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Global Change Biology (2012) 18, 2111–2125, doi: 10.1111/j.1365-2486.2012.02667.x REVIEW Climate change and multitrophic interactions in soil: the primacy of plants and functional domains S U K U M A R C H A K R A B O R T Y * , I R E N E O B . P A N G G A † and M A R G A R E T M . R O P E R ‡ *CSIRO Plant Industry, Queensland Bioscience Precinct, 306 Carmody Road, St. Lucia, Queensland 4067, Australia, †Crop Protection Cluster, College of Agriculture, University of the Philippines Los Baños, College, Laguna 4031, Philippines, ‡CSIRO Plant Industry, Underwood Avenue, Floreat, Western Australia 6014, Australia Abstract Soil multitrophic interactions transfer energy from plants as the predominant primary producer to communities of organisms that occupy different positions in the food chain and are linked by multiple ecological networks, which is the soil food web. Soil food web sequesters carbon, cycles nutrients, maintains soil health to suppress pathogens, helps plants tolerate abiotic and biotic stress, and maintains ecosystem resilience and sustainability. Understanding the influence of climate change on soil multitrophic interactions is necessary to maintain these essential ecosystem services. But summarising this influence is a daunting task due to a paucity of knowledge and a lack of clarity on the ecological networks that constitute these interactions. The scant literature is fragmented along disciplinary lines, often reporting inconsistent findings that are context and scale-dependent. We argue for the differentiation of soil multitrophic interactions along functional and spatial domains to capture cross-disciplinary knowledge and mechanistically link all ecological networks to reproduce full functionalities of the soil food web. Distinct from litter mediated interactions in detritosphere or elsewhere in the soil, the proposed ‘pathogen suppression’ and ‘stress tolerance’ interactions operate in the rhizosphere. A review of the literature suggests that climate change will influence the relative importance, frequency and composition of functional groups, their trophic interactions and processes controlling these interactions. Specific climate change factors generally have a beneficial influence on pathogen suppression and stress tolerance, but findings on the overall soil food web are inconsistent due to a high level of uncertainty. In addition to an overall improvement in the understanding of soil multitrophic interactions using empirical and modelling approaches, we recommend linking biodiversity to function, understanding influence of combinations of climatic factors on multitrophic interactions and the evolutionary ecology of multitrophic interactions in a changing climate as areas that deserve most attention. Keywords: biological control, carbon sequestration, endophyte, mycorrhiza, plant growth promotion, rhizosphere, soil borne plant pathogens, soil food web, soil health, suppressive soil Received 9 January 2012; revised version received 6 February 2012 and accepted 10 February 2012 Introduction Soil multitrophic interactions involve plants, herbivores, predators, endophytes, pathogens, decomposers and other functional groups that occupy different positions in the food chain and perform vital functions to deliver ecosystem services that support life and cultural services not associated with material benefits [United Nation’s Millennium Ecosystem Assessments, (MEA, 2005)]. As the dominant primary producer in terrestrial and soil ecosystems, plants are the main source of food for all organisms at higher trophic levels, such as herbivores at level 2, predators at levels 3 and beyond. Soil multitrophic interactions mediate > 80% of processes to Correspondence: Sukumar Chakraborty, tel. + 617 3214 2677, fax + 617 3214 2900, e-mail: [email protected] © 2012 Blackwell Publishing Ltd sequester carbon, decompose organic matter, cycle nutrients, maintain soil fabric and structure and regulate the population of pest and pathogens (Barrios, 2007; Kabouw et al., 2011). Therefore, it is essential to determine whether climate change will adversely influence multitrophic interactions to affect ecosystem services. The estimated number of species in soil is 100 000 for protozoa; 500 000 for nematodes; 7000 for earthworms; and a significant proportion of the 1.5 million fungal species (Susilo et al., 2004; Coleman & Whitman, 2005). The number of bacterial species range between 6000 and 50 000 (Van Der Heijden et al., 2008). With 55–98% of the total biodiversity on Earth (Beed et al., 2011), few other ecosystems can match the size, complexity or the biodiversity of the soil biota. The complex interactions involving this biodiversity (McCann, 2007) in a heterogeneous 2111 2112 S . C H A K R A B O R T Y et al. soil environment (Wolfe & Klironomos, 2005; Wardle, 2006) makes soil multitrophic interactions scale-dependent (Van Der Putten et al., 2004) and difficult to understand (Van Der Putten et al., 2001; Pritchard, 2011). This is reflected in the limited literature on soil multitrophic interactions (De Román et al., 2011; Johnson et al., 2011; Van Dam & Heil, 2011). The complexity also obscures understanding of essential processes such as the temperature sensitivity of soil carbon decomposition and feedbacks to climate change, despite much research (Davidson & Janssens, 2006; Conant et al., 2011). While Earth’s climate has always changed over time, since the industrial revolution, human-induced CO2 emission has risen from 280 mg kg 1 in 1750 to 379 mg kg 1 in 2005. The radiative forcing due to greenhouse gas emissions has increased global surface temperatures by 0.74 °C over the past century and this is projected to continue by between 0.15 and 0.3 °C per decade, depending on the emission scenario (IPCC, 2007). Recent observations indicate that between 2000 and 2007 emissions have risen by 3.4% per year, exceeding almost all projections from the Intergovernmental Panel on Climate Change (Raupach & Canadell, 2010). Rising sea levels, shrinking glaciers and increased rainfall in the middle and high latitudes of the Northern Hemisphere but a decrease over the subtropics are among other projected changes. Heat waves and heavy precipitation may become more frequent and tropical cyclones may be more intense in the 21st century (IPCC, 2007). Historically, reduced agricultural production under cooling has caused price inflation, famine and war, reducing human populations (Zhang et al., 2007). The ‘fertilization effect’ of rising CO2 concentration can increase crop biomass and grain yield (Ainsworth & Long, 2005), potentially increasing food production. But yield increases are moderated by interactions, including multitrophic interactions controlling water and nutrient availability, and pest and disease outbreaks. These and other biophysical elements will combine with social and economic factors to determine food security under future climates (Chakraborty & Newton, 2011). For individual species, rising CO2 and temperature will modify its biology and shift its geographical range, and some will face extinction if these rises continue beyond their tolerance limit. But influences on individual species cannot be used to project influences on multitrophic interactions, which involve many species/ functional groups linked by networks of ecological interactions that operate simultaneously (Olff et al., 2009). With more than one species carrying out the same function, there is redundancy. This richness of species that underpins soil resilience (Wakelin et al., 2010), also contributes to the variability inherent in most studies on multitrophic interactions. Despite proposed frameworks for community interactions (Hassall et al., 2006; Gilman et al., 2010) very little published works have considered the influence of climate change on soil multitrophic interactions. Reviews have mostly covered some theoretical (Newman, 2007) and empirical aspects (Van Der Putten et al., 2004; Blankinship & Hungate, 2007; Brussaard et al., 2007; Pritchard, 2011) of climate change and multitrophic interactions. This review argues for a clear differentiation of multitrophic interaction networks that comprise the ‘amorphous’ soil food web and a renewed focus on the primacy of plants as the mediator of climate change impacts on soil multitrophic interactions. We recognise and describe two distinct spatial and functional domains under ‘stress tolerance’ and ‘pathogen suppression’ as components of soil food web. We briefly review recent literature on the influence of climate change on these multitrophic interaction networks to synthesise cross-disciplinary knowledge. We recommend four major lines of enquiry to help guide future research. The review aspires to stimulate debate and discussion rather than offer an exhaustive review of literature on the potential influence of climate change on soil multitrophic interactions. Multitrophic interactions in soil: the need for clear differentiation of multitrophic interaction networks Microbial activity does not occur uniformly throughout the soil but in ‘hot spots’ of specialised ecological niches like the rhizosphere and detritosphere (environment surrounding decomposing litter), and physical, chemical and biological heterogeneity support and maintain these niches. Functional dynamics of biological processes can be better understood by focusing on ‘hot spots’ (Blackwood & Paul, 2003; Wakelin et al., 2010). The literature mostly ignores the networks of ecological interactions comprising soil food web that operate simultaneously to perform specific functions. Classifying soil food web according to energy channels (Moore et al., 1988; Holtkamp et al., 2008), trophic controls (Scherber et al., 2010) or size-based templates (Olff et al., 2009) have not improved understanding. On the other hand, disciplinary research in ecology, soil microbiology, plant pathology, and others, offers understanding of specific aspects of soil multitrophic interactions but overlooks important processes and mechanisms that operate at different scales. Food webs are more than the sum of their trophic elements (Cohen et al., 2009) and the failure of mathematical models to predict climate change impacts on soil food web (Smith et al., 1998) is a reflection of knowledge gaps. This has © 2012 Blackwell Publishing Ltd, Global Change Biology, 18, 2111–2125 C L I M A T E C H A N G E I N F L U E N C E O N S O I L F O O D W E B 2113 prompted calls for an integration of disciplinary knowledge (Van Der Putten et al., 2004; Shennan, 2008). Plants directly or indirectly control and mediate all soil multitrophic interactions. Root exudates, sloughed off root tissue and rhizodeposition attract bacteria, fungi and nematodes as pathogens or parasites of live roots. As plants die, canopy and root litter continue to supply nutrients to these and other microbes operating as saprophytes and other functional groups. Plants determine the composition of fungal and bacterial communities in the rhizosphere through the production of specific flavonoids in root exudates (Straney et al., 2002). Other specific chemical signals control associations between plant roots and mycorrhizae (Shefferson et al., 2007), and pathogens and plant growth promoting organisms (Haas & Defago, 2005). Glucosinolate produced by cruciferous plants decomposes in soil into compounds that act as a fumigant against soil-borne pathogens (Gimsing & Kirkegaard, 2009) and other microbes such as nitrifying bacteria (Brown & Morra, 2009). The role of overall biodiversity in soil multitrophic interactions is not well understood. This is unlike in terrestrial multitrophic interactions where a loss of biodiversity affects the delivery of ecosystem services (Hooper et al., 2005; Cardinale et al., 2006; Scherber et al., 2010). This poor understanding is largely because only 0.1% of soil fungi and bacteria have been cultured and assigned clear metabolic roles (Barrios, 2007). The difficulty of linking biodiversity to function persists despite the use of metagenomics (Elsas et al., 2008) and other molecular tools to expand our knowledge of biodiversity (Beed et al., 2011) and the functional potential of species or communities (Phillips et al., 2003; MonteroBarrientos et al., 2010). Although increased activity of more diverse soil food web points to the importance of biodiversity in soil multitrophic interactions (Krumins et al., 2006), the effect of species richness decreases with trophic distance (Scherber et al., 2010) and biodiversity may have a different role at each trophic level. There is some evidence that microbial diversity per se is not necessary at least for soil carbon sequestration (King, 2011). Carbon is sequestered in soil aggregates (Blanco-Canqui & Lal, 2004) and Arbuscular mycorrhizae (AM) (Bedini et al., 2009), saprophytic fungi and bacteria contribute to the formation and stabilization of soil aggregates (Gupta, 2011). Differences in community composition do not explain differences in organic matter content of soils (Kim et al., 2007). In this review we recognise two distinct spatial and functional domains under ‘stress tolerance’ and ‘pathogen suppression’ as components of soil food web (Fig. 1) to help improve understanding of the constituent multitrophic interactions and to reinforce the primacy of plants as the driver of multitrophic interactions © 2012 Blackwell Publishing Ltd, Global Change Biology, 18, 2111–2125 (Scherber et al., 2010; Johnson et al., 2011). Multitrophic interactions involved in pathogen suppression operate in the rhizosphere where bacteria, fungi, nematodes, protozoa and possibly other microbes perform specific functions to help suppress infection and colonisation of plant roots by pathogenic microbes. Multitrophic interactions that impart stress tolerance to plants also operate in the rhizosphere and involve mycorrhizae, endophytic fungi, bacteria and viruses. This distinction is not to detract from the important role of soil food web or its network of multitrophic interactions but to propose a framework to help synthesise cross-disciplinary knowledge. All trophic processes including parasitism, predation, competition and mutualism are essential elements of the overall soil food web (Susilo et al., 2004; Lambers et al., 2009), but only specific combinations of microbes and trophic processes deliver stress tolerance or pathogen suppression. Also, the same group of organisms can participate in different multitrophic interaction networks. Necrotrophic fungi, for instance, use enzymes and other chemicals to decompose organic matter but use a very different set of virulence factors to invade living plant tissue as a pathogen. Soil food web Soil food web is the network for the transfer of energy among and between communities of organisms living all or part of their lives in the soil ecosystem (Barrios, 2007; Blankinship & Hungate, 2007). In its simplest form, soil food web shows ‘connectivity’ between various species, groups or feeders; while food webs showing the ‘transfer of energy’ between organisms at various trophic levels are at the next level of complexity; and webs showing per capita ‘interaction strengths’ between organisms are among the most detailed to offer functional insights. However, there is a lack of integration of horizontal and vertical complexity and biodiversity within and between trophic levels, respectively, and their interactions (Duffy et al., 2007). Consequently, knowledge of soil food web is fragmented. Models incorporating elements of belowground interactions suffer from deficiencies and are not often validated using independent data (Matthews et al., 2004). Energy flows from primary producers to higher trophic levels via one of three basic channels, (a) bacterial channel of saprophytic and pathogenic bacteria and their consumers; (b) fungal channel of saprophytic, mycorrhizal and pathogenic fungi; and (c) the root energy channel of herbivores, nematodes, bacteria, micro-arthropods and their consumers (Moore et al., 1988; Holtkamp et al., 2008). However, food webs are dynamic energy flow systems without a fixed structure over time and both bacterial and fungal energy channels 2114 S . C H A K R A B O R T Y et al. Climate and atmospheric composiƟon MulƟtrophic interacƟonmediated feedback to global climate Plant-mediated influence of climate change Above-below ground interacƟons LiƩer Root feeding Protozoa Endophyte mutualism Grazing resistance DETRITOSPHERE Nematode predaƟon ISR elicitaƟon Bacteria Growth promoƟon AnƟbiosis compeƟƟon symbiosis Mycorrhiza RHIZOSPHERE Stress tolerance DecomposiƟon Fungi Pathogen suppression Arthropods Grazing MineralisaƟon pathogenicity Soil food web DRILOSPHERE Earthworms Fig. 1 A conceptual diagram of plant-mediated influences of climate change on soil food web and feedback to global climate showing important niches (in capital), and processes and mechanisms (in italics) involved in the network of multitrophic interactions between plants as the primary producer and soil organisms in the overall soil food web and its two constituent multitrophic interactions involved in pathogen suppression and stress tolerance (delineated by dotted line). Arrows with solid lines represent known interactions and arrows with dashed lines represent processes and interactions that are not clearly understood. operate simultaneously in most soil food webs with temporal and spatial variation (Hassall et al., 2006). The dominance of fungal or bacterial energy channels are often determined by the quality and quantity of soil organic matter (Holtkamp et al., 2008). Soil food webs with bottom-up trophic control where biomass and energy transfers from lower to higher trophic levels (Scherber et al., 2010) are influenced by nutrient availability. Multitrophic interactions involved in pathogen suppression Soil-borne pathogens are responsible for 90% of diseases that affect major crops in the USA (Lewis & Papavizas, 1991) and together with parasitic nematodes inflict enormous loss to agriculture each year (Lumsden et al., 1995; Bird & Kaloshian, 2003). Fungal pathogens in soil are necrotrophs that derive nutrition from dead organic substrates but have the capacity to infect and kill live plant roots by producing toxins and other substances. Their broad host range and saprophytic ability allows them to sustain large populations. Plant pathogens are important in the structure and function of food webs (Borer et al., 2007; Holdo et al., 2009; Olofsson et al., 2011), but their importance extends beyond food webs. At the ecosystem level, pathogens influence the structure, composition and evolution of plant communities (Dobson & Crawley, 1994; Roy et al., 2004; Kardol et al., 2006) affecting the © 2012 Blackwell Publishing Ltd, Global Change Biology, 18, 2111–2125 C L I M A T E C H A N G E I N F L U E N C E O N S O I L F O O D W E B 2115 delivery of ecosystem services (Cheatham et al., 2009) including carbon exchange (Olofsson et al., 2011). The soil borne pathogen Phytophthora cinnamomi has altered some Australian forest communities by replacing susceptible Eucalyptus trees with resistant sedge and grass communities while another soil borne pathogen, Phellinus weirii, has been a major agent for forest disturbance in North America (Alexander, 2010). Soil health and pathogen suppressiveness are two important aspects that function due to multi-species interactions between organisms at different trophic levels (Verhage et al., 2010), but their multitrophic nature has not always been explicitly demonstrated. Soil quality and soil health are related concepts used to designate the functional and/or productive status of soil. There is considerable scientific debate about the concepts and indicators to measure soil quality and health (Van Bruggen & Semenov, 2000; Janvier et al., 2007). Using keystone species like Rhizobium, or soil dwelling nematodes and their trophic groups provide workable estimates of soil health, but methods that combine physical, chemical and biological parameters, make them cumbersome and expensive (Van Bruggen & Semenov, 2000; Pattison et al., 2008). Suppressive soils are ‘soils in which disease severity or incidence remains low, in spite of the presence of a pathogen, a susceptible host, and climatic conditions suitable for disease development’ (Baker & Cook, 1974). Soils suppressive to fungal and bacterial pathogens and nematodes have been described. Different mechanisms have been postulated to explain suppressiveness including microbial diversity and composition, population size of certain groups or species, competition for nutrients, antibiosis and predation by amoebae (Chakraborty et al., 1983). Pseudomonas, Lysobacter and other bacteria and nonpathogenic Fusarium and Trichoderma species are implicated in the suppression of fungal pathogens including Gaeumannomyces graminis var. tritici, Pythium ultimum and Thielaviopsis basicola (Haas & Defago, 2005; Borneman & Becker, 2007; Postma et al., 2010). Antibiosis, induced systemic resistance (ISR) and specific pathogen-antagonist interactions are three modes of action involved in pathogen suppression by bacteria (Haas & Defago, 2005). Strains of the fungus, Trichoderma harzianum commonly found among rhizosphere organisms also trigger ISR (Shoresh et al., 2010). ISR makes plants more resistant to necrotrophic fungal pathogens, some viruses and insects, and it extends to all parts of a plant. Some Actinobacteria form endophytic relationships to protect roots from infection by several fungal pathogens (Franco et al., 2007). The protection of host roots by ISR and antibiotic production also promotes plant emergence and growth. © 2012 Blackwell Publishing Ltd, Global Change Biology, 18, 2111–2125 These changes in plant composition and signalling pathways link soil microbe – plant interactions to aboveground trophic processes such as herbivory (Pineda et al., 2010). Other changes such as pathogeninduced mycotoxin in cereals makes straw attractive to earthworms and leads to its rapid decomposition (Wolfarth et al., 2011). Multitrophic interactions involved in stress tolerance Mutualism by mycorrhizae and endophytes confers benefits such as nutrient acquisition and stress tolerance to their plant hosts (Frey-Klett et al., 2007). Mycorrhizae mediate plant nutrient foraging, carbon allocation and root architecture, changes in soil structure and soil carbon storage (Staddon et al., 2002), and shift plant communities by suppressing non-mycorrhizal species (Cameron, 2010; Klironomos et al., 2011). Ectomycorrhizal fungi (EM) proliferate outside the root and form a sheath around the root as a physical barrier to protect against pathogens by antibiosis and by inducing fungistatic compounds (Duchesne, 1994). AM form arbuscules as sites of energy transfer between the host and fungus, and vesicles or hyphal swellings as storage organs (Rillig, 2007). AM enhance nutrient uptake by the plant, prevent root infection by pathogens and stimulate plant defence by lignification (Azcón-Aguilar & Barea, 1997). AM increase host plant fitness by modulating multitrophic interactions (Hoffmann et al., 2011). An example of multitrophic interactions involving AM and EM is their association with members of Pseudomonas, Bacillus, Klebsiella and Streptomyces as mycorrhiza helper bacteria (Frey-Klett et al., 2007). This association makes the mycorrhizal symbiont more effective in mobilising soil nutrients, fixation of atmospheric nitrogen and the protection of roots against soil borne pathogens. Endophytic fungi reside entirely within plant tissues and emerge to sporulate at plant senescence (Bacon et al., 1991). This association, ranging from mutualistic to parasitic, can confer tolerance to environmental stress such as heat and water stress (Rodriguez et al., 2009). Endophytes enhance survival and primary production of host plants (Newsham, 2011), prompting suggestions for their use for climate change mitigation (Redman et al., 2011). Many endophytes produce alkaloids and other secondary fungal metabolites that offer resistance to intense grazing from animals, insect herbivores and pathogens (Pineda et al., 2010). A typical example of multitrophic interaction involving an endophyte is the symbiosis between a virus-infected Curvularia protuberata and its grass host Dichanthelium lanuginosum (Márquez et al., 2007). Neither the fungus nor its host 2116 S . C H A K R A B O R T Y et al. plant can grow in geothermal soils above 38 °C, but when the fungus is infected by a virus, the plant can grow at soil temperatures of 50 °C. This thermotolerance allows the plant to thrive in soils where annual temperatures fluctuate between 20 and 50 °C. Climate change influence on soil multitrophic interactions Recent reviews have dealt with climate change influence on some aspects of soil food web such as, beneficial and harmful organisms (Compant et al., 2010; Pritchard, 2011), genetic resources of soil micro-organisms (Beed et al., 2011), soil community response to warming and precipitation (Briones et al., 2009; Hawkes et al., 2011), rhizosphere microbial community response to rising atmospheric CO2 (Drigo et al., 2008), and climate change influence on mycorrhizae (Nannipieri, 2011) and plant pathogens (Chakraborty & Newton, 2011). With only a single review dealing with soil food web (Blankinship & Hungate, 2007), a comprehensive analysis of climate change impact on soil multitrophic interactions has been lacking. Influences will be mediated through qualitative changes in plant Climate change influence on soil organisms and their multitrophic interactions will be mostly plant mediated (Johnson et al., 2011). Qualitative changes in physiology, tissue composition and signalling pathways under rising CO2 may influence soil multitrophic interactions. As CO2 levels in soil pores often exceed projected future atmospheric concentrations by several fold (Flechard et al., 2007), CO2 may not directly influence multitrophic interactions. Plants with increased root growth and root to shoot ratio at elevated CO2 will modify root architecture, exudation of labile compounds in the rhizosphere and root turnover rate (Pritchard, 2011) to influence plant-pathogen and plantmycorrhiza interactions (Melloy et al., 2010; Eastburn et al., 2011; Pickles et al., 2012). Unlike CO2, warming will directly influence multitrophic interactions if rises in soil temperature exceed the buffering capacity of soils. Indirect influences of temperature will be mediated through changes in the quality, quantity, species composition and structure of plant communities. Of particular interest are the large number of plant genes and gene networks and some hormones that are regulated in a coordinated manner in response to infection by fungal pathogens, cold or drought stress (Singh et al., 2002; Eastburn et al., 2011) and insect herbivory (Verhage et al., 2010), albeit with different signalling pathways (Ramı́rez et al., 2009). Table 1 lists some examples of changes to the structure, composition and signalling pathways of plants under climate change and their influence on plant-microbe interactions from a multitrophic interactions perspective. This list is neither exhaustive nor definitive, as plants can respond in a different way to heat and drought stress when applied together compared with each stress being applied separately (Rizhsky et al., 2002). A comprehensive list of host-pathogen changes in response to elevated CO2 and O3 has recently been published (Eastburn et al., 2011). Root maintenance respiration increases with rising soil temperature, increasing root turnover and reducing root longevity (Pritchard, 2011). Root production and turnover increases with raised soil water content, leading to increased root surface area for microbial colonization and herbivory (Gill & Jackson, 2000). The composition, diversity and productivity of plant communities change with changing precipitation pattern to influence belowground interactions (Suttle et al., 2007) including those involving mycorrhizae and pathogens. Geographical distribution of plants will change with changing temperature and precipitation. One estimate projects a 51% reduction in the 32 million hectares of highly productive area under wheat, covering northwestern Mexico, the Indo-Gangetic plains and the Nile valley (Ortiz et al., 2008). Changed distribution will cause habitat fragmentation and expose plant communities to new stresses if soils and other conditions are unsuitable in areas with suitable climate. The poleward shift of plant species and changes in species assemblages due to warming of about 3 °C can be more important for soil organisms than the direct effects of warming (Wardle, 2002). At least in the short-term there will be an uncoupling of above and belowground multitrophic interactions, and new networks may evolve (Van Der Putten et al., 2010). Climate change influence on soil food web Increased abundance and altered quality of plant litter at elevated CO2 will influence microbial decomposition of litter and the release of nutrients. In general, decreased nitrogen concentration and increased carbohydrate and phenolics increase the carbon/nitrogen ratio of plant litter at high CO2. While some studies show a delayed degradation of plant litter produced at high CO2 (Ulainen et al., 2003), a meta-analysis failed to show any overall delay in litter degradation (Norby et al., 2001). However, as most studies have used soil respiration as an indicator of microbial activity, the influence of altered litter quality on the structure and function of soil communities and their subsequent influence on soil food web remains unclear. Herbivores © 2012 Blackwell Publishing Ltd, Global Change Biology, 18, 2111–2125 Element of climate change Drought Drought Drought Elevated CO2 Elevated CO2 Elevated CO2 Elevated CO2 Elevated CO2 Elevated CO2 Elevated CO2 Plant Arabidopsis thaliana Arabidopsis thaliana Hordeum vulgare and others Brassicaceae family Acer rubrum © 2012 Blackwell Publishing Ltd, Global Change Biology, 18, 2111–2125 Nicotiana tabacum Glycine max Solidago rigida Hordium vulgare Several species ↑Glucosinolate ↓Stomatal conductance ↑Phenolics & tannins ↑Plant defence against pathogen ↓Leaf nicotine ↑Phytoalexin Glyceollin in resistant plants ↑Plant defence against pathogen ↓Nitrogen concentration ↑Net photosynthesis ↑Papillae production ↑Silicon accumulation ↓Nitrogen concentration ↑Phenolics Induced resistance to pathogens ↑Abscisic acid ↑Stomatal closure ↑Abscisic acid ↑Methyl jasmonate ↓Shoot and root biomass ↑Shoot N Potentially delayed litter degradation Increased resistance to potato virus Y Potentially increased resistance to fungal pathogen Phytophthora sojae from ß-glucan elicitor Reduced fungal leaf spot by Cercospora and Septoria Reduced fungal penetration by Blumeria graminis Reduced disease incidence by fungal pathogen Botrytis cinerea Reduced effect of drought by earthworm Aporrectodea caliginosa Reduced aphid abundance Increased number of parasitoid Reduced soil microbial population Reduced foliar disease incidence by fungal pathogen Phyllosticta minima Influence relating to multitrophic interactions Change(s) in plant response (Lindroth, 2010) (Strengbom & Reich, 2006) (Hibberd et al., 1996) (Matros et al., 2006) (Braga et al., 2006) (Schonhof et al., 2007) (McElrone et al., 2005) (Johnson et al., 2011) (Ramı́rez et al., 2009) (Jakab et al., 2005) Reference Table 1 Selected examples of changes in plant form and function under elements of climate change with demonstrated/potential effect on microorganisms involved in multitrophic interactions in soil, with arrows indicating an increase (↑) or decrease (↓) in plant response C L I M A T E C H A N G E I N F L U E N C E O N S O I L F O O D W E B 2117 2118 S . C H A K R A B O R T Y et al. and soil invertebrates feeding on plant tissue containing high levels of secondary or structural compounds show reduced growth, development and population densities, with potential impacts on soil food web (Lindroth, 2010). Herbivory also increases due to compensatory feeding on plant tissue with reduced nutritional value (Schadler et al., 2007). A high carbon/nitrogen ratio of plant litter and the exudation of organic carbon compounds may shift soil food webs from bacteria to fungi-dominated (Drigo et al., 2007), increasing fungal abundance across different ecosystems (Janus et al., 2005; Lipson et al., 2006). Mycorrhiza and heterotrophic fungi may also be boosted by increased photosynthesis and transfer of carbon to fine roots (Bardgett et al., 2008), but this will be moderated by shifts in the composition and diversity of the vegetation. Some plants may selectively enrich certain fungi by secreting toxins in soil (Van Der Putten, 2009). Findings on bacteria are variable. Some CO2-enrichment studies show a stimulation of rhizosphere bacteria including nitrogen-fixing rhizobia and increased size and number of root nodules (Compant et al., 2010; Pritchard, 2011) and increased bacterial biomass (Drigo et al., 2008), while others show no general trend (Zak et al., 2000). Elevated CO2 can boost population size, colonisation, and/or diversity of AM and EM fungi (Compant et al., 2010). A meta-analysis of 65 field studies where mycorrhizal response to CO2 enrichment was measured for > 2 months, showed a 47% increase in growth of AM or EM (Treseder, 2004). AM association supplies all of the plant phosphorous nutrition in some crops (Smith et al., 2004). The boost in AM population could further improve the acquisition of phosphorous, nitrogen, zinc and other nutrients (Cavagnaro et al., 2011). But the benefit to mycorrhizal association from CO2 enrichment will be determined by phosphorous and nitrogen availability in soil. At the second trophic level there is no significant and consistent response of high CO2 in the majority of over 50 studies (Blankinship & Hungate, 2007). At the third trophic level, population size and/or diversity of some root feeding nematodes (Yeates & Newton, 2009) and collembolans increase with CO2-enrichment. But other studies show no change (Hungate et al., 2000), or enrichment of nematodes only under low fertility (Li et al., 2009), pointing to the complexity of these interactions. Eight out of 15 studies of the third trophic level showed increased abundance or activity, six showed no change and one showed a reduction of bacterivores and/or fungivores but individual groups such as protozoa, enchytraeid and nematodes did not show any consistent trend (Blankinship & Hungate, 2007). In one long-term study, the effect of elevated CO2 on fungal communities was transmitted to higher trophic levels and influenced the abundance and species composition of fungal feeders (Jones et al., 1998). Nevertheless, the relationships between community structure and CO2 enrichment are complicated by spatial heterogeneity and other factors (Ge et al., 2010). Soil microbial activity and mineralization are increased in warmer soils (Gill & Jackson, 2000) before acclimation reduces temperature sensitivity (Balser et al., 2006), but changes in litter quality and physiology of soil organisms at high temperatures modify these (Heinemeyer et al., 2006). Fungal populations and nematodes grazing on fungi and bacteria generally increase due to warming, while nematode diversity is reduced despite increased growth, fertility and mobility (Convey & Wynn-Williams, 2002; Blankinship & Hungate, 2007). Soil water content can modify the effect of rising temperatures. The algal-feeding Endorylaimus that prefers a moist habitat, increases under warming in preference to microbe-feeding nematodes (Simmons et al., 2009). Increasing soil temperature generally decreases soil microbial biomass in controlled experiments but long term field studies either show no effect or a positive effect (Pritchard, 2011). Decreased precipitation and repeated wetting of soils reduce both bacterial and fungal biomass but fungal dominated food webs respond more readily to changing precipitation (Hawkes et al., 2011). Altered precipitation regulates the population of microbial grazers and bacterial-feeding nematodes are more sensitive to drought than fungal feeders (Landesman et al., 2011). Drier conditions can lead to changes at higher trophic levels due to bottom-up resource limitation as soil organisms appear to be more sensitive to dry conditions than to increased precipitation. Increased precipitation generally benefits detritivores and herbivores at the second trophic level. Climate change influence on multitrophic interactions involved in pathogen suppression Increased concentration of plant phenolics (Hartley et al., 2000; Percy et al., 2002) and tannins (McElrone et al., 2005) at high CO2 directly increases the resistance of plant tissue to pathogen invasion. Phenolics are antifungal compounds with a well-established role in defence against pathogens and herbivores, and flavonoids are involved in plant-pathogen signalling (Bednarek & Schulze-Lefert, 2009). These and other changes in host plants at high CO2 may affect survival, ecological/reproductive fitness and/or the severity of diseases caused by soil borne pathogens. Increased photosynthesis and water use efficiency raise tolerance of tomato © 2012 Blackwell Publishing Ltd, Global Change Biology, 18, 2111–2125 C L I M A T E C H A N G E I N F L U E N C E O N S O I L F O O D W E B 2119 roots to Phytophthora parasitica infection (Jwa & Walling, 2001); increased b-1, 3 glucanase reduce potato leaf necrosis due to Phytophthora infestans (Plessl et al., 2007); and production of the phytoalexin glyceollin increases resistance in soybean in response to an elicitor from Phytophthora sojae (Braga et al., 2006). The concentration of Glucosinolate can increase under elevated CO2 (Schonhof et al., 2007), but how this increase impacts on pathogens, other soil microbes and their multitrophic interactions has not been addressed. Altered rhizodeposition and root exudates under elevated CO2 boost the frequency of iron-chelating Pseudomonas spp. (Tarnawski et al., 2006) and rhizosphere populations of other microbes associated with pathogen suppression. These and other rhizosphere bacteria, collectively known as plant growth promoting bacteria, stimulate plant growth by producing growth-promoting hormones, alleviating biotic and abiotic stresses and imparting ISR to plants (Hardoim et al., 2011). Populations of some plant growth promoting bacteria such as Pseudomonas and Actinobacteria are selectively enriched by certain host plants under CO2 enrichment (Compant et al., 2010). Nevertheless, the overall impact on pathogen suppression is difficult to predict due to a lack of understanding of important interacting factors. For instance, the biomass of Fusarium pseudograminearum increases per unit of plant tissue at high CO2 increasing the amount of inoculum (Melloy et al., 2010). Potentially this may balance the effects of increased populations of suppressive microbes. But this cereal pathogen has low saprophytic fitness and can be rapidly eliminated from organic matter by other microbes including fungi (Pereyra et al., 2004) and nematodes (Wolfarth et al., 2011). The resistance to Fusarium subglutinans increases in pineapple under raised temperatures (Matos et al., 2000), but the influence is species-specific (Chakraborty & Newton, 2011; Eastburn et al., 2011). High temperature reduces resistance against Phytophthora infestans in potato (Mizubuti & Fry, 1998), against Fusarium oxysporum f. sp. ciceris in chickpea (Landa et al., 2006) and against two bacterial pathogens in pepper, but resistance remains unchanged against two fungal pathogens in pepper (Shin & Yun, 2010). Crop plants now grow in areas where soil and climate are very different to their centres of origin. Often pathogens have migrated with their host, expanding their range. This trend is likely to continue with rising temperature as cropping areas shift pole-ward. Warming will expand the geographical range of Phytophthora cinnamomi (Bergot et al., 2004; Desprez-Loustau et al., 2007); increase the risk of severe Phytophthora infestans epidemics (Hannukkala et al., 2007) and the number of Meloidogyne incognita generations (Ghini et al., 2008). At © 2012 Blackwell Publishing Ltd, Global Change Biology, 18, 2111–2125 least in the short term, habitat fragmentation is likely to uncouple above and belowground multitrophic interactions, which control the biological suppression of soil borne pathogens. The literature on the effect of drought (McElrone et al., 2003; Cotty & Jaime-Garcia, 2007), flooding (Barta & Schmitthenner, 1986) and rainfall (Bowers et al., 1990) on plant pathogens show species-specific responses. A meta-analysis indicates that insect and pathogen feeding behaviour, plant parts affected and the severity of water stress are important factors that determine the impacts of changing precipitation on pathogens (Jactel et al., 2012). Realistic impact assessment requires the combined influence of changing temperature, soil moisture and CO2 on pathogen suppressiveness. As pasteurisation removes some forms of soil suppressiveness, pathogen suppression may be eliminated by small rises in soil temperature (Borneman & Becker, 2007; Bent et al., 2008). Under experimental conditions, Gaeumannomyces graminis var. tritici, survives in cool dry soils but a moist soil > 30 °C eliminates the pathogen within 3 months (Wong, 1984). However, these findings may not apply directly to field soils which are buffered from the effect of rising temperatures. Suppression of the potato common scab pathogen in cold and wet soil by volatile secondary metabolic gases from Pseudomonas, Bacillus and Streptomyces becomes ineffective in hot and dry soils (Sturz et al., 2004). Other interactions in the rhizosphere will be favoured under rising temperatures. Strains of plant growth promoting bacteria including rhizobia that grow better at high temperature will dominate under warming to alleviate temperature and drought stress (Compant et al., 2010). Plants such as sunflower growing under drought stress may select strains of Achromobacter that offer higher growth promotion under drought (Forchetti et al., 2007). Climate change influence on multitrophic interactions involved in plant stress tolerance Elevated CO2 can boost populations of mycorrhizal fungi and selectively enrich species or strains efficient at acquiring mineral nutrients (Pritchard, 2011). Increased levels of plant phenolics at high CO2 boost mycorrhizal spore germination and colonisation, and certain flavonoids boost hyphal branching in AM (Scervino et al., 2007). This may increase nutrient and water uptake, overall fitness and health of plants to potentially increase their stress tolerance. However, these benefits will depend on the dynamics of fine root turnover rate, and the equilibrium between soil mineral nutrients and carbon fixation by plants (Pritchard, 2011). 2120 S . C H A K R A B O R T Y et al. Colonisation by some endophytic fungi can increase at elevated CO2 leading to changes in biomass and chemical composition of plants, including alkaloid, protein and carbohydrate levels (Newsham, 2011). Elevated CO2 increased colonisation of Lolium arundinaceum by Neotyphodium coenophialum but decreased concentrations of ergovaline and loline alkaloids (Brosi et al., 2011). However, endophytes have failed to improve plant function at elevated CO2 in some studies (Alberton et al., 2010). Warming generally increases root colonization and hyphal length by AM but findings are varied on EM from limited studies (Compant et al., 2010). Warming increases mycorrhizal colonization by directly stimulating fungal growth and indirectly by stimulating plant growth to accelerate the rate of transfer of plant photosynthates to the symbiont (Hawkes et al., 2008). Mycorrhizal response to warming is modulated by the duration of warming (Simard & Austin, 2010), and the acclimatization of the symbiont community over time (Deslippe et al., 2011). Warming alters the structure of mycorrhizal networks (Hawkes et al., 2008; Deslippe et al., 2011). Larger EM networks under warming may explain the expansion and dominance of Betula nana in the Arctic plant community (Clemmensen et al., 2006). Drought generally reduces mycorrhizal colonisation but the response is species-specific and EM may be more severely affected than AM. This can influence the competition between AM-shrubs and EM-trees. Mycorrhizae can make its host drought tolerant by improving water uptake by roots, tolerance of lower xylem pressure, greater lateral root formation, and osmotic adjustment to avoid dehydration (Compant et al., 2010). Warming generally favours endophytic colonisation that protects the host plant from abiotic stress. The influence of elevated CO2, warming and precipitation on Lolium arundinaceum–Neotyphodium coenophialum interaction has revealed complex but interesting findings (Brosi et al., 2011). Contrary to previous studies, endophytic colonisation was not affected by warming or precipitation. Warming increased loline concentrations by 28% but had no effect on ergovaline. The two alkaloids influence two different groups of grazers with very different ecological and economic significance. Consumption of ergovaline containing plant materials causes ‘tall fescue toxicosis’ in livestock, with symptoms of poor weight gain, reduced fertility and lactation, and gangrene (Panaccione et al., 2001). Loline alkaloids, on the other hand, have insecticidal properties making their host plant tolerant to insect and nematode attack (Yule et al., 2011). By enhancing the insecticidal property of tall fescue pastures without increasing their detrimental effect on livestock grazing, climate change may have an overall beneficial effect. Conclusions and recommendations Summarising the influence of climate change on soil multitrophic interactions is a daunting task due to an overall paucity of knowledge and a lack of clarity on the ecological networks that constitute these interactions. The scant literature is fragmented along disciplinary lines, often reporting inconsistent findings that are context and scale-dependent. We have argued for the differentiation of soil multitrophic interactions along functional and spatial domains as a framework to synthesise cross-disciplinary knowledge. Distinct from litter mediated interactions in detritosphere or elsewhere in the soil, the proposed ‘pathogen suppression’ and ‘stress tolerance’ interactions operate in the rhizosphere. While partitioning soil multitrophic interactions into functional domains will improve understanding, these networks must be mechanistically linked to reproduce all functionalities of the overall soil food web. A review of the literature suggests that climate change will influence the relative importance, frequency and composition of functional groups, their trophic interactions and processes controlling these interactions. The key influences of elevated CO2 and temperature, and changed precipitation are summarised for the three networks of multitrophic interactions (Table 2). Soil microbial resources offer great promise in improving tolerance of plants to biotic and abiotic stresses (Mazzola, 2010; Pritchard, 2011), but amendments to enhance nutrient availability, disease suppressiveness or biological control of pests and pathogens often give inconsistent results (Juroszek & Von Tiedemann, 2011). Climate change will increase uncertainty by giving rise to novel interactions and by uncoupling above and belowground multitrophic interactions (Van Der Putten, 2009). Even without climate change considerations, improved understanding of soil multitrophic interactions will have definite scientific and practical benefits in managing soil biota. Improved understanding of soil multitrophic interactions is a prerequisite to predicting how a changing climate will influence these interactions to impact on the delivery of vital ecosystem services. A lack of clarity on soil multitrophic interactions has obscured important processes such as the sequestration of carbon in soil and its release from organic matter and feedback to global climate systems despite much research. There is a risk of multiplying ignorance without a clear framework and well-formulated research questions. We propose four major lines of enquiry. Improved understanding of soil multitrophic interactions Additional baseline information on specific soil multitrophic interactions has to be the foundation for any © 2012 Blackwell Publishing Ltd, Global Change Biology, 18, 2111–2125 C L I M A T E C H A N G E I N F L U E N C E O N S O I L F O O D W E B 2121 Table 2 A summary of observed and potential influence of climate change on soil multitrophic interactions (MI) Soil MI Elevated CO2 Elevated temperature and changed precipitation Soil food web Increased litter and roots with altered quality Potentially delay litter decomposition and nutrient cycling Potential fungal domination of soil food web Stimulation of N2-fixing bacteria Inconsistent findings on multitrophic interactions Increased fungal and nematode population Increased mineralisation Fungi dominated food webs respond more readily to moisture changes Drier conditions influence trophic interactions due to bottom-up resource limitation Pathogen suppression Increased resistance to fungal pathogens due to rising secondary metabolites Growth stimulation and changed mycorrhizal community Improved plant health from increased activity of plant growth promoting bacteria Pathogen suppression determined by the balance between increased pathogen inoculum and population of suppressive microbes Enhanced mycorrhizal growth Pole-ward shift of plants and their pathogens from changed climate suitability Necrotrophic pathogens becoming more damaging if plants are stressed in the new environment Uncoupling of above and below ground links due to habitat fragmentation Altered effectiveness of disease resistance genes Plant stress tolerance Boosted population and diversity of mycorrhizae and enrichment of species efficient at nutrient acquisition Boosted phosphorous and nitrogen nutrition of plants Increased stress tolerance and plant defence against herbivore and pathogen Potentially improved stress tolerance from increased alkaloid production by endophytes Improved stress tolerance from increased mycorrhizal colonisation Potentially increased biotic and abiotic stress tolerance in combination with high CO2 improved understanding. Empirical and modelling approaches will be equally important in balancing roles and links between the functional domains and multitrophic interaction networks. The lack of understanding of soil multitrophic interaction multiplies with increasing spatial and temporal scales. One approach will be to use a combination of process and organism-oriented models with the flexibility to incorporate new properties that become evident only at a higher spatial/trophic level. Linking biodiversity to function The use of molecular tools has greatly expanded knowledge of soil microbial biodiversity but its role in multitrophic interactions is yet to be addressed. A large biodiversity by itself is not enough for soil resilience. The functional potential of soil biota has to be optimally expressed under climate change and determining thresholds for important interactions between functional groups will be essential. Other characteristics that determine soil resilience and sustainability, and how these are influenced by climate change will be important to understand the buffering and inherent adaptive capacity of soils. Influence of combinations of climatic factors on multitrophic interactions Most studies have mainly dealt with the influence of single climatic factors such as elevated temperature © 2012 Blackwell Publishing Ltd, Global Change Biology, 18, 2111–2125 and/or CO2 on specific interactions at lower trophic levels over short to medium time periods. A multi-factorial approach (Singh et al., 2010) based on realistic field studies using temperature and CO2 gradients to mimic gradual climate change (Chakraborty et al., 2008) will avoid overestimation of community response to abrupt rise in CO2 (Klironomos et al., 2005). These studies are necessary to identify processes that will be significantly altered and to develop options to maintain ecosystem services. New research must also address how multitrophic interactions will cope with increased frequency and magnitude of extreme events. Evolutionary ecology of multitrophic interactions in a changing climate Soil microbial communities can rapidly adapt to elevated CO2 (Allison et al., 2010), temperature (Compant et al., 2010) and raised fecundity at high CO2 can accelerate micro-evolution (Chakraborty & Datta, 2003). But evolutionary ecology is not often considered for soil organisms (Hassall et al., 2006). Multitrophic interactions are an important driver of selection processes for organisms and functional groups to alter their ability to adapt to a changing climate, and/or new geographical range (Van Der Putten et al., 2010). New long-term research on climate change mediated evolution of microbial communities and their multitrophic interactions, with or without habitat fragmentation, will be essential. 2122 S . C H A K R A B O R T Y et al. Acknowledgements This review stems from an invited presentation by the senior author at the 6th IOBC working group meeting on multitrophic interactions in soil held in Cordoba, Spain during 4–7 April 2011. We acknowledge the numerous discussions with colleagues in forming opinions expressed in this review. Some of the findings come from research by graduate students including Peter Wilson, Femi Akinsanmi, Rhyannyn Westecott and Paul Melloy and technical assistance from Ross Perrott. Co-investment in research from the Cooperative Research Centre for National Plant Biosecurity, CSIRO Plant Industry and the Grains Research and Development Corporation is gratefully acknowledged. References Ainsworth EA, Long SP (2005) What have we learned from 15 years of free-air CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy properties and plant production to rising CO2. New Phytologist, 165, 351– 372. Alberton O, Kuyper T, Summerbell R (2010) Dark septate root endophytic fungi increase growth of Scots pine seedlings under elevated CO2 through enhanced nitrogen use efficiency. Plant and Soil, 328, 459–470. Alexander HM (2010) Disease in natural plant populations, communities, and ecosystems: insights into ecological and evolutionary processes. Plant Disease, 94, 492– 503. Allison SD, Wallenstein MD, Bradford MA (2010) Soil-carbon response to warming dependent on microbial physiology. Nature Geoscience, 3, 336–340. Azcón-Aguilar C, Barea J (1997) Arbuscular mycorrhizas and biological control of soil-borne plant pathogens – an overview of the mechanisms involved. Mycorrhiza, 6, 457–464. Bacon C, Battista JD (1991) Endophytic fungi of grasses. In: Handbook of Applied Mycology Volume 1: Soils and Plants (eds Arora DK, Rai B, Mukerji KG, Knudsen GR), pp. 231–256. Marcel Dekker, New York. Baker KF, Cook RJ (1974) Biological Control of Plant Pathogens. American Phytopathology Society, San Francisco. Balser T, Mcmahon K, Bart D et al. (2006) Bridging the gap between micro – and macro-scale perspectives on the role of microbial communities in global change ecology. Plant and Soil, 289, 59–70. Bardgett R, Freeman C, Ostle N (2008) Microbial contributions to climate change through carbon cycle feedbacks. The ISME Journal, 2, 805–814. Barrios E (2007) Soil biota, ecosystem services and land productivity. Ecological Economics, 64, 269–285. Barta A, Schmitthenner A (1986) Interaction between flooding stress and Phytophthora root rot among alfalfa cultivars. Plant Disease, 70, 310–313. Bedini S, Pellegrino E, Avio L, Pellegrini S, Bazzoffi P, Argese E, Giovannetti M (2009) Changes in soil aggregation and glomalin-related soil protein content as affected by the arbuscular mycorrhizal fungal species Glomus mosseae and Glomus intraradices. Soil Biology and Biochemistry, 41, 1491–1496. Bednarek P, Schulze-Lefert P (2009) Role of plant secondary metabolites at the hostpathogen interface. In: Annual Plant Reviews Volume 34: Molecular Aspects of Plant Disease Resistance (ed. Parker J), pp 220–260. Wiley-Blackwell. Available at: http:// au.wiley.com/WileyCDA/WileyTitle/productCd-140517532X.html (accessed 29 february 2012). Beed F, Benedetti A, Cardinali G, Chakraborty S, Dubois T, Garrett K, Halewood M (2011) Climate Change and Micro-organism Genetic Resources for Food and Agriculture: State of Knowledge, Risks and Opportunities. Commission on genetic resources for food and agriculture, FAO, Rome. Available at: http://www.fao.org/docrep/ meeting/022/mb392e.pdf (accessed 28 february 2012). Bent E, Loffredo A, Mckenry MV, Becker JO, Borneman J (2008) Detection and investigation of soil biological activity against Meloidogyne incognita. Journal of Nematology, 40, 109–118. Bergot M, Cloppet E, Rarnaudw VP, De′Que′Z M, BenoiˆT M, Ai S, Desprez-Loustau M (2004) Simulation of potential range expansion of oak disease caused by Phytophthora cinnamomi under climate change. Global Change Biology, 10, 1539–1552. Bird D, Kaloshian I (2003) Are nematodes special? Nematodes have their say. Physiological and Molecular Plant Pathology, 62, 5–123. Blackwood CB, Paul EA (2003) Eubacterial community structure and population size within the soil light fraction, rhizosphere, and heavy fraction of several agricultural systems. Soil Biology and Biochemistry, 35, 1245–1255. Blanco-Canqui H, Lal R (2004) Mechanisms of carbon sequestration in soil aggregates. Critical Reviews in Plant Sciences, 23, 481–504. Blankinship JC, Hungate BC (2007) Belowground food webs in a changing climate. In: Agroecosystems in a changing climate (eds Newton PCD, Carran RA, Edwards GR, Niklaus PA), pp. 117–150. Taylor and Francis, Boca Raton. Borer ET, Hosseini PR, Seabloom EW, Dobson AP (2007) Pathogen-induced reversal of native dominance in a grassland community. Proceedings of the National Academy of Sciences, 104, 5473–5478. Borneman J, Becker JO (2007) Identifying microorganisms involved in specific pathogen suppression in soil. Annual Review of Phytopathology, 45, 153–172. Bowers J, Sonoda R, Mitchell D (1990) Path coefficient analysis of the effect of rainfall variables on the epidemiology of Phytophthora blight of pepper caused by Phytophthora capsici. Phytopathology, 80, 1439–1446. Braga MR, Aidar MPM, Marabesi MA, De Godoy JRL (2006) Effects of elevated CO2 on the phytoalexin production of two soybean cultivars differing in the resistance to stem canker disease. Environmental and Experimental Botany, 58, 85–92. Briones MJI, Ostle NJ, Mcnamara NP, Poskitt J (2009) Functional shifts of grassland soil communities in response to soil warming. Soil Biology and Biochemistry, 41, 315–322. Brosi GB, Mcculley RL, Bush LP, Nelson JA, Classen AT, Norby RJ (2011) Effects of multiple climate change factors on the tall fescue–fungal endophyte symbiosis: infection frequency and tissue chemistry. New Phytologist, 189, 797–805. Brown PD, Morra MJ (2009) Brassicaceae tissues as inhibitors of nitrification in soil. Journal of Agricultural and Food Chemistry, 57, 7706–7711. Brussaard L, De Ruiter PC, Brown GG (2007) Soil biodiversity for agricultural sustainability. Agriculture, Ecosystems and Environment, 121, 233–244. Cameron D (2010) Arbuscular mycorrhizal fungi as (agro)ecosystem engineers. Plant and Soil, 333, 1–5. Cardinale BJ, Srivastava DS, Emmett Duffy J, Wright JP, Downing AL, Sankaran M, Jouseau C (2006) Effects of biodiversity on the functioning of trophic groups and ecosystems. Nature, 443, 989–992. Cavagnaro TR, Gleadow RM, Miller RE (2011) Plant nutrient acquisition and utilisation in a high carbon dioxide world. Functional Plant Biology, 38, 87–96. Chakraborty S, Datta S (2003) How will plant pathogens adapt to host plant resistance at elevated CO2 under a changing climate? New Phytologist, 159, 733–742. Chakraborty S, Newton AC (2011) Climate change, plant diseases and food security: an overview. Plant Pathology, 60, 2–14. Chakraborty S, Old KM, Warcup JH (1983) Amoebae from a Take-all suppressive soil which feed on Gaeumannomyces graminis tritici and other soil fungi. Soil Biology and Biochemistry, 15, 17–24. Chakraborty S, Luck J, Hollaway G et al. (2008) Impacts of global change on diseases of agricultural crops and forest trees. CAB Reviews: Perspectives in Agriculture, Veterinary Science, Nutrition and Natural Resources, 3, 1–15. Cheatham MR, Rouse MN, Esker PD et al. (2009) Beyond yield: plant disease in the context of ecosystem services. Phytopathology, 99, 1228–1236. Clemmensen K, Michelsen A, Jonasson S, Shaver G (2006) Increased ectomycorrhizal fungal abundance after long-term fertilization and warming of two arctic tundra ecosystems. New Phytologist, 171, 1–404. Cohen JE, Schittler DN, Raffaelli DG, Reuman DC (2009) Food webs are more than the sum of their tritrophic parts. Proceedings of the National Academy of Sciences, 106, 22335–22340. Coleman DC, Whitman WB (2005) Linking species richness, biodiversity and ecosystem function in soil systems. Pedobiologia, 49, 9–497. Compant S, Van Der Heijden MGA, Sessitsch A (2010) Climate change effects on beneficial plant–microorganism interactions. FEMS Microbiology Ecology, 73, 197–214. Conant RT, Ryan MG, Ågren GI et al. (2011) Temperature and soil organic matter decomposition rates – synthesis of current knowledge and a way forward. Global Change Biology, 17, 3392–3404. Convey C, Wynn-Williams D (2002) Antarctic soil nematode response to artificial climate amelioration. European Journal of Soil Biology, 38, 255–259. Cotty PJ, Jaime-Garcia R (2007) Influences of climate on aflatoxin producing fungi and aflatoxin contamination. International Journal of Food Microbiology, 119, 109– 115. Davidson EA, Janssens IA (2006) Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature, 440, 165–173. De Román M, Fernández I, Wyatt T, Sahrawy M, Heil M, Pozo MJ (2011) Elicitation of foliar resistance mechanisms transiently impairs root association with arbuscular mycorrhizal fungi. Journal of Ecology, 99, 36–45. © 2012 Blackwell Publishing Ltd, Global Change Biology, 18, 2111–2125 C L I M A T E C H A N G E I N F L U E N C E O N S O I L F O O D W E B 2123 Deslippe J, Hartmann M, Mohn W, Simard S (2011) Long-term experimental manipulation of climate alters the ectomycorrhizal community of Betula nana in Hoffmann D, Vierheilig H, Peneder S, Schausberger P (2011) Mycorrhiza modulates aboveground tri-trophic interactions to the fitness benefit of its host plant. Ecologi- Arctic tundra. Global Change Biology, 17, 1625–1636. Desprez-Loustau M-L, Robin C, Buée M et al. (2007) The fungal dimension of biological invasions. Trends in Ecology & Evolution, 22, 472–480. Dobson A, Crawley M (1994) Pathogens and the structure of plant communities. Trends in Ecology & Evolution, 9, 393–398. Drigo B, Kowalchuk G, Yergeau E, Bezemer T, Boschker H, Veen JV (2007) Impact of elevated carbon dioxide on the rhizosphere communities of Carex arenaria and cal Entomology, 36, 574–581. Holdo RM, Sinclair ARE, Dobson AP, Metzger KL, Bolker BM, Ritchie ME, Holt RD (2009) A disease-mediated trophic cascade in the Serengeti and its implications for ccosystem C. PLoS Biology, 7, e1000210. Holtkamp R, Kardol P, Wal AVD, Dekker SC, Van Der Putten WH, Ruiter PCD (2008) Soil food web structure during ecosystem development after land abandonment. Applied Soil Ecology, 39, 23–34. Festuca rubra. Global Change Biology, 13, 2396–2410. Drigo B, Kowalchuk G, Veen AV (2008) Climate change goes underground: effect of elevated atmospheric CO2 on microbial community structure and activities in the rhizosphere. Biology and Fertility of Soils, 44, 667–679. Duchesne L (1994) Role of ectomycorrhizal fungi in biocontrol. In: Mycorrhizae and Plant Health (eds Pfleger FL, Linderman RG), pp. 27–45. APS Press, St. Paul, MN. Hooper DU, Chapin FS, Ewel JJ et al. (2005) Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecological Monographs, 75, 3–35. Hungate BA, Iii CHJ, Gamara G, Iii FSC, Field CB (2000) Soil microbiota in two annual grasslands: responses to elevated atmospheric CO . Oecologia, 124, 589–598. IPCC (2007) Climate Change 2007: Synthesis Report. Contribution of Working Groups I, II and III to the Fourth Assessment Report of the Intergovernmental Panel on Climate Duffy JE, Cardinale BJ, France KE, Mcintyre PB, Thébault E, Loreau M (2007) The functional role of biodiversity in ecosystems: incorporating trophic complexity. Ecology Letters, 10, 522–538. Eastburn DM, Mcelrone AJ, Bilgin DD (2011) Influence of atmospheric and climatic change on plant–pathogen interactions. Plant Pathology, 60, 54–69. Elsas JDV, Speksnijder A, Overbeek LV (2008) A procedure for the metagenomics exploration of disease-suppressive soils. Journal of Microbiological Methods, 75, 515–522. Change (eds Core Writing Team, Pachauri RK, Reisinger A). IPCC, Geneva, Switzerland. Jactel H, Petit J, Desprez-Loustau M-L, Delzon S, Piou D, Battisti A, Koricheva J (2012) Drought effects on damage by forest insects and pathogens: a meta-analysis. Global Change Biology, 18, 267–276. Jakab G, Ton J, Flors V, Zimmerli L, Métraux J-P, Mauch-Mani B (2005) Enhancing Arabidopsis salt and drought stress tolerance by chemical priming for Its Abscisic Flechard CR, Neftel A, Jocher M, Ammann C, Leifeld J, Fuhrer J (2007) Temporal changes in soil pore space CO2 concentration and storage under permanent grassland. Agricultural and Eorest Meteorology, 142, 66–84. Forchetti G, Masciarelli O, Alemano S, Alvarez D, Abdala G (2007) Endophytic bacteria in sunflower (Helianthus annuus L.): isolation, characterization, and production of jasmonates and abscisic acid in culture medium. Applied Microbiology and Bio- acid responses. Plant Physiology, 139, 267–274. Janus L, Angeloni N, Mccormack J, Rier S, Tuchman N, Kelly J (2005) Elevated atmospheric CO2 alters soil microbial communities associated with trembling aspen (Populus tremuloides) roots. Microbial Ecology, 50, 102–109. Janvier C, Villeneuve F, Alabouvette C, Edel-Hermann V, Mateille T, Steinberg C (2007) Soil health through soil disease suppression: which strategy from descrip- technology, 76, 1145–1152. Franco C, Michelsen P, Percy N et al. (2007) Actinobacterial endophytes for improved crop performance. Australasian Plant Pathology, 36, 524–531. Frey-Klett P, Garbaye J, Tarkka M (2007) The mycorrhiza helper bacteria revisited. New Phytologist, 176, 22–36. Ge Y, Chen C, Xu Z, Oren R, He J-Z (2010) The spatial factor, rather than elevated CO2, controls the soil bacterial community in a temperate forest ecosystem. Applied tors to indicators? Soil Biology and Biochemistry, 39, 1–23. Johnson S, Staley JT, Mcleod FaL, Hartley SE (2011) Plant-mediated effects of soil invertebrates and summer drought on above-ground multitrophic interactions. Journal of Ecology, 99, 57–65. Jones TH, Thompson LJ, Lawton JH et al. (1998) Impacts of rising atmospheric carbon dioxide on model terrestrial ecosystems. Science, 280, 441–443. Juroszek P, Von Tiedemann A (2011) Potential strategies and future requirements and Environmental Microbiology, 76, 7429–7436. Ghini R, Hamada E, Bettiol W (2008) Climate change and plant diseases. Scientia Agricola, 65, 98–107. Gill RA, Jackson RB (2000) Global patterns of root turnover for terrestrial ecosystems. New Phytologist, 147, 13–31. Gilman SE, Urban MC, Tewksbury J, Gilchrist GW, Holt RD (2010) A framework for for plant disease management under a changing climate. Plant Pathology, 60, 100– 112. Jwa N-S, Walling LL (2001) Influence of elevated CO2 concentration on disease development in tomato. New Phytologist, 149, 509–518. Kabouw P, Kos M, Kleine S et al. (2011) Effects of soil organisms on aboveground multitrophic interactions are consistent between plant genotypes mediating the community interactions under climate change. Trends in Ecology & Evolution, 25, 325–331. Gimsing A, Kirkegaard J (2009) Glucosinolates and biofumigation: fate of glucosinolates and their hydrolysis products in soil. Phytochemistry Reviews, 8, 299–310. Gupta VVSR (2011) Microbes and soil structure. In: Encyclopedia of Agrophysics (eds Glinski J, Horabik J, Lipiec J), pp. 470–472. Springer, Dordrecht. Haas D, Defago G (2005) Biological control of soil-borne pathogens by fluorescent interaction. Entomologia Experimentalis et Applicata, 139, 197–206. Kardol P, Bezemer T, Van Der Putten WH (2006) Temporal variation in plant-soil feedback controls succession. Ecology Letters, 9, 1080–1088. Kim J-S, Sparovek G, Longo RM, De Melo WJ, Crowley D (2007) Bacterial diversity of terra preta and pristine forest soil from the Western Amazon. Soil Biology and Biochemistry, 39, 684–690. King GM (2011) Enhancing soil carbon storage for carbon remediation: potential con- pseudomonads. Nature Reviews Microbiology, 3, 307–319. Hannukkala AO, Kaukoranta T, Lehtinen A, Rahkonen A (2007) Late-blight epidemics on potato in Finland, 1933–2002; increased and earlier occurrence of epidemics associated with climate change and lack of rotation. Plant Pathology, 56, 167–176. Hardoim PR, Andreote FD, Reinhold-Hurek B, Sessitsch A, Van Overbeek LS, Van Elsas JD (2011) Rice root-associated bacteria: insights into community structures tributions and constraints by microbes. Trends in Microbiology, 19, 75–84. Klironomos JN, Allen MF, Rillig MC, Piotrowski J, Makvandi-Nejad S, Wolfe BE, Powell JR (2005) Abrupt rise in atmospheric CO2 overestimates community response in a model plant-soil system. Nature, 433, 621–624. Klironomos J, Zobel M, Tibbett M et al. (2011) Forces that structure plant communities: quantifying the importance of the mycorrhizal symbiosis. New Phytologist, across 10 cultivars. FEMS Microbiology Ecology, 77, 154–164. Hartley S, Jones C, Couper G, Jones T (2000) Biosynthesis of plant phenolic compounds in elevated atmospheric CO2. Global Change Biology, 6, 497–506. Hassall M, Adl S, Berg M, Griffiths B, Scheu S (2006) Soil fauna microbe interactions: towards a conceptual framework for research. European Journal of Soil Biology, 42, S54–S60. Hawkes CV, Hartley IP, Ineson P, Fitter AH (2008) Soil temperature affects carbon 189, 366–370. Krumins JA, Long ZT, Steiner CF, Morin PJ (2006) Indirect effects of food web diversity and productivity on bacterial community function and composition. Functional Ecology, 20, 514–521. Lambers H, Mougel C, Jaillard B, Hinsinger P (2009) Plant-microbe-soil interactions in the rhizosphere: an evolutionary perspective. Plant and Soil, 321, 83–115. Landa B, Navas-Cortés J, Jiménez-Gasco M, Katan J, Retig B, Jiménez-Dı́az R (2006) allocation within arbuscular mycorrhizal networks and carbon transport from plant to fungus. Global Change Biology, 14, 1181–1190. Hawkes CV, Kivlin SN, Rocca JD, Huguet V, Thomsen MA, Suttle KB (2011) Fungal community responses to precipitation. Global Change Biology, 17, 1637–1645. Heinemeyer A, Ineson P, Ostle N, Fitter A (2006) Respiration of the external mycelium in the arbuscular mycorrhizal symbiosis shows strong dependence on recent Temperature response of chickpea cultivars to races of Fusarium oxysporum f. sp. ciceris, causal agent of fusarium wilt. Plant Disease, 90, 5–374. Landesman W, Treonis A, Dighton J (2011) Effects of a one-year rainfall manipulation on soil nematodes, microbial communities and nitrogen mineralization. Pedobiologia, 54, 87–91. Lewis J, Papavizas G (1991) Biocontrol of plant disease: the approach for tomorrow. photosynthates and acclimation to temperature. New Phytologist, 171, 159–170. Hibberd JM, Whitbread R, Farrar JF (1996) Effect of elevated concentrations of CO2 on infection of barley by Erysiphe graminis. Physiological and Molecular Plant Pathology, 48, 37–53. Crop Protection, 10, 5–105. Li Q, Xu C, Liang W, Zhong S, Zheng X, Zhu J (2009) Residue incorporation and N fertilization affect the response of soil nematodes to the elevated CO2 in a Chinese wheat field. Soil Biology and Biochemistry, 41, 1497–1503. © 2012 Blackwell Publishing Ltd, Global Change Biology, 18, 2111–2125 2124 S . C H A K R A B O R T Y et al. Lindroth R (2010) Impacts of elevated atmospheric CO2 and O3 on forests: phytochemistry, trophic interactions, and ecosystem dynamics. Journal of Chemical Ecol- Percy K, Awmack C, Lindroth R et al. (2002) Altered performance of forest pests under atmospheres enriched by CO2 and O3. Nature, 420, 403–407. ogy, 36, 2–21. Lipson D, Blair M, Barron-Gafford G, Grieve K, Murthy R (2006) Relationships between microbial community structure and soil processes under elevated atmospheric carbon dioxide. Microbial Ecology, 51, 302–314. Lumsden R, Lewis J, Fravel D (1995) Formulation and delivery of biocontrol agents for use against soilborne plant pathogens. In: Biorational Pest Control Agents. Formulation and Delivery (eds Hall F, Barry J), pp. 166–182. American Chemical Pereyra SA, Dill-Macky R, Sims AL (2004) Survival and inoculum production of Gibberella zeae in wheat residue. Plant Disease, 88, 724–730. Phillips DA, Ferris H, Cook DR, Strong DR (2003) Molecular control points in rhizosphere food webs. Ecology, 84, 816–826. Pickles BJ, Egger KN, Massicotte HB, Green DS (2012) Ectomycorrhizas and climate change. Fungal Ecology, 5, 73–84. Pineda A, Zheng S-J, Loon JJaV, Pieterse CMJ, Dicke M (2010) Helping plants to deal Society, Washington DC. Márquez LM, Redman RS, Rodriguez RJ, Roossinck MJ (2007) A virus in a fungus in a plant: three-way symbiosis required for thermal tolerance. Science, 315, 513–515. Matos AD, Cabral J, Sanches N, Caldas R (2000) Effect of temperature and rainfall on the incidence of Fusarium subglutinans on pineapple fruits. Acta Horticulturae, 529, 265–271. with insects: the role of beneficial soil-borne microbes. Trends in Plant Science, 15, 507–514. Plessl M, Elstner EF, Rennenberg H, Habermeyer J, Heiser I (2007) Influence of elevated CO2 and ozone concentrations on late blight resistance and growth of potato plants. Environmental and Experimental Botany, 60, 447–457. Postma J, Nijhuis EH, Yassin AF (2010) Genotypic and phenotypic variation among Matros A, Amme S, Kettig B, Buck-Sorlin GH, Sonnewald U, Mock HP (2006) Growth at elevated CO2 concentrations leads to modified profiles of secondary metabolites in tobacco cv. SamsunNN and to increased resistance against infection with potato virus Y. Plant Cell and Environment, 29, 126–137. Matthews R, Noordwijk MV, Gijman AJ, Cadisch G (2004) Models of below-ground interactions: their validity, applicability and beneficiaries. In: Below-ground Interactions in Tropical Agroecosystems Concepts and Models with Multiple Plant Components Lysobacter capsici strains isolated from Rhizoctonia suppressive soils. Systematic and Applied Microbiology, 33, 232–235. Pritchard SG (2011) Soil organisms and global climate change. Plant Pathology, 60, 82–99. Ramı́rez V, Coego A, López A, Agorio A, Flors V, Vera P (2009) Drought tolerance in Arabidopsis is controlled by the OCP3 disease resistance regulator. The Plant Journal, 58, 578–591. Raupach MR, Canadell JG (2010) Carbon and the Anthropocene. Current Opinion in (eds Noordwijk MV, Cadisch G, Ong CK), pp. 41–60. CABI, Wallingford. Mazzola M (2010) Management of resident soil microbial community structure and function to suppress soilborne disease development. In: Climate Change and Crop Production (ed. Reynolds M), pp. 200–218. CAB International, Wallingford. McCann K (2007) Protecting biostructure. Nature, 446, 29. McElrone A, Sherald J, Forseth I (2003) Interactive effects of water stress and xylem- Environmental Sustainability, 2, 210–218. Redman RS, Kim YO, Woodward CJDA, Greer C, Espino L, Doty SL, Rodriguez RJ (2011) Increased fitness of rice plants to abiotic stress via habitat adapted symbiosis: a strategy for mitigating impacts of climate change. PLoS ONE, 6, e14823. Rillig M (2007) Climate change effects on fungi in egroecosystems. In: Agroecosystems in a Changing Climate (eds Newton PCD, Carran RA, Edwards GR, Niklaus PA), limited bacterial infection on the water relations of a host vine. Journal of Experimental Botany, 54, 419–430. McElrone AJ, Reid CD, Hoye KA, Hart E, Jackson RB (2005) Elevated CO2 reduces disease incidence and severity of a red maple fungal pathogen via changes in host physiology and leaf chemistry. Global Change Biology, 11, 1828–1836. MEA (2005) Ecosystems and Human Wellbeing: Synthesis. The Centre for Resource Economics, Washington. pp. 211–230. CRC Taylor and Francis, Boca Raton. Rizhsky L, Liang H, Mittler R (2002) The combined effect of drought stress and heat shock on gene expression in Tobacco. Plant Physiology, 130, 3–1151. Rodriguez RJ, White JF Jr, Arnold AE, Redman RS (2009) Fungal endophytes: diversity and functional roles. New Phytologist, 182, 314–330. Roy BA, Güsewell S, Harte J (2004) Response of plant pathogens and herbivores to a warming experiment. Ecology, 85, 2570–2581. Melloy P, Hollaway G, Luck JO, Norton ROB, Aitken E, Chakraborty S (2010) Production and fitness of Fusarium pseudograminearum inoculum at elevated carbon dioxide in FACE. Global Change Biology, 16, 3363–3373. Mizubuti E, Fry W (1998) Temperature effects on developmental stages of isolates from three clonal lineages of Phytophthora infestans. Phytopathology, 88, 837–843. Montero-Barrientos M, Hermosa R, Cardoza RE, Gutierrez S, Nicolas C, Monte E Scervino J, Ponce M, Erra-Bassells R, Bompadre J, Vierheilig H, Ocampo J, Godeas A (2007) The effect of flavones and flavonols on colonization of tomato plants by arbuscular mycorrhizal fungi of the genera Gigaspora and Glomus. Canadian Journal of Microbiology, 53, 702–709. Schadler M, Roeder M, Brandl R, Matthies D (2007) Interacting effects of elevated CO2, nutrient availability and plant species on a generalist invertebrate herbivore. (2010) Transgenic expression of the Trichoderma harzianum hsp70 gene increases Arabidopsis resistance to heat and other abiotic stresses. Journal of Plant Physiology, 167, 659–665. Moore J, Walter D, Hunt H (1988) Arthropod regulation of micro- and mesobiota in below-ground detrital food webs. Annual Review of Entomology, 33, 419–439. Nannipieri P (2011) Potential impacts of climate change on microbial function in soil: the effect of elevated CO2 concentration. In: Sustaining Soil Productivity in Response Global Change Biology, 13, 1005–1015. Scherber C, Eisenhauer N, Weisser WW et al. (2010) Bottom-up effects of plant diversity on multitrophic interactions in a biodiversity experiment. Nature, 468, 553–556. Schonhof I, Kläring H, Krumbein A, Schreiner M (2007) Interaction between atmospheric CO2 and glucosinolates in broccoli. Journal of Chemical Ecology, 33, 105–114. Shefferson RP, Taylor DL, Weiß M et al. (2007) The evolutionary history of mycorrhizal specificity among Lady’s slipper orchids. Evolution, 61, 1380–1390. to Global Climate Change: Science, Policy, and Ethics (eds Sauer TJ, Norman J, Sivakumar MVK), pp. 201–211. Wiley-Blackwell, West Sussex, UK. Newman J (2007) Trophic interactions and climate change. In: Agroecosystems in a Changing Climate (eds Newton PCD, Carran RA, Edwards GR, Niklaus PA), pp. 231–259. Taylor and Francis, Boca Raton. Newsham KK (2011) A meta-analysis of plant responses to dark septate root endo- Shennan C (2008) Biotic interactions, ecological knowledge and agriculture. Philosophical Transactions of the Royal Society B, 363, 717–739. Shin J, Yun S (2010) Elevated CO2 and temperature effects on the incidence of four major chili pepper diseases. Plant Pathology Journal, 26, 178–184. Shoresh M, Harman GE, Mastouri F (2010) Induced systemic resistance and plant responses to fungal biocontrol agents. Annual Review of Phytopathology, 48, 21–43. phytes. New Phytologist, 190, 783–793. Norby RJ, Cortufo MF, Ineson P, Neill EGO, Canadell JG (2001) Elevated CO2, litter chemistry, and decomposition: a synthesis. Oecologia, 127, 153–165. Olff H, Alonso D, Berg MP, Eriksson BK, Loreau M, Piersma T, Rooney N (2009) Parallel ecological networks in ecosystems. Philosophical Transactions of the Royal Society B: Biological Sciences, 364, 1755–1779. Olofsson J, Ericson L, Torp M, Stark S, Baxter R (2011) Carbon balance of Arctic tun- Simard S, Austin M (2010) The role of mycorrhizas in forest soil stability with climate change. In: Climate Change and Variability (eds Simard S, Austin M), pp. 279–302. Sciyo, Croatia. Simmons B, Wall D, Adams B, Ayres E, Barrett J, Virginia R (2009) Terrestrial mesofauna in above- and below-ground habitats: Taylor Valley, Antarctica. Polar Biology, 32, 1549–1558. Singh KB, Foley RC, Oñate-Sánchez L (2002) Transcription factors in plant defense dra under increased snow cover mediated by a plant pathogen. Nature Climate Change, 1, 220–223. Ortiz R, Sayre KD, Govaerts B et al. (2008) Climate change: can wheat beat the heat? Agriculture, Ecosystems and Environment, 126, 46–58. Panaccione DG, Johnson RD, Wang J, Young CA, Damrongkool P, Scott B, Schardl CL (2001) Elimination of ergovaline from a grass–Neotyphodium endophyte sym- and stress responses. Current Opinion in Plant Biology, 5, 430–436. Singh B, Bardgett R, Smith P, Reay D (2010) Microorganisms and climate change: terrestrial feedbacks and mitigation options. Nature Reviews Microbiology, 8, 779–790. Smith P, Andrén O, Brussaard L, Dangerfield M, Ekschmitt K, Lavelle P, Tate K (1998) Soil biota and global change at the ecosystem level: describing soil biota in mathematical models. Global Change Biology, 4, 773–784. biosis by genetic modification of the endophyte. Proceedings of the National Academy of Sciences, 98, 12820–12825. Pattison AB, Moody PW, Badcock KA et al. (2008) Development of key soil health indicators for the Australian banana industry. Applied Soil Ecology, 40, 155–164. Smith SE, Smith FA, Jakobsen I (2004) Functional diversity in arbuscular mycorrhizal (AM) symbioses: the contribution of the mycorrhizal P uptake pathway is not correlated with mycorrhizal responses in growth or total P uptake. New Phytologist, 162, 511–524. © 2012 Blackwell Publishing Ltd, Global Change Biology, 18, 2111–2125 C L I M A T E C H A N G E I N F L U E N C E O N S O I L F O O D W E B 2125 Staddon P, Heinemeyer A, Fitter A (2002) Mycorrhizas and global environmental change: research at different scales. Plant and Soil, 244, 253–261. Van Der Putten WH, De Ruiter PC, Martijn Bezemer T, Harvey JA, Wassen M, Wolters V (2004) Trophic interactions in a changing world. Basic and Applied Ecology, 5, Straney D, Khan R, Tan R, Bagga S (2002) Host recognition by pathogenic fungi through plant flavonoids. Advances in Experimental Medicine and Biology, 505, 9–22. Strengbom J, Reich PB (2006) Elevated [CO2] and increased N supply reduce leaf disease and related photosynthetic impacts on Solidago rigida. Oecologia, 149, 519–525. Sturz AV, Ryan DAJ, Coffin AD, Matheson BG, Arsenault WJ, Kimpinski J, Christie BR (2004) Stimulating disease suppression in soils: sulphate fertilizers can increase biodiversity and antibiosis ability of root zone bacteria against Streptomyces scabies. 487–494. Van Der Putten WH, Macel M, Visser ME (2010) Predicting species distribution and abundance responses to climate change: why it is essential to include biotic interactions across trophic levels. Philosophical Transactions of the Royal Society B, 365, 2025–2034. Verhage A, Van Wees SCM, Pieterse CMJ (2010) Plant immunity: it’s the hormones talking, but what do they say? Plant Physiology, 154, 536–540. Soil Biology and Biochemistry, 36, 343–352. Susilo FX, Neutel AM, Noordwijk MV, Hairiah K, Brown G, Swift MJ (2004) Soil biodiversity and food webs. In: Below-ground Interactions in Tropical Agroecosystems Concepts and Models with Multiple Plant Components (eds Van Noordwijk M, Cadish G, Ong CK), pp. 285–307. CABI Publishing, Wallingford. Suttle KB, Thomsen MA, Power ME (2007) Species interactions reverse grassland Wakelin SA, Gupta VVSR, Forrester ST (2010) Regional and local factors affecting diversity, abundance and activity of free-living, N2-fixing bacteria in Australian agricultural soils. Pedobiologia, 53, 391–399. Wardle DA (2002) Communities and Ecosystems: Linking the Aboveground and Belowground Components. Princeton University Press, Princeton, NJ. Wardle DA (2006) The influence of biotic interactions on soil biodiversity. Ecology Let- responses to changing climate. Science, 315, 640–642. Tarnawski S, Hamelin J, Jossi M, Aragno M, Fromin N (2006) Phenotypic structure of Pseudomonas populations is altered under elevated pCO2 in the rhizosphere of perennial grasses. Soil Biology and Biochemistry, 38, 1193–1201. Treseder KK (2004) A meta-analysis of mycorrhizal responses to nitrogen, phosphorus, and atmospheric CO2 in field studies. New Phytologist, 164, 347–355. Ulainen PK, Holopainen T, Holopainen JK (2003) Decomposition of secondary com- ters, 9, 870–886. Wolfarth F, Schrader S, Oldenburg E, Weinert J, Brunotte J (2011) Earthworms promote the reduction of Fusarium biomass and deoxynivalenol content in wheat straw under field conditions. Soil Biology & Biochemistry, 43, 1858– 1865. Wolfe B, Klironomos J (2005) Breaking new ground: soil communities and exotic plant invasion. BioScience, 55, 477–487. pounds from needle litter of Scots pine grown under elevated CO2 and O3. Global Change Biology, 9, 295–304. Van Bruggen AHC, Semenov AM (2000) In search of biological indicators for soil health and disease suppression. Applied Soil Ecology, 15, 13–24. Van Dam NM, Heil M (2011) Multitrophic interactions below and above ground: en route to the next level. Journal of Ecology, 99, 77–88. Wong PTW (1984) Saprophtyic survival of Gaeumannomyces graminis and Phialophora spp. at various temperature-moisture regimes. Annals of Applied Biology, 105, 455– 461. Yeates G, Newton P (2009) Long-term changes in topsoil nematode populations in grazed pasture under elevated atmospheric carbon dioxide. Biology and Fertility of Soils, 45, 799–808. Van Der Heijden MGA, Bardgett RD, Van Straalen NM (2008) The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecology Letters, 11, 296–310. Van Der Putten WH (2009) A multitrophic perspective on functioning and evolution of facilitation in plant communities. Journal of Ecology, 97, 1131–1138. Van Der Putten WH, Vet LEM, Harvey JA, Wackers FL (2001) Linking aboveground and belowground multitrophic interactions of plants, herbivores, pathogens, and Yule K, Woolley J, Rudgers J (2011) Water availability alters the tri-trophic consequences of a plant-fungal symbiosis. Arthropod-Plant Interactions, 5, 19–27. Zak D, Pregitzer K, King J, Holmes W (2000) Elevated atmospheric CO2, fine roots and the response of soil microorganisms: a review and hypothesis. New Phytologist, 147, 201–222. Zhang DD, Breckle P, Lee HF, He YQ, Zhang J (2007) Global climate change, war, and population decline in recent human history. Proceedings of National Academy of their antagonists. Trends in Ecologoy and Evolution, 16, 547–554. © 2012 Blackwell Publishing Ltd, Global Change Biology, 18, 2111–2125 Sciences, 104, 19214–19219.