (Jenkinson et al 1991 Davidson and Janssens 2006) The concern here is that because rates of soil respiration are more sensitive than is primary production to temperature (Jenkinson et al 1991 Schimel et al 1994) it is thought that climate warming will increase the net transfer of carbon from soil to atmosphere thus creating a positive feedback on climate change (Cox et al 2000) Although it is well known that temperature is an important determinant of rates of organic matter decomposition the nature of the relationship between temperature and microbial respiration is far from clear (Davidson and Janssens 2006) There are several reasons for this uncertainty but key factors include potential for variations in organic matter quality to influence the temperature sensitivity of microbial decomposition (Fang et al 2005 Conen et al 2006 Davidson and Janssens 2006) and for environmental constraints such as physical and chemical protection of organic matter to decrease substrate availability for microbial attack and thereby dampen microbial responses to warming (Davidson and Janssens 2006) Also there is uncertainty about how reactive different microbial and faunal groups and species are to temperature change with several studies showing that soil microbial and animal communities are insensitive to small increases in temperature (eg Kandeler et al 1998 Bardgett et al 1999 Wardle 2002) whereas others show that soil organisms and the carbon cycling processes that they drive are responsive to temperature change For instance the abundance of enchytraeid worms which dominate the fauna of acid peat soils have been shown to be strongly related to temperature and it is has been suggested that climate warming could increase their abundance leading to enhanced carbon mineralization and carbon loss from soil (Briones et al 1998 Cole et al 2002ab) Also a recent analysis by Gange et al (2007) related temporal shifts in autumnal fruiting patterns of macrofungi in southern England to shifts in climate and found that the average first fruiting date of 315 species is now earlier while last fruiting date is now later than was the case 56 years ago Their study also found that many species are now fruiting twice a year indicative of increased mycelial activity and possibly greater decomposition rates in ecosystems

Increases in the frequency of extreme weather events with climate change such as droughting and freezing may have an even greater effect on soil organisms and their activities than will overall changes in temperature and precipitation It is well know for example that droughting and freezing have substantial direct effects on microbial physiology and the composition of the soil microbial community with important consequences for ecosystem-level carbon dynamics (Schimel et al 2007) For example increased drought and drying in wetlands and peatlands which will lower the water

Page 9

table and introduce oxygen into previously anaerobic soil will create a more favorable environment for microbial activity (Freeman et al 2004) potentially enhancing the activity of enzymes (eg phenol oxidases) which play a pivotal role in the breakdown of recalcitrant organic matter (Freeman et al 2004) Because peatlands and wetlands represent amongst the largest stocks of terrestrial carbon globally (Ward et al 2007) such enhanced breakdown of recalcitrant organic matter under drying could have major implications for the global carbon cycle (Freeman et al 2004) Before leaving this topic it is important to note that methanogenic pathways are also affected by increased oxygen availability associated with drought in that methane emissions are reduced by toxic effects of oxygen on methanogens (Roulet and Moore 1995 Freeman et al 2002) Also drought can have marked effects on nitrous oxide emission from soils a potent greenhouse gas that is increasing in atmospheric concentrations at the rate of 02ndash03 per year (Houghton et al 1996) However responses depend on the severity of drought in that modest summer drought is likely to have limited effect on soil nitrous oxide emissions whereas more extreme drought can greatly increase them (Dowrick et al 1999)

The majority of studies to date that have explored effects of climate change on biological systems and soil organisms have considered single factors such as elevated atmospheric carbon dioxide concentration warming and drought However there is much potential for interactions between these factors to have additive or antagonistic effects on soil organisms and the activities that they drive (Mikkelsen et al 2008 Bardgett et al 2008 Tylianakis et al 2008) Very little is known about the influence of multiple and interacting climate drivers on soil organisms and their activities although some studies do point to strong non-additive belowground effects of these drivers with feedback consequences for carbon exchange For instance microbial decomposition of peat was found to be significantly greater when subject to both elevated temperature and atmospheric carbon dioxide than when these factors were each elevated singly (Fenner et al 2007ab) thereby potentially causing an even stronger feedback on carbon loss from soil as dissolved organic carbon in drainage water and respiration Added to this complexity is our knowledge that other organisms and trophic groups that influence soil microbes directly such as microbial-feeding fauna will also respond to multiple climate change factors (Wardle 2002 Bardgett 2005 Tylianakis et al 2008) This complexity further hampers our ability to predict effects of multiple climate change drivers on soil biological communities and carbon exchange feedbacks

In addition to multiple climate change drivers soil organisms and their activities are also affected substantially by other global change phenomena such as nitrogen deposition invasion of new species and land use change Perhaps the strongest driver is land use change (cf Sala et al 2000) and it is widely documented that changes in the intensity of land use or the conversion of natural vegetation to agriculture or forestry can have substantial and often strongly negative and irreversible effects on soil biological communities and their activities (Brussaard et al 1997 Wardle 2002 Bardgett 2005) One pattern that commonly emerges in the context of land use change is that intensification of farming including increased tillage fertilizer use and grazing is typically associated with an increased role of the bacterial-based energy channel relative to the fungal-based channel (Wardle 2002 Bardgett 2005 Bardgett and Wardle 2010) which is away from what would typically found in more stable late successional ecosystems with large fungalbacterial ratios (Harris 2009) As discussed above this increased bacterial role is associated with faster leakier nutrient cycling and more losses of nutrients and carbon in water and greenhouse gases to the atmosphere (Wardle et al 2004 van der Heijden et al 2008) In contrast low intensity management systems often encourage fungal-based soil food webs that are more similar to those of natural systems and tend to be associated with more efficient nutrient cycling (Bardgett and McAlister 1999 Gordon et al 2008) and enhanced soil carbon sequestration (De Deyn et al 2008) Although not tested global change drivers may alter the balance of communities in favour bacterial populations thereby accelerating rates of nutrient and carbon mineralization with implications for carbon sequestration and C loss to the atmosphere

Soil biological communities are also strongly affected by nitrogen enrichment which is of high relevance because anthropogenic activities have substantially increased global rates of nitrogen fixation and deposition (Schlesinger 2009) For instance it is well known that nitrogen enrichment can have direct and differential impacts on extracellular enzymes involved in decomposition processes This typically involves stimulation of the synthesis of cellulases which degrade labile high cellulose litter but suppression of the synthesis of ligninolytic enzymes by white rot fungi which decompose recalcitrant high lignin litter (Carreiro et al 2000 Waldrop et al 2004 Allison et al 2008) Also

Page 10

nitrogen enrichment is known to influence the abundance and diversity of different components of the soil microbial community including saprophytic fungi (Donnison et al 2000 Allison et al 2008) mycorrhizal fungi (Egerton-Warburton and Allen 2000 Frey et al 2004) and soil fauna (Scheu and Schaeffer 1998 Ettema et al 1999) which are also affected by climate change and are well known to have substantial effects on decomposition processes and ecosystem-level carbon exchange A recent meta-analysis on this topic revealed that soil microbial biomass declined 15 on average under nitrogen fertilization but that declines in abundance of microbes and fungi were more evident in studies of longer durations and with higher total amounts of nitrogen added (Treseder 2008) Moreover that study showed negative responses of microbial biomass to nitrogen fertilization to be significantly correlated with declines in soil carbon dioxide emissions indicating that moderate declines in microbial biomass under nitrogen fertilization may also have consequences for carbon fluxes However another meta-analysis of 109 studies across the globe revealed that nitrogen enrichment had no significant effect on net ecosystem carbon dioxide exchange in non-forest natural ecosystems but did increase methane and nitrous oxide emissions by 97 and 216 respectively (Liu and Greaver 2009) It was suggested therefore that any potential positive effects of nitrogen enrichment on the global terrestrial carbon sink should be offset by the stimulation of methane and nitrous oxide emissions which are more potent greenhouse gases than is carbon dioxide (Liu and Greaver 2009) Importantly nitrogen deposition and other global changes can also influence soil microbes and decomposition processes indirectly through altering vegetation composition and productivity and by alleviating progressive nitrogen limitation of plant growth which typically occurs under elevated atmospheric carbon dioxide (Finzi et al 2002 Luo et al 2004 de Graaff et al 2006)

The likely effect of drought during summers is well-appreciated but much less is known about the impacts of warmer wetter winters for which plants appear to have fewer adaptations to cope (Whitmore and Whalley 2009) Waterlogging becomes more likely with increased rainfall but at the same time root respiration is likely to increase in response to warmer temperatures There is thus a considerably raised risk of waterlogging of UK soils during the future winter months No additional impact of drought has been found on cereal yields following winter waterlogging and reasonable diversity and resistance to waterlogging has been found in UK cereal varieties (Dickin and Wright 2009 Dickin et al 2008) However soil-dwelling organisms may be at risk some earthworms for example are more intolerant of waterlogging than others (Chuang and Chen 2009) Earthworms are relatively well studied other species less so and in general macrofauna diversity is greatly reduced in flooded grasslands (Plum 2005) with opportunists becoming more abundant Microbes and plants compete for resources in waterlogged soils For example Blom (1999) reported that plants out-competed nitrifiers for ammonium in waterlogged soil It is not clear to what extent plants and microbes compete for oxygen

In general very little is known about the combined effects of global changes on soil biological communities and their activities but they clearly have the potential to amplify suppress or perhaps even neutralize climate change driven effects on soil microbes and their feedback to carbon exchange (Bardgett et al 2008) A recent synthesis by Tylianakis et al (2008) of data from 688 published studies on the effects of global change on biotic interactions in terrestrial ecosystems (including those that occur in the decomposer food web) highlighted that there is substantial variability among studies in both the magnitude and direction of effects of any given global change driver on any given type of biotic interaction Further that analysis highlighted that the unanticipated effects of multiple drivers acting simultaneously create major challenges in predicting future responses to global environmental change Experimental studies that simultaneously vary two or more global change drivers within the same experiment therefore have considerable promise for improving our understanding of how interactions involving soil communities and their effects on ecosystem-level processes may respond to current global change scenarios

Soil structural integrity and dynamics

The architecture of soil the ways in which particles are arranged in space so forming a stable connected pore space determines the habitat of soil dwelling organisms including plants This soil physical environment is mutable however Soil is hard or dusty but transmits gases readily when dry when wet it becomes soft and plastic and gas ingress becomes much reduced These two extremes are expected to become more prevalent with the changes in climate expected for the UK drier

Page 11

summers and wetter winters The presence of plants indirectly exacerbates the effects of climate change by extracting water in summer and oxygen for root respiration in the winter There is a greater risk of compaction with wetter more plastic soils with late-harvested crops such as potatoes or sugar beet and establishment afterwards Working day access to land may be reduced or more variable leading to damage to soil through inappropriate management (Section B Degradation) Drought may affect soil stability and structure and possibly encourage wind erosion Cecillon et al (2010) examined sites along a latitudinal mountain spatial climate gradient for aggregation and aggregate stability and showed that erodibility was linked to climate and therefore susceptible to change under a shifting climatic regime Other studies have shown effects on organisms associated with the genesis of aggregate structure For instance Eggleton et al (2009) demonstrated in southern England pasture woodland hat earthworm community structure was dependant on soil temperature and water This faunal group has long been established as being of critical importance in no and minimal-till systems both organic and inorganic with potential for declines in aggregate stability as a result of climate change linked to declines in earthworm abundance and shifts in earthworm community structure There are also emerging models linking earthworm population dynamics and soil structural components (Blanchart et al 2009) which offer the possibility of modelling a biotic and abiotic component simultaneously under different climate change scenarios with consequences for hydrology erodibility and trophic level effects

Kohler et al (2009) found that increased CO2 concentrations led to a significantly higher percentage of stable aggregates growing under Lectuca sativa in drought conditions and this was linked to increases in soil microbial biomass and inoculation with a vesicular arbuscular mycorrhizal fungus and plant-growth-promoting rhizobacterium Other workers (Rillig et al 2001) had found a similar effect of elevated carbon dioxide and increased water supply by irrigation on increased aggregate stability due to arbuscular mycorrhizal fungi in soils under Sorghum

Earlier work suggested that climate change would not affect accessibility to land unless winter rainfall increased by 15 (Rounsevell and Brignall 1994) Since this is now what is expected it may be necessary to re-calculate workable days for England based on up-to-date climate change scenarios Neither the direct effect of climate change on soil stability via wet-dry cycles nor its indirect effect via the soil fauna is certain and as Horn and Smucker (2005) have noted that changes in aggregate stability and soil structure can be undesirable if the soil becomes difficult to manage We need to better understand the processes underlying soil structure in order to predict direct soil response to climate change and we need to better understand the wider impact of climate change on soil ecosystems if we are to understand and predict the indirect effects of the soil fauna on soil

Warmer wetter winters may lead to increased competition for oxygen among more strongly respiring organisms in wetter soils into which oxygen penetration is slower Drier summers will lead to soils into which root penetration becomes restricted Both effects are likely to impact on the ability of plants to acquire nutrients and on biogeochemical cycles in general Research on waterlogging appears to have concluded in the 1980s that UK cereals could compensate provided waterlogging did not occur during establishment or repetitively (eg Belford et al 1985) While this may have been true of the conditions prevailing at the time the same may not be true for our future climate The effect that plant root extraction of oxygen has on soil fauna and microflora and vice versa appears to be poorly researched especially in the context of our expected climate change

In summary stability of soil is likely to be impacted by the increasing intensity of wet-dry cycles with climate change but note that an increase is not necessarily desirable if the soil becomes less workable Stepniewska and Stepniewska (2009) have stressed the need for a moderate stable redox above 300 mV Soil fauna and community structure is also likely to be impacted by a change in climate with effects on soil stability that are unclear It is also likely that with wetter winters the number of days when soil is safely accessible by heavy farm machinery without causing damage may become more variable and therefore unpredictable

Page 12

4 Methodologies for investigating the impacts of climate change on soil

Experiments on climate change drivers have been carried out over a variety of spatial and temporal scales ranging from short term laboratory incubation studies to ecosystem-level and long-term manipulations of climatic factors (Wullschleger and Strahl 2010) The main approaches for studying climate change include (1) the use of environmental gradients (temperature and water) and reciprocal transplants (2) in situ field manipulation experiments including Free-Air CO2 Enrichment (FACE) experiments for manipulation of atmospheric CO2 and field-scale manipulations of temperature and precipitation (3) controlled environment facilities such as the Ecotron controlled environment facilities at Imperial College Silwood Park UK and Montpellier France and (4) highly artificial often laboratory based microcosm experiments that have little relevance to real systems These approaches in the order listed above follow a spectrum of decreasing realism but increasing mechanistic control We discuss these approaches in turn

Environmental gradients (temperature and water) and reciprocal transplants

Climatic gradients for instance in annual precipitation and temperature that cross continents countries and elevation gradients are commonly used to determine impacts of climatic variation on soil biota and processes While useful for establishing general patterns such approaches leave significant questions about other factors that could explain differences in soil biota along climatic gradients such as soil fertility and mineralogy To overcome this problem an associated approach is the use of transplant experiments whereby intact soil-vegetation turves (or varying size) are transplanted at different places along climatic gradients so that effects of movement to another climate on soil biota can be assessed This approach for example was used by Briones et al (19971998) who transplanted peat soils from high to lower altitudes at Great Dunn Fell Cumbria to simulate climate warming and that this increased the density of enchytraeid worms the dominant fauna of these peat soils leading to enhanced decomposition and DOC concentrations in soil leachates The same system was also used by Tipping et al (1999) to show that warming and drying can accelerate the production of dissolved organic matter in organic soil horizons Such approaches are valuable in that they provide information on the response of soil biota and processes to real changes in climate but they are limited by the lack of control of environmental variables along transects and potential effects of disturbance from moving soil cores from one site to another

The further experimentation moves away from surveys and experiments in the field the less likely they are to represent real world systems This is not necessarily an issue when detailed and specific mechanisms are being explored but become increasingly problematic when large scale predictions are asserted from them

In situ field manipulation experiments

Many studies have used various field-based manipulations of climate including elevated carbon dioxide in the previously mentioned FACE experiments (eg Norby et al 2004 Jackson et al 2009) drought using rainfall roofs (eg Beier et al 2004) and artificial warming using heating cables (eg Grime et al 2008) passive night time warming roofs (eg Beier et al 2004) and infra-red lamps (Zhang et al 2005) Such experiments have contributed significantly to our understanding of the effects of different climate change drivers on vegetation soil biota and soil processes as detailed in the previous section However as stated previously most studies of this kind have explored effects of single climate factors whereas there is much potential for interactions between multiple factors to have additive or antagonistic effects on soil organisms and the activities that they drive (Bardgett et al 2008) Therefore future experiments which manipulate multiple climate change and other site factors are needed to better understand the effects of climate change on soil biota

As an example of in situ field manipulations Zhang et al (2005) artificially heated soils under tall grass prairie using infra-red heaters to simulate an increase in daily soil temperatures of 18 ndash 27oC and studied two clipping regimes clipped and unclipped In the heated treatments they found changes in the soil microbial community structure as determined using phospholipid fatty acid analysis (PLFA) in the unclipped plots with a shift to fungal dominance but not in the clipped

Page 7

UKCP09 predictions are broadly consistent with UKCIP02 predictions Comparisons of UKCIP02 and UKCP09 by Jenkins et al (2009) suggest mean temperature projections are generally greater and summer reduction in rainfall is not as great using UKCP09 The range of increase in winter rainfall is broadly similar with a different geographical pattern Decreases in cloud cover in summer are also broadly in agreement Therefore observations made by Bradley et al (2005) with regard to impact of climate change on soil function are still valid Bradley et al (2005) defined both direct and indirect impacts of climate change on soil functions and these are summarised in Section 1 Table 1 Subsequently there has been more attention paid to the impact of climate change on soil biota and its impact on soil processes and functions This new information is summarised in Table 3

Table 3 Potential implications of predicted climate change on soil biota

Climate change Implications for soil biota

Warmer springs bull Changes in timings of seasonal events may cause loss of synchrony between species and the availability of food (Hopkins et al 2007 Newton et al 2008)

Warmer and drier summers

bull Reduced soil moisture content may limit plant production without additional irrigation

bull Drier soils may affect the mobility of soil fauna such as nematodes and earthworms (Bardgett 2005 Eggleton et al 2009)

bull Changes to habitat may favour drought tolerant soil biota soil may experience a shift in species which may impact on the over all function of the soil depending on redundancy in the system (Castro et al 2010)

bull Summer droughts may cause stress in some soil microbial communities and result in changes in fungal diversity impacting on functional diversity (Toberman et al 2008)

bull Drier conditions and higher temperatures may accelerate decomposition of organic material through increased oxygen availability and increased microbial activity However additional input of leaf litter from increased production may offset net loss of carbon from the soil profile (Dawson and Smith 2007)

bull Decreased loss of methane due to increased oxygen availability impacting on methanogens (McNamara et al 2006)

bull May cause shift in vegetation patterns with subsequent implications for soil biota (Pentildeuelas et al 2007)

Warmer and wetter winters

bull Increase the likely survival of soil pests and diseases (Newton et al 2008)

bull Inward migration of soil biota from warmer areas

bull Water logging will reduce the availability of oxygen in the soil profile affecting both soil fauna and soil flora (Sowerby et al 2008)

bull Soil compaction will impede root penetration and may restrict soil fauna movement within the soil profile (Whally et al 1995)

bull May cause shift in vegetation patterns with subsequent implications for soil biota (Pentildeuelas et al 2007)

Extreme events bull Drying of the top soil followed by sudden rewetting encourages flushes of microbial activity and nutrient loss from soil (Sowerby et al 2008 Gordon et al 2008)

Increased CO2 bull Increased transfer of C through root system into the soil stimulating

Page 8

Climate change Implications for soil biota

microbial abundance and activity (Castro et al 2010)

bull Increased transfer of C to the soil stimulating mycorrhizal fungi which may stimulate nutrient transfer (Tyliankis et al 2008)

bull Stimulation of microbial biomass can lead to microbial immobilization of N thereby enforcing plant N limitation (de Graaff et al 2007)

bull May cause shift in vegetation patterns with subsequent implications for soil biota

Section 3 Potential impacts of climate change on soil processes function and biota

Carbon and nutrient cycling

Climate change has both direct and indirect effects on soil organisms and the processes that they drive often with consequences for the return greenhouse gases to the atmosphere Direct effects include the influence of temperature changing precipitation and extreme climatic events on soil organisms and the processes that they drive whereas indirect effects result from climate-driven changes in plant productivity and species composition which alter soil physicochemical conditions the supply of carbon to soil and the structure and activity of microbial communities involved in decomposition processes and carbon release from soil (Bardgett et al 2008)

One of the most commonly discussed contributions of soil organisms to climate change is their role in soil organic matter decomposition and the idea that warming will accelerate rates of heterotrophic microbial activity thereby increasing the transfer of carbon dioxide from soil to the atmosphere and exports of dissolved organic carbon by hydrologic leaching (Jenkinson et al 1991 Davidson and Janssens 2006) The concern here is that because rates of soil respiration are more sensitive than is primary production to temperature (Jenkinson et al 1991 Schimel et al 1994) it is thought that climate warming will increase the net transfer of carbon from soil to atmosphere thus creating a positive feedback on climate change (Cox et al 2000) Although it is well known that temperature is an important determinant of rates of organic matter decomposition the nature of the relationship between temperature and microbial respiration is far from clear (Davidson and Janssens 2006) There are several reasons for this uncertainty but key factors include potential for variations in organic matter quality to influence the temperature sensitivity of microbial decomposition (Fang et al 2005 Conen et al 2006 Davidson and Janssens 2006) and for environmental constraints such as physical and chemical protection of organic matter to decrease substrate availability for microbial attack and thereby dampen microbial responses to warming (Davidson and Janssens 2006) Also there is uncertainty about how reactive different microbial and faunal groups and species are to temperature change with several studies showing that soil microbial and animal communities are insensitive to small increases in temperature (eg Kandeler et al 1998 Bardgett et al 1999 Wardle 2002) whereas others show that soil organisms and the carbon cycling processes that they drive are responsive to temperature change For instance the abundance of enchytraeid worms which dominate the fauna of acid peat soils have been shown to be strongly related to temperature and it is has been suggested that climate warming could increase their abundance leading to enhanced carbon mineralization and carbon loss from soil (Briones et al 1998 Cole et al 2002ab) Also a recent analysis by Gange et al (2007) related temporal shifts in autumnal fruiting patterns of macrofungi in southern England to shifts in climate and found that the average first fruiting date of 315 species is now earlier while last fruiting date is now later than was the case 56 years ago Their study also found that many species are now fruiting twice a year indicative of increased mycelial activity and possibly greater decomposition rates in ecosystems

Increases in the frequency of extreme weather events with climate change such as droughting and freezing may have an even greater effect on soil organisms and their activities than will overall changes in temperature and precipitation It is well know for example that droughting and freezing have substantial direct effects on microbial physiology and the composition of the soil microbial community with important consequences for ecosystem-level carbon dynamics (Schimel et al 2007) For example increased drought and drying in wetlands and peatlands which will lower the water

Page 9

table and introduce oxygen into previously anaerobic soil will create a more favorable environment for microbial activity (Freeman et al 2004) potentially enhancing the activity of enzymes (eg phenol oxidases) which play a pivotal role in the breakdown of recalcitrant organic matter (Freeman et al 2004) Because peatlands and wetlands represent amongst the largest stocks of terrestrial carbon globally (Ward et al 2007) such enhanced breakdown of recalcitrant organic matter under drying could have major implications for the global carbon cycle (Freeman et al 2004) Before leaving this topic it is important to note that methanogenic pathways are also affected by increased oxygen availability associated with drought in that methane emissions are reduced by toxic effects of oxygen on methanogens (Roulet and Moore 1995 Freeman et al 2002) Also drought can have marked effects on nitrous oxide emission from soils a potent greenhouse gas that is increasing in atmospheric concentrations at the rate of 02ndash03 per year (Houghton et al 1996) However responses depend on the severity of drought in that modest summer drought is likely to have limited effect on soil nitrous oxide emissions whereas more extreme drought can greatly increase them (Dowrick et al 1999)

The majority of studies to date that have explored effects of climate change on biological systems and soil organisms have considered single factors such as elevated atmospheric carbon dioxide concentration warming and drought However there is much potential for interactions between these factors to have additive or antagonistic effects on soil organisms and the activities that they drive (Mikkelsen et al 2008 Bardgett et al 2008 Tylianakis et al 2008) Very little is known about the influence of multiple and interacting climate drivers on soil organisms and their activities although some studies do point to strong non-additive belowground effects of these drivers with feedback consequences for carbon exchange For instance microbial decomposition of peat was found to be significantly greater when subject to both elevated temperature and atmospheric carbon dioxide than when these factors were each elevated singly (Fenner et al 2007ab) thereby potentially causing an even stronger feedback on carbon loss from soil as dissolved organic carbon in drainage water and respiration Added to this complexity is our knowledge that other organisms and trophic groups that influence soil microbes directly such as microbial-feeding fauna will also respond to multiple climate change factors (Wardle 2002 Bardgett 2005 Tylianakis et al 2008) This complexity further hampers our ability to predict effects of multiple climate change drivers on soil biological communities and carbon exchange feedbacks

In addition to multiple climate change drivers soil organisms and their activities are also affected substantially by other global change phenomena such as nitrogen deposition invasion of new species and land use change Perhaps the strongest driver is land use change (cf Sala et al 2000) and it is widely documented that changes in the intensity of land use or the conversion of natural vegetation to agriculture or forestry can have substantial and often strongly negative and irreversible effects on soil biological communities and their activities (Brussaard et al 1997 Wardle 2002 Bardgett 2005) One pattern that commonly emerges in the context of land use change is that intensification of farming including increased tillage fertilizer use and grazing is typically associated with an increased role of the bacterial-based energy channel relative to the fungal-based channel (Wardle 2002 Bardgett 2005 Bardgett and Wardle 2010) which is away from what would typically found in more stable late successional ecosystems with large fungalbacterial ratios (Harris 2009) As discussed above this increased bacterial role is associated with faster leakier nutrient cycling and more losses of nutrients and carbon in water and greenhouse gases to the atmosphere (Wardle et al 2004 van der Heijden et al 2008) In contrast low intensity management systems often encourage fungal-based soil food webs that are more similar to those of natural systems and tend to be associated with more efficient nutrient cycling (Bardgett and McAlister 1999 Gordon et al 2008) and enhanced soil carbon sequestration (De Deyn et al 2008) Although not tested global change drivers may alter the balance of communities in favour bacterial populations thereby accelerating rates of nutrient and carbon mineralization with implications for carbon sequestration and C loss to the atmosphere

Soil biological communities are also strongly affected by nitrogen enrichment which is of high relevance because anthropogenic activities have substantially increased global rates of nitrogen fixation and deposition (Schlesinger 2009) For instance it is well known that nitrogen enrichment can have direct and differential impacts on extracellular enzymes involved in decomposition processes This typically involves stimulation of the synthesis of cellulases which degrade labile high cellulose litter but suppression of the synthesis of ligninolytic enzymes by white rot fungi which decompose recalcitrant high lignin litter (Carreiro et al 2000 Waldrop et al 2004 Allison et al 2008) Also

Page 10

nitrogen enrichment is known to influence the abundance and diversity of different components of the soil microbial community including saprophytic fungi (Donnison et al 2000 Allison et al 2008) mycorrhizal fungi (Egerton-Warburton and Allen 2000 Frey et al 2004) and soil fauna (Scheu and Schaeffer 1998 Ettema et al 1999) which are also affected by climate change and are well known to have substantial effects on decomposition processes and ecosystem-level carbon exchange A recent meta-analysis on this topic revealed that soil microbial biomass declined 15 on average under nitrogen fertilization but that declines in abundance of microbes and fungi were more evident in studies of longer durations and with higher total amounts of nitrogen added (Treseder 2008) Moreover that study showed negative responses of microbial biomass to nitrogen fertilization to be significantly correlated with declines in soil carbon dioxide emissions indicating that moderate declines in microbial biomass under nitrogen fertilization may also have consequences for carbon fluxes However another meta-analysis of 109 studies across the globe revealed that nitrogen enrichment had no significant effect on net ecosystem carbon dioxide exchange in non-forest natural ecosystems but did increase methane and nitrous oxide emissions by 97 and 216 respectively (Liu and Greaver 2009) It was suggested therefore that any potential positive effects of nitrogen enrichment on the global terrestrial carbon sink should be offset by the stimulation of methane and nitrous oxide emissions which are more potent greenhouse gases than is carbon dioxide (Liu and Greaver 2009) Importantly nitrogen deposition and other global changes can also influence soil microbes and decomposition processes indirectly through altering vegetation composition and productivity and by alleviating progressive nitrogen limitation of plant growth which typically occurs under elevated atmospheric carbon dioxide (Finzi et al 2002 Luo et al 2004 de Graaff et al 2006)

The likely effect of drought during summers is well-appreciated but much less is known about the impacts of warmer wetter winters for which plants appear to have fewer adaptations to cope (Whitmore and Whalley 2009) Waterlogging becomes more likely with increased rainfall but at the same time root respiration is likely to increase in response to warmer temperatures There is thus a considerably raised risk of waterlogging of UK soils during the future winter months No additional impact of drought has been found on cereal yields following winter waterlogging and reasonable diversity and resistance to waterlogging has been found in UK cereal varieties (Dickin and Wright 2009 Dickin et al 2008) However soil-dwelling organisms may be at risk some earthworms for example are more intolerant of waterlogging than others (Chuang and Chen 2009) Earthworms are relatively well studied other species less so and in general macrofauna diversity is greatly reduced in flooded grasslands (Plum 2005) with opportunists becoming more abundant Microbes and plants compete for resources in waterlogged soils For example Blom (1999) reported that plants out-competed nitrifiers for ammonium in waterlogged soil It is not clear to what extent plants and microbes compete for oxygen

In general very little is known about the combined effects of global changes on soil biological communities and their activities but they clearly have the potential to amplify suppress or perhaps even neutralize climate change driven effects on soil microbes and their feedback to carbon exchange (Bardgett et al 2008) A recent synthesis by Tylianakis et al (2008) of data from 688 published studies on the effects of global change on biotic interactions in terrestrial ecosystems (including those that occur in the decomposer food web) highlighted that there is substantial variability among studies in both the magnitude and direction of effects of any given global change driver on any given type of biotic interaction Further that analysis highlighted that the unanticipated effects of multiple drivers acting simultaneously create major challenges in predicting future responses to global environmental change Experimental studies that simultaneously vary two or more global change drivers within the same experiment therefore have considerable promise for improving our understanding of how interactions involving soil communities and their effects on ecosystem-level processes may respond to current global change scenarios

Soil structural integrity and dynamics

The architecture of soil the ways in which particles are arranged in space so forming a stable connected pore space determines the habitat of soil dwelling organisms including plants This soil physical environment is mutable however Soil is hard or dusty but transmits gases readily when dry when wet it becomes soft and plastic and gas ingress becomes much reduced These two extremes are expected to become more prevalent with the changes in climate expected for the UK drier

Page 11

summers and wetter winters The presence of plants indirectly exacerbates the effects of climate change by extracting water in summer and oxygen for root respiration in the winter There is a greater risk of compaction with wetter more plastic soils with late-harvested crops such as potatoes or sugar beet and establishment afterwards Working day access to land may be reduced or more variable leading to damage to soil through inappropriate management (Section B Degradation) Drought may affect soil stability and structure and possibly encourage wind erosion Cecillon et al (2010) examined sites along a latitudinal mountain spatial climate gradient for aggregation and aggregate stability and showed that erodibility was linked to climate and therefore susceptible to change under a shifting climatic regime Other studies have shown effects on organisms associated with the genesis of aggregate structure For instance Eggleton et al (2009) demonstrated in southern England pasture woodland hat earthworm community structure was dependant on soil temperature and water This faunal group has long been established as being of critical importance in no and minimal-till systems both organic and inorganic with potential for declines in aggregate stability as a result of climate change linked to declines in earthworm abundance and shifts in earthworm community structure There are also emerging models linking earthworm population dynamics and soil structural components (Blanchart et al 2009) which offer the possibility of modelling a biotic and abiotic component simultaneously under different climate change scenarios with consequences for hydrology erodibility and trophic level effects

Kohler et al (2009) found that increased CO2 concentrations led to a significantly higher percentage of stable aggregates growing under Lectuca sativa in drought conditions and this was linked to increases in soil microbial biomass and inoculation with a vesicular arbuscular mycorrhizal fungus and plant-growth-promoting rhizobacterium Other workers (Rillig et al 2001) had found a similar effect of elevated carbon dioxide and increased water supply by irrigation on increased aggregate stability due to arbuscular mycorrhizal fungi in soils under Sorghum

Earlier work suggested that climate change would not affect accessibility to land unless winter rainfall increased by 15 (Rounsevell and Brignall 1994) Since this is now what is expected it may be necessary to re-calculate workable days for England based on up-to-date climate change scenarios Neither the direct effect of climate change on soil stability via wet-dry cycles nor its indirect effect via the soil fauna is certain and as Horn and Smucker (2005) have noted that changes in aggregate stability and soil structure can be undesirable if the soil becomes difficult to manage We need to better understand the processes underlying soil structure in order to predict direct soil response to climate change and we need to better understand the wider impact of climate change on soil ecosystems if we are to understand and predict the indirect effects of the soil fauna on soil

Warmer wetter winters may lead to increased competition for oxygen among more strongly respiring organisms in wetter soils into which oxygen penetration is slower Drier summers will lead to soils into which root penetration becomes restricted Both effects are likely to impact on the ability of plants to acquire nutrients and on biogeochemical cycles in general Research on waterlogging appears to have concluded in the 1980s that UK cereals could compensate provided waterlogging did not occur during establishment or repetitively (eg Belford et al 1985) While this may have been true of the conditions prevailing at the time the same may not be true for our future climate The effect that plant root extraction of oxygen has on soil fauna and microflora and vice versa appears to be poorly researched especially in the context of our expected climate change

In summary stability of soil is likely to be impacted by the increasing intensity of wet-dry cycles with climate change but note that an increase is not necessarily desirable if the soil becomes less workable Stepniewska and Stepniewska (2009) have stressed the need for a moderate stable redox above 300 mV Soil fauna and community structure is also likely to be impacted by a change in climate with effects on soil stability that are unclear It is also likely that with wetter winters the number of days when soil is safely accessible by heavy farm machinery without causing damage may become more variable and therefore unpredictable

Page 12

4 Methodologies for investigating the impacts of climate change on soil

Experiments on climate change drivers have been carried out over a variety of spatial and temporal scales ranging from short term laboratory incubation studies to ecosystem-level and long-term manipulations of climatic factors (Wullschleger and Strahl 2010) The main approaches for studying climate change include (1) the use of environmental gradients (temperature and water) and reciprocal transplants (2) in situ field manipulation experiments including Free-Air CO2 Enrichment (FACE) experiments for manipulation of atmospheric CO2 and field-scale manipulations of temperature and precipitation (3) controlled environment facilities such as the Ecotron controlled environment facilities at Imperial College Silwood Park UK and Montpellier France and (4) highly artificial often laboratory based microcosm experiments that have little relevance to real systems These approaches in the order listed above follow a spectrum of decreasing realism but increasing mechanistic control We discuss these approaches in turn

Environmental gradients (temperature and water) and reciprocal transplants

Climatic gradients for instance in annual precipitation and temperature that cross continents countries and elevation gradients are commonly used to determine impacts of climatic variation on soil biota and processes While useful for establishing general patterns such approaches leave significant questions about other factors that could explain differences in soil biota along climatic gradients such as soil fertility and mineralogy To overcome this problem an associated approach is the use of transplant experiments whereby intact soil-vegetation turves (or varying size) are transplanted at different places along climatic gradients so that effects of movement to another climate on soil biota can be assessed This approach for example was used by Briones et al (19971998) who transplanted peat soils from high to lower altitudes at Great Dunn Fell Cumbria to simulate climate warming and that this increased the density of enchytraeid worms the dominant fauna of these peat soils leading to enhanced decomposition and DOC concentrations in soil leachates The same system was also used by Tipping et al (1999) to show that warming and drying can accelerate the production of dissolved organic matter in organic soil horizons Such approaches are valuable in that they provide information on the response of soil biota and processes to real changes in climate but they are limited by the lack of control of environmental variables along transects and potential effects of disturbance from moving soil cores from one site to another

The further experimentation moves away from surveys and experiments in the field the less likely they are to represent real world systems This is not necessarily an issue when detailed and specific mechanisms are being explored but become increasingly problematic when large scale predictions are asserted from them

In situ field manipulation experiments

Many studies have used various field-based manipulations of climate including elevated carbon dioxide in the previously mentioned FACE experiments (eg Norby et al 2004 Jackson et al 2009) drought using rainfall roofs (eg Beier et al 2004) and artificial warming using heating cables (eg Grime et al 2008) passive night time warming roofs (eg Beier et al 2004) and infra-red lamps (Zhang et al 2005) Such experiments have contributed significantly to our understanding of the effects of different climate change drivers on vegetation soil biota and soil processes as detailed in the previous section However as stated previously most studies of this kind have explored effects of single climate factors whereas there is much potential for interactions between multiple factors to have additive or antagonistic effects on soil organisms and the activities that they drive (Bardgett et al 2008) Therefore future experiments which manipulate multiple climate change and other site factors are needed to better understand the effects of climate change on soil biota

As an example of in situ field manipulations Zhang et al (2005) artificially heated soils under tall grass prairie using infra-red heaters to simulate an increase in daily soil temperatures of 18 ndash 27oC and studied two clipping regimes clipped and unclipped In the heated treatments they found changes in the soil microbial community structure as determined using phospholipid fatty acid analysis (PLFA) in the unclipped plots with a shift to fungal dominance but not in the clipped

Page 8

Climate change Implications for soil biota

microbial abundance and activity (Castro et al 2010)

bull Increased transfer of C to the soil stimulating mycorrhizal fungi which may stimulate nutrient transfer (Tyliankis et al 2008)

bull Stimulation of microbial biomass can lead to microbial immobilization of N thereby enforcing plant N limitation (de Graaff et al 2007)

bull May cause shift in vegetation patterns with subsequent implications for soil biota

Section 3 Potential impacts of climate change on soil processes function and biota

Carbon and nutrient cycling

Climate change has both direct and indirect effects on soil organisms and the processes that they drive often with consequences for the return greenhouse gases to the atmosphere Direct effects include the influence of temperature changing precipitation and extreme climatic events on soil organisms and the processes that they drive whereas indirect effects result from climate-driven changes in plant productivity and species composition which alter soil physicochemical conditions the supply of carbon to soil and the structure and activity of microbial communities involved in decomposition processes and carbon release from soil (Bardgett et al 2008)

One of the most commonly discussed contributions of soil organisms to climate change is their role in soil organic matter decomposition and the idea that warming will accelerate rates of heterotrophic microbial activity thereby increasing the transfer of carbon dioxide from soil to the atmosphere and exports of dissolved organic carbon by hydrologic leaching (Jenkinson et al 1991 Davidson and Janssens 2006) The concern here is that because rates of soil respiration are more sensitive than is primary production to temperature (Jenkinson et al 1991 Schimel et al 1994) it is thought that climate warming will increase the net transfer of carbon from soil to atmosphere thus creating a positive feedback on climate change (Cox et al 2000) Although it is well known that temperature is an important determinant of rates of organic matter decomposition the nature of the relationship between temperature and microbial respiration is far from clear (Davidson and Janssens 2006) There are several reasons for this uncertainty but key factors include potential for variations in organic matter quality to influence the temperature sensitivity of microbial decomposition (Fang et al 2005 Conen et al 2006 Davidson and Janssens 2006) and for environmental constraints such as physical and chemical protection of organic matter to decrease substrate availability for microbial attack and thereby dampen microbial responses to warming (Davidson and Janssens 2006) Also there is uncertainty about how reactive different microbial and faunal groups and species are to temperature change with several studies showing that soil microbial and animal communities are insensitive to small increases in temperature (eg Kandeler et al 1998 Bardgett et al 1999 Wardle 2002) whereas others show that soil organisms and the carbon cycling processes that they drive are responsive to temperature change For instance the abundance of enchytraeid worms which dominate the fauna of acid peat soils have been shown to be strongly related to temperature and it is has been suggested that climate warming could increase their abundance leading to enhanced carbon mineralization and carbon loss from soil (Briones et al 1998 Cole et al 2002ab) Also a recent analysis by Gange et al (2007) related temporal shifts in autumnal fruiting patterns of macrofungi in southern England to shifts in climate and found that the average first fruiting date of 315 species is now earlier while last fruiting date is now later than was the case 56 years ago Their study also found that many species are now fruiting twice a year indicative of increased mycelial activity and possibly greater decomposition rates in ecosystems

Increases in the frequency of extreme weather events with climate change such as droughting and freezing may have an even greater effect on soil organisms and their activities than will overall changes in temperature and precipitation It is well know for example that droughting and freezing have substantial direct effects on microbial physiology and the composition of the soil microbial community with important consequences for ecosystem-level carbon dynamics (Schimel et al 2007) For example increased drought and drying in wetlands and peatlands which will lower the water

Page 9

table and introduce oxygen into previously anaerobic soil will create a more favorable environment for microbial activity (Freeman et al 2004) potentially enhancing the activity of enzymes (eg phenol oxidases) which play a pivotal role in the breakdown of recalcitrant organic matter (Freeman et al 2004) Because peatlands and wetlands represent amongst the largest stocks of terrestrial carbon globally (Ward et al 2007) such enhanced breakdown of recalcitrant organic matter under drying could have major implications for the global carbon cycle (Freeman et al 2004) Before leaving this topic it is important to note that methanogenic pathways are also affected by increased oxygen availability associated with drought in that methane emissions are reduced by toxic effects of oxygen on methanogens (Roulet and Moore 1995 Freeman et al 2002) Also drought can have marked effects on nitrous oxide emission from soils a potent greenhouse gas that is increasing in atmospheric concentrations at the rate of 02ndash03 per year (Houghton et al 1996) However responses depend on the severity of drought in that modest summer drought is likely to have limited effect on soil nitrous oxide emissions whereas more extreme drought can greatly increase them (Dowrick et al 1999)

The majority of studies to date that have explored effects of climate change on biological systems and soil organisms have considered single factors such as elevated atmospheric carbon dioxide concentration warming and drought However there is much potential for interactions between these factors to have additive or antagonistic effects on soil organisms and the activities that they drive (Mikkelsen et al 2008 Bardgett et al 2008 Tylianakis et al 2008) Very little is known about the influence of multiple and interacting climate drivers on soil organisms and their activities although some studies do point to strong non-additive belowground effects of these drivers with feedback consequences for carbon exchange For instance microbial decomposition of peat was found to be significantly greater when subject to both elevated temperature and atmospheric carbon dioxide than when these factors were each elevated singly (Fenner et al 2007ab) thereby potentially causing an even stronger feedback on carbon loss from soil as dissolved organic carbon in drainage water and respiration Added to this complexity is our knowledge that other organisms and trophic groups that influence soil microbes directly such as microbial-feeding fauna will also respond to multiple climate change factors (Wardle 2002 Bardgett 2005 Tylianakis et al 2008) This complexity further hampers our ability to predict effects of multiple climate change drivers on soil biological communities and carbon exchange feedbacks

In addition to multiple climate change drivers soil organisms and their activities are also affected substantially by other global change phenomena such as nitrogen deposition invasion of new species and land use change Perhaps the strongest driver is land use change (cf Sala et al 2000) and it is widely documented that changes in the intensity of land use or the conversion of natural vegetation to agriculture or forestry can have substantial and often strongly negative and irreversible effects on soil biological communities and their activities (Brussaard et al 1997 Wardle 2002 Bardgett 2005) One pattern that commonly emerges in the context of land use change is that intensification of farming including increased tillage fertilizer use and grazing is typically associated with an increased role of the bacterial-based energy channel relative to the fungal-based channel (Wardle 2002 Bardgett 2005 Bardgett and Wardle 2010) which is away from what would typically found in more stable late successional ecosystems with large fungalbacterial ratios (Harris 2009) As discussed above this increased bacterial role is associated with faster leakier nutrient cycling and more losses of nutrients and carbon in water and greenhouse gases to the atmosphere (Wardle et al 2004 van der Heijden et al 2008) In contrast low intensity management systems often encourage fungal-based soil food webs that are more similar to those of natural systems and tend to be associated with more efficient nutrient cycling (Bardgett and McAlister 1999 Gordon et al 2008) and enhanced soil carbon sequestration (De Deyn et al 2008) Although not tested global change drivers may alter the balance of communities in favour bacterial populations thereby accelerating rates of nutrient and carbon mineralization with implications for carbon sequestration and C loss to the atmosphere

Soil biological communities are also strongly affected by nitrogen enrichment which is of high relevance because anthropogenic activities have substantially increased global rates of nitrogen fixation and deposition (Schlesinger 2009) For instance it is well known that nitrogen enrichment can have direct and differential impacts on extracellular enzymes involved in decomposition processes This typically involves stimulation of the synthesis of cellulases which degrade labile high cellulose litter but suppression of the synthesis of ligninolytic enzymes by white rot fungi which decompose recalcitrant high lignin litter (Carreiro et al 2000 Waldrop et al 2004 Allison et al 2008) Also

Page 10

nitrogen enrichment is known to influence the abundance and diversity of different components of the soil microbial community including saprophytic fungi (Donnison et al 2000 Allison et al 2008) mycorrhizal fungi (Egerton-Warburton and Allen 2000 Frey et al 2004) and soil fauna (Scheu and Schaeffer 1998 Ettema et al 1999) which are also affected by climate change and are well known to have substantial effects on decomposition processes and ecosystem-level carbon exchange A recent meta-analysis on this topic revealed that soil microbial biomass declined 15 on average under nitrogen fertilization but that declines in abundance of microbes and fungi were more evident in studies of longer durations and with higher total amounts of nitrogen added (Treseder 2008) Moreover that study showed negative responses of microbial biomass to nitrogen fertilization to be significantly correlated with declines in soil carbon dioxide emissions indicating that moderate declines in microbial biomass under nitrogen fertilization may also have consequences for carbon fluxes However another meta-analysis of 109 studies across the globe revealed that nitrogen enrichment had no significant effect on net ecosystem carbon dioxide exchange in non-forest natural ecosystems but did increase methane and nitrous oxide emissions by 97 and 216 respectively (Liu and Greaver 2009) It was suggested therefore that any potential positive effects of nitrogen enrichment on the global terrestrial carbon sink should be offset by the stimulation of methane and nitrous oxide emissions which are more potent greenhouse gases than is carbon dioxide (Liu and Greaver 2009) Importantly nitrogen deposition and other global changes can also influence soil microbes and decomposition processes indirectly through altering vegetation composition and productivity and by alleviating progressive nitrogen limitation of plant growth which typically occurs under elevated atmospheric carbon dioxide (Finzi et al 2002 Luo et al 2004 de Graaff et al 2006)

The likely effect of drought during summers is well-appreciated but much less is known about the impacts of warmer wetter winters for which plants appear to have fewer adaptations to cope (Whitmore and Whalley 2009) Waterlogging becomes more likely with increased rainfall but at the same time root respiration is likely to increase in response to warmer temperatures There is thus a considerably raised risk of waterlogging of UK soils during the future winter months No additional impact of drought has been found on cereal yields following winter waterlogging and reasonable diversity and resistance to waterlogging has been found in UK cereal varieties (Dickin and Wright 2009 Dickin et al 2008) However soil-dwelling organisms may be at risk some earthworms for example are more intolerant of waterlogging than others (Chuang and Chen 2009) Earthworms are relatively well studied other species less so and in general macrofauna diversity is greatly reduced in flooded grasslands (Plum 2005) with opportunists becoming more abundant Microbes and plants compete for resources in waterlogged soils For example Blom (1999) reported that plants out-competed nitrifiers for ammonium in waterlogged soil It is not clear to what extent plants and microbes compete for oxygen

In general very little is known about the combined effects of global changes on soil biological communities and their activities but they clearly have the potential to amplify suppress or perhaps even neutralize climate change driven effects on soil microbes and their feedback to carbon exchange (Bardgett et al 2008) A recent synthesis by Tylianakis et al (2008) of data from 688 published studies on the effects of global change on biotic interactions in terrestrial ecosystems (including those that occur in the decomposer food web) highlighted that there is substantial variability among studies in both the magnitude and direction of effects of any given global change driver on any given type of biotic interaction Further that analysis highlighted that the unanticipated effects of multiple drivers acting simultaneously create major challenges in predicting future responses to global environmental change Experimental studies that simultaneously vary two or more global change drivers within the same experiment therefore have considerable promise for improving our understanding of how interactions involving soil communities and their effects on ecosystem-level processes may respond to current global change scenarios

Soil structural integrity and dynamics

The architecture of soil the ways in which particles are arranged in space so forming a stable connected pore space determines the habitat of soil dwelling organisms including plants This soil physical environment is mutable however Soil is hard or dusty but transmits gases readily when dry when wet it becomes soft and plastic and gas ingress becomes much reduced These two extremes are expected to become more prevalent with the changes in climate expected for the UK drier

Page 11

summers and wetter winters The presence of plants indirectly exacerbates the effects of climate change by extracting water in summer and oxygen for root respiration in the winter There is a greater risk of compaction with wetter more plastic soils with late-harvested crops such as potatoes or sugar beet and establishment afterwards Working day access to land may be reduced or more variable leading to damage to soil through inappropriate management (Section B Degradation) Drought may affect soil stability and structure and possibly encourage wind erosion Cecillon et al (2010) examined sites along a latitudinal mountain spatial climate gradient for aggregation and aggregate stability and showed that erodibility was linked to climate and therefore susceptible to change under a shifting climatic regime Other studies have shown effects on organisms associated with the genesis of aggregate structure For instance Eggleton et al (2009) demonstrated in southern England pasture woodland hat earthworm community structure was dependant on soil temperature and water This faunal group has long been established as being of critical importance in no and minimal-till systems both organic and inorganic with potential for declines in aggregate stability as a result of climate change linked to declines in earthworm abundance and shifts in earthworm community structure There are also emerging models linking earthworm population dynamics and soil structural components (Blanchart et al 2009) which offer the possibility of modelling a biotic and abiotic component simultaneously under different climate change scenarios with consequences for hydrology erodibility and trophic level effects

Kohler et al (2009) found that increased CO2 concentrations led to a significantly higher percentage of stable aggregates growing under Lectuca sativa in drought conditions and this was linked to increases in soil microbial biomass and inoculation with a vesicular arbuscular mycorrhizal fungus and plant-growth-promoting rhizobacterium Other workers (Rillig et al 2001) had found a similar effect of elevated carbon dioxide and increased water supply by irrigation on increased aggregate stability due to arbuscular mycorrhizal fungi in soils under Sorghum

Earlier work suggested that climate change would not affect accessibility to land unless winter rainfall increased by 15 (Rounsevell and Brignall 1994) Since this is now what is expected it may be necessary to re-calculate workable days for England based on up-to-date climate change scenarios Neither the direct effect of climate change on soil stability via wet-dry cycles nor its indirect effect via the soil fauna is certain and as Horn and Smucker (2005) have noted that changes in aggregate stability and soil structure can be undesirable if the soil becomes difficult to manage We need to better understand the processes underlying soil structure in order to predict direct soil response to climate change and we need to better understand the wider impact of climate change on soil ecosystems if we are to understand and predict the indirect effects of the soil fauna on soil

Warmer wetter winters may lead to increased competition for oxygen among more strongly respiring organisms in wetter soils into which oxygen penetration is slower Drier summers will lead to soils into which root penetration becomes restricted Both effects are likely to impact on the ability of plants to acquire nutrients and on biogeochemical cycles in general Research on waterlogging appears to have concluded in the 1980s that UK cereals could compensate provided waterlogging did not occur during establishment or repetitively (eg Belford et al 1985) While this may have been true of the conditions prevailing at the time the same may not be true for our future climate The effect that plant root extraction of oxygen has on soil fauna and microflora and vice versa appears to be poorly researched especially in the context of our expected climate change

In summary stability of soil is likely to be impacted by the increasing intensity of wet-dry cycles with climate change but note that an increase is not necessarily desirable if the soil becomes less workable Stepniewska and Stepniewska (2009) have stressed the need for a moderate stable redox above 300 mV Soil fauna and community structure is also likely to be impacted by a change in climate with effects on soil stability that are unclear It is also likely that with wetter winters the number of days when soil is safely accessible by heavy farm machinery without causing damage may become more variable and therefore unpredictable

Page 12

4 Methodologies for investigating the impacts of climate change on soil

Experiments on climate change drivers have been carried out over a variety of spatial and temporal scales ranging from short term laboratory incubation studies to ecosystem-level and long-term manipulations of climatic factors (Wullschleger and Strahl 2010) The main approaches for studying climate change include (1) the use of environmental gradients (temperature and water) and reciprocal transplants (2) in situ field manipulation experiments including Free-Air CO2 Enrichment (FACE) experiments for manipulation of atmospheric CO2 and field-scale manipulations of temperature and precipitation (3) controlled environment facilities such as the Ecotron controlled environment facilities at Imperial College Silwood Park UK and Montpellier France and (4) highly artificial often laboratory based microcosm experiments that have little relevance to real systems These approaches in the order listed above follow a spectrum of decreasing realism but increasing mechanistic control We discuss these approaches in turn

Environmental gradients (temperature and water) and reciprocal transplants

Climatic gradients for instance in annual precipitation and temperature that cross continents countries and elevation gradients are commonly used to determine impacts of climatic variation on soil biota and processes While useful for establishing general patterns such approaches leave significant questions about other factors that could explain differences in soil biota along climatic gradients such as soil fertility and mineralogy To overcome this problem an associated approach is the use of transplant experiments whereby intact soil-vegetation turves (or varying size) are transplanted at different places along climatic gradients so that effects of movement to another climate on soil biota can be assessed This approach for example was used by Briones et al (19971998) who transplanted peat soils from high to lower altitudes at Great Dunn Fell Cumbria to simulate climate warming and that this increased the density of enchytraeid worms the dominant fauna of these peat soils leading to enhanced decomposition and DOC concentrations in soil leachates The same system was also used by Tipping et al (1999) to show that warming and drying can accelerate the production of dissolved organic matter in organic soil horizons Such approaches are valuable in that they provide information on the response of soil biota and processes to real changes in climate but they are limited by the lack of control of environmental variables along transects and potential effects of disturbance from moving soil cores from one site to another

The further experimentation moves away from surveys and experiments in the field the less likely they are to represent real world systems This is not necessarily an issue when detailed and specific mechanisms are being explored but become increasingly problematic when large scale predictions are asserted from them

In situ field manipulation experiments

Many studies have used various field-based manipulations of climate including elevated carbon dioxide in the previously mentioned FACE experiments (eg Norby et al 2004 Jackson et al 2009) drought using rainfall roofs (eg Beier et al 2004) and artificial warming using heating cables (eg Grime et al 2008) passive night time warming roofs (eg Beier et al 2004) and infra-red lamps (Zhang et al 2005) Such experiments have contributed significantly to our understanding of the effects of different climate change drivers on vegetation soil biota and soil processes as detailed in the previous section However as stated previously most studies of this kind have explored effects of single climate factors whereas there is much potential for interactions between multiple factors to have additive or antagonistic effects on soil organisms and the activities that they drive (Bardgett et al 2008) Therefore future experiments which manipulate multiple climate change and other site factors are needed to better understand the effects of climate change on soil biota

As an example of in situ field manipulations Zhang et al (2005) artificially heated soils under tall grass prairie using infra-red heaters to simulate an increase in daily soil temperatures of 18 ndash 27oC and studied two clipping regimes clipped and unclipped In the heated treatments they found changes in the soil microbial community structure as determined using phospholipid fatty acid analysis (PLFA) in the unclipped plots with a shift to fungal dominance but not in the clipped

Page 9

table and introduce oxygen into previously anaerobic soil will create a more favorable environment for microbial activity (Freeman et al 2004) potentially enhancing the activity of enzymes (eg phenol oxidases) which play a pivotal role in the breakdown of recalcitrant organic matter (Freeman et al 2004) Because peatlands and wetlands represent amongst the largest stocks of terrestrial carbon globally (Ward et al 2007) such enhanced breakdown of recalcitrant organic matter under drying could have major implications for the global carbon cycle (Freeman et al 2004) Before leaving this topic it is important to note that methanogenic pathways are also affected by increased oxygen availability associated with drought in that methane emissions are reduced by toxic effects of oxygen on methanogens (Roulet and Moore 1995 Freeman et al 2002) Also drought can have marked effects on nitrous oxide emission from soils a potent greenhouse gas that is increasing in atmospheric concentrations at the rate of 02ndash03 per year (Houghton et al 1996) However responses depend on the severity of drought in that modest summer drought is likely to have limited effect on soil nitrous oxide emissions whereas more extreme drought can greatly increase them (Dowrick et al 1999)

The majority of studies to date that have explored effects of climate change on biological systems and soil organisms have considered single factors such as elevated atmospheric carbon dioxide concentration warming and drought However there is much potential for interactions between these factors to have additive or antagonistic effects on soil organisms and the activities that they drive (Mikkelsen et al 2008 Bardgett et al 2008 Tylianakis et al 2008) Very little is known about the influence of multiple and interacting climate drivers on soil organisms and their activities although some studies do point to strong non-additive belowground effects of these drivers with feedback consequences for carbon exchange For instance microbial decomposition of peat was found to be significantly greater when subject to both elevated temperature and atmospheric carbon dioxide than when these factors were each elevated singly (Fenner et al 2007ab) thereby potentially causing an even stronger feedback on carbon loss from soil as dissolved organic carbon in drainage water and respiration Added to this complexity is our knowledge that other organisms and trophic groups that influence soil microbes directly such as microbial-feeding fauna will also respond to multiple climate change factors (Wardle 2002 Bardgett 2005 Tylianakis et al 2008) This complexity further hampers our ability to predict effects of multiple climate change drivers on soil biological communities and carbon exchange feedbacks

In addition to multiple climate change drivers soil organisms and their activities are also affected substantially by other global change phenomena such as nitrogen deposition invasion of new species and land use change Perhaps the strongest driver is land use change (cf Sala et al 2000) and it is widely documented that changes in the intensity of land use or the conversion of natural vegetation to agriculture or forestry can have substantial and often strongly negative and irreversible effects on soil biological communities and their activities (Brussaard et al 1997 Wardle 2002 Bardgett 2005) One pattern that commonly emerges in the context of land use change is that intensification of farming including increased tillage fertilizer use and grazing is typically associated with an increased role of the bacterial-based energy channel relative to the fungal-based channel (Wardle 2002 Bardgett 2005 Bardgett and Wardle 2010) which is away from what would typically found in more stable late successional ecosystems with large fungalbacterial ratios (Harris 2009) As discussed above this increased bacterial role is associated with faster leakier nutrient cycling and more losses of nutrients and carbon in water and greenhouse gases to the atmosphere (Wardle et al 2004 van der Heijden et al 2008) In contrast low intensity management systems often encourage fungal-based soil food webs that are more similar to those of natural systems and tend to be associated with more efficient nutrient cycling (Bardgett and McAlister 1999 Gordon et al 2008) and enhanced soil carbon sequestration (De Deyn et al 2008) Although not tested global change drivers may alter the balance of communities in favour bacterial populations thereby accelerating rates of nutrient and carbon mineralization with implications for carbon sequestration and C loss to the atmosphere

Soil biological communities are also strongly affected by nitrogen enrichment which is of high relevance because anthropogenic activities have substantially increased global rates of nitrogen fixation and deposition (Schlesinger 2009) For instance it is well known that nitrogen enrichment can have direct and differential impacts on extracellular enzymes involved in decomposition processes This typically involves stimulation of the synthesis of cellulases which degrade labile high cellulose litter but suppression of the synthesis of ligninolytic enzymes by white rot fungi which decompose recalcitrant high lignin litter (Carreiro et al 2000 Waldrop et al 2004 Allison et al 2008) Also

Page 10

nitrogen enrichment is known to influence the abundance and diversity of different components of the soil microbial community including saprophytic fungi (Donnison et al 2000 Allison et al 2008) mycorrhizal fungi (Egerton-Warburton and Allen 2000 Frey et al 2004) and soil fauna (Scheu and Schaeffer 1998 Ettema et al 1999) which are also affected by climate change and are well known to have substantial effects on decomposition processes and ecosystem-level carbon exchange A recent meta-analysis on this topic revealed that soil microbial biomass declined 15 on average under nitrogen fertilization but that declines in abundance of microbes and fungi were more evident in studies of longer durations and with higher total amounts of nitrogen added (Treseder 2008) Moreover that study showed negative responses of microbial biomass to nitrogen fertilization to be significantly correlated with declines in soil carbon dioxide emissions indicating that moderate declines in microbial biomass under nitrogen fertilization may also have consequences for carbon fluxes However another meta-analysis of 109 studies across the globe revealed that nitrogen enrichment had no significant effect on net ecosystem carbon dioxide exchange in non-forest natural ecosystems but did increase methane and nitrous oxide emissions by 97 and 216 respectively (Liu and Greaver 2009) It was suggested therefore that any potential positive effects of nitrogen enrichment on the global terrestrial carbon sink should be offset by the stimulation of methane and nitrous oxide emissions which are more potent greenhouse gases than is carbon dioxide (Liu and Greaver 2009) Importantly nitrogen deposition and other global changes can also influence soil microbes and decomposition processes indirectly through altering vegetation composition and productivity and by alleviating progressive nitrogen limitation of plant growth which typically occurs under elevated atmospheric carbon dioxide (Finzi et al 2002 Luo et al 2004 de Graaff et al 2006)

The likely effect of drought during summers is well-appreciated but much less is known about the impacts of warmer wetter winters for which plants appear to have fewer adaptations to cope (Whitmore and Whalley 2009) Waterlogging becomes more likely with increased rainfall but at the same time root respiration is likely to increase in response to warmer temperatures There is thus a considerably raised risk of waterlogging of UK soils during the future winter months No additional impact of drought has been found on cereal yields following winter waterlogging and reasonable diversity and resistance to waterlogging has been found in UK cereal varieties (Dickin and Wright 2009 Dickin et al 2008) However soil-dwelling organisms may be at risk some earthworms for example are more intolerant of waterlogging than others (Chuang and Chen 2009) Earthworms are relatively well studied other species less so and in general macrofauna diversity is greatly reduced in flooded grasslands (Plum 2005) with opportunists becoming more abundant Microbes and plants compete for resources in waterlogged soils For example Blom (1999) reported that plants out-competed nitrifiers for ammonium in waterlogged soil It is not clear to what extent plants and microbes compete for oxygen

In general very little is known about the combined effects of global changes on soil biological communities and their activities but they clearly have the potential to amplify suppress or perhaps even neutralize climate change driven effects on soil microbes and their feedback to carbon exchange (Bardgett et al 2008) A recent synthesis by Tylianakis et al (2008) of data from 688 published studies on the effects of global change on biotic interactions in terrestrial ecosystems (including those that occur in the decomposer food web) highlighted that there is substantial variability among studies in both the magnitude and direction of effects of any given global change driver on any given type of biotic interaction Further that analysis highlighted that the unanticipated effects of multiple drivers acting simultaneously create major challenges in predicting future responses to global environmental change Experimental studies that simultaneously vary two or more global change drivers within the same experiment therefore have considerable promise for improving our understanding of how interactions involving soil communities and their effects on ecosystem-level processes may respond to current global change scenarios

Soil structural integrity and dynamics

The architecture of soil the ways in which particles are arranged in space so forming a stable connected pore space determines the habitat of soil dwelling organisms including plants This soil physical environment is mutable however Soil is hard or dusty but transmits gases readily when dry when wet it becomes soft and plastic and gas ingress becomes much reduced These two extremes are expected to become more prevalent with the changes in climate expected for the UK drier

Page 11

summers and wetter winters The presence of plants indirectly exacerbates the effects of climate change by extracting water in summer and oxygen for root respiration in the winter There is a greater risk of compaction with wetter more plastic soils with late-harvested crops such as potatoes or sugar beet and establishment afterwards Working day access to land may be reduced or more variable leading to damage to soil through inappropriate management (Section B Degradation) Drought may affect soil stability and structure and possibly encourage wind erosion Cecillon et al (2010) examined sites along a latitudinal mountain spatial climate gradient for aggregation and aggregate stability and showed that erodibility was linked to climate and therefore susceptible to change under a shifting climatic regime Other studies have shown effects on organisms associated with the genesis of aggregate structure For instance Eggleton et al (2009) demonstrated in southern England pasture woodland hat earthworm community structure was dependant on soil temperature and water This faunal group has long been established as being of critical importance in no and minimal-till systems both organic and inorganic with potential for declines in aggregate stability as a result of climate change linked to declines in earthworm abundance and shifts in earthworm community structure There are also emerging models linking earthworm population dynamics and soil structural components (Blanchart et al 2009) which offer the possibility of modelling a biotic and abiotic component simultaneously under different climate change scenarios with consequences for hydrology erodibility and trophic level effects

Kohler et al (2009) found that increased CO2 concentrations led to a significantly higher percentage of stable aggregates growing under Lectuca sativa in drought conditions and this was linked to increases in soil microbial biomass and inoculation with a vesicular arbuscular mycorrhizal fungus and plant-growth-promoting rhizobacterium Other workers (Rillig et al 2001) had found a similar effect of elevated carbon dioxide and increased water supply by irrigation on increased aggregate stability due to arbuscular mycorrhizal fungi in soils under Sorghum

Earlier work suggested that climate change would not affect accessibility to land unless winter rainfall increased by 15 (Rounsevell and Brignall 1994) Since this is now what is expected it may be necessary to re-calculate workable days for England based on up-to-date climate change scenarios Neither the direct effect of climate change on soil stability via wet-dry cycles nor its indirect effect via the soil fauna is certain and as Horn and Smucker (2005) have noted that changes in aggregate stability and soil structure can be undesirable if the soil becomes difficult to manage We need to better understand the processes underlying soil structure in order to predict direct soil response to climate change and we need to better understand the wider impact of climate change on soil ecosystems if we are to understand and predict the indirect effects of the soil fauna on soil

Warmer wetter winters may lead to increased competition for oxygen among more strongly respiring organisms in wetter soils into which oxygen penetration is slower Drier summers will lead to soils into which root penetration becomes restricted Both effects are likely to impact on the ability of plants to acquire nutrients and on biogeochemical cycles in general Research on waterlogging appears to have concluded in the 1980s that UK cereals could compensate provided waterlogging did not occur during establishment or repetitively (eg Belford et al 1985) While this may have been true of the conditions prevailing at the time the same may not be true for our future climate The effect that plant root extraction of oxygen has on soil fauna and microflora and vice versa appears to be poorly researched especially in the context of our expected climate change

In summary stability of soil is likely to be impacted by the increasing intensity of wet-dry cycles with climate change but note that an increase is not necessarily desirable if the soil becomes less workable Stepniewska and Stepniewska (2009) have stressed the need for a moderate stable redox above 300 mV Soil fauna and community structure is also likely to be impacted by a change in climate with effects on soil stability that are unclear It is also likely that with wetter winters the number of days when soil is safely accessible by heavy farm machinery without causing damage may become more variable and therefore unpredictable

Page 12

4 Methodologies for investigating the impacts of climate change on soil

Experiments on climate change drivers have been carried out over a variety of spatial and temporal scales ranging from short term laboratory incubation studies to ecosystem-level and long-term manipulations of climatic factors (Wullschleger and Strahl 2010) The main approaches for studying climate change include (1) the use of environmental gradients (temperature and water) and reciprocal transplants (2) in situ field manipulation experiments including Free-Air CO2 Enrichment (FACE) experiments for manipulation of atmospheric CO2 and field-scale manipulations of temperature and precipitation (3) controlled environment facilities such as the Ecotron controlled environment facilities at Imperial College Silwood Park UK and Montpellier France and (4) highly artificial often laboratory based microcosm experiments that have little relevance to real systems These approaches in the order listed above follow a spectrum of decreasing realism but increasing mechanistic control We discuss these approaches in turn

Environmental gradients (temperature and water) and reciprocal transplants

Climatic gradients for instance in annual precipitation and temperature that cross continents countries and elevation gradients are commonly used to determine impacts of climatic variation on soil biota and processes While useful for establishing general patterns such approaches leave significant questions about other factors that could explain differences in soil biota along climatic gradients such as soil fertility and mineralogy To overcome this problem an associated approach is the use of transplant experiments whereby intact soil-vegetation turves (or varying size) are transplanted at different places along climatic gradients so that effects of movement to another climate on soil biota can be assessed This approach for example was used by Briones et al (19971998) who transplanted peat soils from high to lower altitudes at Great Dunn Fell Cumbria to simulate climate warming and that this increased the density of enchytraeid worms the dominant fauna of these peat soils leading to enhanced decomposition and DOC concentrations in soil leachates The same system was also used by Tipping et al (1999) to show that warming and drying can accelerate the production of dissolved organic matter in organic soil horizons Such approaches are valuable in that they provide information on the response of soil biota and processes to real changes in climate but they are limited by the lack of control of environmental variables along transects and potential effects of disturbance from moving soil cores from one site to another

The further experimentation moves away from surveys and experiments in the field the less likely they are to represent real world systems This is not necessarily an issue when detailed and specific mechanisms are being explored but become increasingly problematic when large scale predictions are asserted from them

In situ field manipulation experiments

Many studies have used various field-based manipulations of climate including elevated carbon dioxide in the previously mentioned FACE experiments (eg Norby et al 2004 Jackson et al 2009) drought using rainfall roofs (eg Beier et al 2004) and artificial warming using heating cables (eg Grime et al 2008) passive night time warming roofs (eg Beier et al 2004) and infra-red lamps (Zhang et al 2005) Such experiments have contributed significantly to our understanding of the effects of different climate change drivers on vegetation soil biota and soil processes as detailed in the previous section However as stated previously most studies of this kind have explored effects of single climate factors whereas there is much potential for interactions between multiple factors to have additive or antagonistic effects on soil organisms and the activities that they drive (Bardgett et al 2008) Therefore future experiments which manipulate multiple climate change and other site factors are needed to better understand the effects of climate change on soil biota

As an example of in situ field manipulations Zhang et al (2005) artificially heated soils under tall grass prairie using infra-red heaters to simulate an increase in daily soil temperatures of 18 ndash 27oC and studied two clipping regimes clipped and unclipped In the heated treatments they found changes in the soil microbial community structure as determined using phospholipid fatty acid analysis (PLFA) in the unclipped plots with a shift to fungal dominance but not in the clipped

Page 10

nitrogen enrichment is known to influence the abundance and diversity of different components of the soil microbial community including saprophytic fungi (Donnison et al 2000 Allison et al 2008) mycorrhizal fungi (Egerton-Warburton and Allen 2000 Frey et al 2004) and soil fauna (Scheu and Schaeffer 1998 Ettema et al 1999) which are also affected by climate change and are well known to have substantial effects on decomposition processes and ecosystem-level carbon exchange A recent meta-analysis on this topic revealed that soil microbial biomass declined 15 on average under nitrogen fertilization but that declines in abundance of microbes and fungi were more evident in studies of longer durations and with higher total amounts of nitrogen added (Treseder 2008) Moreover that study showed negative responses of microbial biomass to nitrogen fertilization to be significantly correlated with declines in soil carbon dioxide emissions indicating that moderate declines in microbial biomass under nitrogen fertilization may also have consequences for carbon fluxes However another meta-analysis of 109 studies across the globe revealed that nitrogen enrichment had no significant effect on net ecosystem carbon dioxide exchange in non-forest natural ecosystems but did increase methane and nitrous oxide emissions by 97 and 216 respectively (Liu and Greaver 2009) It was suggested therefore that any potential positive effects of nitrogen enrichment on the global terrestrial carbon sink should be offset by the stimulation of methane and nitrous oxide emissions which are more potent greenhouse gases than is carbon dioxide (Liu and Greaver 2009) Importantly nitrogen deposition and other global changes can also influence soil microbes and decomposition processes indirectly through altering vegetation composition and productivity and by alleviating progressive nitrogen limitation of plant growth which typically occurs under elevated atmospheric carbon dioxide (Finzi et al 2002 Luo et al 2004 de Graaff et al 2006)

The likely effect of drought during summers is well-appreciated but much less is known about the impacts of warmer wetter winters for which plants appear to have fewer adaptations to cope (Whitmore and Whalley 2009) Waterlogging becomes more likely with increased rainfall but at the same time root respiration is likely to increase in response to warmer temperatures There is thus a considerably raised risk of waterlogging of UK soils during the future winter months No additional impact of drought has been found on cereal yields following winter waterlogging and reasonable diversity and resistance to waterlogging has been found in UK cereal varieties (Dickin and Wright 2009 Dickin et al 2008) However soil-dwelling organisms may be at risk some earthworms for example are more intolerant of waterlogging than others (Chuang and Chen 2009) Earthworms are relatively well studied other species less so and in general macrofauna diversity is greatly reduced in flooded grasslands (Plum 2005) with opportunists becoming more abundant Microbes and plants compete for resources in waterlogged soils For example Blom (1999) reported that plants out-competed nitrifiers for ammonium in waterlogged soil It is not clear to what extent plants and microbes compete for oxygen

In general very little is known about the combined effects of global changes on soil biological communities and their activities but they clearly have the potential to amplify suppress or perhaps even neutralize climate change driven effects on soil microbes and their feedback to carbon exchange (Bardgett et al 2008) A recent synthesis by Tylianakis et al (2008) of data from 688 published studies on the effects of global change on biotic interactions in terrestrial ecosystems (including those that occur in the decomposer food web) highlighted that there is substantial variability among studies in both the magnitude and direction of effects of any given global change driver on any given type of biotic interaction Further that analysis highlighted that the unanticipated effects of multiple drivers acting simultaneously create major challenges in predicting future responses to global environmental change Experimental studies that simultaneously vary two or more global change drivers within the same experiment therefore have considerable promise for improving our understanding of how interactions involving soil communities and their effects on ecosystem-level processes may respond to current global change scenarios

Soil structural integrity and dynamics

The architecture of soil the ways in which particles are arranged in space so forming a stable connected pore space determines the habitat of soil dwelling organisms including plants This soil physical environment is mutable however Soil is hard or dusty but transmits gases readily when dry when wet it becomes soft and plastic and gas ingress becomes much reduced These two extremes are expected to become more prevalent with the changes in climate expected for the UK drier

Page 11

summers and wetter winters The presence of plants indirectly exacerbates the effects of climate change by extracting water in summer and oxygen for root respiration in the winter There is a greater risk of compaction with wetter more plastic soils with late-harvested crops such as potatoes or sugar beet and establishment afterwards Working day access to land may be reduced or more variable leading to damage to soil through inappropriate management (Section B Degradation) Drought may affect soil stability and structure and possibly encourage wind erosion Cecillon et al (2010) examined sites along a latitudinal mountain spatial climate gradient for aggregation and aggregate stability and showed that erodibility was linked to climate and therefore susceptible to change under a shifting climatic regime Other studies have shown effects on organisms associated with the genesis of aggregate structure For instance Eggleton et al (2009) demonstrated in southern England pasture woodland hat earthworm community structure was dependant on soil temperature and water This faunal group has long been established as being of critical importance in no and minimal-till systems both organic and inorganic with potential for declines in aggregate stability as a result of climate change linked to declines in earthworm abundance and shifts in earthworm community structure There are also emerging models linking earthworm population dynamics and soil structural components (Blanchart et al 2009) which offer the possibility of modelling a biotic and abiotic component simultaneously under different climate change scenarios with consequences for hydrology erodibility and trophic level effects

Kohler et al (2009) found that increased CO2 concentrations led to a significantly higher percentage of stable aggregates growing under Lectuca sativa in drought conditions and this was linked to increases in soil microbial biomass and inoculation with a vesicular arbuscular mycorrhizal fungus and plant-growth-promoting rhizobacterium Other workers (Rillig et al 2001) had found a similar effect of elevated carbon dioxide and increased water supply by irrigation on increased aggregate stability due to arbuscular mycorrhizal fungi in soils under Sorghum

Earlier work suggested that climate change would not affect accessibility to land unless winter rainfall increased by 15 (Rounsevell and Brignall 1994) Since this is now what is expected it may be necessary to re-calculate workable days for England based on up-to-date climate change scenarios Neither the direct effect of climate change on soil stability via wet-dry cycles nor its indirect effect via the soil fauna is certain and as Horn and Smucker (2005) have noted that changes in aggregate stability and soil structure can be undesirable if the soil becomes difficult to manage We need to better understand the processes underlying soil structure in order to predict direct soil response to climate change and we need to better understand the wider impact of climate change on soil ecosystems if we are to understand and predict the indirect effects of the soil fauna on soil

Warmer wetter winters may lead to increased competition for oxygen among more strongly respiring organisms in wetter soils into which oxygen penetration is slower Drier summers will lead to soils into which root penetration becomes restricted Both effects are likely to impact on the ability of plants to acquire nutrients and on biogeochemical cycles in general Research on waterlogging appears to have concluded in the 1980s that UK cereals could compensate provided waterlogging did not occur during establishment or repetitively (eg Belford et al 1985) While this may have been true of the conditions prevailing at the time the same may not be true for our future climate The effect that plant root extraction of oxygen has on soil fauna and microflora and vice versa appears to be poorly researched especially in the context of our expected climate change

In summary stability of soil is likely to be impacted by the increasing intensity of wet-dry cycles with climate change but note that an increase is not necessarily desirable if the soil becomes less workable Stepniewska and Stepniewska (2009) have stressed the need for a moderate stable redox above 300 mV Soil fauna and community structure is also likely to be impacted by a change in climate with effects on soil stability that are unclear It is also likely that with wetter winters the number of days when soil is safely accessible by heavy farm machinery without causing damage may become more variable and therefore unpredictable

Page 12

4 Methodologies for investigating the impacts of climate change on soil

Experiments on climate change drivers have been carried out over a variety of spatial and temporal scales ranging from short term laboratory incubation studies to ecosystem-level and long-term manipulations of climatic factors (Wullschleger and Strahl 2010) The main approaches for studying climate change include (1) the use of environmental gradients (temperature and water) and reciprocal transplants (2) in situ field manipulation experiments including Free-Air CO2 Enrichment (FACE) experiments for manipulation of atmospheric CO2 and field-scale manipulations of temperature and precipitation (3) controlled environment facilities such as the Ecotron controlled environment facilities at Imperial College Silwood Park UK and Montpellier France and (4) highly artificial often laboratory based microcosm experiments that have little relevance to real systems These approaches in the order listed above follow a spectrum of decreasing realism but increasing mechanistic control We discuss these approaches in turn

Environmental gradients (temperature and water) and reciprocal transplants

Climatic gradients for instance in annual precipitation and temperature that cross continents countries and elevation gradients are commonly used to determine impacts of climatic variation on soil biota and processes While useful for establishing general patterns such approaches leave significant questions about other factors that could explain differences in soil biota along climatic gradients such as soil fertility and mineralogy To overcome this problem an associated approach is the use of transplant experiments whereby intact soil-vegetation turves (or varying size) are transplanted at different places along climatic gradients so that effects of movement to another climate on soil biota can be assessed This approach for example was used by Briones et al (19971998) who transplanted peat soils from high to lower altitudes at Great Dunn Fell Cumbria to simulate climate warming and that this increased the density of enchytraeid worms the dominant fauna of these peat soils leading to enhanced decomposition and DOC concentrations in soil leachates The same system was also used by Tipping et al (1999) to show that warming and drying can accelerate the production of dissolved organic matter in organic soil horizons Such approaches are valuable in that they provide information on the response of soil biota and processes to real changes in climate but they are limited by the lack of control of environmental variables along transects and potential effects of disturbance from moving soil cores from one site to another

The further experimentation moves away from surveys and experiments in the field the less likely they are to represent real world systems This is not necessarily an issue when detailed and specific mechanisms are being explored but become increasingly problematic when large scale predictions are asserted from them

In situ field manipulation experiments

Many studies have used various field-based manipulations of climate including elevated carbon dioxide in the previously mentioned FACE experiments (eg Norby et al 2004 Jackson et al 2009) drought using rainfall roofs (eg Beier et al 2004) and artificial warming using heating cables (eg Grime et al 2008) passive night time warming roofs (eg Beier et al 2004) and infra-red lamps (Zhang et al 2005) Such experiments have contributed significantly to our understanding of the effects of different climate change drivers on vegetation soil biota and soil processes as detailed in the previous section However as stated previously most studies of this kind have explored effects of single climate factors whereas there is much potential for interactions between multiple factors to have additive or antagonistic effects on soil organisms and the activities that they drive (Bardgett et al 2008) Therefore future experiments which manipulate multiple climate change and other site factors are needed to better understand the effects of climate change on soil biota

As an example of in situ field manipulations Zhang et al (2005) artificially heated soils under tall grass prairie using infra-red heaters to simulate an increase in daily soil temperatures of 18 ndash 27oC and studied two clipping regimes clipped and unclipped In the heated treatments they found changes in the soil microbial community structure as determined using phospholipid fatty acid analysis (PLFA) in the unclipped plots with a shift to fungal dominance but not in the clipped

Page 11

summers and wetter winters The presence of plants indirectly exacerbates the effects of climate change by extracting water in summer and oxygen for root respiration in the winter There is a greater risk of compaction with wetter more plastic soils with late-harvested crops such as potatoes or sugar beet and establishment afterwards Working day access to land may be reduced or more variable leading to damage to soil through inappropriate management (Section B Degradation) Drought may affect soil stability and structure and possibly encourage wind erosion Cecillon et al (2010) examined sites along a latitudinal mountain spatial climate gradient for aggregation and aggregate stability and showed that erodibility was linked to climate and therefore susceptible to change under a shifting climatic regime Other studies have shown effects on organisms associated with the genesis of aggregate structure For instance Eggleton et al (2009) demonstrated in southern England pasture woodland hat earthworm community structure was dependant on soil temperature and water This faunal group has long been established as being of critical importance in no and minimal-till systems both organic and inorganic with potential for declines in aggregate stability as a result of climate change linked to declines in earthworm abundance and shifts in earthworm community structure There are also emerging models linking earthworm population dynamics and soil structural components (Blanchart et al 2009) which offer the possibility of modelling a biotic and abiotic component simultaneously under different climate change scenarios with consequences for hydrology erodibility and trophic level effects

Kohler et al (2009) found that increased CO2 concentrations led to a significantly higher percentage of stable aggregates growing under Lectuca sativa in drought conditions and this was linked to increases in soil microbial biomass and inoculation with a vesicular arbuscular mycorrhizal fungus and plant-growth-promoting rhizobacterium Other workers (Rillig et al 2001) had found a similar effect of elevated carbon dioxide and increased water supply by irrigation on increased aggregate stability due to arbuscular mycorrhizal fungi in soils under Sorghum

Earlier work suggested that climate change would not affect accessibility to land unless winter rainfall increased by 15 (Rounsevell and Brignall 1994) Since this is now what is expected it may be necessary to re-calculate workable days for England based on up-to-date climate change scenarios Neither the direct effect of climate change on soil stability via wet-dry cycles nor its indirect effect via the soil fauna is certain and as Horn and Smucker (2005) have noted that changes in aggregate stability and soil structure can be undesirable if the soil becomes difficult to manage We need to better understand the processes underlying soil structure in order to predict direct soil response to climate change and we need to better understand the wider impact of climate change on soil ecosystems if we are to understand and predict the indirect effects of the soil fauna on soil

Warmer wetter winters may lead to increased competition for oxygen among more strongly respiring organisms in wetter soils into which oxygen penetration is slower Drier summers will lead to soils into which root penetration becomes restricted Both effects are likely to impact on the ability of plants to acquire nutrients and on biogeochemical cycles in general Research on waterlogging appears to have concluded in the 1980s that UK cereals could compensate provided waterlogging did not occur during establishment or repetitively (eg Belford et al 1985) While this may have been true of the conditions prevailing at the time the same may not be true for our future climate The effect that plant root extraction of oxygen has on soil fauna and microflora and vice versa appears to be poorly researched especially in the context of our expected climate change

In summary stability of soil is likely to be impacted by the increasing intensity of wet-dry cycles with climate change but note that an increase is not necessarily desirable if the soil becomes less workable Stepniewska and Stepniewska (2009) have stressed the need for a moderate stable redox above 300 mV Soil fauna and community structure is also likely to be impacted by a change in climate with effects on soil stability that are unclear It is also likely that with wetter winters the number of days when soil is safely accessible by heavy farm machinery without causing damage may become more variable and therefore unpredictable

Page 12

4 Methodologies for investigating the impacts of climate change on soil

Experiments on climate change drivers have been carried out over a variety of spatial and temporal scales ranging from short term laboratory incubation studies to ecosystem-level and long-term manipulations of climatic factors (Wullschleger and Strahl 2010) The main approaches for studying climate change include (1) the use of environmental gradients (temperature and water) and reciprocal transplants (2) in situ field manipulation experiments including Free-Air CO2 Enrichment (FACE) experiments for manipulation of atmospheric CO2 and field-scale manipulations of temperature and precipitation (3) controlled environment facilities such as the Ecotron controlled environment facilities at Imperial College Silwood Park UK and Montpellier France and (4) highly artificial often laboratory based microcosm experiments that have little relevance to real systems These approaches in the order listed above follow a spectrum of decreasing realism but increasing mechanistic control We discuss these approaches in turn

Environmental gradients (temperature and water) and reciprocal transplants

Climatic gradients for instance in annual precipitation and temperature that cross continents countries and elevation gradients are commonly used to determine impacts of climatic variation on soil biota and processes While useful for establishing general patterns such approaches leave significant questions about other factors that could explain differences in soil biota along climatic gradients such as soil fertility and mineralogy To overcome this problem an associated approach is the use of transplant experiments whereby intact soil-vegetation turves (or varying size) are transplanted at different places along climatic gradients so that effects of movement to another climate on soil biota can be assessed This approach for example was used by Briones et al (19971998) who transplanted peat soils from high to lower altitudes at Great Dunn Fell Cumbria to simulate climate warming and that this increased the density of enchytraeid worms the dominant fauna of these peat soils leading to enhanced decomposition and DOC concentrations in soil leachates The same system was also used by Tipping et al (1999) to show that warming and drying can accelerate the production of dissolved organic matter in organic soil horizons Such approaches are valuable in that they provide information on the response of soil biota and processes to real changes in climate but they are limited by the lack of control of environmental variables along transects and potential effects of disturbance from moving soil cores from one site to another

The further experimentation moves away from surveys and experiments in the field the less likely they are to represent real world systems This is not necessarily an issue when detailed and specific mechanisms are being explored but become increasingly problematic when large scale predictions are asserted from them

In situ field manipulation experiments

Many studies have used various field-based manipulations of climate including elevated carbon dioxide in the previously mentioned FACE experiments (eg Norby et al 2004 Jackson et al 2009) drought using rainfall roofs (eg Beier et al 2004) and artificial warming using heating cables (eg Grime et al 2008) passive night time warming roofs (eg Beier et al 2004) and infra-red lamps (Zhang et al 2005) Such experiments have contributed significantly to our understanding of the effects of different climate change drivers on vegetation soil biota and soil processes as detailed in the previous section However as stated previously most studies of this kind have explored effects of single climate factors whereas there is much potential for interactions between multiple factors to have additive or antagonistic effects on soil organisms and the activities that they drive (Bardgett et al 2008) Therefore future experiments which manipulate multiple climate change and other site factors are needed to better understand the effects of climate change on soil biota

As an example of in situ field manipulations Zhang et al (2005) artificially heated soils under tall grass prairie using infra-red heaters to simulate an increase in daily soil temperatures of 18 ndash 27oC and studied two clipping regimes clipped and unclipped In the heated treatments they found changes in the soil microbial community structure as determined using phospholipid fatty acid analysis (PLFA) in the unclipped plots with a shift to fungal dominance but not in the clipped

Page 12

4 Methodologies for investigating the impacts of climate change on soil

Experiments on climate change drivers have been carried out over a variety of spatial and temporal scales ranging from short term laboratory incubation studies to ecosystem-level and long-term manipulations of climatic factors (Wullschleger and Strahl 2010) The main approaches for studying climate change include (1) the use of environmental gradients (temperature and water) and reciprocal transplants (2) in situ field manipulation experiments including Free-Air CO2 Enrichment (FACE) experiments for manipulation of atmospheric CO2 and field-scale manipulations of temperature and precipitation (3) controlled environment facilities such as the Ecotron controlled environment facilities at Imperial College Silwood Park UK and Montpellier France and (4) highly artificial often laboratory based microcosm experiments that have little relevance to real systems These approaches in the order listed above follow a spectrum of decreasing realism but increasing mechanistic control We discuss these approaches in turn

Environmental gradients (temperature and water) and reciprocal transplants

Climatic gradients for instance in annual precipitation and temperature that cross continents countries and elevation gradients are commonly used to determine impacts of climatic variation on soil biota and processes While useful for establishing general patterns such approaches leave significant questions about other factors that could explain differences in soil biota along climatic gradients such as soil fertility and mineralogy To overcome this problem an associated approach is the use of transplant experiments whereby intact soil-vegetation turves (or varying size) are transplanted at different places along climatic gradients so that effects of movement to another climate on soil biota can be assessed This approach for example was used by Briones et al (19971998) who transplanted peat soils from high to lower altitudes at Great Dunn Fell Cumbria to simulate climate warming and that this increased the density of enchytraeid worms the dominant fauna of these peat soils leading to enhanced decomposition and DOC concentrations in soil leachates The same system was also used by Tipping et al (1999) to show that warming and drying can accelerate the production of dissolved organic matter in organic soil horizons Such approaches are valuable in that they provide information on the response of soil biota and processes to real changes in climate but they are limited by the lack of control of environmental variables along transects and potential effects of disturbance from moving soil cores from one site to another

The further experimentation moves away from surveys and experiments in the field the less likely they are to represent real world systems This is not necessarily an issue when detailed and specific mechanisms are being explored but become increasingly problematic when large scale predictions are asserted from them

In situ field manipulation experiments

Many studies have used various field-based manipulations of climate including elevated carbon dioxide in the previously mentioned FACE experiments (eg Norby et al 2004 Jackson et al 2009) drought using rainfall roofs (eg Beier et al 2004) and artificial warming using heating cables (eg Grime et al 2008) passive night time warming roofs (eg Beier et al 2004) and infra-red lamps (Zhang et al 2005) Such experiments have contributed significantly to our understanding of the effects of different climate change drivers on vegetation soil biota and soil processes as detailed in the previous section However as stated previously most studies of this kind have explored effects of single climate factors whereas there is much potential for interactions between multiple factors to have additive or antagonistic effects on soil organisms and the activities that they drive (Bardgett et al 2008) Therefore future experiments which manipulate multiple climate change and other site factors are needed to better understand the effects of climate change on soil biota

As an example of in situ field manipulations Zhang et al (2005) artificially heated soils under tall grass prairie using infra-red heaters to simulate an increase in daily soil temperatures of 18 ndash 27oC and studied two clipping regimes clipped and unclipped In the heated treatments they found changes in the soil microbial community structure as determined using phospholipid fatty acid analysis (PLFA) in the unclipped plots with a shift to fungal dominance but not in the clipped

Page 13

treatment which did however have lower microbial biomass However in a study of a forested system Frey et al (2008) used buried heating cables over 12 years and detected an increase in abundance of bacteria and actinomycetes However it is difficult to determine whether the differences in these two studies are due to the differences in the ecosystems studied the length of study or the method of warming Manipulation of rainfall (Cruz-Martinez et al 2009) has been shown to lead to no major changes in bacterial species leading to the conclusion that soil microbial consortia were more resilient but this study was limited to ammonia oxidisers The University of Sheffield field experiments at Buxton Derbyshire set up under the then NERC Unit of Comparative Plant Ecology represents a nationally important resource ndash much insight into potential climate change effects in vegetation have already been gained from this careful comprehensive set of experiments and offers potential for greatly expanded work on the soil plant system Likewise EU-funded infrastructure project INCREASE (httpwwwincrease-infrastructureeuAboutaspx) provides a framework of six large-scale climate change experiments to explore effects of climate change on shrubland soils and already this approach has yielded insights into effects of warming and drought on soil processes across sites (Emmett et al 2004) and at individual sites on soil carbon fluxes (Sowerby et al 2006) and fungal diversity (Toberman et al 2008)

Long-term experiments (LTE) are able to track the slow changes in soil and plant properties including changes in soil carbon storage It may be possible to deduce the anticipated effect of changes in climate from a study of such data from experiments in regions where the climate already approximates what is expected Currently the best database of LTEs with agronomic and soils data world-wide uploads by members of the soil and agricultural community is maintained at Duke University North Carolina USA (httpltseenvdukeedu) A single database overcomes the difficulty of varying presentation and storage of data but it cannot overcome the difficulties pose by (i) different reasons for setting up the experiments initially (ii) changes in an experiment and recording of data during the course of the experiment (iii) different statistical resolving power due to different numbers of replicates experimental design and so on (iv) rights of access to the data and (v) small but important details specific to each experiment and understood by the data-holder only For this reason LTEs and datasets cannot be viewed as a simple resource into which to tap rapidly

Controlled environment facilities

A number of experiments have been done using various kinds of controlled environmental facilities for studying climate change impacts on plants and soils These studies have the benefit of being able to manipulate plant and soil communities while also controlling environmental conditions that would otherwise vary in the field thereby confounding experimental treatments Moreover the scale of these experiments means that replicate experimental treatments can be established and detailed mechanistic responses to climate change can be detected The down side is that they are artificial to varying degrees and they are often very costly and labour intensive to run The controlled environment facilities such as the Ecotron controlled environment facilities at Imperial College Silwood Park UK and Montpellier France (httpwwwecotroncnrsfr) are good examples of this approach as are the solardomes which used to be at Lancaster University but no longer exist here climatic conditions (eg elevated CO2) within sixteen large glasshouses or lsquosolardomesrsquo could be manipulated and plant and soil responses could be detected over time (Heath et al 2005)

Microcosm experiments

There have been numerous laboratory experimental manipulations to determine the response of soil biota and their activities to climate change These kind of studies are often short‐term and are done under very artificial and structurally simple conditions and use a limited range of organisms that vary greatly in performance in microcosms As already highlighted soil food webs nature are highly complex and involve a multitude of interactions that cannot be revealed under simple laboratory conditions As a consequence such experiments are not accurate simulations of actual soil-plant systems The suite of methodologies for determining the structure composition and functional potential of the soil biological community identified in the project ldquoSQID Prioritising biological indicators of soil quality for deployment in a national-scale soil monitoring schemerdquo (Defra Project No

Page 14

SP0529) will continue to provide objective and interpretable data when used in these contexts (Black et al 2008) Critically the ldquological sieverdquo approached developed in SQID can be used to provide an indication of the most appropriate techniques for studying climate change (Ritz et al 2009) New methodological approaches are being tested in Defra Project SP0570 ldquoClimate change impacts on soil biotardquo Critically many studies use very limited methodologies to study changes in microbial communities sometimes even single groups (eg ammonia oxidising bacteria) using molecular approaches are used to draw wider inferences ndash this can be potentially misleading As suggested by the SQID programme (Ritz et al 2009) the only way to obtain credible whole community structure and function data is to use the broad phenotypic genotypic and functional capability approach applied in a wide variety of climate change experiments

5 Conclusions

The last two decades have witnessed a greatly improved understanding of the potential effects of climate change on soil biota and the functions that they drive From this research it is evident that climate change can impact on soil biota and soil functioning both directly and indirectly often with significant consequences for ecosystem services such as carbon sequestration and carbon-cycle feedbacks to the atmosphere Despite this much remains to be learned about the mechanisms by which climate change impacts on soil biota and the consequences of this for soil processes including respiratory fluxes from soil For example while it is now well known that temperature acts as an important determinant of the rate of organic matter decomposition the nature of the relationship between temperature and the activity of decomposer organisms and its potential to feedback to climate change is unclear Also while there is mounting evidence that soil biota and their activities are strongly affected by extreme events associated with climate change the consequences of this for decomposition processes nutrient and carbon cycling remains poorly understood As noted recently by several authors this uncertainty extends to unreliable model predictions of soil carbon feedbacks and resolving this issue is a major challenge for the future

One thing that is becoming increasingly clear is that understanding the effects of climate change on ecosystem processes requires a holistic ecosystem-level approach whereby responses of plant and soil biological communities and resulting feedbacks on nutrient and carbon cycling are considered in tandem over often long timescales However to achieve this goal requires a focused effort on three research questions

(1) Research is needed to understand how feedbacks between plant and soil communities are altered by climate change and the influence of this on ecosystem processes This includes a need for greater understanding of the relative direct and indirect effects of climate change on soil biota and functions that they drive and how they vary with environmental context

(2) There is a need for a greater integration of physical chemical and biological responses of soils to climate change in particular exploring the role of soil biota in modifying soil biophysical properties under climate change For instance little is known about the effects on soil physical properties and oxygen availability of climate change induced changes in plant root growth and extraction and of the role of soil biota in these interactions Also greater understanding is required of the processes underlying soil structure in order to predict direct soil responses to climate change and indirect effects of this on soil biota and their roles in biogeochemical processes

(3) It is important to recognize that climate change does not operate independently of other factors such as land use change and atmospheric nitrogen deposition and therefore there is an urgent need for studies that simultaneously consider multiple drivers on soil biota and their activities As highlighted in this review multiple climate change drivers (eg temperature extreme events and elevated carbon dioxide) have the potential to amplify suppress or perhaps even neutralize climate change driven effects on soil biota and ecosystem processes and in this sense there has only been modest (at best) advances since Defra project SP0538 (see Bradley et al 2005) in understanding climate effects on soil biota Experimental studies that simultaneously vary two or more global change

Page 15

drivers within the same experiment therefore have considerable promise for improving our understanding of how interactions involving soil communities and their effects on ecosystem-level processes may respond to current global change scenarios

There are a variety of experimental approaches for exploring effects of climate change on soil biota and the processes that they drive To address the above challenges we highlight the need for (a) greater exploitation of current nationally important facilities (eg Rothamsted and Buxton Climate Change Experiments Derbyshire) and funding of more detailed studies into responses of soil biota to long-term in situ climate manipulations along with associated mesocosm studies to refine mechanistic understanding (b) simultaneous assessment of soil biota responses at the phenotypic genotypic and functional level (c) studies to be performed along environmental gradients using similar climatic manipulations to better understand how responses to climate vary in different situations and (d) multi-factor experiments with large-scale long term manipulations of multiple climate change (eg precipitation temperature etc) and other factors such as land use

References Allison SD CI Czimczik and KK Treseder 2008 Microbial activity and soil respiration under nitrogen addition in Alaskan boreal forest Global Change Biology 14 1156 ndash 1168

Bardgett RD and Wardle DA 2010 Aboveground-Belowground Linkages Biotic Interactions Ecosystem Processes and Global Change Oxford Ecology and Evolution Series Oxford University Press

Bardgett RD Freeman C Ostle N (2008) Microbial contributions to climate change through carbon-cycle feedbacks The ISME Journal 2 805-814

Bardgett RD Kandeler E Tscherko D Hobbs PJ Jones TH Thompson LJ and Bezemer TM (1999) Below-ground microbial community development in a high temperature world Oikos 85 193-203

Bardgett RD and E McAlister 1999 The measurement of soil fungalbacterial biomass ratios as an indicator of ecosystem self-regulation in temperate meadow grasslands Biology and Fertility of Soils 29 282-290

Bardgett RD (2005) The Biology of Soil A Community and Ecosystem Approach Oxford University Press Oxford UK

Beier C Emmett B Gundersen P Tietema A Penuelas J Estiarte M Gordon C Gorissen A Llorens L Roda F and Williams D (2004) Novel approaches to study climate change effects on terrestrial ecosystems in the field - drought and passive night time warming Ecosystems 7 583-597

Belford RL Cannell RQ and Thomson RJ (1985) Effects of single and multiple waterloggings on the growth and yield of winter wheat on a clay soil Journal of the Science fo Food and Agriculture 36 142-156

Black H I J Ritz K Campbell C D Harris J A Wood C Chamberlain P M Parekh N Towers W and Scott A (2008) Prioritising biological indicators of soil quality for deployment in a national-scale soil monitoring scheme Final Report Defra Project SP0529

Blanchart E Marilleau N Chotte J-L Drogoul A Perrier E and Cambier Ch (2009) SWORM an agent-based model tosimulate the effects of earthworms on soil structure European Journal of Soil Science 60 13 ndash 21

Blom CWPM (1999) Adaptations to flooding stress From plant community to molecule Plant Biology 1 261-273

Bradley RI Moffat A Vanguelova E Falloon P and Harris J (2005) Defra Project SP0538 - The Impact of Climate Change on Soil Functions SP0538

Page 16

Briones MJI Ineson P and Piearce TG (1997) Effects of climate change on soil fauna responses of enchytraeids Diptera larvae and tardigrades in a transplant experiment Applied Soil Ecology 6 117-134

Briones MJI Ineson P and Poskitt J (1998) Climate change and Cognettia sphagnetorum effects on carbon dynamics in organic soils Functional Ecology 12 528-535

Brussaard L BehanPelletier VM Bignell DE Brown VK Didden W Folgarait P Fragoso C Freckman DW Gupta VVSR Hattori T Hawksworth DL Klopatek C Lavelle P Malloch DW Rusek J Soderstrom B Tiedje JM and Virginia RA (1997) Biodiversity and ecosystem functioning in soil Ambio 26 563-570

Carreiro MM Sinsabaugh RL Repert DA and Pankhurst DF (2000) Microbial enzyme shifts explain litter decay responses to simulated nitrogen deposition Ecology 81 2359-2365

Cecillon L de Mello NA De Danieli S Brun J-J (2010) Soil macroaggregate dynamics in a mountain spatial climate gradient Biogeochemistry 97 31 ndash 43

Chuang S-C and Chen JH 2008 Role of diurnal rhythm of oxygen consumption in emergence from soil at night after heavy rain by earthworms Invertebrate Biology 127 80ndash86

Cole L Bardgett RD Ineson P and Adamson J (2002a) Relationships between enchytraeid worms (Oligochaeta) temperature and the release of dissolved organic carbon from blanket peat in northern England Soil Biology and Biochemistry 34 599-607

Cole L Bardgett RD Ineson P and Hobbs PJ (2002b) Enchytraeid worm (Oligochaeta) influences on microbial community structure nutrient dynamics and plant growth in blanket peat subjected to warming Soil Biology and Biochemistry 34 83-92

Cox PM Betts RA Jones CD Spall SA and Totterdell IJ (2000) Acceleration of global warming due to carbon-cycle feedbacks in a coupled climate model Nature 408 184-187

Conen F J Leifeld B Seth and C Alewell (2006) Warming mobilises young and old soil carbon equally Biogeosciences 3515ndash519

Cruz-Martinez K Suttle KB Brodie EL Power ME Anderson GL and Banfield JF (2009) Despite strong seasonal responses soil microbial consortia are more resilient to long-term changes in rainfall than overlying grassland The ISME Journal 3 738 ndash 744

Davidson EA and Janssens IA (2006) Temperature sensitivity of soil carbon decomposition and feedbacks to climate change Nature 440 165-173

De Deyn GB HC Cornelissen and RD Bardgett 2008 Plant functional traits and soil carbon sequestration in contrasting biomes Ecology Letters 11 516ndash531

De Graaff MA KJ van Groenigen J Six B Hungate and C van Kessel 2006 Interactions between plant growth and soil nutrient cycling under elevated CO2 a meta-analysis Global Change Biology 12 2077ndash2091

Donnison LM Griffith GS and Bardgett RD (2000b) Determinants of fungal growth and activity in botanically diverse haymeadows effects of litter type and fertilizer additions Soil Biology and Biochemistry 32 289-294

Dowrick DJ S Hughes C Freeman MA Lock B Reynolds and JA Hudson 1999 Nitrous oxide emissions from a gully mire in mid-Wales UK under simulated summer drought Biogeochemistry 44 151-162

Dickin E Bennett S Wright D 2009 Growth and yield responses of UK wheat cultivars to winter waterlogging Journal of Agricultural Science 147 127-140

Dickin E Wright D 2008 The effects of winter waterlogging and summer drought on the growth and yield of winter wheat (Triticum aestivum L) European Journal of Agronomy 28 234-244

Emmett BA Beier C Estiarte M Tietema A Kristensen HL Williams D Pentildeuelas J Schmidt IK and Sowerby A (2004) The response of soil processes to climate change Results from manipulation studies across an environmental gradient Ecosystems 7 625-637

Page 17

Ettema CH R Lowrance and D C Coleman (1999) Riparian soil response to surface nitrogen input the indicator potential of free-living soil nematode populations Soil Biology and Biochemistry 31 1625-1638

Egerton-Warburton LM and Allen EB (2000) Shifts in arbuscular mycorrhizal communities along an anthropogenic nitrogen deposition gradient Ecological Applications 10 484-496

Eggleton P Inward K Smith J Jones DT and Sherlock E (2009) A six year study of earthworm (Lumbricidae) populations in pasture woodland in southern England shows their responses to soil temperature and soil moisture Soil Biology and Biochemistry 41 1857 ndash 1865

Fang CM P Smith JB Moncrieff JU Smith (2005) Similar response of labile and resistant soil organic matter pools to changes in temperature Nature 433 57-59

Fenner N Ostle NJ McNamara N Sparks T Freeman C (2007a) Elevated CO2 Effects on Peatland plant community carbon dynamics and DOC production Ecosystems 10 635-647

Fenner N Freeman C Lock MA Harmens H Sparks T (2007b) Interactions between elevated CO2 and warming could amplify DOC exports from peatland catchments Environmental Science and Technology 41 3146-3152

Finzi AC DeLucia EH Hamilton JG Richter DD and Schelsinger WH (2002) The nitrogen budget of a pine forest under free-air CO2 enrichment Oecologia 132 567-578

Freeman C GB Nevison H Kang S Hughes B Reynolds and JA Hudson 2002 Contrasted effects of simulated drought on the production and oxidation of methane in a mid-Wales wetland Soil Biology and Biochemistry 34 61-67

Freeman C NJ Ostle N Fenner H Kang 2004 A regulatory role for phenol oxidase during decomposition in peatlands Soil Biology and Biochemistry 36 1663-1667

Frey SD Knorr M Parrent JL and Simpson RT (2004) Chronic nitrogen enrichment affects the structure and function of the soil microbial community in temperate hardwood and pine forests Forest Ecology and Management 196 159-171

Frey SD Drijber R Smith H and Melillo J (2008) Microbial biomass functional capacity and community structure after 12 years of soil warming Soil Biology and Biochemistry 40 2904 ndash 2907

Friedlingstein P Cox P Betts R Bopp L Von Bloh W Brovkin V Cadule P Doney S Eby M Fung I Bala G John J Jones C Joos F Kato T Kawamiya M Knorr W Lindsay K Matthews HD Raddatz T Rayner P Reick C Roeckner E Schnitzler KG Schnur R Strassmann K Weaver AJ Yoshikawa C and Zeng N (2006) Climate-carbon cycle feedback analysis Results from the (CMIP)-M-4 model intercomparison Journal of Climate 19 3337-3353

Gange AC EG Gange TH Sparks L Boddy 2007 Rapid and recent changes in fungal fruiting patterns Science 316 71

Gordon H PM Haygarth and RD Bardgett 2008 Drying and rewetting effects on soil microbial community composition and nutrient leaching Soil Biology and Biochemistry 40 302-311

Gregory AS Watts CW Griffiths BS Hallett PD Kuan HS and Whitmore AP (2009) The effect of long-term soil management on the physical and biological resilience of a range of arable and grassland soils in England Geoderma 153 172-185

Grime JP Fridley JD Askew AP Thompson K Hodgson JG and Bennett CR (2008) Long-term resistance to simulated climate change in an infertile grassland Proceedings of the National Academy of Sciences USA 105 100028-10032

Harris JA (2009) Soil microbial communities and restoration ecology facilitators or followers Science 325 573-574

Heath J Ayres E Possell M Bardgett RD Black HIJ Grant H Ineson P and Kersteins G (2005) Rising atmospheric CO2 reduces soil carbon sequestration Science 309 1711-1713

Houghton JT LG Meira Filho BA Callender 1996 Climate Change 1995 The Science of Climate Change Intergovernmental Panel on Climate Change Cambridge University Press Cambridge

Page 18

Horn R and Smucker A (2005) Structure formation and its consequences for gas and water transport in unsaturated arable and forest soils Soil amp Tillage Research 82 5ndash14

Jackson RB CW Cook JS Poppen et al (2009) Increased belowground biomass and soil CO2 fluxes after a decade of carbon dioxide enrichment in a warm-temperate forest Ecology 90 3352-3366

Jenkins GJ Murphy JM Sexton DS Lowe JA Jones P and Kilsby CG (2009) Uk Climate Projections Briefing report Met Office Hadley Centre Exeter UK

Jenkinson DS Adams DE and Wild A (1991) Model Estimates of Co2 Emissions from Soil in Response to Global Warming Nature 351 304-306

Jenkinson DS and Coleman K (2008) The turnover of organic carbon in subsoils Part 2 Modelling carbon turnover European Journal of Soil Science 59 400-413

Kandeler E Tscherko D Bardgett RD Hobbs PJ Kampichler C and Jones TH (1998) The response of soil microorganisms and roots to elevated CO2 and temperature in a terrestrial model ecosystem Plant and Soil 202 251-262

Kohler J Caravaca F Alguacil MdM and Roldan A (2009) Elevated CO2 increases the effect of an arbuscular mycorrhizal fungus and a plant-growth-promoting rhizobacterium on structural stability of a semiarid agricultural soil under drought conditions Soil Biology and Biochemistry 41 1710 ndash 1716

Kuan HL Hallet PD Griffiths BS Gregory AS Watts CW and Whitmore AP (2007) The resilience of a selection of Scottish soils to biological and physical stress European Journal of Soil Science 58 811-821

Liu L and TL Greaver 2009 A review of nitrogen enrichment effects on three biogenic GHGs the CO2 sink may be largely offset by stimulated N2O and CH4 emission Ecology Letters 12 1103 ndash 1117

Luo Y Su B Currie WS Dukes JS Finzi A Hartwig U Hungate B McMurtrie RE Oren R Parton WJ Pataki DE Shaw MR Zak DR and Field CB (2004) Progressive nitrogen limitation responses to rising atmopsheric carbon dioxide BioScience 54 731-739

Meyer KM Mooij WM Vos M Hol WHG and van der Putten WH (2009) The power of simulating experiments Ecological Modelling 220 2594 ndash 2597

Mikkelsen TN Beier C Jonasson S Holmstrup M Schmidt IK Ambus P Pilegaard K Michelsen A Albert K Andresen LC Arndal MF Bruun N Christensen S Danbaek S Gundersen P Jorgensen P Linden LG Kongstad J Maraldo K Prieme A Riis-Nielsen T Ro-Poulsen H Stevnbak K Selsted MB Sorensen P Larsen KS Carter MS Ibrom A Martinussen T Miglietta F and Sverdrup H (2008) Experimental design of multifactor climate change experiments with elevated CO2 warming and drought the CLIMAITE project Functional Ecology 22 185-195

Norby R J J Ledford C D Reilly et al (2004) Fine-root production dominates response of a deciduous forest to atmospheric CO2 enrichment Proceedings of the National Academy of Sciences USA 101 9689ndash9693

Plum N Terrestrial invertebrates in flooded grassland A literature review 2005 Wetlands 25 721-737

Ritz K amp Black HIJ amp Campbell CD amp Harris JA (2009) Selecting biological indicators for monitoring soils A framework for balancing scientific and technical opinion to assist policy development Ecological Indicators 1212 - 1221

Robinson DA Lebron I Vereecken H (2009) On the definition of the natural capital of soils A framework for description evaluation and monitoring Soil Science Society of America Journal 73 1904 ndash 1911

Roulet NT and TR Moore 1995 The effect of forestry drainage practices on the emissions of methane from northern peatlands Canadian Journal of Forest Research 25 491ndash499

Page 19

Rounsevell MDA amp Brignall AP (1994) The potential effects of climate change on autumn soil tillage opportunities in England and Wales Soil amp Tillage Research 32 275-289

Sala O E F S Chapin J J Armesto R Berlow J Bloomfield R Dirzo E Huber-Sanwald LF Huenneke RB Jackson A Kinzig R Leemans D Lodge HA Mooney M Oesterheld NL Poff MT Sykes BH Walker M Walker and DH Wall 2000 Global biodiversity scenarios for the year 2100 Science 287 1770-1774

Scheu S and Schaefer M (1998) Bottom-up control of the soil macrofauna community in a beechwood on limestone Manipulation of food sources Ecology 79 1573-1585

Schimel J TC Balser and M Wallenstein 2007 Microbial stress-response physiology and its implications for ecosystem function Ecology 88 1386-1394

Sowerby A Emmett BA et al (2008) Contrasting effects of repeated summer drought on soil carbon efflux in hydric and mesic heathland soils Global Change Biology 14 2388-2404

Tillig MC Wright SF Kimball BA Pinter PJ Wall GW Ottman MJ Leavitt SW (2001) Elevated carbon dioxide and irrigation effects on water stable aggregates in a Sorghum field a possible role for arbuscular mycorrhizal fungi Global Change Biology 7 333 ndash 337

Tipping E Woof C Rigg E Harrison AF Ineson P Taylor K Benham D Poskitt J Rowland AP Bol R and Harkness DD (1999) Climatic influences on the leaching of dissolved organic matter from upland UK moorland soils investigated by a field manipulation experiment Environment International 25 83-95

Toberman H Freeman C et al (2008) Summer drought decreases soil fungal diversity and associated phenol oxidase activity in upland Calluna heathland soil FEMS Microbiology Ecology 66 426-436

Treseder KK 2008 Nitrogen additions and microbial biomass a meta-analysis of ecosystem studies Ecology Letters 11 1111-1120

Ritz K Black HIJ Campbell CD Harris JA and Wood C (2009) Selecting ecological indicators for monitoring soils a framework for balancing scientific opinion to assist policy development Ecological Indicators 9 1212-1221

Schlesinger WH 2009 On the fate of anthropogenic nitrogen Proceedings of the National Academy Sciences USA 106 203-208

Stanhill G Cohen S 2001 Global dimming a review of the evidence for a widespread and significant reduction in global radiation with discussion of its probable causes and possible agricultural consequences Agricultural and Forest Meteorology 107 255-278

Stepniewska W and Stepniewska Z (2009) Selected oxygen-dependent proceses ndash Response to soil management and tillage Soil Tillage Research 102 193-200

Tylianakis JM Didham RK Bascompte J and Wardle DA (2008) Global change and species interactions in terrestrial ecosystems Ecology Letters 11 1351-1363

Van der Heijden MGA RD Bardgett and NM van Straalen 2008 The unseen majority soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems Ecology Letters 11 296-310

Waldrop MP Zak DR and Sinsabaugh RL (2004) Microbial community responses to nitrogen deposition in northern forest ecosystems Soil Biology and Biochemistry 36 1443-1451

Ward SE RD Bardgett NP McNamara JK Adamson and NJ Ostle 2007 Long-term consequences of grazing and buring on northern peatland carbon dynamics Ecosystems 10 1069-1083

Wardle DA (2002) Communities and Ecosystems Linking Aboveground and Belowground Components Princeton University Press Princeton NJ USA

Wardle DA Bardgett RD Klironomos JN Setaumllauml H van der Putten WH and Wall DH (2004) Ecological linkages between aboveground and belowground biota Science 304 1629-1633

Page 20

Whitmore AP and Whalley WR (2009) Physical effects of soil drying on roots and crop growth Journal of Experimental Botany 60 2845-2857

Wullschleger SD and Strahl M (2010) Climate change A controlled experiment Scientific American 302 60 ndash 65

Zhang W parker KM Luo Y Wan S Wallace LL and Hu S (2005) Soil microbial responses to experimental warming and clipping in a tallgrass prairie Global Change Biology 11 266 ndash 277

• Heath J Ayres E Possell M Bardgett RD Black HIJ Grant H Ineson P and Kersteins G (2005) Rising atmospheric CO2 reduces soil carbon sequestration Science 309 1711-1713

Page 14

SP0529) will continue to provide objective and interpretable data when used in these contexts (Black et al 2008) Critically the ldquological sieverdquo approached developed in SQID can be used to provide an indication of the most appropriate techniques for studying climate change (Ritz et al 2009) New methodological approaches are being tested in Defra Project SP0570 ldquoClimate change impacts on soil biotardquo Critically many studies use very limited methodologies to study changes in microbial communities sometimes even single groups (eg ammonia oxidising bacteria) using molecular approaches are used to draw wider inferences ndash this can be potentially misleading As suggested by the SQID programme (Ritz et al 2009) the only way to obtain credible whole community structure and function data is to use the broad phenotypic genotypic and functional capability approach applied in a wide variety of climate change experiments

5 Conclusions

The last two decades have witnessed a greatly improved understanding of the potential effects of climate change on soil biota and the functions that they drive From this research it is evident that climate change can impact on soil biota and soil functioning both directly and indirectly often with significant consequences for ecosystem services such as carbon sequestration and carbon-cycle feedbacks to the atmosphere Despite this much remains to be learned about the mechanisms by which climate change impacts on soil biota and the consequences of this for soil processes including respiratory fluxes from soil For example while it is now well known that temperature acts as an important determinant of the rate of organic matter decomposition the nature of the relationship between temperature and the activity of decomposer organisms and its potential to feedback to climate change is unclear Also while there is mounting evidence that soil biota and their activities are strongly affected by extreme events associated with climate change the consequences of this for decomposition processes nutrient and carbon cycling remains poorly understood As noted recently by several authors this uncertainty extends to unreliable model predictions of soil carbon feedbacks and resolving this issue is a major challenge for the future

One thing that is becoming increasingly clear is that understanding the effects of climate change on ecosystem processes requires a holistic ecosystem-level approach whereby responses of plant and soil biological communities and resulting feedbacks on nutrient and carbon cycling are considered in tandem over often long timescales However to achieve this goal requires a focused effort on three research questions

(1) Research is needed to understand how feedbacks between plant and soil communities are altered by climate change and the influence of this on ecosystem processes This includes a need for greater understanding of the relative direct and indirect effects of climate change on soil biota and functions that they drive and how they vary with environmental context

(2) There is a need for a greater integration of physical chemical and biological responses of soils to climate change in particular exploring the role of soil biota in modifying soil biophysical properties under climate change For instance little is known about the effects on soil physical properties and oxygen availability of climate change induced changes in plant root growth and extraction and of the role of soil biota in these interactions Also greater understanding is required of the processes underlying soil structure in order to predict direct soil responses to climate change and indirect effects of this on soil biota and their roles in biogeochemical processes

(3) It is important to recognize that climate change does not operate independently of other factors such as land use change and atmospheric nitrogen deposition and therefore there is an urgent need for studies that simultaneously consider multiple drivers on soil biota and their activities As highlighted in this review multiple climate change drivers (eg temperature extreme events and elevated carbon dioxide) have the potential to amplify suppress or perhaps even neutralize climate change driven effects on soil biota and ecosystem processes and in this sense there has only been modest (at best) advances since Defra project SP0538 (see Bradley et al 2005) in understanding climate effects on soil biota Experimental studies that simultaneously vary two or more global change

Page 15

drivers within the same experiment therefore have considerable promise for improving our understanding of how interactions involving soil communities and their effects on ecosystem-level processes may respond to current global change scenarios

There are a variety of experimental approaches for exploring effects of climate change on soil biota and the processes that they drive To address the above challenges we highlight the need for (a) greater exploitation of current nationally important facilities (eg Rothamsted and Buxton Climate Change Experiments Derbyshire) and funding of more detailed studies into responses of soil biota to long-term in situ climate manipulations along with associated mesocosm studies to refine mechanistic understanding (b) simultaneous assessment of soil biota responses at the phenotypic genotypic and functional level (c) studies to be performed along environmental gradients using similar climatic manipulations to better understand how responses to climate vary in different situations and (d) multi-factor experiments with large-scale long term manipulations of multiple climate change (eg precipitation temperature etc) and other factors such as land use

References Allison SD CI Czimczik and KK Treseder 2008 Microbial activity and soil respiration under nitrogen addition in Alaskan boreal forest Global Change Biology 14 1156 ndash 1168

Bardgett RD and Wardle DA 2010 Aboveground-Belowground Linkages Biotic Interactions Ecosystem Processes and Global Change Oxford Ecology and Evolution Series Oxford University Press

Bardgett RD Freeman C Ostle N (2008) Microbial contributions to climate change through carbon-cycle feedbacks The ISME Journal 2 805-814

Bardgett RD Kandeler E Tscherko D Hobbs PJ Jones TH Thompson LJ and Bezemer TM (1999) Below-ground microbial community development in a high temperature world Oikos 85 193-203

Bardgett RD and E McAlister 1999 The measurement of soil fungalbacterial biomass ratios as an indicator of ecosystem self-regulation in temperate meadow grasslands Biology and Fertility of Soils 29 282-290

Bardgett RD (2005) The Biology of Soil A Community and Ecosystem Approach Oxford University Press Oxford UK

Beier C Emmett B Gundersen P Tietema A Penuelas J Estiarte M Gordon C Gorissen A Llorens L Roda F and Williams D (2004) Novel approaches to study climate change effects on terrestrial ecosystems in the field - drought and passive night time warming Ecosystems 7 583-597

Belford RL Cannell RQ and Thomson RJ (1985) Effects of single and multiple waterloggings on the growth and yield of winter wheat on a clay soil Journal of the Science fo Food and Agriculture 36 142-156

Black H I J Ritz K Campbell C D Harris J A Wood C Chamberlain P M Parekh N Towers W and Scott A (2008) Prioritising biological indicators of soil quality for deployment in a national-scale soil monitoring scheme Final Report Defra Project SP0529

Blanchart E Marilleau N Chotte J-L Drogoul A Perrier E and Cambier Ch (2009) SWORM an agent-based model tosimulate the effects of earthworms on soil structure European Journal of Soil Science 60 13 ndash 21

Blom CWPM (1999) Adaptations to flooding stress From plant community to molecule Plant Biology 1 261-273

Bradley RI Moffat A Vanguelova E Falloon P and Harris J (2005) Defra Project SP0538 - The Impact of Climate Change on Soil Functions SP0538

Page 16

Briones MJI Ineson P and Piearce TG (1997) Effects of climate change on soil fauna responses of enchytraeids Diptera larvae and tardigrades in a transplant experiment Applied Soil Ecology 6 117-134

Briones MJI Ineson P and Poskitt J (1998) Climate change and Cognettia sphagnetorum effects on carbon dynamics in organic soils Functional Ecology 12 528-535

Brussaard L BehanPelletier VM Bignell DE Brown VK Didden W Folgarait P Fragoso C Freckman DW Gupta VVSR Hattori T Hawksworth DL Klopatek C Lavelle P Malloch DW Rusek J Soderstrom B Tiedje JM and Virginia RA (1997) Biodiversity and ecosystem functioning in soil Ambio 26 563-570

Carreiro MM Sinsabaugh RL Repert DA and Pankhurst DF (2000) Microbial enzyme shifts explain litter decay responses to simulated nitrogen deposition Ecology 81 2359-2365

Cecillon L de Mello NA De Danieli S Brun J-J (2010) Soil macroaggregate dynamics in a mountain spatial climate gradient Biogeochemistry 97 31 ndash 43

Chuang S-C and Chen JH 2008 Role of diurnal rhythm of oxygen consumption in emergence from soil at night after heavy rain by earthworms Invertebrate Biology 127 80ndash86

Cole L Bardgett RD Ineson P and Adamson J (2002a) Relationships between enchytraeid worms (Oligochaeta) temperature and the release of dissolved organic carbon from blanket peat in northern England Soil Biology and Biochemistry 34 599-607

Cole L Bardgett RD Ineson P and Hobbs PJ (2002b) Enchytraeid worm (Oligochaeta) influences on microbial community structure nutrient dynamics and plant growth in blanket peat subjected to warming Soil Biology and Biochemistry 34 83-92

Cox PM Betts RA Jones CD Spall SA and Totterdell IJ (2000) Acceleration of global warming due to carbon-cycle feedbacks in a coupled climate model Nature 408 184-187

Conen F J Leifeld B Seth and C Alewell (2006) Warming mobilises young and old soil carbon equally Biogeosciences 3515ndash519

Cruz-Martinez K Suttle KB Brodie EL Power ME Anderson GL and Banfield JF (2009) Despite strong seasonal responses soil microbial consortia are more resilient to long-term changes in rainfall than overlying grassland The ISME Journal 3 738 ndash 744

Davidson EA and Janssens IA (2006) Temperature sensitivity of soil carbon decomposition and feedbacks to climate change Nature 440 165-173

De Deyn GB HC Cornelissen and RD Bardgett 2008 Plant functional traits and soil carbon sequestration in contrasting biomes Ecology Letters 11 516ndash531

De Graaff MA KJ van Groenigen J Six B Hungate and C van Kessel 2006 Interactions between plant growth and soil nutrient cycling under elevated CO2 a meta-analysis Global Change Biology 12 2077ndash2091

Donnison LM Griffith GS and Bardgett RD (2000b) Determinants of fungal growth and activity in botanically diverse haymeadows effects of litter type and fertilizer additions Soil Biology and Biochemistry 32 289-294

Dowrick DJ S Hughes C Freeman MA Lock B Reynolds and JA Hudson 1999 Nitrous oxide emissions from a gully mire in mid-Wales UK under simulated summer drought Biogeochemistry 44 151-162

Dickin E Bennett S Wright D 2009 Growth and yield responses of UK wheat cultivars to winter waterlogging Journal of Agricultural Science 147 127-140

Dickin E Wright D 2008 The effects of winter waterlogging and summer drought on the growth and yield of winter wheat (Triticum aestivum L) European Journal of Agronomy 28 234-244

Emmett BA Beier C Estiarte M Tietema A Kristensen HL Williams D Pentildeuelas J Schmidt IK and Sowerby A (2004) The response of soil processes to climate change Results from manipulation studies across an environmental gradient Ecosystems 7 625-637

Page 17

Ettema CH R Lowrance and D C Coleman (1999) Riparian soil response to surface nitrogen input the indicator potential of free-living soil nematode populations Soil Biology and Biochemistry 31 1625-1638

Egerton-Warburton LM and Allen EB (2000) Shifts in arbuscular mycorrhizal communities along an anthropogenic nitrogen deposition gradient Ecological Applications 10 484-496

Eggleton P Inward K Smith J Jones DT and Sherlock E (2009) A six year study of earthworm (Lumbricidae) populations in pasture woodland in southern England shows their responses to soil temperature and soil moisture Soil Biology and Biochemistry 41 1857 ndash 1865

Fang CM P Smith JB Moncrieff JU Smith (2005) Similar response of labile and resistant soil organic matter pools to changes in temperature Nature 433 57-59

Fenner N Ostle NJ McNamara N Sparks T Freeman C (2007a) Elevated CO2 Effects on Peatland plant community carbon dynamics and DOC production Ecosystems 10 635-647

Fenner N Freeman C Lock MA Harmens H Sparks T (2007b) Interactions between elevated CO2 and warming could amplify DOC exports from peatland catchments Environmental Science and Technology 41 3146-3152

Finzi AC DeLucia EH Hamilton JG Richter DD and Schelsinger WH (2002) The nitrogen budget of a pine forest under free-air CO2 enrichment Oecologia 132 567-578

Freeman C GB Nevison H Kang S Hughes B Reynolds and JA Hudson 2002 Contrasted effects of simulated drought on the production and oxidation of methane in a mid-Wales wetland Soil Biology and Biochemistry 34 61-67

Freeman C NJ Ostle N Fenner H Kang 2004 A regulatory role for phenol oxidase during decomposition in peatlands Soil Biology and Biochemistry 36 1663-1667

Frey SD Knorr M Parrent JL and Simpson RT (2004) Chronic nitrogen enrichment affects the structure and function of the soil microbial community in temperate hardwood and pine forests Forest Ecology and Management 196 159-171

Frey SD Drijber R Smith H and Melillo J (2008) Microbial biomass functional capacity and community structure after 12 years of soil warming Soil Biology and Biochemistry 40 2904 ndash 2907

Friedlingstein P Cox P Betts R Bopp L Von Bloh W Brovkin V Cadule P Doney S Eby M Fung I Bala G John J Jones C Joos F Kato T Kawamiya M Knorr W Lindsay K Matthews HD Raddatz T Rayner P Reick C Roeckner E Schnitzler KG Schnur R Strassmann K Weaver AJ Yoshikawa C and Zeng N (2006) Climate-carbon cycle feedback analysis Results from the (CMIP)-M-4 model intercomparison Journal of Climate 19 3337-3353

Gange AC EG Gange TH Sparks L Boddy 2007 Rapid and recent changes in fungal fruiting patterns Science 316 71

Gordon H PM Haygarth and RD Bardgett 2008 Drying and rewetting effects on soil microbial community composition and nutrient leaching Soil Biology and Biochemistry 40 302-311

Gregory AS Watts CW Griffiths BS Hallett PD Kuan HS and Whitmore AP (2009) The effect of long-term soil management on the physical and biological resilience of a range of arable and grassland soils in England Geoderma 153 172-185

Grime JP Fridley JD Askew AP Thompson K Hodgson JG and Bennett CR (2008) Long-term resistance to simulated climate change in an infertile grassland Proceedings of the National Academy of Sciences USA 105 100028-10032

Harris JA (2009) Soil microbial communities and restoration ecology facilitators or followers Science 325 573-574

Heath J Ayres E Possell M Bardgett RD Black HIJ Grant H Ineson P and Kersteins G (2005) Rising atmospheric CO2 reduces soil carbon sequestration Science 309 1711-1713

Houghton JT LG Meira Filho BA Callender 1996 Climate Change 1995 The Science of Climate Change Intergovernmental Panel on Climate Change Cambridge University Press Cambridge

Page 18

Horn R and Smucker A (2005) Structure formation and its consequences for gas and water transport in unsaturated arable and forest soils Soil amp Tillage Research 82 5ndash14

Jackson RB CW Cook JS Poppen et al (2009) Increased belowground biomass and soil CO2 fluxes after a decade of carbon dioxide enrichment in a warm-temperate forest Ecology 90 3352-3366

Jenkins GJ Murphy JM Sexton DS Lowe JA Jones P and Kilsby CG (2009) Uk Climate Projections Briefing report Met Office Hadley Centre Exeter UK

Jenkinson DS Adams DE and Wild A (1991) Model Estimates of Co2 Emissions from Soil in Response to Global Warming Nature 351 304-306

Jenkinson DS and Coleman K (2008) The turnover of organic carbon in subsoils Part 2 Modelling carbon turnover European Journal of Soil Science 59 400-413

Kandeler E Tscherko D Bardgett RD Hobbs PJ Kampichler C and Jones TH (1998) The response of soil microorganisms and roots to elevated CO2 and temperature in a terrestrial model ecosystem Plant and Soil 202 251-262

Kohler J Caravaca F Alguacil MdM and Roldan A (2009) Elevated CO2 increases the effect of an arbuscular mycorrhizal fungus and a plant-growth-promoting rhizobacterium on structural stability of a semiarid agricultural soil under drought conditions Soil Biology and Biochemistry 41 1710 ndash 1716

Kuan HL Hallet PD Griffiths BS Gregory AS Watts CW and Whitmore AP (2007) The resilience of a selection of Scottish soils to biological and physical stress European Journal of Soil Science 58 811-821

Liu L and TL Greaver 2009 A review of nitrogen enrichment effects on three biogenic GHGs the CO2 sink may be largely offset by stimulated N2O and CH4 emission Ecology Letters 12 1103 ndash 1117

Luo Y Su B Currie WS Dukes JS Finzi A Hartwig U Hungate B McMurtrie RE Oren R Parton WJ Pataki DE Shaw MR Zak DR and Field CB (2004) Progressive nitrogen limitation responses to rising atmopsheric carbon dioxide BioScience 54 731-739

Meyer KM Mooij WM Vos M Hol WHG and van der Putten WH (2009) The power of simulating experiments Ecological Modelling 220 2594 ndash 2597

Mikkelsen TN Beier C Jonasson S Holmstrup M Schmidt IK Ambus P Pilegaard K Michelsen A Albert K Andresen LC Arndal MF Bruun N Christensen S Danbaek S Gundersen P Jorgensen P Linden LG Kongstad J Maraldo K Prieme A Riis-Nielsen T Ro-Poulsen H Stevnbak K Selsted MB Sorensen P Larsen KS Carter MS Ibrom A Martinussen T Miglietta F and Sverdrup H (2008) Experimental design of multifactor climate change experiments with elevated CO2 warming and drought the CLIMAITE project Functional Ecology 22 185-195

Norby R J J Ledford C D Reilly et al (2004) Fine-root production dominates response of a deciduous forest to atmospheric CO2 enrichment Proceedings of the National Academy of Sciences USA 101 9689ndash9693

Plum N Terrestrial invertebrates in flooded grassland A literature review 2005 Wetlands 25 721-737

Ritz K amp Black HIJ amp Campbell CD amp Harris JA (2009) Selecting biological indicators for monitoring soils A framework for balancing scientific and technical opinion to assist policy development Ecological Indicators 1212 - 1221

Robinson DA Lebron I Vereecken H (2009) On the definition of the natural capital of soils A framework for description evaluation and monitoring Soil Science Society of America Journal 73 1904 ndash 1911

Roulet NT and TR Moore 1995 The effect of forestry drainage practices on the emissions of methane from northern peatlands Canadian Journal of Forest Research 25 491ndash499

Page 19

Rounsevell MDA amp Brignall AP (1994) The potential effects of climate change on autumn soil tillage opportunities in England and Wales Soil amp Tillage Research 32 275-289

Sala O E F S Chapin J J Armesto R Berlow J Bloomfield R Dirzo E Huber-Sanwald LF Huenneke RB Jackson A Kinzig R Leemans D Lodge HA Mooney M Oesterheld NL Poff MT Sykes BH Walker M Walker and DH Wall 2000 Global biodiversity scenarios for the year 2100 Science 287 1770-1774

Scheu S and Schaefer M (1998) Bottom-up control of the soil macrofauna community in a beechwood on limestone Manipulation of food sources Ecology 79 1573-1585

Schimel J TC Balser and M Wallenstein 2007 Microbial stress-response physiology and its implications for ecosystem function Ecology 88 1386-1394

Sowerby A Emmett BA et al (2008) Contrasting effects of repeated summer drought on soil carbon efflux in hydric and mesic heathland soils Global Change Biology 14 2388-2404

Tillig MC Wright SF Kimball BA Pinter PJ Wall GW Ottman MJ Leavitt SW (2001) Elevated carbon dioxide and irrigation effects on water stable aggregates in a Sorghum field a possible role for arbuscular mycorrhizal fungi Global Change Biology 7 333 ndash 337

Tipping E Woof C Rigg E Harrison AF Ineson P Taylor K Benham D Poskitt J Rowland AP Bol R and Harkness DD (1999) Climatic influences on the leaching of dissolved organic matter from upland UK moorland soils investigated by a field manipulation experiment Environment International 25 83-95

Toberman H Freeman C et al (2008) Summer drought decreases soil fungal diversity and associated phenol oxidase activity in upland Calluna heathland soil FEMS Microbiology Ecology 66 426-436

Treseder KK 2008 Nitrogen additions and microbial biomass a meta-analysis of ecosystem studies Ecology Letters 11 1111-1120

Ritz K Black HIJ Campbell CD Harris JA and Wood C (2009) Selecting ecological indicators for monitoring soils a framework for balancing scientific opinion to assist policy development Ecological Indicators 9 1212-1221

Schlesinger WH 2009 On the fate of anthropogenic nitrogen Proceedings of the National Academy Sciences USA 106 203-208

Stanhill G Cohen S 2001 Global dimming a review of the evidence for a widespread and significant reduction in global radiation with discussion of its probable causes and possible agricultural consequences Agricultural and Forest Meteorology 107 255-278

Stepniewska W and Stepniewska Z (2009) Selected oxygen-dependent proceses ndash Response to soil management and tillage Soil Tillage Research 102 193-200

Tylianakis JM Didham RK Bascompte J and Wardle DA (2008) Global change and species interactions in terrestrial ecosystems Ecology Letters 11 1351-1363

Van der Heijden MGA RD Bardgett and NM van Straalen 2008 The unseen majority soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems Ecology Letters 11 296-310

Waldrop MP Zak DR and Sinsabaugh RL (2004) Microbial community responses to nitrogen deposition in northern forest ecosystems Soil Biology and Biochemistry 36 1443-1451

Ward SE RD Bardgett NP McNamara JK Adamson and NJ Ostle 2007 Long-term consequences of grazing and buring on northern peatland carbon dynamics Ecosystems 10 1069-1083

Wardle DA (2002) Communities and Ecosystems Linking Aboveground and Belowground Components Princeton University Press Princeton NJ USA

Wardle DA Bardgett RD Klironomos JN Setaumllauml H van der Putten WH and Wall DH (2004) Ecological linkages between aboveground and belowground biota Science 304 1629-1633

Page 20

Whitmore AP and Whalley WR (2009) Physical effects of soil drying on roots and crop growth Journal of Experimental Botany 60 2845-2857

Wullschleger SD and Strahl M (2010) Climate change A controlled experiment Scientific American 302 60 ndash 65

Zhang W parker KM Luo Y Wan S Wallace LL and Hu S (2005) Soil microbial responses to experimental warming and clipping in a tallgrass prairie Global Change Biology 11 266 ndash 277

• Heath J Ayres E Possell M Bardgett RD Black HIJ Grant H Ineson P and Kersteins G (2005) Rising atmospheric CO2 reduces soil carbon sequestration Science 309 1711-1713

Page 15

drivers within the same experiment therefore have considerable promise for improving our understanding of how interactions involving soil communities and their effects on ecosystem-level processes may respond to current global change scenarios

There are a variety of experimental approaches for exploring effects of climate change on soil biota and the processes that they drive To address the above challenges we highlight the need for (a) greater exploitation of current nationally important facilities (eg Rothamsted and Buxton Climate Change Experiments Derbyshire) and funding of more detailed studies into responses of soil biota to long-term in situ climate manipulations along with associated mesocosm studies to refine mechanistic understanding (b) simultaneous assessment of soil biota responses at the phenotypic genotypic and functional level (c) studies to be performed along environmental gradients using similar climatic manipulations to better understand how responses to climate vary in different situations and (d) multi-factor experiments with large-scale long term manipulations of multiple climate change (eg precipitation temperature etc) and other factors such as land use

References Allison SD CI Czimczik and KK Treseder 2008 Microbial activity and soil respiration under nitrogen addition in Alaskan boreal forest Global Change Biology 14 1156 ndash 1168

Bardgett RD and Wardle DA 2010 Aboveground-Belowground Linkages Biotic Interactions Ecosystem Processes and Global Change Oxford Ecology and Evolution Series Oxford University Press

Bardgett RD Freeman C Ostle N (2008) Microbial contributions to climate change through carbon-cycle feedbacks The ISME Journal 2 805-814

Bardgett RD Kandeler E Tscherko D Hobbs PJ Jones TH Thompson LJ and Bezemer TM (1999) Below-ground microbial community development in a high temperature world Oikos 85 193-203

Bardgett RD and E McAlister 1999 The measurement of soil fungalbacterial biomass ratios as an indicator of ecosystem self-regulation in temperate meadow grasslands Biology and Fertility of Soils 29 282-290

Bardgett RD (2005) The Biology of Soil A Community and Ecosystem Approach Oxford University Press Oxford UK

Beier C Emmett B Gundersen P Tietema A Penuelas J Estiarte M Gordon C Gorissen A Llorens L Roda F and Williams D (2004) Novel approaches to study climate change effects on terrestrial ecosystems in the field - drought and passive night time warming Ecosystems 7 583-597

Belford RL Cannell RQ and Thomson RJ (1985) Effects of single and multiple waterloggings on the growth and yield of winter wheat on a clay soil Journal of the Science fo Food and Agriculture 36 142-156

Black H I J Ritz K Campbell C D Harris J A Wood C Chamberlain P M Parekh N Towers W and Scott A (2008) Prioritising biological indicators of soil quality for deployment in a national-scale soil monitoring scheme Final Report Defra Project SP0529

Blanchart E Marilleau N Chotte J-L Drogoul A Perrier E and Cambier Ch (2009) SWORM an agent-based model tosimulate the effects of earthworms on soil structure European Journal of Soil Science 60 13 ndash 21

Blom CWPM (1999) Adaptations to flooding stress From plant community to molecule Plant Biology 1 261-273

Bradley RI Moffat A Vanguelova E Falloon P and Harris J (2005) Defra Project SP0538 - The Impact of Climate Change on Soil Functions SP0538

Page 16

Briones MJI Ineson P and Piearce TG (1997) Effects of climate change on soil fauna responses of enchytraeids Diptera larvae and tardigrades in a transplant experiment Applied Soil Ecology 6 117-134

Briones MJI Ineson P and Poskitt J (1998) Climate change and Cognettia sphagnetorum effects on carbon dynamics in organic soils Functional Ecology 12 528-535

Brussaard L BehanPelletier VM Bignell DE Brown VK Didden W Folgarait P Fragoso C Freckman DW Gupta VVSR Hattori T Hawksworth DL Klopatek C Lavelle P Malloch DW Rusek J Soderstrom B Tiedje JM and Virginia RA (1997) Biodiversity and ecosystem functioning in soil Ambio 26 563-570

Carreiro MM Sinsabaugh RL Repert DA and Pankhurst DF (2000) Microbial enzyme shifts explain litter decay responses to simulated nitrogen deposition Ecology 81 2359-2365

Cecillon L de Mello NA De Danieli S Brun J-J (2010) Soil macroaggregate dynamics in a mountain spatial climate gradient Biogeochemistry 97 31 ndash 43

Chuang S-C and Chen JH 2008 Role of diurnal rhythm of oxygen consumption in emergence from soil at night after heavy rain by earthworms Invertebrate Biology 127 80ndash86

Cole L Bardgett RD Ineson P and Adamson J (2002a) Relationships between enchytraeid worms (Oligochaeta) temperature and the release of dissolved organic carbon from blanket peat in northern England Soil Biology and Biochemistry 34 599-607

Cole L Bardgett RD Ineson P and Hobbs PJ (2002b) Enchytraeid worm (Oligochaeta) influences on microbial community structure nutrient dynamics and plant growth in blanket peat subjected to warming Soil Biology and Biochemistry 34 83-92

Cox PM Betts RA Jones CD Spall SA and Totterdell IJ (2000) Acceleration of global warming due to carbon-cycle feedbacks in a coupled climate model Nature 408 184-187

Conen F J Leifeld B Seth and C Alewell (2006) Warming mobilises young and old soil carbon equally Biogeosciences 3515ndash519

Cruz-Martinez K Suttle KB Brodie EL Power ME Anderson GL and Banfield JF (2009) Despite strong seasonal responses soil microbial consortia are more resilient to long-term changes in rainfall than overlying grassland The ISME Journal 3 738 ndash 744

Davidson EA and Janssens IA (2006) Temperature sensitivity of soil carbon decomposition and feedbacks to climate change Nature 440 165-173

De Deyn GB HC Cornelissen and RD Bardgett 2008 Plant functional traits and soil carbon sequestration in contrasting biomes Ecology Letters 11 516ndash531

De Graaff MA KJ van Groenigen J Six B Hungate and C van Kessel 2006 Interactions between plant growth and soil nutrient cycling under elevated CO2 a meta-analysis Global Change Biology 12 2077ndash2091

Donnison LM Griffith GS and Bardgett RD (2000b) Determinants of fungal growth and activity in botanically diverse haymeadows effects of litter type and fertilizer additions Soil Biology and Biochemistry 32 289-294

Dowrick DJ S Hughes C Freeman MA Lock B Reynolds and JA Hudson 1999 Nitrous oxide emissions from a gully mire in mid-Wales UK under simulated summer drought Biogeochemistry 44 151-162

Dickin E Bennett S Wright D 2009 Growth and yield responses of UK wheat cultivars to winter waterlogging Journal of Agricultural Science 147 127-140

Dickin E Wright D 2008 The effects of winter waterlogging and summer drought on the growth and yield of winter wheat (Triticum aestivum L) European Journal of Agronomy 28 234-244

Emmett BA Beier C Estiarte M Tietema A Kristensen HL Williams D Pentildeuelas J Schmidt IK and Sowerby A (2004) The response of soil processes to climate change Results from manipulation studies across an environmental gradient Ecosystems 7 625-637

Page 17

Ettema CH R Lowrance and D C Coleman (1999) Riparian soil response to surface nitrogen input the indicator potential of free-living soil nematode populations Soil Biology and Biochemistry 31 1625-1638

Egerton-Warburton LM and Allen EB (2000) Shifts in arbuscular mycorrhizal communities along an anthropogenic nitrogen deposition gradient Ecological Applications 10 484-496

Eggleton P Inward K Smith J Jones DT and Sherlock E (2009) A six year study of earthworm (Lumbricidae) populations in pasture woodland in southern England shows their responses to soil temperature and soil moisture Soil Biology and Biochemistry 41 1857 ndash 1865

Fang CM P Smith JB Moncrieff JU Smith (2005) Similar response of labile and resistant soil organic matter pools to changes in temperature Nature 433 57-59

Fenner N Ostle NJ McNamara N Sparks T Freeman C (2007a) Elevated CO2 Effects on Peatland plant community carbon dynamics and DOC production Ecosystems 10 635-647

Fenner N Freeman C Lock MA Harmens H Sparks T (2007b) Interactions between elevated CO2 and warming could amplify DOC exports from peatland catchments Environmental Science and Technology 41 3146-3152

Finzi AC DeLucia EH Hamilton JG Richter DD and Schelsinger WH (2002) The nitrogen budget of a pine forest under free-air CO2 enrichment Oecologia 132 567-578

Freeman C GB Nevison H Kang S Hughes B Reynolds and JA Hudson 2002 Contrasted effects of simulated drought on the production and oxidation of methane in a mid-Wales wetland Soil Biology and Biochemistry 34 61-67

Freeman C NJ Ostle N Fenner H Kang 2004 A regulatory role for phenol oxidase during decomposition in peatlands Soil Biology and Biochemistry 36 1663-1667

Frey SD Knorr M Parrent JL and Simpson RT (2004) Chronic nitrogen enrichment affects the structure and function of the soil microbial community in temperate hardwood and pine forests Forest Ecology and Management 196 159-171

Frey SD Drijber R Smith H and Melillo J (2008) Microbial biomass functional capacity and community structure after 12 years of soil warming Soil Biology and Biochemistry 40 2904 ndash 2907

Friedlingstein P Cox P Betts R Bopp L Von Bloh W Brovkin V Cadule P Doney S Eby M Fung I Bala G John J Jones C Joos F Kato T Kawamiya M Knorr W Lindsay K Matthews HD Raddatz T Rayner P Reick C Roeckner E Schnitzler KG Schnur R Strassmann K Weaver AJ Yoshikawa C and Zeng N (2006) Climate-carbon cycle feedback analysis Results from the (CMIP)-M-4 model intercomparison Journal of Climate 19 3337-3353

Gange AC EG Gange TH Sparks L Boddy 2007 Rapid and recent changes in fungal fruiting patterns Science 316 71

Gordon H PM Haygarth and RD Bardgett 2008 Drying and rewetting effects on soil microbial community composition and nutrient leaching Soil Biology and Biochemistry 40 302-311

Gregory AS Watts CW Griffiths BS Hallett PD Kuan HS and Whitmore AP (2009) The effect of long-term soil management on the physical and biological resilience of a range of arable and grassland soils in England Geoderma 153 172-185

Grime JP Fridley JD Askew AP Thompson K Hodgson JG and Bennett CR (2008) Long-term resistance to simulated climate change in an infertile grassland Proceedings of the National Academy of Sciences USA 105 100028-10032

Harris JA (2009) Soil microbial communities and restoration ecology facilitators or followers Science 325 573-574

Heath J Ayres E Possell M Bardgett RD Black HIJ Grant H Ineson P and Kersteins G (2005) Rising atmospheric CO2 reduces soil carbon sequestration Science 309 1711-1713

Houghton JT LG Meira Filho BA Callender 1996 Climate Change 1995 The Science of Climate Change Intergovernmental Panel on Climate Change Cambridge University Press Cambridge

Page 18

Horn R and Smucker A (2005) Structure formation and its consequences for gas and water transport in unsaturated arable and forest soils Soil amp Tillage Research 82 5ndash14

Jackson RB CW Cook JS Poppen et al (2009) Increased belowground biomass and soil CO2 fluxes after a decade of carbon dioxide enrichment in a warm-temperate forest Ecology 90 3352-3366

Jenkins GJ Murphy JM Sexton DS Lowe JA Jones P and Kilsby CG (2009) Uk Climate Projections Briefing report Met Office Hadley Centre Exeter UK

Jenkinson DS Adams DE and Wild A (1991) Model Estimates of Co2 Emissions from Soil in Response to Global Warming Nature 351 304-306

Jenkinson DS and Coleman K (2008) The turnover of organic carbon in subsoils Part 2 Modelling carbon turnover European Journal of Soil Science 59 400-413

Kandeler E Tscherko D Bardgett RD Hobbs PJ Kampichler C and Jones TH (1998) The response of soil microorganisms and roots to elevated CO2 and temperature in a terrestrial model ecosystem Plant and Soil 202 251-262

Kohler J Caravaca F Alguacil MdM and Roldan A (2009) Elevated CO2 increases the effect of an arbuscular mycorrhizal fungus and a plant-growth-promoting rhizobacterium on structural stability of a semiarid agricultural soil under drought conditions Soil Biology and Biochemistry 41 1710 ndash 1716

Kuan HL Hallet PD Griffiths BS Gregory AS Watts CW and Whitmore AP (2007) The resilience of a selection of Scottish soils to biological and physical stress European Journal of Soil Science 58 811-821

Liu L and TL Greaver 2009 A review of nitrogen enrichment effects on three biogenic GHGs the CO2 sink may be largely offset by stimulated N2O and CH4 emission Ecology Letters 12 1103 ndash 1117

Luo Y Su B Currie WS Dukes JS Finzi A Hartwig U Hungate B McMurtrie RE Oren R Parton WJ Pataki DE Shaw MR Zak DR and Field CB (2004) Progressive nitrogen limitation responses to rising atmopsheric carbon dioxide BioScience 54 731-739

Meyer KM Mooij WM Vos M Hol WHG and van der Putten WH (2009) The power of simulating experiments Ecological Modelling 220 2594 ndash 2597

Mikkelsen TN Beier C Jonasson S Holmstrup M Schmidt IK Ambus P Pilegaard K Michelsen A Albert K Andresen LC Arndal MF Bruun N Christensen S Danbaek S Gundersen P Jorgensen P Linden LG Kongstad J Maraldo K Prieme A Riis-Nielsen T Ro-Poulsen H Stevnbak K Selsted MB Sorensen P Larsen KS Carter MS Ibrom A Martinussen T Miglietta F and Sverdrup H (2008) Experimental design of multifactor climate change experiments with elevated CO2 warming and drought the CLIMAITE project Functional Ecology 22 185-195

Norby R J J Ledford C D Reilly et al (2004) Fine-root production dominates response of a deciduous forest to atmospheric CO2 enrichment Proceedings of the National Academy of Sciences USA 101 9689ndash9693

Plum N Terrestrial invertebrates in flooded grassland A literature review 2005 Wetlands 25 721-737

Ritz K amp Black HIJ amp Campbell CD amp Harris JA (2009) Selecting biological indicators for monitoring soils A framework for balancing scientific and technical opinion to assist policy development Ecological Indicators 1212 - 1221

Robinson DA Lebron I Vereecken H (2009) On the definition of the natural capital of soils A framework for description evaluation and monitoring Soil Science Society of America Journal 73 1904 ndash 1911

Roulet NT and TR Moore 1995 The effect of forestry drainage practices on the emissions of methane from northern peatlands Canadian Journal of Forest Research 25 491ndash499

Page 19

Rounsevell MDA amp Brignall AP (1994) The potential effects of climate change on autumn soil tillage opportunities in England and Wales Soil amp Tillage Research 32 275-289

Sala O E F S Chapin J J Armesto R Berlow J Bloomfield R Dirzo E Huber-Sanwald LF Huenneke RB Jackson A Kinzig R Leemans D Lodge HA Mooney M Oesterheld NL Poff MT Sykes BH Walker M Walker and DH Wall 2000 Global biodiversity scenarios for the year 2100 Science 287 1770-1774

Scheu S and Schaefer M (1998) Bottom-up control of the soil macrofauna community in a beechwood on limestone Manipulation of food sources Ecology 79 1573-1585

Schimel J TC Balser and M Wallenstein 2007 Microbial stress-response physiology and its implications for ecosystem function Ecology 88 1386-1394

Sowerby A Emmett BA et al (2008) Contrasting effects of repeated summer drought on soil carbon efflux in hydric and mesic heathland soils Global Change Biology 14 2388-2404

Tillig MC Wright SF Kimball BA Pinter PJ Wall GW Ottman MJ Leavitt SW (2001) Elevated carbon dioxide and irrigation effects on water stable aggregates in a Sorghum field a possible role for arbuscular mycorrhizal fungi Global Change Biology 7 333 ndash 337

Tipping E Woof C Rigg E Harrison AF Ineson P Taylor K Benham D Poskitt J Rowland AP Bol R and Harkness DD (1999) Climatic influences on the leaching of dissolved organic matter from upland UK moorland soils investigated by a field manipulation experiment Environment International 25 83-95

Toberman H Freeman C et al (2008) Summer drought decreases soil fungal diversity and associated phenol oxidase activity in upland Calluna heathland soil FEMS Microbiology Ecology 66 426-436

Treseder KK 2008 Nitrogen additions and microbial biomass a meta-analysis of ecosystem studies Ecology Letters 11 1111-1120

Ritz K Black HIJ Campbell CD Harris JA and Wood C (2009) Selecting ecological indicators for monitoring soils a framework for balancing scientific opinion to assist policy development Ecological Indicators 9 1212-1221

Schlesinger WH 2009 On the fate of anthropogenic nitrogen Proceedings of the National Academy Sciences USA 106 203-208

Stanhill G Cohen S 2001 Global dimming a review of the evidence for a widespread and significant reduction in global radiation with discussion of its probable causes and possible agricultural consequences Agricultural and Forest Meteorology 107 255-278

Stepniewska W and Stepniewska Z (2009) Selected oxygen-dependent proceses ndash Response to soil management and tillage Soil Tillage Research 102 193-200

Tylianakis JM Didham RK Bascompte J and Wardle DA (2008) Global change and species interactions in terrestrial ecosystems Ecology Letters 11 1351-1363

Van der Heijden MGA RD Bardgett and NM van Straalen 2008 The unseen majority soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems Ecology Letters 11 296-310

Waldrop MP Zak DR and Sinsabaugh RL (2004) Microbial community responses to nitrogen deposition in northern forest ecosystems Soil Biology and Biochemistry 36 1443-1451

Ward SE RD Bardgett NP McNamara JK Adamson and NJ Ostle 2007 Long-term consequences of grazing and buring on northern peatland carbon dynamics Ecosystems 10 1069-1083

Wardle DA (2002) Communities and Ecosystems Linking Aboveground and Belowground Components Princeton University Press Princeton NJ USA

Wardle DA Bardgett RD Klironomos JN Setaumllauml H van der Putten WH and Wall DH (2004) Ecological linkages between aboveground and belowground biota Science 304 1629-1633

Page 20

Whitmore AP and Whalley WR (2009) Physical effects of soil drying on roots and crop growth Journal of Experimental Botany 60 2845-2857

Wullschleger SD and Strahl M (2010) Climate change A controlled experiment Scientific American 302 60 ndash 65

Zhang W parker KM Luo Y Wan S Wallace LL and Hu S (2005) Soil microbial responses to experimental warming and clipping in a tallgrass prairie Global Change Biology 11 266 ndash 277

• Heath J Ayres E Possell M Bardgett RD Black HIJ Grant H Ineson P and Kersteins G (2005) Rising atmospheric CO2 reduces soil carbon sequestration Science 309 1711-1713

Page 16

Briones MJI Ineson P and Piearce TG (1997) Effects of climate change on soil fauna responses of enchytraeids Diptera larvae and tardigrades in a transplant experiment Applied Soil Ecology 6 117-134

Briones MJI Ineson P and Poskitt J (1998) Climate change and Cognettia sphagnetorum effects on carbon dynamics in organic soils Functional Ecology 12 528-535

Brussaard L BehanPelletier VM Bignell DE Brown VK Didden W Folgarait P Fragoso C Freckman DW Gupta VVSR Hattori T Hawksworth DL Klopatek C Lavelle P Malloch DW Rusek J Soderstrom B Tiedje JM and Virginia RA (1997) Biodiversity and ecosystem functioning in soil Ambio 26 563-570

Carreiro MM Sinsabaugh RL Repert DA and Pankhurst DF (2000) Microbial enzyme shifts explain litter decay responses to simulated nitrogen deposition Ecology 81 2359-2365

Cecillon L de Mello NA De Danieli S Brun J-J (2010) Soil macroaggregate dynamics in a mountain spatial climate gradient Biogeochemistry 97 31 ndash 43

Chuang S-C and Chen JH 2008 Role of diurnal rhythm of oxygen consumption in emergence from soil at night after heavy rain by earthworms Invertebrate Biology 127 80ndash86

Cole L Bardgett RD Ineson P and Adamson J (2002a) Relationships between enchytraeid worms (Oligochaeta) temperature and the release of dissolved organic carbon from blanket peat in northern England Soil Biology and Biochemistry 34 599-607

Cole L Bardgett RD Ineson P and Hobbs PJ (2002b) Enchytraeid worm (Oligochaeta) influences on microbial community structure nutrient dynamics and plant growth in blanket peat subjected to warming Soil Biology and Biochemistry 34 83-92

Cox PM Betts RA Jones CD Spall SA and Totterdell IJ (2000) Acceleration of global warming due to carbon-cycle feedbacks in a coupled climate model Nature 408 184-187

Conen F J Leifeld B Seth and C Alewell (2006) Warming mobilises young and old soil carbon equally Biogeosciences 3515ndash519

Cruz-Martinez K Suttle KB Brodie EL Power ME Anderson GL and Banfield JF (2009) Despite strong seasonal responses soil microbial consortia are more resilient to long-term changes in rainfall than overlying grassland The ISME Journal 3 738 ndash 744

Davidson EA and Janssens IA (2006) Temperature sensitivity of soil carbon decomposition and feedbacks to climate change Nature 440 165-173

De Deyn GB HC Cornelissen and RD Bardgett 2008 Plant functional traits and soil carbon sequestration in contrasting biomes Ecology Letters 11 516ndash531

De Graaff MA KJ van Groenigen J Six B Hungate and C van Kessel 2006 Interactions between plant growth and soil nutrient cycling under elevated CO2 a meta-analysis Global Change Biology 12 2077ndash2091

Donnison LM Griffith GS and Bardgett RD (2000b) Determinants of fungal growth and activity in botanically diverse haymeadows effects of litter type and fertilizer additions Soil Biology and Biochemistry 32 289-294

Dowrick DJ S Hughes C Freeman MA Lock B Reynolds and JA Hudson 1999 Nitrous oxide emissions from a gully mire in mid-Wales UK under simulated summer drought Biogeochemistry 44 151-162

Dickin E Bennett S Wright D 2009 Growth and yield responses of UK wheat cultivars to winter waterlogging Journal of Agricultural Science 147 127-140

Dickin E Wright D 2008 The effects of winter waterlogging and summer drought on the growth and yield of winter wheat (Triticum aestivum L) European Journal of Agronomy 28 234-244

Emmett BA Beier C Estiarte M Tietema A Kristensen HL Williams D Pentildeuelas J Schmidt IK and Sowerby A (2004) The response of soil processes to climate change Results from manipulation studies across an environmental gradient Ecosystems 7 625-637

Page 17

Ettema CH R Lowrance and D C Coleman (1999) Riparian soil response to surface nitrogen input the indicator potential of free-living soil nematode populations Soil Biology and Biochemistry 31 1625-1638

Egerton-Warburton LM and Allen EB (2000) Shifts in arbuscular mycorrhizal communities along an anthropogenic nitrogen deposition gradient Ecological Applications 10 484-496

Eggleton P Inward K Smith J Jones DT and Sherlock E (2009) A six year study of earthworm (Lumbricidae) populations in pasture woodland in southern England shows their responses to soil temperature and soil moisture Soil Biology and Biochemistry 41 1857 ndash 1865

Fang CM P Smith JB Moncrieff JU Smith (2005) Similar response of labile and resistant soil organic matter pools to changes in temperature Nature 433 57-59

Fenner N Ostle NJ McNamara N Sparks T Freeman C (2007a) Elevated CO2 Effects on Peatland plant community carbon dynamics and DOC production Ecosystems 10 635-647

Fenner N Freeman C Lock MA Harmens H Sparks T (2007b) Interactions between elevated CO2 and warming could amplify DOC exports from peatland catchments Environmental Science and Technology 41 3146-3152

Finzi AC DeLucia EH Hamilton JG Richter DD and Schelsinger WH (2002) The nitrogen budget of a pine forest under free-air CO2 enrichment Oecologia 132 567-578

Freeman C GB Nevison H Kang S Hughes B Reynolds and JA Hudson 2002 Contrasted effects of simulated drought on the production and oxidation of methane in a mid-Wales wetland Soil Biology and Biochemistry 34 61-67

Freeman C NJ Ostle N Fenner H Kang 2004 A regulatory role for phenol oxidase during decomposition in peatlands Soil Biology and Biochemistry 36 1663-1667

Frey SD Knorr M Parrent JL and Simpson RT (2004) Chronic nitrogen enrichment affects the structure and function of the soil microbial community in temperate hardwood and pine forests Forest Ecology and Management 196 159-171

Frey SD Drijber R Smith H and Melillo J (2008) Microbial biomass functional capacity and community structure after 12 years of soil warming Soil Biology and Biochemistry 40 2904 ndash 2907

Friedlingstein P Cox P Betts R Bopp L Von Bloh W Brovkin V Cadule P Doney S Eby M Fung I Bala G John J Jones C Joos F Kato T Kawamiya M Knorr W Lindsay K Matthews HD Raddatz T Rayner P Reick C Roeckner E Schnitzler KG Schnur R Strassmann K Weaver AJ Yoshikawa C and Zeng N (2006) Climate-carbon cycle feedback analysis Results from the (CMIP)-M-4 model intercomparison Journal of Climate 19 3337-3353

Gange AC EG Gange TH Sparks L Boddy 2007 Rapid and recent changes in fungal fruiting patterns Science 316 71

Gordon H PM Haygarth and RD Bardgett 2008 Drying and rewetting effects on soil microbial community composition and nutrient leaching Soil Biology and Biochemistry 40 302-311

Gregory AS Watts CW Griffiths BS Hallett PD Kuan HS and Whitmore AP (2009) The effect of long-term soil management on the physical and biological resilience of a range of arable and grassland soils in England Geoderma 153 172-185

Grime JP Fridley JD Askew AP Thompson K Hodgson JG and Bennett CR (2008) Long-term resistance to simulated climate change in an infertile grassland Proceedings of the National Academy of Sciences USA 105 100028-10032

Harris JA (2009) Soil microbial communities and restoration ecology facilitators or followers Science 325 573-574

Heath J Ayres E Possell M Bardgett RD Black HIJ Grant H Ineson P and Kersteins G (2005) Rising atmospheric CO2 reduces soil carbon sequestration Science 309 1711-1713

Houghton JT LG Meira Filho BA Callender 1996 Climate Change 1995 The Science of Climate Change Intergovernmental Panel on Climate Change Cambridge University Press Cambridge

Page 18

Horn R and Smucker A (2005) Structure formation and its consequences for gas and water transport in unsaturated arable and forest soils Soil amp Tillage Research 82 5ndash14

Jackson RB CW Cook JS Poppen et al (2009) Increased belowground biomass and soil CO2 fluxes after a decade of carbon dioxide enrichment in a warm-temperate forest Ecology 90 3352-3366

Jenkins GJ Murphy JM Sexton DS Lowe JA Jones P and Kilsby CG (2009) Uk Climate Projections Briefing report Met Office Hadley Centre Exeter UK

Jenkinson DS Adams DE and Wild A (1991) Model Estimates of Co2 Emissions from Soil in Response to Global Warming Nature 351 304-306

Jenkinson DS and Coleman K (2008) The turnover of organic carbon in subsoils Part 2 Modelling carbon turnover European Journal of Soil Science 59 400-413

Kandeler E Tscherko D Bardgett RD Hobbs PJ Kampichler C and Jones TH (1998) The response of soil microorganisms and roots to elevated CO2 and temperature in a terrestrial model ecosystem Plant and Soil 202 251-262

Kohler J Caravaca F Alguacil MdM and Roldan A (2009) Elevated CO2 increases the effect of an arbuscular mycorrhizal fungus and a plant-growth-promoting rhizobacterium on structural stability of a semiarid agricultural soil under drought conditions Soil Biology and Biochemistry 41 1710 ndash 1716

Kuan HL Hallet PD Griffiths BS Gregory AS Watts CW and Whitmore AP (2007) The resilience of a selection of Scottish soils to biological and physical stress European Journal of Soil Science 58 811-821

Liu L and TL Greaver 2009 A review of nitrogen enrichment effects on three biogenic GHGs the CO2 sink may be largely offset by stimulated N2O and CH4 emission Ecology Letters 12 1103 ndash 1117

Luo Y Su B Currie WS Dukes JS Finzi A Hartwig U Hungate B McMurtrie RE Oren R Parton WJ Pataki DE Shaw MR Zak DR and Field CB (2004) Progressive nitrogen limitation responses to rising atmopsheric carbon dioxide BioScience 54 731-739

Meyer KM Mooij WM Vos M Hol WHG and van der Putten WH (2009) The power of simulating experiments Ecological Modelling 220 2594 ndash 2597

Mikkelsen TN Beier C Jonasson S Holmstrup M Schmidt IK Ambus P Pilegaard K Michelsen A Albert K Andresen LC Arndal MF Bruun N Christensen S Danbaek S Gundersen P Jorgensen P Linden LG Kongstad J Maraldo K Prieme A Riis-Nielsen T Ro-Poulsen H Stevnbak K Selsted MB Sorensen P Larsen KS Carter MS Ibrom A Martinussen T Miglietta F and Sverdrup H (2008) Experimental design of multifactor climate change experiments with elevated CO2 warming and drought the CLIMAITE project Functional Ecology 22 185-195

Norby R J J Ledford C D Reilly et al (2004) Fine-root production dominates response of a deciduous forest to atmospheric CO2 enrichment Proceedings of the National Academy of Sciences USA 101 9689ndash9693

Plum N Terrestrial invertebrates in flooded grassland A literature review 2005 Wetlands 25 721-737

Ritz K amp Black HIJ amp Campbell CD amp Harris JA (2009) Selecting biological indicators for monitoring soils A framework for balancing scientific and technical opinion to assist policy development Ecological Indicators 1212 - 1221

Robinson DA Lebron I Vereecken H (2009) On the definition of the natural capital of soils A framework for description evaluation and monitoring Soil Science Society of America Journal 73 1904 ndash 1911

Roulet NT and TR Moore 1995 The effect of forestry drainage practices on the emissions of methane from northern peatlands Canadian Journal of Forest Research 25 491ndash499

Page 19

Rounsevell MDA amp Brignall AP (1994) The potential effects of climate change on autumn soil tillage opportunities in England and Wales Soil amp Tillage Research 32 275-289

Sala O E F S Chapin J J Armesto R Berlow J Bloomfield R Dirzo E Huber-Sanwald LF Huenneke RB Jackson A Kinzig R Leemans D Lodge HA Mooney M Oesterheld NL Poff MT Sykes BH Walker M Walker and DH Wall 2000 Global biodiversity scenarios for the year 2100 Science 287 1770-1774

Scheu S and Schaefer M (1998) Bottom-up control of the soil macrofauna community in a beechwood on limestone Manipulation of food sources Ecology 79 1573-1585

Schimel J TC Balser and M Wallenstein 2007 Microbial stress-response physiology and its implications for ecosystem function Ecology 88 1386-1394

Sowerby A Emmett BA et al (2008) Contrasting effects of repeated summer drought on soil carbon efflux in hydric and mesic heathland soils Global Change Biology 14 2388-2404

Tillig MC Wright SF Kimball BA Pinter PJ Wall GW Ottman MJ Leavitt SW (2001) Elevated carbon dioxide and irrigation effects on water stable aggregates in a Sorghum field a possible role for arbuscular mycorrhizal fungi Global Change Biology 7 333 ndash 337

Tipping E Woof C Rigg E Harrison AF Ineson P Taylor K Benham D Poskitt J Rowland AP Bol R and Harkness DD (1999) Climatic influences on the leaching of dissolved organic matter from upland UK moorland soils investigated by a field manipulation experiment Environment International 25 83-95

Toberman H Freeman C et al (2008) Summer drought decreases soil fungal diversity and associated phenol oxidase activity in upland Calluna heathland soil FEMS Microbiology Ecology 66 426-436

Treseder KK 2008 Nitrogen additions and microbial biomass a meta-analysis of ecosystem studies Ecology Letters 11 1111-1120

Ritz K Black HIJ Campbell CD Harris JA and Wood C (2009) Selecting ecological indicators for monitoring soils a framework for balancing scientific opinion to assist policy development Ecological Indicators 9 1212-1221

Schlesinger WH 2009 On the fate of anthropogenic nitrogen Proceedings of the National Academy Sciences USA 106 203-208

Stanhill G Cohen S 2001 Global dimming a review of the evidence for a widespread and significant reduction in global radiation with discussion of its probable causes and possible agricultural consequences Agricultural and Forest Meteorology 107 255-278

Stepniewska W and Stepniewska Z (2009) Selected oxygen-dependent proceses ndash Response to soil management and tillage Soil Tillage Research 102 193-200

Tylianakis JM Didham RK Bascompte J and Wardle DA (2008) Global change and species interactions in terrestrial ecosystems Ecology Letters 11 1351-1363

Van der Heijden MGA RD Bardgett and NM van Straalen 2008 The unseen majority soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems Ecology Letters 11 296-310

Waldrop MP Zak DR and Sinsabaugh RL (2004) Microbial community responses to nitrogen deposition in northern forest ecosystems Soil Biology and Biochemistry 36 1443-1451

Ward SE RD Bardgett NP McNamara JK Adamson and NJ Ostle 2007 Long-term consequences of grazing and buring on northern peatland carbon dynamics Ecosystems 10 1069-1083

Wardle DA (2002) Communities and Ecosystems Linking Aboveground and Belowground Components Princeton University Press Princeton NJ USA

Wardle DA Bardgett RD Klironomos JN Setaumllauml H van der Putten WH and Wall DH (2004) Ecological linkages between aboveground and belowground biota Science 304 1629-1633

Page 20

Whitmore AP and Whalley WR (2009) Physical effects of soil drying on roots and crop growth Journal of Experimental Botany 60 2845-2857

Wullschleger SD and Strahl M (2010) Climate change A controlled experiment Scientific American 302 60 ndash 65

Zhang W parker KM Luo Y Wan S Wallace LL and Hu S (2005) Soil microbial responses to experimental warming and clipping in a tallgrass prairie Global Change Biology 11 266 ndash 277

• Heath J Ayres E Possell M Bardgett RD Black HIJ Grant H Ineson P and Kersteins G (2005) Rising atmospheric CO2 reduces soil carbon sequestration Science 309 1711-1713

Page 17

Ettema CH R Lowrance and D C Coleman (1999) Riparian soil response to surface nitrogen input the indicator potential of free-living soil nematode populations Soil Biology and Biochemistry 31 1625-1638

Egerton-Warburton LM and Allen EB (2000) Shifts in arbuscular mycorrhizal communities along an anthropogenic nitrogen deposition gradient Ecological Applications 10 484-496

Eggleton P Inward K Smith J Jones DT and Sherlock E (2009) A six year study of earthworm (Lumbricidae) populations in pasture woodland in southern England shows their responses to soil temperature and soil moisture Soil Biology and Biochemistry 41 1857 ndash 1865

Fang CM P Smith JB Moncrieff JU Smith (2005) Similar response of labile and resistant soil organic matter pools to changes in temperature Nature 433 57-59

Fenner N Ostle NJ McNamara N Sparks T Freeman C (2007a) Elevated CO2 Effects on Peatland plant community carbon dynamics and DOC production Ecosystems 10 635-647

Fenner N Freeman C Lock MA Harmens H Sparks T (2007b) Interactions between elevated CO2 and warming could amplify DOC exports from peatland catchments Environmental Science and Technology 41 3146-3152

Finzi AC DeLucia EH Hamilton JG Richter DD and Schelsinger WH (2002) The nitrogen budget of a pine forest under free-air CO2 enrichment Oecologia 132 567-578

Freeman C GB Nevison H Kang S Hughes B Reynolds and JA Hudson 2002 Contrasted effects of simulated drought on the production and oxidation of methane in a mid-Wales wetland Soil Biology and Biochemistry 34 61-67

Freeman C NJ Ostle N Fenner H Kang 2004 A regulatory role for phenol oxidase during decomposition in peatlands Soil Biology and Biochemistry 36 1663-1667

Frey SD Knorr M Parrent JL and Simpson RT (2004) Chronic nitrogen enrichment affects the structure and function of the soil microbial community in temperate hardwood and pine forests Forest Ecology and Management 196 159-171

Frey SD Drijber R Smith H and Melillo J (2008) Microbial biomass functional capacity and community structure after 12 years of soil warming Soil Biology and Biochemistry 40 2904 ndash 2907

Friedlingstein P Cox P Betts R Bopp L Von Bloh W Brovkin V Cadule P Doney S Eby M Fung I Bala G John J Jones C Joos F Kato T Kawamiya M Knorr W Lindsay K Matthews HD Raddatz T Rayner P Reick C Roeckner E Schnitzler KG Schnur R Strassmann K Weaver AJ Yoshikawa C and Zeng N (2006) Climate-carbon cycle feedback analysis Results from the (CMIP)-M-4 model intercomparison Journal of Climate 19 3337-3353

Gange AC EG Gange TH Sparks L Boddy 2007 Rapid and recent changes in fungal fruiting patterns Science 316 71

Gordon H PM Haygarth and RD Bardgett 2008 Drying and rewetting effects on soil microbial community composition and nutrient leaching Soil Biology and Biochemistry 40 302-311

Gregory AS Watts CW Griffiths BS Hallett PD Kuan HS and Whitmore AP (2009) The effect of long-term soil management on the physical and biological resilience of a range of arable and grassland soils in England Geoderma 153 172-185

Grime JP Fridley JD Askew AP Thompson K Hodgson JG and Bennett CR (2008) Long-term resistance to simulated climate change in an infertile grassland Proceedings of the National Academy of Sciences USA 105 100028-10032

Harris JA (2009) Soil microbial communities and restoration ecology facilitators or followers Science 325 573-574

Heath J Ayres E Possell M Bardgett RD Black HIJ Grant H Ineson P and Kersteins G (2005) Rising atmospheric CO2 reduces soil carbon sequestration Science 309 1711-1713

Houghton JT LG Meira Filho BA Callender 1996 Climate Change 1995 The Science of Climate Change Intergovernmental Panel on Climate Change Cambridge University Press Cambridge

Page 18

Horn R and Smucker A (2005) Structure formation and its consequences for gas and water transport in unsaturated arable and forest soils Soil amp Tillage Research 82 5ndash14

Jackson RB CW Cook JS Poppen et al (2009) Increased belowground biomass and soil CO2 fluxes after a decade of carbon dioxide enrichment in a warm-temperate forest Ecology 90 3352-3366

Jenkins GJ Murphy JM Sexton DS Lowe JA Jones P and Kilsby CG (2009) Uk Climate Projections Briefing report Met Office Hadley Centre Exeter UK

Jenkinson DS Adams DE and Wild A (1991) Model Estimates of Co2 Emissions from Soil in Response to Global Warming Nature 351 304-306

Jenkinson DS and Coleman K (2008) The turnover of organic carbon in subsoils Part 2 Modelling carbon turnover European Journal of Soil Science 59 400-413

Kandeler E Tscherko D Bardgett RD Hobbs PJ Kampichler C and Jones TH (1998) The response of soil microorganisms and roots to elevated CO2 and temperature in a terrestrial model ecosystem Plant and Soil 202 251-262

Kohler J Caravaca F Alguacil MdM and Roldan A (2009) Elevated CO2 increases the effect of an arbuscular mycorrhizal fungus and a plant-growth-promoting rhizobacterium on structural stability of a semiarid agricultural soil under drought conditions Soil Biology and Biochemistry 41 1710 ndash 1716

Kuan HL Hallet PD Griffiths BS Gregory AS Watts CW and Whitmore AP (2007) The resilience of a selection of Scottish soils to biological and physical stress European Journal of Soil Science 58 811-821

Liu L and TL Greaver 2009 A review of nitrogen enrichment effects on three biogenic GHGs the CO2 sink may be largely offset by stimulated N2O and CH4 emission Ecology Letters 12 1103 ndash 1117

Luo Y Su B Currie WS Dukes JS Finzi A Hartwig U Hungate B McMurtrie RE Oren R Parton WJ Pataki DE Shaw MR Zak DR and Field CB (2004) Progressive nitrogen limitation responses to rising atmopsheric carbon dioxide BioScience 54 731-739

Meyer KM Mooij WM Vos M Hol WHG and van der Putten WH (2009) The power of simulating experiments Ecological Modelling 220 2594 ndash 2597

Mikkelsen TN Beier C Jonasson S Holmstrup M Schmidt IK Ambus P Pilegaard K Michelsen A Albert K Andresen LC Arndal MF Bruun N Christensen S Danbaek S Gundersen P Jorgensen P Linden LG Kongstad J Maraldo K Prieme A Riis-Nielsen T Ro-Poulsen H Stevnbak K Selsted MB Sorensen P Larsen KS Carter MS Ibrom A Martinussen T Miglietta F and Sverdrup H (2008) Experimental design of multifactor climate change experiments with elevated CO2 warming and drought the CLIMAITE project Functional Ecology 22 185-195

Norby R J J Ledford C D Reilly et al (2004) Fine-root production dominates response of a deciduous forest to atmospheric CO2 enrichment Proceedings of the National Academy of Sciences USA 101 9689ndash9693

Plum N Terrestrial invertebrates in flooded grassland A literature review 2005 Wetlands 25 721-737

Ritz K amp Black HIJ amp Campbell CD amp Harris JA (2009) Selecting biological indicators for monitoring soils A framework for balancing scientific and technical opinion to assist policy development Ecological Indicators 1212 - 1221

Robinson DA Lebron I Vereecken H (2009) On the definition of the natural capital of soils A framework for description evaluation and monitoring Soil Science Society of America Journal 73 1904 ndash 1911

Roulet NT and TR Moore 1995 The effect of forestry drainage practices on the emissions of methane from northern peatlands Canadian Journal of Forest Research 25 491ndash499

Page 19

Rounsevell MDA amp Brignall AP (1994) The potential effects of climate change on autumn soil tillage opportunities in England and Wales Soil amp Tillage Research 32 275-289

Sala O E F S Chapin J J Armesto R Berlow J Bloomfield R Dirzo E Huber-Sanwald LF Huenneke RB Jackson A Kinzig R Leemans D Lodge HA Mooney M Oesterheld NL Poff MT Sykes BH Walker M Walker and DH Wall 2000 Global biodiversity scenarios for the year 2100 Science 287 1770-1774

Scheu S and Schaefer M (1998) Bottom-up control of the soil macrofauna community in a beechwood on limestone Manipulation of food sources Ecology 79 1573-1585

Schimel J TC Balser and M Wallenstein 2007 Microbial stress-response physiology and its implications for ecosystem function Ecology 88 1386-1394

Sowerby A Emmett BA et al (2008) Contrasting effects of repeated summer drought on soil carbon efflux in hydric and mesic heathland soils Global Change Biology 14 2388-2404

Tillig MC Wright SF Kimball BA Pinter PJ Wall GW Ottman MJ Leavitt SW (2001) Elevated carbon dioxide and irrigation effects on water stable aggregates in a Sorghum field a possible role for arbuscular mycorrhizal fungi Global Change Biology 7 333 ndash 337

Tipping E Woof C Rigg E Harrison AF Ineson P Taylor K Benham D Poskitt J Rowland AP Bol R and Harkness DD (1999) Climatic influences on the leaching of dissolved organic matter from upland UK moorland soils investigated by a field manipulation experiment Environment International 25 83-95

Toberman H Freeman C et al (2008) Summer drought decreases soil fungal diversity and associated phenol oxidase activity in upland Calluna heathland soil FEMS Microbiology Ecology 66 426-436

Treseder KK 2008 Nitrogen additions and microbial biomass a meta-analysis of ecosystem studies Ecology Letters 11 1111-1120

Ritz K Black HIJ Campbell CD Harris JA and Wood C (2009) Selecting ecological indicators for monitoring soils a framework for balancing scientific opinion to assist policy development Ecological Indicators 9 1212-1221

Schlesinger WH 2009 On the fate of anthropogenic nitrogen Proceedings of the National Academy Sciences USA 106 203-208

Stanhill G Cohen S 2001 Global dimming a review of the evidence for a widespread and significant reduction in global radiation with discussion of its probable causes and possible agricultural consequences Agricultural and Forest Meteorology 107 255-278

Stepniewska W and Stepniewska Z (2009) Selected oxygen-dependent proceses ndash Response to soil management and tillage Soil Tillage Research 102 193-200

Tylianakis JM Didham RK Bascompte J and Wardle DA (2008) Global change and species interactions in terrestrial ecosystems Ecology Letters 11 1351-1363

Van der Heijden MGA RD Bardgett and NM van Straalen 2008 The unseen majority soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems Ecology Letters 11 296-310

Waldrop MP Zak DR and Sinsabaugh RL (2004) Microbial community responses to nitrogen deposition in northern forest ecosystems Soil Biology and Biochemistry 36 1443-1451

Ward SE RD Bardgett NP McNamara JK Adamson and NJ Ostle 2007 Long-term consequences of grazing and buring on northern peatland carbon dynamics Ecosystems 10 1069-1083

Wardle DA (2002) Communities and Ecosystems Linking Aboveground and Belowground Components Princeton University Press Princeton NJ USA

Wardle DA Bardgett RD Klironomos JN Setaumllauml H van der Putten WH and Wall DH (2004) Ecological linkages between aboveground and belowground biota Science 304 1629-1633

Page 20

Whitmore AP and Whalley WR (2009) Physical effects of soil drying on roots and crop growth Journal of Experimental Botany 60 2845-2857

Wullschleger SD and Strahl M (2010) Climate change A controlled experiment Scientific American 302 60 ndash 65

Zhang W parker KM Luo Y Wan S Wallace LL and Hu S (2005) Soil microbial responses to experimental warming and clipping in a tallgrass prairie Global Change Biology 11 266 ndash 277

• Heath J Ayres E Possell M Bardgett RD Black HIJ Grant H Ineson P and Kersteins G (2005) Rising atmospheric CO2 reduces soil carbon sequestration Science 309 1711-1713

Page 18

Horn R and Smucker A (2005) Structure formation and its consequences for gas and water transport in unsaturated arable and forest soils Soil amp Tillage Research 82 5ndash14

Jackson RB CW Cook JS Poppen et al (2009) Increased belowground biomass and soil CO2 fluxes after a decade of carbon dioxide enrichment in a warm-temperate forest Ecology 90 3352-3366

Jenkins GJ Murphy JM Sexton DS Lowe JA Jones P and Kilsby CG (2009) Uk Climate Projections Briefing report Met Office Hadley Centre Exeter UK

Jenkinson DS Adams DE and Wild A (1991) Model Estimates of Co2 Emissions from Soil in Response to Global Warming Nature 351 304-306

Jenkinson DS and Coleman K (2008) The turnover of organic carbon in subsoils Part 2 Modelling carbon turnover European Journal of Soil Science 59 400-413

Kandeler E Tscherko D Bardgett RD Hobbs PJ Kampichler C and Jones TH (1998) The response of soil microorganisms and roots to elevated CO2 and temperature in a terrestrial model ecosystem Plant and Soil 202 251-262

Kohler J Caravaca F Alguacil MdM and Roldan A (2009) Elevated CO2 increases the effect of an arbuscular mycorrhizal fungus and a plant-growth-promoting rhizobacterium on structural stability of a semiarid agricultural soil under drought conditions Soil Biology and Biochemistry 41 1710 ndash 1716

Kuan HL Hallet PD Griffiths BS Gregory AS Watts CW and Whitmore AP (2007) The resilience of a selection of Scottish soils to biological and physical stress European Journal of Soil Science 58 811-821

Liu L and TL Greaver 2009 A review of nitrogen enrichment effects on three biogenic GHGs the CO2 sink may be largely offset by stimulated N2O and CH4 emission Ecology Letters 12 1103 ndash 1117

Luo Y Su B Currie WS Dukes JS Finzi A Hartwig U Hungate B McMurtrie RE Oren R Parton WJ Pataki DE Shaw MR Zak DR and Field CB (2004) Progressive nitrogen limitation responses to rising atmopsheric carbon dioxide BioScience 54 731-739

Meyer KM Mooij WM Vos M Hol WHG and van der Putten WH (2009) The power of simulating experiments Ecological Modelling 220 2594 ndash 2597

Mikkelsen TN Beier C Jonasson S Holmstrup M Schmidt IK Ambus P Pilegaard K Michelsen A Albert K Andresen LC Arndal MF Bruun N Christensen S Danbaek S Gundersen P Jorgensen P Linden LG Kongstad J Maraldo K Prieme A Riis-Nielsen T Ro-Poulsen H Stevnbak K Selsted MB Sorensen P Larsen KS Carter MS Ibrom A Martinussen T Miglietta F and Sverdrup H (2008) Experimental design of multifactor climate change experiments with elevated CO2 warming and drought the CLIMAITE project Functional Ecology 22 185-195

Norby R J J Ledford C D Reilly et al (2004) Fine-root production dominates response of a deciduous forest to atmospheric CO2 enrichment Proceedings of the National Academy of Sciences USA 101 9689ndash9693

Plum N Terrestrial invertebrates in flooded grassland A literature review 2005 Wetlands 25 721-737

Ritz K amp Black HIJ amp Campbell CD amp Harris JA (2009) Selecting biological indicators for monitoring soils A framework for balancing scientific and technical opinion to assist policy development Ecological Indicators 1212 - 1221

Robinson DA Lebron I Vereecken H (2009) On the definition of the natural capital of soils A framework for description evaluation and monitoring Soil Science Society of America Journal 73 1904 ndash 1911

Roulet NT and TR Moore 1995 The effect of forestry drainage practices on the emissions of methane from northern peatlands Canadian Journal of Forest Research 25 491ndash499

Page 19

Rounsevell MDA amp Brignall AP (1994) The potential effects of climate change on autumn soil tillage opportunities in England and Wales Soil amp Tillage Research 32 275-289

Sala O E F S Chapin J J Armesto R Berlow J Bloomfield R Dirzo E Huber-Sanwald LF Huenneke RB Jackson A Kinzig R Leemans D Lodge HA Mooney M Oesterheld NL Poff MT Sykes BH Walker M Walker and DH Wall 2000 Global biodiversity scenarios for the year 2100 Science 287 1770-1774

Scheu S and Schaefer M (1998) Bottom-up control of the soil macrofauna community in a beechwood on limestone Manipulation of food sources Ecology 79 1573-1585

Schimel J TC Balser and M Wallenstein 2007 Microbial stress-response physiology and its implications for ecosystem function Ecology 88 1386-1394

Sowerby A Emmett BA et al (2008) Contrasting effects of repeated summer drought on soil carbon efflux in hydric and mesic heathland soils Global Change Biology 14 2388-2404

Tillig MC Wright SF Kimball BA Pinter PJ Wall GW Ottman MJ Leavitt SW (2001) Elevated carbon dioxide and irrigation effects on water stable aggregates in a Sorghum field a possible role for arbuscular mycorrhizal fungi Global Change Biology 7 333 ndash 337

Tipping E Woof C Rigg E Harrison AF Ineson P Taylor K Benham D Poskitt J Rowland AP Bol R and Harkness DD (1999) Climatic influences on the leaching of dissolved organic matter from upland UK moorland soils investigated by a field manipulation experiment Environment International 25 83-95

Toberman H Freeman C et al (2008) Summer drought decreases soil fungal diversity and associated phenol oxidase activity in upland Calluna heathland soil FEMS Microbiology Ecology 66 426-436

Treseder KK 2008 Nitrogen additions and microbial biomass a meta-analysis of ecosystem studies Ecology Letters 11 1111-1120

Ritz K Black HIJ Campbell CD Harris JA and Wood C (2009) Selecting ecological indicators for monitoring soils a framework for balancing scientific opinion to assist policy development Ecological Indicators 9 1212-1221

Schlesinger WH 2009 On the fate of anthropogenic nitrogen Proceedings of the National Academy Sciences USA 106 203-208

Stanhill G Cohen S 2001 Global dimming a review of the evidence for a widespread and significant reduction in global radiation with discussion of its probable causes and possible agricultural consequences Agricultural and Forest Meteorology 107 255-278

Stepniewska W and Stepniewska Z (2009) Selected oxygen-dependent proceses ndash Response to soil management and tillage Soil Tillage Research 102 193-200

Tylianakis JM Didham RK Bascompte J and Wardle DA (2008) Global change and species interactions in terrestrial ecosystems Ecology Letters 11 1351-1363

Van der Heijden MGA RD Bardgett and NM van Straalen 2008 The unseen majority soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems Ecology Letters 11 296-310

Waldrop MP Zak DR and Sinsabaugh RL (2004) Microbial community responses to nitrogen deposition in northern forest ecosystems Soil Biology and Biochemistry 36 1443-1451

Ward SE RD Bardgett NP McNamara JK Adamson and NJ Ostle 2007 Long-term consequences of grazing and buring on northern peatland carbon dynamics Ecosystems 10 1069-1083

Wardle DA (2002) Communities and Ecosystems Linking Aboveground and Belowground Components Princeton University Press Princeton NJ USA

Wardle DA Bardgett RD Klironomos JN Setaumllauml H van der Putten WH and Wall DH (2004) Ecological linkages between aboveground and belowground biota Science 304 1629-1633

Page 20

Whitmore AP and Whalley WR (2009) Physical effects of soil drying on roots and crop growth Journal of Experimental Botany 60 2845-2857

Wullschleger SD and Strahl M (2010) Climate change A controlled experiment Scientific American 302 60 ndash 65

Zhang W parker KM Luo Y Wan S Wallace LL and Hu S (2005) Soil microbial responses to experimental warming and clipping in a tallgrass prairie Global Change Biology 11 266 ndash 277

• Heath J Ayres E Possell M Bardgett RD Black HIJ Grant H Ineson P and Kersteins G (2005) Rising atmospheric CO2 reduces soil carbon sequestration Science 309 1711-1713

Page 19

Rounsevell MDA amp Brignall AP (1994) The potential effects of climate change on autumn soil tillage opportunities in England and Wales Soil amp Tillage Research 32 275-289

Sala O E F S Chapin J J Armesto R Berlow J Bloomfield R Dirzo E Huber-Sanwald LF Huenneke RB Jackson A Kinzig R Leemans D Lodge HA Mooney M Oesterheld NL Poff MT Sykes BH Walker M Walker and DH Wall 2000 Global biodiversity scenarios for the year 2100 Science 287 1770-1774

Scheu S and Schaefer M (1998) Bottom-up control of the soil macrofauna community in a beechwood on limestone Manipulation of food sources Ecology 79 1573-1585

Schimel J TC Balser and M Wallenstein 2007 Microbial stress-response physiology and its implications for ecosystem function Ecology 88 1386-1394

Sowerby A Emmett BA et al (2008) Contrasting effects of repeated summer drought on soil carbon efflux in hydric and mesic heathland soils Global Change Biology 14 2388-2404

Tillig MC Wright SF Kimball BA Pinter PJ Wall GW Ottman MJ Leavitt SW (2001) Elevated carbon dioxide and irrigation effects on water stable aggregates in a Sorghum field a possible role for arbuscular mycorrhizal fungi Global Change Biology 7 333 ndash 337

Tipping E Woof C Rigg E Harrison AF Ineson P Taylor K Benham D Poskitt J Rowland AP Bol R and Harkness DD (1999) Climatic influences on the leaching of dissolved organic matter from upland UK moorland soils investigated by a field manipulation experiment Environment International 25 83-95

Toberman H Freeman C et al (2008) Summer drought decreases soil fungal diversity and associated phenol oxidase activity in upland Calluna heathland soil FEMS Microbiology Ecology 66 426-436

Treseder KK 2008 Nitrogen additions and microbial biomass a meta-analysis of ecosystem studies Ecology Letters 11 1111-1120

Ritz K Black HIJ Campbell CD Harris JA and Wood C (2009) Selecting ecological indicators for monitoring soils a framework for balancing scientific opinion to assist policy development Ecological Indicators 9 1212-1221

Schlesinger WH 2009 On the fate of anthropogenic nitrogen Proceedings of the National Academy Sciences USA 106 203-208

Stanhill G Cohen S 2001 Global dimming a review of the evidence for a widespread and significant reduction in global radiation with discussion of its probable causes and possible agricultural consequences Agricultural and Forest Meteorology 107 255-278

Stepniewska W and Stepniewska Z (2009) Selected oxygen-dependent proceses ndash Response to soil management and tillage Soil Tillage Research 102 193-200

Tylianakis JM Didham RK Bascompte J and Wardle DA (2008) Global change and species interactions in terrestrial ecosystems Ecology Letters 11 1351-1363

Van der Heijden MGA RD Bardgett and NM van Straalen 2008 The unseen majority soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems Ecology Letters 11 296-310

Waldrop MP Zak DR and Sinsabaugh RL (2004) Microbial community responses to nitrogen deposition in northern forest ecosystems Soil Biology and Biochemistry 36 1443-1451

Ward SE RD Bardgett NP McNamara JK Adamson and NJ Ostle 2007 Long-term consequences of grazing and buring on northern peatland carbon dynamics Ecosystems 10 1069-1083

Wardle DA (2002) Communities and Ecosystems Linking Aboveground and Belowground Components Princeton University Press Princeton NJ USA

Wardle DA Bardgett RD Klironomos JN Setaumllauml H van der Putten WH and Wall DH (2004) Ecological linkages between aboveground and belowground biota Science 304 1629-1633

Page 20

Whitmore AP and Whalley WR (2009) Physical effects of soil drying on roots and crop growth Journal of Experimental Botany 60 2845-2857

Wullschleger SD and Strahl M (2010) Climate change A controlled experiment Scientific American 302 60 ndash 65

Zhang W parker KM Luo Y Wan S Wallace LL and Hu S (2005) Soil microbial responses to experimental warming and clipping in a tallgrass prairie Global Change Biology 11 266 ndash 277

• Heath J Ayres E Possell M Bardgett RD Black HIJ Grant H Ineson P and Kersteins G (2005) Rising atmospheric CO2 reduces soil carbon sequestration Science 309 1711-1713

Page 20

Whitmore AP and Whalley WR (2009) Physical effects of soil drying on roots and crop growth Journal of Experimental Botany 60 2845-2857

Wullschleger SD and Strahl M (2010) Climate change A controlled experiment Scientific American 302 60 ndash 65

Zhang W parker KM Luo Y Wan S Wallace LL and Hu S (2005) Soil microbial responses to experimental warming and clipping in a tallgrass prairie Global Change Biology 11 266 ndash 277

• Heath J Ayres E Possell M Bardgett RD Black HIJ Grant H Ineson P and Kersteins G (2005) Rising atmospheric CO2 reduces soil carbon sequestration Science 309 1711-1713