Abstract

Soil is increasingly under environmental pressures that alter its capacity to fulfil essential ecosystem services. To maintain these crucial soil functions, it is important to know how soil microorganisms respond to disturbance or environmental change. Here, we summarize the recent progress in understanding the resistance and resilience (stability) of soil microbial communities and discuss the underlying mechanisms of soil biological stability together with the factors affecting it. Biological stability is not solely owing to the structure or diversity of the microbial community but is linked to a range of other vegetation and soil properties including aggregation and substrate quality. We suggest that resistance and resilience are governed by soil physico-chemical structure through its effect on microbial community composition and physiology, but that there is no general response to disturbance because stability is particular to the disturbance and soil history. Soil stability results from a combination of biotic and abiotic soil characteristics and so could provide a quantitative measure of soil health that can be translated into practice.

Introduction

Microorganisms living in soil are abundant and highly diverse, with estimates of up to 109 cells (Gans et al., 2005) and 104 species (Curtis et al., 2002) per gram of soil. These microorganisms are the key players of many soil functions such as biogeochemical cycling, plant productivity or climate regulation and are essential for the integrity of terrestrial ecosystems. Soil, which is a nonrenewable resource, is increasingly under environmental pressure most often related to the intensification of human activities (Creamer et al., 2010). Given the crucial importance of maintaining soil functions, there has been considerable effort invested in understanding the response of soil ecosystems to disturbance or environmental change and the resistance and resilience of soil microorganisms (Fig. 1). This increasing number of studies of soil microorganisms in relation to the functional stability of soil ecosystems is probably also due to the upsurge in research on the connections between biodiversity and ecosystem functioning (Loreau, 2010). Loss of biodiversity has been identified as a major threat to soil (COM(2006)231) but because of the complexity and variability of soil, microbial ecologists face a huge challenge in quantifying the role of microorganisms in enabling the soil to cope with disturbance and the underlying mechanisms remain poorly understood.

Figure 1

The response of the soil ecosystem to disturbance is influenced by the resistance and resilience of the soil microbial community.

Figure 1

The response of the soil ecosystem to disturbance is influenced by the resistance and resilience of the soil microbial community.

Resistance and resilience are also considered as ecological concepts of high policy relevance, that is, ‘how can we increase the resilience of habitats and species to cope with climate change?' (Sutherland et al., 2006). Almost any study could be considered in terms of resilience, in that the common experimental format – the effect of X on Y – will have information about the effect of a disturbance on the system if X is a disturbance. To get an understanding of resilience, there needs to be a measurement soon after the disturbance to gauge resistance and then several subsequent measurements to assess the pattern of resilience. The time period can be a matter of days in a laboratory incubation, or even minutes for some physical measurements (Zhang et al., 2005), through to years for field-based observations and is generally related to the nature of the disturbance. Thus, there have been studies spanning hundreds of years, for a postglacial chronosequence (Orwin et al., 2006); tens of years for field-based restoration projects (Zhang et al., 2010); or generally from 3 to 60 days in microcosm experiments. Studies have investigated the resilience of microbial communities to disturbance due to human activities such as land use and agricultural practices but also to natural disturbance such as fire or freeze–thaw.

There is now a sufficient body of literature on the biological resilience of soils to draw a synthesis of the controlling factors and to examine the underlying mechanisms. This body of literature is summarized in Table 1 which groups studies according to the primary disturbance or the research theme. While resilience can refer to either a population or a function (Botton et al., 2006), the majority of studies reviewed in this study have included a microbial function (e.g. nitrification, denitrification and decomposition), while some have also simultaneously measured changes in microbial community structure or diversity.

Table 1

Summary of soil microbial stability studies grouped by disturbance or research theme

Ecosystem Location Soil type Soil treatment Situation Experimental disturbance Duration Resistance and resilience of Microbial community measures Reference 
Cultivation 
BR L (FForest or agriculture Heat 30 days Enzyme activity, respiration PLFA Chaer et al. (2009
NZ SiCL Grassland or tillage HCl; NaCl; Cu; D-W; F-T 14 days Cmic, catabolic potential   Degens et al. (2001
US SL Grassland or tillage D-W 5 days Cmic, C & N dynamics PLFA Steenwerth et al. (2005
A, P UK C, CL, SCL, SC, SL, LS Grassland or tillage Heat; Cu; compression 28 days Decomposition, physical structure ELFA Gregory et al. (2009
Fire 
US ORG over SiL Burning Warming (in field plots) 3 years Cmic, enzyme activity Clone & sequence Allison et al. (2010
AU Burning, topology Heat 37 days Cmic, decomposition DGGE, PLFA Banning & Murphy (2008
ES DC & DR Burning, retardant n/a 1 year Bacterial & fungal growth, CLPP – Velasco et al. (2009
TN SC (CLCn/a Heat +/− glucose 56 days Respiration – Hamdi et al. (2011
Land management 
JP A, E, U Org/Con fertilizer Fumigation, grinding 56 days Cmic, decomposition; nematodes – Fujino et al. (2008
UK SL, SCL, C Compaction Compression 7 days Physical structure ELFA Gregory et al. (2007
UK LS Org/Con cultivation Heat; Cu 60 days Decomposition –  
UK SCL Reseed, sludge, biocide, N + lime Heat; Cu 28 days Decomposition DGGE Kuan et al. (2006
CN U, C Soil restoration Heat; Cu; grinding 28 days Decomposition TRFLP Zhang et al. (2010
UK Subsoil (DFCSoil restoration Heat; Cu; compression 28 days Decomposition, physical structure ELFA Griffiths et al. (2008a
FR – Sterile/fresh compost 1 year Cmic, SIR ARISA, PLFA Saison et al. (2006
Metal contamination 
CN – Copper (1 year) Cu 40 days Cmic, SIR, PNR, qPCR PLFA Deng et al. (2009
DK SL Copper (5 years) Cu, organic matter 84 days PICT, CLPP, respiration TRFLP Brandt et al. (2010
ES C, R Copper (long-term) Cu (53 soils) 1 day PICT, growth rate – Fernández-Calviño et al. (2011
NL Copper (long-term) Heat; D-W 60 days Decomposition, bacterial growth rate – Tobor-Kaplon et al. (2005
NL Copper (long-term) Pb; NaCl 60 days Decomposition, bacterial & fungal growth rate – Tobor-Kaplon et al. (2006b
BE S, SL Lime or compost Cu 160 days Nitrification – Kostov & Van Cleemput (2001
FR SiCL Straw or compost (15 years) Cu – Bacterial growth on Cu media Clone & sequence Lejon et al. (2010
BE SL Zinc (10 years) Pesticide, D-W, F-T 21 days PNR – Mertens et al. (2007
NL Zinc (long-term) Heat; NaCl; Pb 60 days Decomposition, bacterial & fungal growth rate – Tobor-Kaplon et al. (2006a
BE SL – Zn; NH4Cl 1 year PNR DGGE Ruyters et al. (2010a
BE SL – Zn, organic matter 1 year PDR, qPCR nosZ DGGE Ruyters et al. (2010a, b
DK – Mercury (14 years) Heat 180 days Decomposition, CLPP DGGE Müller et al. (2002
FR SiC Heat (35 °C), Cu, atrazine Hg 150 days – ARISA Bressan et al. (2008
FR EC Heat (35 °C), Cu, atrazine Hg 120 days NO3 reducing activity RFLP Philippot et al. (2008
UK CL (ECMetal contaminated sludge Heat; Cu; compression 28 days Decomposition, physical structure – Griffiths et al. (2005
NO SL – Cu, CD, Zn mixture 60 days PDR, tolerance – Holtan-Hartwig et al. (2002
Pollution 
DE Subsoil (SL) Petroleum contamination Heat; Cu 60 days Decomposition – Griffiths et al. (2001a
DK Tylosin Heat 60 days Decomposition, CLPP DGGE Müller et al. (2002
DK – Tylosin 60 days Bacteria, fungi, protozoa, CLPP DGGE Westergaard et al. (2001
US SiL – 2,4,5-T 42 days Tolerance, culture phenotype DNA re-association Atlas et al. (1991
Soil properties 
A, P UK SL Mineral or organo-mineral Cu; benzene 63 days Decomposition, CLPP DGGE Girvan et al. (2005
A, F UK CL; S Contrasting soils Heat; Cu 28 days Decomposition PLFA Griffiths et al. (2008b
A, P, F, M UK SC, SL, L, CL, S, SCL 26 soils across Scotland Heat; Cu; compression 28 days Decomposition, physical structure – Kuan et al. (2007
CA C, TILL – D-W; Cu; HCl 2 days Cmic, SIR, tolerance PLFA Royer-Tardif et al. (2010
Biodiversity related studies 
UK SCL Fum & inoculation Matric potential 96 days Cmic, catabolic potential, decomposition PLFA Degens (1998
UK CL Differential fum Heat; Cu 63 days Decomposition DGGE, PLFA Griffiths et al. (2000
FR CL Plant species richness Heat; Cu 60 days Decomposition – Griffiths et al. (2001a
UK CL Sterile soil inoculated Heat; Cu 60 days Decomposition – Griffiths et al. (2001b
UK SCL Fum & inoculation Heat; Cu 28 days Cmic, decomposition DGGE Griffiths et al. (2004
NZ n/a Plant species richness D-W 16 months Cmic, respiration, decomposition – Orwin & Wardle (2005
FR Sterile soil inoculated Heat 28 days Respiration, PDR, PNR DGGE Wertz et al. (2007
Experimental studies 
UK CL n/a Drying, sieving 56 days Cmic, catabolic potential, decomp – Degens (1998
Chr NZ, US PM Vegetation chronosequence D-W 3 days Cmic, respiration, decomposition, mineral N – Orwin et al. (2006
Al, A NP, SI SL, LS, SiL, H – F-T 60 cycles Enzyme activity, respiration, qPCR 16S – Stres et al. (2010
NZ – Physical disturbance n/a 120 days  454 sequencing Lekberg et al. (2011
Ecosystem Location Soil type Soil treatment Situation Experimental disturbance Duration Resistance and resilience of Microbial community measures Reference 
Cultivation 
BR L (FForest or agriculture Heat 30 days Enzyme activity, respiration PLFA Chaer et al. (2009
NZ SiCL Grassland or tillage HCl; NaCl; Cu; D-W; F-T 14 days Cmic, catabolic potential   Degens et al. (2001
US SL Grassland or tillage D-W 5 days Cmic, C & N dynamics PLFA Steenwerth et al. (2005
A, P UK C, CL, SCL, SC, SL, LS Grassland or tillage Heat; Cu; compression 28 days Decomposition, physical structure ELFA Gregory et al. (2009
Fire 
US ORG over SiL Burning Warming (in field plots) 3 years Cmic, enzyme activity Clone & sequence Allison et al. (2010
AU Burning, topology Heat 37 days Cmic, decomposition DGGE, PLFA Banning & Murphy (2008
ES DC & DR Burning, retardant n/a 1 year Bacterial & fungal growth, CLPP – Velasco et al. (2009
TN SC (CLCn/a Heat +/− glucose 56 days Respiration – Hamdi et al. (2011
Land management 
JP A, E, U Org/Con fertilizer Fumigation, grinding 56 days Cmic, decomposition; nematodes – Fujino et al. (2008
UK SL, SCL, C Compaction Compression 7 days Physical structure ELFA Gregory et al. (2007
UK LS Org/Con cultivation Heat; Cu 60 days Decomposition –  
UK SCL Reseed, sludge, biocide, N + lime Heat; Cu 28 days Decomposition DGGE Kuan et al. (2006
CN U, C Soil restoration Heat; Cu; grinding 28 days Decomposition TRFLP Zhang et al. (2010
UK Subsoil (DFCSoil restoration Heat; Cu; compression 28 days Decomposition, physical structure ELFA Griffiths et al. (2008a
FR – Sterile/fresh compost 1 year Cmic, SIR ARISA, PLFA Saison et al. (2006
Metal contamination 
CN – Copper (1 year) Cu 40 days Cmic, SIR, PNR, qPCR PLFA Deng et al. (2009
DK SL Copper (5 years) Cu, organic matter 84 days PICT, CLPP, respiration TRFLP Brandt et al. (2010
ES C, R Copper (long-term) Cu (53 soils) 1 day PICT, growth rate – Fernández-Calviño et al. (2011
NL Copper (long-term) Heat; D-W 60 days Decomposition, bacterial growth rate – Tobor-Kaplon et al. (2005
NL Copper (long-term) Pb; NaCl 60 days Decomposition, bacterial & fungal growth rate – Tobor-Kaplon et al. (2006b
BE S, SL Lime or compost Cu 160 days Nitrification – Kostov & Van Cleemput (2001
FR SiCL Straw or compost (15 years) Cu – Bacterial growth on Cu media Clone & sequence Lejon et al. (2010
BE SL Zinc (10 years) Pesticide, D-W, F-T 21 days PNR – Mertens et al. (2007
NL Zinc (long-term) Heat; NaCl; Pb 60 days Decomposition, bacterial & fungal growth rate – Tobor-Kaplon et al. (2006a
BE SL – Zn; NH4Cl 1 year PNR DGGE Ruyters et al. (2010a
BE SL – Zn, organic matter 1 year PDR, qPCR nosZ DGGE Ruyters et al. (2010a, b
DK – Mercury (14 years) Heat 180 days Decomposition, CLPP DGGE Müller et al. (2002
FR SiC Heat (35 °C), Cu, atrazine Hg 150 days – ARISA Bressan et al. (2008
FR EC Heat (35 °C), Cu, atrazine Hg 120 days NO3 reducing activity RFLP Philippot et al. (2008
UK CL (ECMetal contaminated sludge Heat; Cu; compression 28 days Decomposition, physical structure – Griffiths et al. (2005
NO SL – Cu, CD, Zn mixture 60 days PDR, tolerance – Holtan-Hartwig et al. (2002
Pollution 
DE Subsoil (SL) Petroleum contamination Heat; Cu 60 days Decomposition – Griffiths et al. (2001a
DK Tylosin Heat 60 days Decomposition, CLPP DGGE Müller et al. (2002
DK – Tylosin 60 days Bacteria, fungi, protozoa, CLPP DGGE Westergaard et al. (2001
US SiL – 2,4,5-T 42 days Tolerance, culture phenotype DNA re-association Atlas et al. (1991
Soil properties 
A, P UK SL Mineral or organo-mineral Cu; benzene 63 days Decomposition, CLPP DGGE Girvan et al. (2005
A, F UK CL; S Contrasting soils Heat; Cu 28 days Decomposition PLFA Griffiths et al. (2008b
A, P, F, M UK SC, SL, L, CL, S, SCL 26 soils across Scotland Heat; Cu; compression 28 days Decomposition, physical structure – Kuan et al. (2007
CA C, TILL – D-W; Cu; HCl 2 days Cmic, SIR, tolerance PLFA Royer-Tardif et al. (2010
Biodiversity related studies 
UK SCL Fum & inoculation Matric potential 96 days Cmic, catabolic potential, decomposition PLFA Degens (1998
UK CL Differential fum Heat; Cu 63 days Decomposition DGGE, PLFA Griffiths et al. (2000
FR CL Plant species richness Heat; Cu 60 days Decomposition – Griffiths et al. (2001a
UK CL Sterile soil inoculated Heat; Cu 60 days Decomposition – Griffiths et al. (2001b
UK SCL Fum & inoculation Heat; Cu 28 days Cmic, decomposition DGGE Griffiths et al. (2004
NZ n/a Plant species richness D-W 16 months Cmic, respiration, decomposition – Orwin & Wardle (2005
FR Sterile soil inoculated Heat 28 days Respiration, PDR, PNR DGGE Wertz et al. (2007
Experimental studies 
UK CL n/a Drying, sieving 56 days Cmic, catabolic potential, decomp – Degens (1998
Chr NZ, US PM Vegetation chronosequence D-W 3 days Cmic, respiration, decomposition, mineral N – Orwin et al. (2006
Al, A NP, SI SL, LS, SiL, H – F-T 60 cycles Enzyme activity, respiration, qPCR 16S – Stres et al. (2010
NZ – Physical disturbance n/a 120 days  454 sequencing Lekberg et al. (2011

Only those papers specifically referring to resistance and resilience are included in this summary table.

Ecosystem: A, tillage agriculture; AL, alpine; Chr, primary vegetation chronosequence; F, forest; M, moor; P, pasture (grassland); V, vineyard. Soil type: C, clay; L, loam; ORG, organic; S, sand; Si, silt; TILL, glacial till; A, andisol; C, cambisol; CLC, calcaric-leptic cambisol; DC, dystric-cambisol; DR, dystric-regosol; DFC, dystric-fluvic cambisol; E, entisol; EC, eutric cambisol; F, fragiudult; H, histosol; R, regosol; U, ultisol. Soil treatment: fum, fumigation; org/con, organic/conventional. Situation: F, field; G, glasshouse; L, laboratory. Experimental disturbance: D-W, dry–wet cycle; F-T, freeze–thaw cycle. Resistance and resilience of: CLPP, community level physiological profile; Cmic, microbial biomass carbon; Decomp, decomposition; PDR, potential denitrification rate; PICT, pollution induced community tolerance; PNR, potential nitrification rate; SIR, substrate induced respiration. Microbial community measures: ARISA, automated ribosomal intergenic spacer analysis; DGGE, denaturing gradient gel electrophoresis; ELFA, ester linked fatty acid; PLFA, phospho lipid fatty acid.

Resistance, resilience and functional stability

Definitions

Throughout this review, we will adopt the definitions proposed by Rykiel (1985), that ‘disturbance’ is a biotic or abiotic cause which results in the effect of either a ‘perturbation’, response of an ecological component or process, or a ‘stress’, physiological response of an individual or functional response of the system. Definitions of resistance, resilience and stability in biological systems have been reviewed previously (Botton et al., 2006; Brand & Jax, 2007). Resistance is commonly defined as the ability of a system to withstand a disturbance, while definitions of resilience fall into two categories, engineering or ecological resilience (Fig. 2). Engineering resilience is where the behaviour of the system is treated like an engineering material that will show displacement and recovery towards its predisturbance state or a new stable state. Resistance to disturbance and the speed of return (resilience) are the two components of ecosystem stability as described by Pimm (1984), McNaughton (1994) and Loreau et al. (2002).

Figure 2

Schematic representation of engineering (a) and ecological resilience (b). In the engineering definition, stability is defined by the immediate response to disturbance (resistance) and then recovery over time (resilience). In the ecological definition, the ball in the basin represents the ‘state’ of the system. Resilience is a measure of how much disturbance can the system (ball) absorb so that it still remains in the same basin, before it flips over into another stable state (different basin).

Figure 2

Schematic representation of engineering (a) and ecological resilience (b). In the engineering definition, stability is defined by the immediate response to disturbance (resistance) and then recovery over time (resilience). In the ecological definition, the ball in the basin represents the ‘state’ of the system. Resilience is a measure of how much disturbance can the system (ball) absorb so that it still remains in the same basin, before it flips over into another stable state (different basin).

Ecological resilience considers how much disturbance is required to move the system from one stable state to another alternate stable state, using the ‘ball and cup’ model (Holling, 1973; Gunderson et al., 2002; Fig. 1). Both definitions of resilience suffer from the difficulty of applying the concept of ‘stable state’ to natural ecosystems because they change not only in response to disturbance but are also subjected to gradual natural changes. However, Potts et al. (2006) were able to identify two stable states of ecosystem carbon and water fluxes following a wetting event, Gao et al. (2011) noted a degradation threshold for soil services at about 20% vegetation cover, while in experimental systems increasing disturbance did lead to alternative stable states in the community assembly of protists (Jiang & Patel, 2008). In a comprehensive review by Scheffer et al. (2001), analysis of several case studies suggested the presence of alternative stable states in various ecosystems but the authors also highlighted the difficulty of proving their existence, which required combinations of different approaches and modelling. There is a link between ecological and engineering resilience in that the theory of ‘critical slowing down’ proposes that recovery rates from small disturbances (i.e. engineering resilience) get slower and slower as a system approaches the tipping point between one stable state and another (i.e. ecological resilience) (Van Nes & Scheffer, 2007). This connection between engineering and ecological resilience has also been demonstrated for a range of complex systems, including: financial markets; epileptic seizure; fish stocks; catastrophic desertification and past climatic changes (Scheffer et al., 2009).

The engineering resilience approach predominates in the studies of soil biology and also in the study of soil physical parameters (Munkholm & Schjønning, 2004) and soil quality (Seybold et al., 1999). This review will therefore use the engineering definition of resilience; largely because experimentally it is convenient to consider the response and recovery of a population or function to a perturbation.

Calculating resistance and resilience

Calculations of resistance and resilience following disturbance can be performed by comparing between samples taken pre- and post-disturbance. However, such an approach does not take into account any changes occurring in control soils over time, either seasonal changes in the field or changes over time in an incubation. The use of control and disturbed samples at the same time eliminates this uncertainty and the calculation of resilience and resistance are usually presented as a proportion or percentage of the variable measured in the disturbed treatment to the control (undisturbed) treatment at the same time. Variations in the calculations are detailed in Table 2. Equations have generally taken the form of: change relative to the control (Sousa, 1980; Kaufman, 1982; Griffiths et al., 2000; Chaer et al., 2009); accounting for absolute differences between soils (Orwin & Wardle, 2004); or integrated measures (O'Neill, 1976; Fujino et al., 2008; Zhang et al., 2010).

Table 2

Calculation of resistance and resilience indices

Resistance Resilience Reference 
graphic graphic Kaufman (1982
graphic graphic Sousa (1980
graphic graphic Griffiths et al. (2000
graphic NC Chaer et al. (2009
graphic graphic Orwin & Wardle (2004
graphic graphic Zhang et al. (2010
NC graphic O'Neill (1976
Resistance Resilience Reference 
graphic graphic Kaufman (1982
graphic graphic Sousa (1980
graphic graphic Griffiths et al. (2000
graphic NC Chaer et al. (2009
graphic graphic Orwin & Wardle (2004
graphic graphic Zhang et al. (2010
NC graphic O'Neill (1976

C, variable measured in the control soil (undisturbed) at time 0 (immediately after disturbance) or at time x after disturbance; D, variable measured in disturbed soil at time 0 (immediately after disturbance) or at time x after disturbance; NC, not calculated.

Response of soil microorganisms to environmental disturbances

Changes occurring over primary successional gradients provided a means of testing several hypotheses regarding the interaction between soil nutrients and microbial stability (Orwin et al., 2006). These gradients covered the development of soils spanning hundreds of years but interactions, for example, between soil C, N, P status and the stability of microbial respiration to drying, depended on the location and the response variables considered. There were few consistent patterns of resistance and resilience and it was concluded that several factors might be affecting the outcome, such as: soil microbial community composition, plant community composition, adaptation to disturbance, soil texture and clay content, substrate diversity and food web structure.

Commonly studied environmental disturbances include, for example, fire, desiccation and freeze–thaw cycles. Adaptation to repeated freezing was demonstrated by comparing the response of Himalayan and temperate soils to repeated freeze–thaw cycles (Stres et al., 2010). Microbial respiration in temperate soils was far more susceptible to freezing than the Himalayan soils, but surviving temperate soil microorganisms eventually adapted to the changed environmental conditions. Adaptation was also evident in the stability of bacterial growth rates in Mediterranean pasture soils with high resistance and resilience to fire (Velasco et al., 2009). In a Mediterranean-type forest system subject to periodic burning, Banning & Murphy (2008) compared resilience of both a function (malate decomposition) and microbial biomass following a heat disturbance, in burnt or unburnt soil sampled from mounds or furrows. There were differences in both resistance and resilience related to nutrient limitation (soil C and N contents) as well as microbial biomass. They hypothesized that there was a threshold content below which the microbial biomass was no longer able to respond to the added substrate. Hamdi et al. (2011) also noted increased resistance of respiration to subsequent heat disturbance as a result of lower microbial biomass and reduced substrate availability. Similarly, Allison et al. (2010) suggested that nutrient limitation (depletion of labile C from the soil), resulting from burning of a boreal forest several years previously, increased the resistance of fungal community composition or microbial biomass to soil warming. This links with observations that C starvation increases microbial resistance to disturbance (Van Overbeck et al., 1995). In pure or mixed boreal forest stands resulting from wildfire, harvesting and soil type, resilience of the microbial biomass to experimental disturbances (dry–wet, Cu and HCl) was probably also related to nutrient limitation and thus to the parent geological material (Royer-Tardif et al., 2010). Resistance, on the other hand, was greatest in mixed stands, probably resulting from increased resource diversity leading to greater microbial diversity and more resistant taxa (Royer-Tardif et al., 2010). To study the effect of desiccation and rewetting, McKew et al. (2011) experimentally extended the desiccation period in a salt-marsh system and showed that while soil microbial function (extracellular enzyme activity) was resilient after flooding, microbial community structure was irreversibly altered with a different microbial community developing in the desiccated sediments compared with the control even after rewetting. The bacterial community composition was resistant to drying–rewetting cycles in grassland soils but not in an oak forest soil, while taxonomic diversity and richness were relatively insensitive to drying–rewetting frequency (Fierer et al., 2003).

Altogether, these findings partly reflect those of Orwin & Wardle (2005) that stability results from complex interactions but indicates that microbial community structure is not the sole determinant of functional resilience.

Response of soil microorganisms to management disturbances

As well as environmental disturbances experienced by many soil systems, disturbances often arise from land management. Tillage causes major changes to the soil system and direct effects on soil biology have been extensively documented (Wardle, 1995). For example, soil tillage resulted in significant modifications of the mycorrhizal fungal community structure (Jansa et al., 2002, 2003). Tillage also reduced the stability, compared with grassland soil, of C and N dynamics to a dry/wet event and caused a greater shift in microbial community structure (Steenwerth et al., 2005). Tilled soils also had functional characteristics that were less resistant to a range of disturbances (e.g. pH, osmotic, copper, dry/wet, freeze/thaw) than grassland soils, but this difference was independent of the size of the microbial biomass and more related to the functional characteristics of the community (the so-called catabolic response profile) (Degens et al., 2001). In a comparison of 15 soils from a range of long-term grassland and arable sites in the United Kingdom, grassland soils showed greater physical stability (to compression and wet/dry cycles) and biological stability (of plant decomposition to heat and copper disturbance) largely related to management effects on organic matter and interactions with clay content (Gregory et al., 2009). In tropical forest, sites converted to agriculture, enzyme activities were more stable to experimental heat disturbance in the forest soils, although there were clear differences in the stability depending on the functions monitored. Thus, a general function (i.e. fluorescein diacetate hydrolysis, which is a ubiquitous microbial activity) was equally stable in the forest and agriculture sites, while substrate-specific activities (i.e. cellulose and laccase which are not utilized by all microorganisms) were less resilient in the agriculture sites (Chaer et al., 2009). The conclusion was that the agriculture sites had a less diverse community of microorganisms capable of degrading the specific substrates than the unconverted forest sites. On the other hand, in temperate upland grassland plots where different management scenarios affected soil functional stability (of plant decomposition to heat and copper disturbance), there was no association between stability and broadscale changes in microbial community structure revealed by PCR-DGGE (Kuan et al., 2006). The authors suggested that there was a protective effect of certain soil properties and that microbial functions were more susceptible to a second disturbance following the initial disturbance represented by the agricultural practices (Kuan et al., 2006). Tobor-Kaplon et al. (2005, 2006a, b) tested this further in soils under long-term disturbance from copper, zinc or low pH. In soil collected from a pine forest, a transient heat disturbance imposed stronger changes in the stability of lucerne decomposition than lead or salt disturbances, but in soil of a similar texture from an arable site heat had the least effect on stability (Tobor-Kaplon et al., 2006a). However, in soil of a similar texture from an arable site under the influence of copper or low pH, a transient heat disturbance had the least effect on stability (Tobor-Kaplon et al., 2005, 2006b). This was related to the environmental fluctuations experienced by microorganisms at the two sites.

A practical application of heat disturbance is the use of soil solarization to decrease the incidence of disease in any subsequent crop. Although the vast majority of studies have concentrated on populations of specific pathogens, there has been some measurement of the effects on the broader soil microbial community structure. Culman et al. (2006) followed bacterial and fungal community structures by terminal restriction fragment length polymorphism (TRFLP) in a rice–wheat cropping system and reported clear and consistent effects of solarization (average temperature increase in 10 °C) only for fungi. Differences persisted into the next cropping cycle but there was resilience in that the communities became more similar over time. In a wheat–legume rotation with an average temperature increase in 20 °C, solarization was the main factor driving differences in the eubacterial community with similar but less pronounced effects for beta-proteobacteria, actinomycetes and alpha-proteobacteria (Gelsomino & Cacco, 2006). Bacterial diversity changed over time following solarization, increasing and then decreasing in this example, which might explain changes in functional resilience in soils given an experimental heat disturbance. These shifts in microbial community structure following solarization were not attributed to a direct thermal effect but rather to changes in the physico-chemical habitat or other ecological factors (Gelsomino & Cacco, 2006).

Organic amendments are often added to soils and can generally increase soil resilience. For example, Fujino et al. (2008) observed an increase in both resistance and resilience of cellulose activity to disinfection using sodium methyl dithiocarbamate (metam sodium) in soil amended with manure. Organically managed arable soils showed greater resilience of plant decomposition to experimentally applied heat or copper disturbances than intensively managed soils with no addition of organic matter (Griffiths et al., 2001a). Physical resilience of soil is also enhanced by the addition of organic matter, as demonstrated by the addition of peat to a clay soil (Zhang et al., 2005). Here, resistance to compression was actually reduced by the addition of peat but resilience increased and the authors related these fundamental observations to practical issues regarding the compaction of soils.

As a measure of the restoration of degraded soils, biological resilience took longer to improve than measures of the physical resilience of a subsoil (Griffiths et al., 2008a) which may indicate that a comparison of the two could indicate the stage of restoration reached.

Response of soil microorganisms to heavy-metal contaminated soils

At the extreme end of land management, soils may become contaminated with a variety of compounds such as heavy metals. A large body of microcosm and field studies provide evidence of a low resistance and resilience of most microbial functions to heavy metal. Copper is one of the most commonly investigated soil contaminants and so has attracted its fair share of stability studies. It has a broad-spectrum effect and alters the structure of the archaeal, bacterial and fungal communities (Wakelin et al., 2010a; Macdonald et al., 2011), with particular negative effects on Acidobacteria (Wakelin et al., 2010b; Macdonald et al., 2011) and positive effects on Actinobacteria (Lejon et al., 2008). Bacillus and Sphingomonas were particularly resistant to copper (Wakelin et al., 2010b). Brandt et al. (2010) concluded that the long-term response of microbial respiration to copper resulted from the ability of the microorganisms to develop Cu tolerance without affecting overall community structure. Lejon et al. (2010) suggested that copper adaptation was related to soil organic matter composition. The effects of an experimental, short-term, disturbance (Pb or NaCl) on the functional stability of soil from plots under a long-term disturbance from copper or low pH was dependent on the function measured (short-term decomposition of plant residues or the growth rates of bacteria and fungi) but was generally reduced by the long-term disturbance (Tobor-Kaplon et al., 2005).

The impact of heavy metals has been investigated on specific microbial guilds, in particular N-cycling microorganisms because nitrogen is the nutrient most often limiting for plant growth (Bollag & Barabasz, 1979; Bardgett et al., 1994). Kandeler et al. (1996) showed that enzymes involved in N-cycling were less resistant to increasing heavy-metal contamination than those involved in C-cycling. This is supported by the finding that decomposition of glucose was more stable than potential nitrification in a copper-contaminated arable soil (Deng et al., 2009). Resilience of nitrifying activity occurred over 1–2 years following contamination by Zn (Rusk et al., 2004; Ruyters et al., 2010a) and adaptation to the heavy metal resulted from a shift in the structure in the ammonia-oxidizing bacterial community that gradually dominated the nitrifying community (Ruyters et al., 2010b). Denitrifying activity, in contrast, was partly recovered 8 days after heavy-metal addition (Cu, Cd and Zn) with complete resilience after 2 months (Holtan-Hartwig et al., 2002). Exposure of cells extracted from the contaminated soils to heavy metals indicated that they had developed a tolerance to the heavy metals (Holtan-Hartwig et al., 2002), as has been shown for bacteria in general (Bååth et al., 1998, 2005; Fernández-Calviño et al., 2011). In contrast, no resilience of the denitrifying activity was observed 3 months after silver addition while silver induced the enrichment of novel denitrifiers (Throback et al., 2007).

Several factors can lead to the resilience of microbial communities and functions to heavy-metal contamination, including substitution of sensitive strains by tolerant ones; genetic modifications to produce heavy-metal resistance; transfer of genes encoding resistance or tolerance against heavy metals; or decreased heavy-metal bioavailability. The transfer of mobile genetic element by plasmids among taxonomically diverse bacteria in soil is well described (Springael & Top, 2004) and can contribute to the dissemination of genes that provide resistance to contaminant stress (reviewed in Smalla & Sobecky, 2002; Sobecky & Coombs, 2009). As such, the emergence of resistance to heavy metals or other contaminants in the soil microbial community can be regarded as a process describing deterioration of the ecosystems and is a bioindicator of contaminant exposition (Bérard et al., 2004).

Insights into the underlying mechanisms

Resistance, resilience and the biodiversity–ecosystem functioning relationships debate

According to the insurance hypothesis (Loreau et al., 2002), one of the proposed consequences of biodiversity loss is a reduction in the ecosystem stability. This hypothesis is based on the intuitive idea that the probability of finding species able to adapt to changing conditions and allowing ecosystem functioning is greater in a more diverse ecosystem. A test of this hypothesis in soil using differential fumigation with chloroform to decrease soil biodiversity showed reduced resilience of plant decomposition to heat and copper disturbance in soils with the lowest biodiversity (Griffiths et al., 2000). Subsequent experiments with an arable soil that was sterilized and then inoculated with diluted soil suspensions to alter biodiversity (Griffiths et al., 2001b) or with an upland grassland soil, whose biodiversity had been altered by both fumigation or dilution (Griffiths et al., 2004), showed no consistent effects of biodiversity on stability. This may have arisen because the way in which biodiversity is manipulated (i.e. fumigation or sterilization and inoculation) can affect the response of the soil microbial community to disturbance (De Ruiter et al., 2002). Thus, fumigation in particular may have selected for certain physiological traits in the surviving microorganisms (Griffiths et al., 2000, 2001b), while changes in stability are thought to be related to the traits of individual species in the community (Griffiths et al., 2004). An alternative approach is to experimentally build up different levels of biodiversity. Assemblages of up to 43 species of fungi did show evidence of increasing stability with increasing biodiversity (Setälä & McClean, 2004; Dang et al., 2005). As did communities containing up to 72 species of bacteria (Bell et al., 2005) in which there was a decelerating relationship between species richness and function (community respiration). This was consistent with there being functional redundancy between the species, but with the caveat that apparently unimportant species in a stable environment might have a role in maintaining function in a fluctuating environment, that is, be important for stability (Bell et al., 2005). However, soils contain far more species than generally used in such community assembly experiments and effects of biodiversity are more evident in systems with low diversity (Nielsen et al., 2011). Changes in species richness are most often considered when investigating the role of biodiversity for ecosystem functioning while biodiversity encompasses other components such as evenness (the relative abundance of species). Manipulation of both richness and evenness of the denitrifier community revealed that resistance to salinity disturbance was lower when initial communities were highly uneven or dominated by a few species, which demonstrated that not only richness but also of evenness can be of importance for ecosystem stability (Wittebolle et al., 2009).

Much research has also been conducted on the intermediate disturbance hypothesis (IDH). This hypothesis is based on the assumption that there is a trade-off between the ability to compete and the ability to withstand a disturbance. According to the IDH, intermediate levels of disturbance result in a higher biodiversity level because of the coexistence of organisms having different life strategies (i.e. r and K), which ensure ecosystem stability (Connell, 1978). Accordingly, resilience of methane oxidation activity to pyrene contamination was observed only at low pyrene concentration, which also increased biodiversity of the methane oxidizers. At high concentrations, diversity was decreased and no recovery was observed (Deng et al., 2011). Similarly, by examining soils from an experimental gradient of copper contamination, Wakelin et al. (2010b) showed that changes in microbial diversity followed a unimodal response (i.e. increased until a critical concentration then decreased) in line with the IDH.

Other studies have manipulated plant diversity to examine the effects on the resilience of soil microorganisms. Orwin & Wardle (2005) found no effect of plant biodiversity but a strong effect of plant species composition on the microbial resistance and resilience to a drought disturbance. They concluded that either nutrient limitation or soil microbial community structure may have altered soil resilience, while resistance was neither related to soil chemical nor to microbial community properties. Increasing the number of grassland plant species from one to six similarly did not alter soil functional stability (Griffiths et al., 2001a). On the other hand, Pfisterer & Schmid (2002) found an inverse relationship between plant species richness and microbial resistance and resilience to drought. Arbuscular-Mycorrhizal fungal communities proved high resilience to the removal of specific plant functional groups, showing a complete recovery in colonization after 30 months (Urcelay et al., 2009), but it was speculated that ericoid and ectomycorrhizal fungi would be less resilient to changes in vegetation. Community composition and richness of arbuscular-mycorrhizal fungal communities in Plantago lanceolata roots were also found to be resistant to disturbance, which was not because of a recolonization of the disturbed area (Lekberg et al., 2011),

These studies showed that the influence of biodiversity on ecosystem stability is complex and depends not only on species richness but also on the evenness or composition of the soil microbial community. Resistance and resilience to disturbance might also vary between functional microbial microbial guilds dependent on their levels of functional redundancy. A high level of functional redundancy, within a functional community, that is, a high number species performing the same function, might act as a buffer against the effect of biodiversity loss on functioning. For example, manipulation by dilution of microbial biodiversity showed that resistance and resilience to a heat disturbance differed between the microbial communities studied, with denitrifiers being less affected than nitrite oxidizers (Wertz et al., 2007). As denitrifiers are more diverse than nitrite oxidizers, it was hypothesized that functional redundancy was higher for denitrifiers that buffered the effect of their decreased diversity. Functional redundancy is also supported by the finding that a narrow scale function (decomposition of dichlorophenol) was significantly reduced following benzene or copper addition, whereas a broadscale function (decomposition of wheat shoots) was unaffected (Girvan et al., 2005). However, the contribution of the redundancy of the soil microbial community to resilience might not hold for specific soil functions if the microbial community is already reduced in diversity because of some previous disturbance (Liebich et al., 2007). In any case, redundancy is a multifaceted concept and whether it really exist or not in natural ecosystem is still debated (Loreau, 2004). Studies addressing the role of redundancy in microbial ecology are also hampered by the difficulty to accurately define functional categories and limited knowledge of the true diversity of the corresponding microbial guilds. For example, functional redundancy was assumed to be low among microorganisms performing the first step of nitrification until the finding in 2005 that microorganisms belonging to another domain, the crenarchaea were also capable to oxidize ammonium into nitrate (Könneke et al., 2005). Finally, the apparent inconsistency of data on the role of microbial diversity for soil functioning is not surprising because the effect of the soil microbial diversity is interwoven with many other factors such as: interactions between species; soil properties; or the disturbance history as discussed below.

Ecological networks

Together with diversity, the importance of interactions between species for ecosystem stability has long been studied in ecology using ecological network to describe these interactions (May, 1972; Pimm, 1984; Montoya et al., 2006). Early theory paradoxally predicted that more complex network are likely to be less stable (May, 1974), the loss of one species following disturbance leading more easily to secondary extinction in highly connected networks (Solé & Montoya, 2001; Dunne et al., 2002). In contrast, compartmentalization, that is, the existence of groups of species that have a higher probability of interacting with each another than with other species, significantly increases both resistance and resilience against perturbation because compartments act to buffer the propagation of extinctions (May, 1972; Stouffer & Bascompte, 2011). The relationship between network architecture and stability can also be affected by the type of interaction. A highly connected and nested architecture promotes community stability in mutualistic networks, whereas stability is increased in compartmented and weakly connected architectures in trophic networks (Thébault & Fontaine, 2010). Allesina & Tang (2012) showed that weak interactions can be either stabilizing or destabilizing depending on the type of interactions between species. Here, weak interactions and a realistic food web structure (as opposed to unstructured networks in which species interact at random) were found to decrease the stability of predator-prey systems. Despite a large body of literature, the identification of the network properties involved in ecosystem stability is still ongoing (Montoya et al., 2006).

Ecological networks are commonly used to understand the resistance of native communities to invasion by new species (Romanuk et al., 2009), which can be considered as a disturbance. While natural invasion by exotic species is difficult to study in microbiology, there is a large body of literature investigating the effects of the introduction of new microbial species in soil, mostly as pest biocontrol, on indigenous microorganisms. In most cases, introduction of a fungal or bacterial biocontrol agent had a minimal impact on the soil microbial community composition. Indeed, application of the nonpathogenic fungal strains of Fusarium oxysporum or Trichoderma atroviride showed minor shifts in both the bacterial and fungal communities that lasted only a few weeks (Edel-Hermann et al., 2009; Savazzini et al., 2009). Similarly, bacterial biocontrol agents caused only minor and transient modifications of the microbial community composition (Bankhead et al., 2004; Scherwinski et al., 2007; Correa et al., 2009). Altogether these results suggest a strong resiliance and resistance of the native microbial community to invading microorganisms. However, a few studies also reported a significant impact of microbial inoculants on the bacterial community structure (Kozdroj et al., 2004). This could be explained by recent work indicating that, accordingly to ecosystem theory, susceptibility of soil ecosystems to invading microbial species is dependent on their complexity (Fließbach et al., 2009).

Tolerance and adaptation of soil microorganisms

Response of individual cells to disturbance, which has consequences for the stability of the total community, is related to the activation of protective or adaptative mechanisms for surviving. Transcriptional regulation of the genes whose products are involved in physiological tolerance and adaptation to withstand disturbances has been described elsewhere (Ramos et al., 2001, 2009). Physiological mechanisms on the effects of drought and dry/wet cycles were reviewed by Schimel et al. (2007). Exposure to drought results in an accumulation of osmolytes by microorganisms either by producing organic solutes or by taking up ions from the extracellular solution (Csonka, 1989) to maintain cell integrity. Rehydration after a long period of drought can be as stressful as dehydration itself and to prevent a rupture of the cell walls during soil rewetting, microorganisms release the osmolyte carbon resulting in a soil respiration flush (Fierer & Schimel, 2003). In the short term, changes in microbial physiology and the energetic cost of adaptive mechanisms for withstanding a disturbance can affect the resistance and resilience of microbial processes. Thus, physiological effects associated with cell dehydration rather than substrate diffusion limitation were inhibiting nitrification at water potentials lower than −0.6 MPa (Stark & Firestone, 1995). Because the energetic cost of adaptation can differ between microorganisms, in the long–term, adaptation can also result in microbial community composition shifts (Schimel et al., 2007).

Several studies have addressed the effect of heat disturbance on microorganisms and the related molecular mechanisms, which include protein denaturation with disruption and possible destruction of both secondary and tertiary structures. Resistance and adaptation of microorganisms to increased temperature are most often owing to the synthesis of heat shock protein folding and unfolding other proteins (Ramos et al., 2001; Tobor-Kaplon et al., 2006b). Interestingly, induction of heat shock proteins is triggered by exposure to other environmental stressors such as osmotic shock or the presence of heavy metals and aromatic compounds (Ramos et al., 2001), which provides a molecular basis for cross-protection (where exposure to one disturbance increases resistance to a different disturbance, Ventura et al., 2006). The ability of some bacteria to form thick-walled and highly resistant spores is also an efficient way to cope with a heat disturbance but also to protect the bacteria from a large range of other environmental stressors. The modifications induced in the soil microbial community by relatively minor disturbances, such as copper, heat or atrazine, led to a significantly increased resistance of the community structure to a subsequent severe disturbance in the form of mercury contamination (Bressan et al., 2008).

Bacterial cells can acquire resistance to xenobiotic compounds through the transfer of genes or genetic mobile elements. There is a large body of evidence of the transfer in soil of organic xenobiotic-degrading genes (reviewed in Springael & Top, 2004). For example, enhanced biodegradation of the herbicide atrazine, which is used to control weeds in maize production, after repeated herbicide applications has been attributed to horizontal transfer of atrazine degrading genes (Devers et al., 2005, 2007). Mobile genetic element and horizontal gene transfer are important for adaptation not only by disseminating the existing xenobiotic-degrading pathways but also by constructing new ones. Thus, assembly of pre-existing gene motifs to generate new genes and recruitment of genes from other pathways combined with mutation events can lead to new pathways (Copley, 2000). Ability to assemble together novel degradation genes has been shown in vitro by construction of a pesticide degrading gene after DNA shuffling (Boubakri et al., 2006). Adaptation to organic xenobiotics by acquisition of the corresponding degrading genes through horizontal gene transfer and patchwork assembly can lead to changes in microbial communities because of the competitive advantage conferred by the ability to incorporate these compounds into their diets (Copley, 2000; Springael & Top, 2004; Ramos et al., 2009; Udiković-Kolić et al., 2011). Such shifts in microbial diversity are in turn likely to affect the resistance and resilience of soil microorganisms to subsequent disturbances.

Contrasting mechanisms have been proposed to account for tolerance to disturbance. Thus, there is a general increase in the physiological tolerance of the microorganisms in contaminated habitats, favouring generalist microorganisms (Atlas et al., 1991), but an alternative mechanism may occur in specifically metal contaminated sites. Here, individual microorganisms show an increased tolerance by only using high energy substrates despite a reduction of catabolic versatility (Wenderoth & Reber, 1999; Witter et al., 2000). Finally, as discussed previously, exposure of the soil microbial community to disturbance can lead to tolerance and adaption of individual cells to subsequent disturbances.

Effects of previous disturbance

To what extent exposure to an initial disturbance is able to affect the stability of soil microorganisms to subsequent disturbances is still unclear. Already stressed microbial communities can be more or less stable to a second disturbance depending on the nature of the disturbance (Tobor-Kaplon et al., 2005). In later work, Tobor-Kaplon et al. (2006a) found that respiration in the most metal contaminated soils was more affected by a subsequent heat or salt disturbance, which supports the hypothesis that stressed systems have less energy to cope with additional disturbance than previously undisturbed systems. Thus, organisms from highly polluted soils have lowered resources because of the allocation of energy to detoxification and damage repair caused by the first disturbance, which makes any additional disturbance harder to cope with (Calow, 1991; Kuperman & Carreiro, 1997). Lower stability after a new disturbance could also be due to decreased diversity following exposure to an initial disturbance. Indeed, Müller et al. (2002) suggested that the decreased resistance in a heavy-metal contaminated soil as compared to the control was because of a reduced microbial diversity. However, measurements of bacterial growth rates in the gradient of metal polluted soils showed that the least contaminated ones were the least stable to increased temperature, suggesting that disturbed systems can also be more stable because they can gained abilities (adaptation and physiological changes) to cope with additional disturbance (Tobor-Kaplon et al. (2006b). Similarly, hydrocarbon polluted soils exhibited greater resilience of plant decomposition to experimentally applied heat and copper disturbances than unpolluted control soils (Griffiths et al., 2001a). Increased physiological tolerance of microorganisms in contaminated habitats (Atlas et al., 1991) has also been discussed earlier. One could also argue that whether the mechanisms with which the organisms deal with the initial and additional disturbances are related or not will likely to contribute to the microbial community stability to successive disturbances. Thus, primary disturbance because of copper addition, but not to heating or pesticide addition, increased the subsequent resilience of the soil nitrate reducing activity to another heavy metal, mercury, which suggests that the relatedness of the disturbances influences the outcome (Philippot et al., 2008). However, soils with a history of copper-contaminated sludge were not more resistant and resilient to laboratory applied copper disturbance than soils amended with uncontaminated sludge (Griffiths et al., 2005). Mertens et al. (2007) also showed that the stability of nitrification to disturbances (biocide, freeze–thaw and dry–wet) was not related to previous Zn contamination and depended on land use history and the nature of the disturbance.

Tobor-Kaplon et al. (2006a, b) and van der Wurff et al. (2007) suggested that the responses of microbial processes and communities to disturbance depend on the nature of the disturbance and whether a subsequent disturbance is similar to the first, in terms of the mechanisms with which the organisms deal with the disturbance.

Role of soil properties

A clear connection between stability and soil structure was demonstrated by reduced resistance after grinding of the soil, which destroyed its structure. Both resistance and resilience were reduced in revegetated degraded soils when the soil structure had been destroyed (Zhang et al., 2010). Similarly, resistance of cellulose decomposition to chemical disinfection was decreased when the soil was ground to destroy structure (Fujino et al., 2008). It is likely that highly structured pore networks provide a shelter for soil microorganisms, akin to the protected pore space that shelters bacteria from faunal predation in soil (Heijnen & Van Veen, 1991). A survey of 26 soils across Scotland showed that organic carbon content was correlated to resilience after chemical (Cu addition) and physical (compaction) disturbances, whereas resilience after heat was correlated to none of the soil properties. This study also revealed that there was no soil uniformly resilient to all disturbances, so that soils resistant to one disturbance tended to be susceptible to a different disturbance (Kuan et al., 2007). When this data were combined with geographic information system (GIS) techniques and the national soil data base, multiobjective regression tree analysis was able to produce a national map of soil resistance and resilience characteristics (Debeljak et al., 2009) (Fig. 3). Resilience of soils to Triclosan (a broad-spectrum antimicrobial agent used in healthcare products) also correlated with organic matter and clay content (Butler et al., 2011). It was speculated that soil properties affected bioavailability of the Triclosan although differences in resilience might also reflect differences in microbial community structure. Confounding effect of soil properties and diversity were also observed by Girvan et al. (2005). Thus, a greater resistance of the genetic diversity and functional resilience to benzene were found in a more diverse organo-mineral soil than in a less diverse mineral soil.

Figure 3

Risk based maps of Scotland, such as this of overall soil stability (resistence and resilience) determined from the responses to four disturbances (copper, heat, compression and waterlogging) from Debeljak et al., 2009, may be a useful addition to aid decision makers.

Figure 3

Risk based maps of Scotland, such as this of overall soil stability (resistence and resilience) determined from the responses to four disturbances (copper, heat, compression and waterlogging) from Debeljak et al., 2009, may be a useful addition to aid decision makers.

Because the diversity (or composition) of the microbial community present in a soil is strongly dependent on its physico-chemical properties, it is very difficult to distinguish the importance of these two factors for soil resistance and resilience. To disentangle the contribution of abiotic and biotic soil factors to soil stability, Griffiths et al. (2008b) inoculated 26 different sterile soils with a single organism, Pseudomonas fluorescens. They showed that the resistance to copper or heat disturbance varied depending on the soils. The resilience of this organism also varied when inoculated in two contrasting, sterile soils (Griffiths et al., 2008b). Similarly, Bárcenas-Moreno et al. (2011) concluded that community assembly when inoculating sterile soil was driven by soil pH. These results demonstrate the importance of the soil physico-chemical properties for its stability. A transplant experimentation was further designed to swap microbial communities between the two contrasting soils by inoculating two different communities into each of two sterile soils. Interestingly, while in one soil, the different microbial communities inoculated converged resulting in a similar microbial community structure, patterns of resilience remained soil specific (Griffiths et al., 2008b).

Concluding remarks

Multiple factors influence soil stability (resistance and resilience). It is clear that it is related to soil properties such as organic matter, aggregation, the quantity and quality of carbon inputs and, to a lesser extent, clay content and soil pH. As a consequence, land management can increase (e.g. through the addition of organic residues to soil) or decrease (e.g. through the tillage of grassland or conversion of forest to agriculture) soil stability. The role of microbial diversity in soil stability is not simply linked to the absolute number of species present but is related to the functional traits of those species, although there appear to be conflicting conclusions. While on one hand microbial community structure is not a major factor and that stability is independent of microbial biomass, on the other hand, the soil response to disturbance depends on microbial cell characteristics and specific microbial functions (such as increased metabolic versatility in contaminated soils, physiological responses and adaptation). However, these conclusions are compatible given the poor resolution of microbial community diversity analyses, which describe only the dominant populations. We propose that soil biological stability is governed by the physico-chemical structure of the soil through its effect on microbial community composition and microbial physiology (Griffiths et al., 2008b) and that there is no general soil response to disturbance because stability is particular to the disturbance and soil history.

As soil stability results from a combination of soil physico-chemical characteristics and species level characteristics of the microbial community, it bridges these two domains. This could provide a quantitative measure of soil health, which could translate into policy advice and improved land management practices (Griffiths et al., 2001a; Kibblewhite et al., 2008). Stability measurements could also provide an indirect indication of ‘critical slowing down’ and the approach of ecosystem tipping points (Veraart et al., 2011). But rather than studying the effects of experimental disturbances, monitoring soil responses to stochastic natural disturbances may be a useful early indicator of an impending ecological state change (Van Nes & Scheffer, 2007).

Acknowledgements

The authors would like to thank the French Embassy in Dublin for supporting the collaboration between the INRA and Teagasc, and Dr Ayme Spor for helpful comments. B.S. Griffiths acknowledges support from Science Foundation Ireland under their Stokes Professorship initiative; Grant No. 07/SK/B1236b. This work was also partly supported by the European Commission within the EcoFINDERS project (FP7-264465).

References

Allesina
S
&
Tang
S
(
2012
)
Stability criteria for complex ecosystems
.
Nature
 
483
:
205
208
.
Allison
SD
McGuire
KL
&
Treseder
KK
(
2010
)
Resistance of microbial and soil properties to warming treatment seven years after boreal fire
.
Soil Biol Biochem
 
42
:
1872
1878
.
Atlas
RM
Horowitz
A
Krichevsky
M
&
Bej
AK
(
1991
)
Response of microbial populations to environmental disturbance
.
Microb Ecol
 
22
:
249
256
.
Bååth
E
Díaz-Raviña
M
Frostegård
Å
&
Campbell
CD
(
1998
)
Effect of metal-rich rich sludge amendments on the soil microbial community
.
Appl Environ Microbiol
 
64
:
238
245
.
Bååth
E
Díaz-Raviña
M
&
Bakken
LR
(
2005
)
Microbial biomass, community structure and metal tolerance of a naturally Pb-enriched forest soil
.
Microb Ecol
 
50
:
496
505
.
Bankhead
SB
Landa
BB
Lutton
E
Weller
DM
&
McSpadden Gardener
BB
(
2004
)
Minimal changes in rhizobacterial population structure following root colonization by wild type and transgenic biocontrol strains
.
FEMS Microbiol Ecol
 
49
:
307
318
.
Banning
NC
&
Murphy
DV
(
2008
)
Effect of heat-induced disturbance on microbial biomass and activity in forest soil and the relationship between disturbance effects and microbial community structure
.
Appl Soil Ecol
 
40
:
109
119
.
Bárcenas-Moreno
G
Rousk
J
&
Bååth
E
(
2011
)
Fungal and bacterial recolonisation of acid and alkaline forest soils following artificial heat treatments
.
Soil Biol Biochem
 
43
:
1023
1033
.
Bardgett
RD
Speir
TW
Ross
DJ
Yeates
GW
&
Kettles
HA
(
1994
)
Impact of pasture contamination by copper, chromium, and arsenic timber preservative on soil microbial properties and nematodes
.
Biol Fertil Soils
 
18
:
71
79
.
Bell
T
Newman
JA
Silverman
BW
Turner
SL
&
Lilley
AK
(
2005
)
The contribution of species richness and composition to bacterial services
.
Nature
 
436
:
1157
1160
.
Bérard
A
Rimet
F
Capowiez
Y
&
Leboulanger
C
(
2004
)
Procedures for determining the pesticide sensitivity of indigenous soil algae – a possible bioindicator of soil contamination?
Arch Environ Contam Toxicol
 
46
:
24
31
.
Bollag
JM
&
Barabasz
W
(
1979
)
Effect of heavy-metals on the denitrification process in soil
.
J Environ Qual
 
8
:
196
201
.
Botton
S
van Heusden
M
Parsons
JR
Smidt
H
&
van Straalen
N
(
2006
)
Resilience of microbial systems towards disturbances
.
Crit Rev Microbiol
 
32
:
101
112
.
Boubakri
H
Beuf
M
Simonet
P
&
Vogel
TM
(
2006
)
Development of metagenomic DNA shuffling for the construction of a xenobiotic gene
.
Gene
 
375
:
87
94
.
Brand
FS
&
Jax
K
(
2007
)
Focusing the meaning(s) of resilience: resilience as a descriptive concept and a boundary object
.
Ecol Soc
 
12
:
23
. http://www.ecologyandsociety.org/vol12/iss1/art23/.
Brandt
KK
Frandsen
RJN
Holm
PE
&
Nybroe
O
(
2010
)
Development of pollution-induced community tolerance is linked to structural and functional resilience of a soil bacterial community following a five-year field exposure to copper
.
Soil Biol Biochem
 
42
:
748
757
.
Bressan
M
Mougel
C
Dequiedt
S
Maron
PA
Lemanceau
P
&
Ranjard
L
(
2008
)
Response of soil bacterial community structure to successive perturbations of different types and intensities
.
Environ Microbiol
 
10
:
2184
2187
.
Butler
E
Whelan
MJ
Ritz
K
Sakrabani
R
&
van Egmond
R
(
2011
)
Effects of triclosan on soil microbial respiration
.
Environ Toxicol Chem
 
30
:
360
366
.
Calow
P
(
1991
)
Physiological costs of combating chemical toxicants: ecological implications
.
Comp Biochem Physiol C, Comp Pharmacol
 
100
:
3
6
.
Chaer
G
Fernandes
M
Myrold
D
&
Bottomley
P
(
2009
)
Comparative resistance and resilience of soil microbial communities and enzyme activities in adjacent native forest and agricultural soils
.
Microb Ecol
 
58
:
414
424
.
COM
(
2006
)231.
Communication from the Commission to the Council, the European Parliament, the European Economic and Social Committee and the Committee of Regions – Thematic Strategy for Soil Protection
 .
Commission of the European Communities
,
Brussels
.
Connell
JH
(
1978
)
Diversity in tropical rain forests and coral reefs
.
Science
 
199
:
1302
1310
.
Copley
SD
(
2000
)
Evolution of metabolic pathway for degradation of a toxic xenobiotic: the patchwork approach
.
Trends Biochem Sci
 
26
:
261
265
.
Correa
OS
Montecchia
MS
Berti
MF
Fernández Ferrari
MC
Pucheu
NL
Kerber
NL
&
Garcıa
AF
(
2009
)
Bacillus amyloliquefaciens BNM122, a potential microbial biocontrol agent applied on soybean seeds, causes a minor impact on rhizosphere and soil microbial communities
.
Appl Soil Ecol
 
41
:
185
194
.
Creamer
RE
Brennan
F
Fenton
O
Healy
MG
Lalor
STJ
Lanigan
GJ
Regan
JT
&
Griffiths
BS
(
2010
)
Implications of the proposed Soil Framework Directive on agricultural systems in Atlantic Europe – a review
.
Soil Use Manage
 
26
:
198
211
.
Csonka
LN
(
1989
)
Physiological and genetic responses of bacteria to osmotic stress
.
Microbiol Rev
 
53
:
121
147
.
Culman
SW
Duxbury
JM
Lauren
JG
&
Thies
JE
(
2006
)
Microbial community response to soil solarization in Nepal's rice-wheat cropping system
.
Soil Biol Biochem
 
38
:
3359
3371
.
Curtis
TP
Sloan
WT
&
Scannel
JW
(
2002
)
Estimating prokaryotic diversity and its limits
.
P Natl Acad Sci USA
 
99
:
10494
10499
.
Dang
CK
Chauvet
E
&
Gessner
MO
(
2005
)
Magnitude and variability of process rates in fungal diversity-litter decomposition relationships
.
Ecol Lett
 
8
:
1129
1137
.
De Ruiter
PC
Griffiths
BS
&
Moore
JC
(
2002
)
Biodiversity and stability in soil ecosystems: patterns, processes and the effects of disturbance
.
Biodiversity and Ecosystem Functioning. Synthesis and Perspectives
  (
Loreau
M
Naeem
S
&
Inchausti
P
, eds), pp.
102
113
.
Oxford University Press
,
Oxford
.
Debeljak
M
Kocev
D
Towers
W
Jones
M
Griffiths
BS
&
Hallett
PD
(
2009
)
Potential of multi-objective models for risk-based mapping of the resilience characteristics of soils: demonstration at a national level
.
Soil Use Manage
 
25
:
66
77
.
Degens
BP
(
1998
)
Decreases in microbial functional diversity do not result in corresponding changes in decomposition under different moisture conditions
.
Soil Biol Biochem
 
30
:
1989
2000
.
Degens
BP
Schipper
LA
Sparling
GP
&
Duncan
LC
(
2001
)
Is the microbial community in a soil with reduced catabolic diversity less resistant to stress or disturbance?
Soil Biol Biochem
 
33
:
1143
1153
.
Deng
H
Li
XF
Cheng
WD
&
Zhu
YG
(
2009
)
Resistance and resilience of Cu-polluted soil after Cu perturbation, tested by a wide range of soil microbial parameters
.
FEMS Microbiol Ecol
 
70
:
293
304
.
Deng
HA
Guo
GX
&
Zhu
YG
(
2011
)
Pyrene effects on methanotroph community and methane oxidation rate, tested by dose-response experiment and resistance and resilience experiment
.
J Soils Sediment
 
11
:
312
321
.
Devers
M
Henry
S
Hartmann
A
&
Martin-Laurent
F
(
2005
)
Horizontal gene transfer of atrazine-degrading genes (atz) from Agrobacterium tumefaciens St96-4 pADP1: Tn5 to bacteria of maize-cultivated soil
.
Pest Manag Sci
 
61
:
870
880
.
Devers
M
Azhari
NE
Kolic
NU
&
Martin-Laurent
F
(
2007
)
Detection and organization of atrazine-degrading genetic potential of seventeen bacterial isolates belonging to divergent taxa indicate a recent common origin of their catabolic functions
.
FEMS Microbiol Lett
 
273
:
78
86
.
Dunne
JA
Williams
RJ
&
Martinez
ND
(
2002
)
Network structure and biodiversity loss in food webs: robustness increases with connectance
.
Ecol Lett
 
5
:
559
567
.
Edel-Hermann
V
Brenot
S
Gautheron
N
Aimé
S
Alabouvette
C
&
Steinberg
C
(
2009
)
Ecological fitness of the biocontrol agent Fusarium oxysporum Fo47 in soil and its impact on the soil microbial communities
.
FEMS Microbiol Ecol
 
68
:
37
45
.
Fernández-Calviño
D
Arias-Estévez
M
Díaz-Raviña
M
&
Bååth
E
(
2011
)
Bacterial pollution induced community tolerance (PICT) to Cu and interactions with pH in long-term polluted vineyard soils
.
Soil Biol Biochem
 
43
:
2324
2331
.
Fierer
N
&
Schimel
JP
(
2003
)
A proposed mechanism for the pulse in carbon dioxide production commonly observed following the rapid rewetting of a dry soil
.
Soil Sci Soc Am J
 
67
:
798
805
.
Fierer
N
Schimel
JP
&
Holden
PA
(
2003
)
Influence of drying-rewetting frequency on soil bacterial community structure
.
Microb Ecol
 
45
:
63
71
.
Fließbach
A
Winkler
M
Lutz
MP
Oberholzer
HR
&
Mäder
P
(
2009
)
Soil amendment with Pseudomonas fluorescens CHA0: lasting effects on soil biological properties in soils low in microbial biomass and activity
.
Microb Ecol
 
57
:
611
623
.
Fujino
C
Wada
S
Konoike
T
Toyota
K
Suga
Y
&
Ikeda
J
(
2008
)
Effect of different organic amendments on the resistance and resilience of the organic matter decomposing ability of soil and the role of aggregated soil structure
.
Soil Sci Plant Nutr
 
54
:
534
542
.
Gans
J
Wolinsky
M
&
Dunbar
J
(
2005
)
Computational improvements reveal great bacterial diversity and high metal toxicity in soil
.
Science
 
309
:
1387
1390
.
Gao
Y
Zhong
BL
Yue
H
Wu
B
&
Cao
SX
(
2011
)
A degradation threshold for irreversible loss of soil productivity: a long-term case study in China
.
J Appl Ecol
 
48
:
1145
1154
.
Gelsomino
A
&
Cacco
G
(
2006
)
Compositional shifts of bacterial groups in a solarized and amended soil as determined by denaturing gradient gel electrophoresis
.
Soil Biol Biochem
 
38
:
91
102
.
Girvan
MS
Campbell
CD
Killham
K
Prosser
JI
&
Glover
LA
(
2005
)
Bacterial diversity promotes community stability and functional resilience after perturbation
.
Environ Microbiol
 
7
:
301
313
.
Gregory
AS
Watts
CW
Whalley
WR
Kuan
HL
Griffiths
BS
Hallett
PD
&
Whitmore
AP
(
2007
)
Physical resilience of soil to field compaction and the interactions with plant growth and microbial community structure
.
Eur J Soil Sci
 
58
:
1221
1232
.
Gregory
AS
Watts
CW
Griffiths
BS
Hallett
PD
Kuan
HL
&
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
.
Griffiths
BS
Ritz
K
Bardgett
RD
et al. (
2000
)
Ecosystem response of pasture soil communities to fumigation-induced microbial diversity reductions: an examination of the biodiversity–ecosystem function relationship
.
Oikos
 
90
:
279
294
.
Griffiths
BS
Bonkowski
M
Roy
J
&
Ritz
K
(
2001a
)
Functional stability, substrate utilisation and biological indicators of soils following environmental impacts
.
Appl Soil Ecol
 
16
:
49
61
.
Griffiths
BS
Ritz
K
Wheatley
RE
Kuan
HL
Boag
B
Christensen
S
Ekelund
F
Sørensen
S
Muller
S
&
Bloem
J
(
2001b
)
An examination of the biodiversity-ecosystem function relationship in arable soil microbial communities
.
Soil Biol Biochem
 
33
:
1713
1722
.
Griffiths
BS
Kuan
HL
Ritz
K
Glover
AE
McCaig
AE
&
Fenwick
C
(
2004
)
The relationship between microbial community structure and functional stability, tested experimentally in an upland pasture soil
.
Microb Ecol
 
47
:
104
113
.
Griffiths
BS
Hallett
PD
Kuan
HL
Pitkin
Y
&
Aitken
MN
(
2005
)
Biological and physical resilience of soil amended with heavy metal-contaminated sewage sludge
.
Eur J Soil Sci
 
56
:
197
205
.
Griffiths
BS
Liu
Q
Wang
H
Zhang
B
Kuan
HL
McKenzie
BM
Hallett
PD
Neilson
R
&
Daniell
TJ
(
2008a
)
Restoration of soil physical and biological stability are not coupled in response to plants and earthworms
.
Ecol Restor
 
26
:
102
104
.
Griffiths
BS
Hallett
PD
Kuan
HL
Gregory
AS
Watts
CW
&
Whitmore
AP
(
2008b
)
Functional resilience of soil microbial communities depends on both soil structure and microbial community composition
.
Biol Fertil Soils
 
44
:
745
754
.
Gunderson
LH
Holling
CS
Pritchard
L
Jr
&
Peterson
GD
(
2002
)
Resilience of large-scale resource systems
.
Resilience and the Behaviour of Large-Scale Systems
  (
Gunderson
LH
&
Pritchard
L
Jr
, eds), pp.
3
20
. The scientific committee on problems of the environment (SCOPE) 60,
Island Press
,
Washington
.
Hamdi
S
Chevallier
T
Ben Aïssa
N
Ben Hammouda
M
Gallali
T
Chotte
JL
&
Bernoux
M
(
2011
)
Short-term temperature dependence of heterotrophic soil respiration after one-month of pre-incubation at different temperatures
.
Soil Biol Biochem
 
43
:
1752
1758
.
Heijnen
CE
&
Van Veen
JA
(
1991
)
A determination of protective microhabitats for bacteria introduced into soil
.
FEMS Microbiol Ecol
 
85
:
73
80
.
Holling
CS
(
1973
)
Resilience and stability of ecological systems
.
Annu Rev Ecol Syst
 
4
:
1
23
.
Holtan-Hartwig
L
Bechmann
M
Hoyas
TR
Linjordet
R
&
Bakken
LR
(
2002
)
Heavy metals tolerance of soil denitrifying communities: N2O dynamics
.
Soil Biol Biochem
 
34
:
1181
1190
.
Jansa
J
Mozafar
A
Anken
T
Ruh
R
Sanders
IR
&
Frossard
E
(
2002
)
Diversity and structure of AMF communities as affected by tillage in a temperate soil
.
Mycorrhiza
 ,
12
:
225
234
.
Jansa
J
Mozafar
A
Kuhn
G
Anken
T
Ruh
R
Sanders
IR
&
Frossard
E
(
2003
)
Soil tillage affects the community structure of mycorrhizal fungi in maize roots
.
Ecol Appl
 ,
13
:
1164
1176
.
Jiang
L
&
Patel
SN
(
2008
)
Community assembly in the presence of disturbance: a microcosm experiment
.
Ecology
 
89
:
1931
1940
.
Kandeler
E
Kampichler
C
&
Horak
O
(
1996
)
Influence of heavy metals on the functional diversity of soil microbial communities
.
Biol Fertil Soils
 
23
:
299
306
.
Kaufman
LH
(
1982
)
Stream aufwuchs accumulation – disturbance frequency and stress resistance and resilience
.
Oecologia
 
52
:
57
63
.
Kibblewhite
MG
Ritz
K
&
Swift
MJ
(
2008
)
Soil health in agricultural systems
.
Philos Trans R Soc Lond B Biol Sci
 
363
:
685
701
.
Könneke
M
Bernhard
AE
de la Torre
JR
Walker
CB
Waterbury
JB
&
Stahl
DA
(
2005
)
Isolation of an autotrophic ammonia-oxidizing marine archaeon
.
Nature
 
22
:
543
546
.
Kostov
O
&
Van Cleemput
O
(
2001
)
Nitrogen transformations in copper-contaminated soils and effects of lime and compost application on soil resiliency
.
Biol Fertil Soils
 
33
:
10
16
.
Kozdroj
J
Trevors
JT
&
van Elsas
JD
(
2004
)
Influence of introduced potential biocontrol agents on maize seedling growth and bacterial community structure in the rhizosphere
.
Soil Biol Biochem
 
36
:
1775
1784
.
Kuan
HL
Fenwick
C
Glover
LA
Griffiths
BS
&
Ritz
K
(
2006
)
Functional resilience of microbial communities from perturbed upland grassland soils to further persistent or transient stresses
.
Soil Biol Biochem
 
38
:
2300
2306
.
Kuan
HL
Hallett
PD
Griffiths
BS
Gregory
AS
Watts
CW
&
Whitmore
AP
(
2007
)
The biological and physical stability and resilience of a selection of Scottish soils to stresses
.
Eur J Soil Sci
 
58
:
811
821
.
Kuperman
RG
&
Carreiro
MM
(
1997
)
Soil heavy metal concentrations, microbial biomass and enzyme activities in a contaminated grassland ecosystem
.
Soil Biol Biochem
 
29
:
179
190
.
Lejon
DPH
Martins
JMF
Leveque
J
Spadini
L
Pascault
N
Landry
D
Milloux
MJ
Nowak
V
Chaussod
R
&
Ranjard
L
(
2008
)
Copper dynamics and impact on microbial communities in soils of variable organic status
.
Environ Sci Technol
 
42
:
2819
2825
.
Lejon
DPH
Pascault
N
&
Ranjard
L
(
2010
)
Differential copper impact on density, diversity and resistance of adapted culturable bacterial populations according to soil organic status
.
Eur J Soil Biol
 
46
:
168
174
.
Lekberg
Y
Schnoor
T
Kjøller
R
Gibbons
SM
Hansen
LH
Al--Soud
WA
Sørensen
SJ
&
Roendahl
S
(
2011
)
454-sequencng reveals stochastic local reassembly and high disturbance tolerance within arbuscular mycorrhizal fungal communities
.
J Ecol
 
100
:
151
160
.
Liebich
J
Schloter
M
Schäffer
A
Vereecken
H
&
Burauel
P
(
2007
)
Degradation and humification of maize straw in soil microcosms inoculated with simple and complex microbial communities
.
Eur J Soil Sci
 
58
:
141
151
.
Loreau
M
(
2004
)
Does functional redundancy exist?
Oikos
 
104
:
606
611
.
Loreau
M
(
2010
)
Linking biodiversity and ecosystems: towards a unifying ecological theory
.
Philos Trans R Soc Lond B Biol Sci
 
365
:
49
60
.
Loreau
M
Downing
A
Emmerson
M
Gonzalez
A
Hughes
J
Inchausti
P
Joshi
J
Norberg
J
&
Sala
O
(
2002
)
A new look at the relationship between diversity and stability
.
Biodiversity and Ecosystem Functioning
  (
Loreau
M
Naeem
S
&
Inchausti
P
, eds), pp.
79
91
.
Oxford University Press
,
Oxford
.
Macdonald
CA
Clark
IM
Zhao
FJ
Hirsch
PR
Singh
BK
&
McGrath
SP
(
2011
)
Long-term impacts of zinc and copper enriched sewage sludge additions on bacterial, archaeal and fungal communities in arable and grassland soils
.
Soil Biol Biochem
 
43
:
932
941
.
May
RM
(
1972
)
Will a large complex system be stable?
Nature
 
238
:
413
414
.
May
RM
(
1974
)
Stability and Complexity in Model Ecosystems
 .
Princeton Univ. Press
,
Princeton
.
McKew
BA
Taylor
JD
McGenity
TJ
&
Underwood
GJC
(
2011
)
Resistance and resilience of benthic biofilm communities from a temperate saltmarsh to desiccation and rewetting
.
ISME J
 
5
:
30
41
.
McNaughton
SJ
(
1994
)
Biodiversity and function of grazing ecosystems
.
Biodiversity and Ecosystem Function
  (
Schulze
ED
&
Mooney
HA
, eds), pp.
361
383
.
Springer-Verlag
,
London
.
Mertens
J
Ruyters
S
Springael
D
&
Smolders
E
(
2007
)
Resistance and resilience of zinc tolerant nitrifying communities is unaffected in long-term zinc contaminated soils
.
Soil Biol Biochem
 
39
:
1828
1831
.
Montoya
JM
Pimm
SL
&
Solé
RV
(
2006
)
Ecological networks and their fragility
.
Nature
 
442
:
259
264
.
Müller
AK
Westergaard
K
Christensen
S
&
Sørensen
SJ
(
2002
)
The diversity and function of soil microbial communities exposed to different disturbances
.
Microb Ecol
 
44
:
49
58
.
Munkholm
LJ
&
Schjønning
P
(
2004
)
Structural vulnerability of a sandy loam exposed to intensive tillage and traffic in wet conditions
.
Soil Tillage Res
 
79
:
79
85
.
Nielsen
UN
Ayres
E
Wall
DH
&
Bardgett
RD
(
2011
)
Soil biodiversity and carbon cycling: a review and synthesis of studies examining diversity-function relationships
.
Eur J Soil Sci
 
62
:
105
116
.
O'Neill
RV
(
1976
)
Ecosystem persistence and heterotrophic regulation
.
Ecology
 
57
:
1244
1253
.
Orwin
KH
&
Wardle
DA
(
2004
)
New indices for quantifying the resistance and resilience of soil biota to exogenous disturbances
.
Soil Biol Biochem
 
36
:
1907
1912
.
Orwin
KH
&
Wardle
DA
(
2005
)
Plant species composition effects on belowground properties and the resistance and resilience of the soil microflora to a drying disturbance
.
Plant Soil
 
278
:
205
221
.
Orwin
KH
Wardle
DA
&
Greenfield
LG
(
2006
)
Context-dependent changes in the resistance and resilience of soil microbes to an experimental disturbance for three primary plant chronosequences
.
Oikos
 
112
:
196
208
.
Pfisterer
AB
&
Schmid
B
(
2002
)
Diversity-dependent production can decrease the stability of ecosystem functioning
.
Nature
 
416
:
84
86
.
Philippot
L
Cregut
M
Chèneby
D
Bressan
M
Dequiet
S
Martin-Laurent
F
Ranjard
L
&
Lemanceau
P
(
2008
)
Effect of primary mild stresses on resilience and resistance of the nitrate reducer community to a subsequent severe stress
.
FEMS Microbiol Lett
 
285
:
51
57
.
Pimm
SL
(
1984
)
The complexity and stability of ecosystems
.
Nature
 
307
:
321
326
.
Potts
DL
Huxman
TE
Enquist
BJ
Weltzin
JF
&
Williams
DG
(
2006
)
Resilience and resistance of ecosystem functional response to a precipitation pulse in a semi-arid grassland
.
J Ecol
 
94
:
23
30
.
Ramos
JL
Duque
E
Gallegos
MT
Godoy
P
Ramos-González
MI
Rojas
A
Terán
W
&
Segura
A
(
2001
)
Mechanisms of solvent tolerance in gram-negative bacteria
.
Annu Rev Microbiol
 
56
:
743
768
.
Ramos
JL
Krell
T
Daniels
C
Segura
A
&
Duque
E
(
2009
)
Responses of Pseudomonas to small toxic molecules by a mosaic of domains
.
Curr Opin Microbiol
 
12
:
215
220
.
Romanuk
TN
Zhou
Y
Brose
U
Berlow
EL
Williams
RJ
&
Martinez
ND
(
2009
)
Predicting invasion success in complex ecological networks
.
Philos Trans R Soc Lond B Biol Sci
 
364
:
1743
1754
.
Royer-Tardif
S
Bradley
RL
&
Parsons
WFJ
(
2010
)
Evidence that plant diversity and site productivity confer stability to forest floor microbial biomass
.
Soil Biol Biochem
 
42
:
813
821
.
Rusk
JA
Hamon
RE
Stevens
DP
&
McLaughlin
MJ
(
2004
)
Adaptation of soil biological nitrification to heavy metals
.
Environ Sci Technol
 
38
:
3092
3097
.
Ruyters
S
Mertens
J
T'Seyen
I
Springael
D
&
Smolders
E
(
2010a
)
Dynamics of the nitrous oxide reducing community during adaptation to Zn stress in soil
.
Soil Biol Biochem
 
42
:
1581
1587
.
Ruyters
S
Mertens
J
Springael
D
&
Smolders
E
(
2010b
)
Stimulated activity of the soil nitrifying community accelerates community adaptation to Zn stress
.
Soil Biol Biochem
 
42
:
766
772
.
Rykiel
EJ
Jr
(
1985
)
Towards a definition of ecological disturbance
.
Aust J Ecol
 
10
:
361
365
.
Saison
C
Degrange
V
Oliver
R
Millard
P
Commeaux
C
Montange
D
&
Le Roux
X
(
2006
)
Alteration and resilience of the soil microbial community following compost amendment: effects of compost level and compost-borne microbial community
.
Environ Microbiol
 
8
:
247
257
.
Savazzini
F
Oliveira Longa
CM
&
Pertot
L
(
2009
)
Impact of the biocontrol agent Trichoderma atroviride SC1 on soil microbial communities of a vineyard in northern Italy
.
Soil Biol Biochem
 
41
:
1457
1465
.
Scheffer
M
Carpenter
S
Foley
JA
Folke
C
&
Walkerk
B
(
2001
)
Catastrophic shifts in ecosystems
.
Nature
 
413
:
591
596
.
Scheffer
M
Bascompte
J
Brock
WA
Brovkin
V
Carpenter
SR
Dakos
V
Held
H
van Nes
EH
Rietkerk
M
&
Sugihara
G
(
2009
)
Early-warning signals for critical transitions
.
Nature
 
461
:
53
59
.
Scherwinski
K
Wolf
A
&
Berg
G
(
2007
)
Assessing the risk of biological control agents on the indigenous microbial communities: Serratia plymuthica HRO-C48 and Streptomyces sp. HRO-71 as model bacteria
.
Biocontrol
 
52
:
87
112
.
Schimel
J
Balser
TC
&
Wallenstein
M
(
2007
)
Microbial stress-response physiology and its implications for ecosystem function
.
Ecology
 
88
:
1386
1394
.
Setälä
H
&
McClean
MA
(
2004
)
Decomposition rate of organic substrates in relation to the species diversity of soil saprophytic fungi
.
Oecologia
 
139
:
98
107
.
Seybold
CA
Herrick
JE
&
Brejda
JJ
(
1999
)
Soil resilience: a fundamental component of soil quality
.
Soil Sci
 
164
:
224
234
.
Smalla
K
&
Sobecky
PA
(
2002
)
The prevalence and diversity of mobile genetic elements in bacterial communities of different environmental habitats: insights gained from different methodological approaches
.
FEMS Microbiol Ecol
 
42
:
165
175
.
Sobecky
PA
&
Coombs
JM
(
2009
)
Horizontal gene transfer in metal and radionuclide contaminated soils
.
Methods Mol Biol
 
532
:
455
472
.
Solé
RV
&
Montoya
JM
(
2001
)
Complexity and fragility in ecological networks
.
Proc R Soc Lond B
 
268
:
2039
2045
.
Sousa
WP
(
1980
)
The responses of a community to disturbance: the importance of successional age and species life history strategies
.
Oecologia
 
45
:
72
81
.
Springael
D
&
Top
E
(
2004
)
Horizontal gene transfer and microbial adaptation to xenobiotics: new types of mobile genetic elements and lessons from ecological studies
.
Trends Microbiol
 
12
:
53
58
.
Stark
JM
&
Firestone
MK
(
1995
)
Mechanisms for soil moisture effects on activity of nitrifying bacteria
.
Appl Environ Microbiol
 
61
:
218
221
.
Steenwerth
JL
Jackson
LE
Calderón
FJ
Scow
KM
&
Rolston
DE
(
2005
)
Response of microbial community composition and activity in agricultural and grassland soils after a simulated rainfall
.
Soil Biol Biochem
 
37
:
2249
2262
.
Stouffer
DB
&
Bascompte
J
(
2011
)
Compartmentalization increases food-web persistence
.
P Natl Acad Sci USA
 
108
:
3648
3652
.
Stres
B
Philippot
L
Faganeli
J
&
Tiedje
JM
(
2010
)
Frequent freeze-thaw cycles yield diminished yet resistant and responsive microbial communities in two temperate soils: a laboratory experiment
.
FEMS Microbiol Ecol
 
74
:
323
335
.
Sutherland
WJ
Armstrong-Brown
S
Armsworth
PR
et al. (
2006
)
The identification of 100 ecological questions of high policy relevance in the UK
.
J Appl Ecol
 
43
:
617
627
.
Thébault
E
&
Fontaine
C
(
2010
)
Stability of ecological communities and the architecture of mutualistic and trophic networks
.
Science
 
329
:
853
856
.
Throback
IN
Johansson
M
Rosenquis
M
Pell
M
Hansson
M
&
Hallin
S
(
2007
)
Silver (Ag+) reduces denitrification and induces enrichment of novel nirK genotypes in soil
.
FEMS Microbiol Lett
 
270
:
189
194
.
Tobor-Kaplon
MA
Bloem
J
Romkens
PFAM
&
De Ruiter
PC
(
2005
)
Functional stability of microbial communities in contaminated soils
.
Oikos
 
111
:
119
129
.
Tobor-Kaplon
MA
Bloem
J
Romkens
PFAM
&
De Ruiter
PC
(
2006a
)
Functional stability of microbial communities in contaminated soils near a zinc smelter (Budel, The Netherlands)
.
Ecotoxicology
 
15
:
187
197
.
Tobor-Kaplon
MA
Bloem
J
&
de Ruiter
PC
(
2006b
)
Functional stability of microbial communities from long-term stressed soils to additional disturbance
.
Environ Toxicol Chem
 
25
:
1993
1999
.
Udiković-Kolić
N
Devers-Lamrani
M
Petrić
I
Hršak
D
&
Martin-Laurent
F
(
2011
)
Evidence for taxonomic and functional drift of an atrazine-degrading culture in response to high atrazine input
.
Appl Microbiol Biotechnol
 
90
:
1547
1554
.
Urcelay
C
Diaz
S
Gurvich
DE
Chapin
FS
III
Cuevas
E
&
Domínguez
LS
(
2009
)
Mycorrhizal community resil in response to experimental plant functional type removals in a woody ecosystem
.
J Ecol
 
97
:
1291
1301
.
van der Wurff
AWG
Kools
SAE
Boivin
MEY
van den Brink
PJ
van Megen
HHM
Riksen
JAG
Doroszuk
A
&
Kammenga
JE
(
2007
)
Type of disturbance and ecological history determine structural stability
.
Ecol Appl
 
17
:
190
202
.
Van Nes
EH
&
Scheffer
M
(
2007
)
Slow recovery from perturbations as a generic indicator of a nearby catastrophic shift
.
Am Nat
 
169
:
738
747
.
Van Overbeck
LS
Eberl
L
Givskov
M
Molin
S
&
Van Elsas
JD
(
1995
)
Survival of, and induced stress resistance in, carbon-starved Pseudomonas fluorescens cells residing in soil
.
Appl Environ Microbiol
 
61
:
4202
4208
.
Velasco
AGV
Probanza
A
Mañero
FJG
Treviño
AC
Moreno
JM
&
Garcia
JAL
(
2009
)
Effect of fire and retardant on soil microbial activity and functional diversity in a Mediterranean pasture
.
Geoderma
 
153
:
186
193
.
Ventura
M
Canchaya
C
Zhang
Z
Bernini
V
Fitzgerald
GF
&
van Sinderen
D
(
2006
)
How highG+C Gram-positive bacteria and in particular bifidobacteria cope with heat stress: protein players and regulators
.
FEMS Microbiol Rev
 
30
:
734
759
.
Veraart
AJ
Faassen
EJ
Dakos
V
van Nes
EH
Lürling
M
&
Scheffer
M
(
2011
)
Recovery rates reflect distance to a tipping point in a living system
.
Nature
 
481
:
357
359
.
Wakelin
SA
Chu
GX
Broos
K
Clarke
KR
Liang
YC
&
McLaughlin
MJ
(
2010a
)
Structural and functional response of soil microbiota to addition of plant substrate are moderated by soil Cu levels
.
Biol Fertil Soils
 
46
:
333
342
.
Wakelin
SA
Chu
GX
Lardner
R
Liang
YC
&
McLaughlin
MJ
(
2010b
)
A single application of Cu to field soil has long-term effects on bacterial community structure, diversity, and soil processes
.
Pedobiologia
 
53
:
149
158
.
Wardle
DA
(
1995
)
Impacts of disturbance on detritus food webs in agro-ecosystems of contrasting tillage and weed management practices
.
Adv Ecol Res
 
26
:
105
185
.
Wenderoth
DF
&
Reber
HH
(
1999
)
Correlation between structural diversity and catabolic versatility of metal-affected prototrophic bacteria in soil
.
Soil Biol Biochem
 
31
:
345
352
.
Wertz
S
Degrange
V
Prosser
JI
Poly
F
&
Le Roux
X
(
2007
)
Decline of soil microbial diversity does not influence the resistance and resilience of key soil microbial functional groups following a model disturbance
.
Environ Microbiol
 
9
:
2211
2219
.
Westergaard
K
Müller
AK
Christensen
S
Bloem
J
&
Sørensen
SJ
(
2001
)
Effects of tylosin as a disturbance on the soil microbial community
.
Soil Biol Biochem
 
33
:
2061
2071
.
Wittebolle
L
Marzorati
M
Clement
L
Ballo
A
Daffonchio
D
Heylen
K
De Vos
P
Verstraete
W
&
Boon
N
(
2009
)
Initial community evenness favours functionality under selective stress
.
Nature
 
458
:
623
626
.
Witter
E
Gong
P
Bååth
E
&
Marstorp
H
(
2000
)
A study of the structure and metal tolerance of the soil microbial community six years after cessation of sewage sludge applications
.
Environ Toxicol Chem
 
19
:
1983
1991
.
Zhang
B
Horn
R
&
Hallett
PD
(
2005
)
Mechanical resilience of degraded soil amended with organic matter
.
Soil Sci Soc Am J
 
69
:
864
871
.
Zhang
B
Deng
H
Wang
H
Yin
R
Hallett
PD
Griffiths
BS
&
Daniell
TJ
(
2010
)
Does microbial habitat or community structure drive the functional stability of microbes to stresses following re-vegetation of a severely degraded soil?
Soil Biol Biochem
 
42
:
850
859
.
Editor: Eva Top