Ecology Letters, (2004) 7: 740–754

doi: 10.1111/j.1461-0248.2004.00620.x

REVIEW

Arbuscular mycorrhizae and terrestrial ecosystem processes

Matthias C. Rillig Microbial Ecology Program, Division of Biological Sciences, The University of Montana, Missoula, MT 59812, USA E-mail: [email protected]

Abstract Arbuscular mycorrhizal fungi (AMF; phylum Glomeromycota) are ubiquitous in terrestrial ecosystems. Despite their acknowledged importance in ecology, most research on AMF has focused on effects on individual plant hosts, with more recent efforts aimed at the level of the plant community. Research at the ecosystem level is less prominent, but potentially very promising. Numerous human-induced disturbances (including global change and agro-ecosystem management) impinge on AMF functioning; hence study of this symbiosis from the ecosystem perspective seems timely and crucial. In this paper, I discuss four (interacting) routes via which AMF can influence ecosystem processes. These include indirect pathways (through changes in plant and soil microbial community composition), and direct pathways (effects on host physiology and resource capture, and direct mycelium effects). I use the case study of carbon cycling to illustrate the potentially pervasive influence of AMF on ecosystem processes. A limited amount of published research on AMF ecology is suited for direct integration into ecosystem studies (because of scale mismatch or ill-adaptation to the Ôpools and fluxÕ paradigm of ecosystem ecology); I finish with an assessment of the tools (experimental designs, response variables) available for studying mycorrhizae at the ecosystem scale. Keywords Arbuscular mycorrhizae, carbon storage, glomalin, microbial community, net primary production, plant community, restoration, soil, soil aggregation. Ecology Letters (2004) 7: 740–754

INTRODUCTION

The concept of the ecosystem is predominantly biogeochemistry/process oriented, placing emphasis on the transfers of materials and energy between abiotic and biotic compartments (Chapin et al. 2002). The pivotal involvement of arbuscular mycorrhizal fungi (AMF) in plant mineral nutrition (Marschner 1995; Smith & Read 1997) positions these fungi at the abiotic/biotic interface in ecosystems. This is a critical point in nutrient cycling, since primary production in the majority of terrestrial ecosystems is limited by belowground resource availability (Chapin 1980; Chapin et al. 2002). As a result of this unique situation, AMF have been described as Ôkeystone mutualistsÕ in terrestrial ecosystems (O’Neill et al. 1991). AMF are responsive to many perturbations that act at the ecosystem level, such as factors of global change (Rillig & Allen 1999; Fitter et al. 2000; Treseder & Allen 2000; Rillig et al. 2002), agricultural management practices (Hamel 1996; Jansa et al. 2003; Oehl et al. 2003), or pollution (e.g. heavy metals: Meharg & Ó2004 Blackwell Publishing Ltd/CNRS

Cairney 2000; nitrogen deposition: Egerton-Warburton & Allen 2000); hence increasing our focus of looking at this symbiosis from the ecosystem perspective seems timely and crucial. Arbuscular mycorrhizae are symbiotic root fungus associations formed by AMF and the majority of species of land plants (Fitter et al. 2000). As such, AMF in roots are a normal occurrence in all but some terrestrial ecosystem types (e.g. boreal forest and heathlands; Read 1991) and all but few plant families (e.g. Brassicaceae). AMF could potentially have played an important role in terrestrial ecosystems for >460 million years, as evidenced by fossilized fungal structures (Redecker et al. 2000). AMF are members of the eumycotan fungal phylum Glomeromycota (Schu¨ßler et al. 2001; formerly in the Zygomycota). The plant is the only source of carbon for the obligately biotrophic AMF. Arbuscular mycorrhizae are a type of endomycorrhizal association, characterized by the formation of intracellular structures such as arbuscules (Smith & Read 1997). Arbuscules, formed as a result of joint plant–fungal

AM fungi and terrestrial ecosystem processes 741

development, are the primary sites of nutrient and carbon exchange between the symbionts. Intraradical structures, such as arbuscules, vesicles (lipid storage structures), coils, and the hyphae growing within the root cortical tissue, are connected to an extraradical mycelium (Allen 1991; Smith & Read 1997). This soil mycelium has a variety of functions (Friese & Allen 1991), including formation of spores (propagules for dispersal in time and space), formation of runner hyphae (exploration of soil and new roots to be colonized), and nutrient uptake. Ecological research on arbuscular mycorrhizae has historically focused at the organismal level, where the role of mycorrhizal colonization for plant physiology, growth and reproductions has been the main interest. Extrapolating from these studies, it is clear that AMF are important and ever-present components of terrestrial ecosystems. However, the appreciation of AMF importance in ecosystem ecology is frequently limited to an acknowledgement that AMF are important in nutrient uptake, and that these fungi may represent important carbon sinks to plants. This limited view of AMF results in part from the fact that many experimental designs and response variables available for quantifying AMF and their functions are not well matched to terrestrial ecosystem scales (e.g. catchment, stand, watershed); a problem long-recognized in mycorrhizal biology (O’Neill et al. 1991; Allen et al. 1992; Miller & Jastrow 1994; Rillig & Allen 1999; Staddon et al. 2002; see also Tool box section in this review). In addition to scale issues, studies on AMF ecology have in general also been ill-adapted to the pool and flux paradigm of ecosystem ecology, i.e. quantifying transfers of matter and energy between compartments in a system. This is nothing unique to mycorrhizal ecology or even microbial ecology in general, but also applies, for example, to the study of fungal plant pathogens: Mitchell (2003) presented the first attempt at quantifying foliar fungal pathogen biomass in an ecosystem. There is no universally accepted way to estimate AMF biomass in an ecosystem. The issue is complicated by the fact that AMF inhabit two functionally distinct locations, the root and soil. It is also not

straightforward to estimate AMF associated fluxes or turnover times (Miller & Kling 2000; Staddon et al. 2003; Steinberg & Rillig 2003; Zhu & Miller 2003). In the few instances where AMF (i.e. the extraradical mycelium) have been represented in simulation models (e.g. soil food web models: Hunt et al. 1987), mostly the plant nutrition aspect of AMF has been considered. AMF are not represented in ecosystem models or even soil carbon models, such as CENTURY (Parton et al. 1987); this is surprising given that estimated soil carbon derived from AMF soil mycelium can range from 50 to 900 kg ha)1 (Zhu & Miller 2003). The purpose of this review is to provide motivation for inclusion of AMF in ecosystem process/ functional studies and models by documenting the pervasive influence of AMF on ecosystem processes (Allen 1991) by a multitude of mechanisms, and also by pointing out gaps in our knowledge. I will first review potential pathways of AMF influence, then highlight AMF involvement in the carbon cycle, and conclude with a brief assessment of the tools (experimental designs, response variables) available for studying AMF at the ecosystem scale. HOW AMF CAN INFLUENCE ECOSYSTEM PROCESSES

Overview of pathways

AMF can influence ecosystem processes through fundamentally different (though by necessity interrelated) pathways, residing at different levels of the biological hierarchy (i.e. individual, community; O’Neill et al. 1991) (Fig. 1): 1 The presence and composition of AMF can influence plant community composition. The plant community, altered in the presence of AMF, can exhibit different process rates compared to a plant community without AMF or with a different species assemblage of AMF. 2 AMF can directly and indirectly influence soil microbial communities. The presence and composition of AMF can alter the composition of microbiota that are directly involved in ecosystem processes.

Figure 1 Arbuscular

mycorrhizal fungi (AMF) can influence ecosystem processes via several pathways. These pathways are separated for the purpose of this discussion, but clearly interact with each other (and provide feedbacks to AMF). Ó2004 Blackwell Publishing Ltd/CNRS

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3 AMF-mediated changes in (individual) host physiology and resource capture can translate into ecosystem effects. 4 Direct effects of the AMF soil mycelium and its products can be manifested at the ecosystem level. These pathways of influence are separated for the purpose of organizing this discussion of AMF effects; it is clear that these mechanisms interact significantly. For example, AMF-caused changes in plant community composition could also lead to changes in other soil microbiota, as soil microbial communities associated with different plant species frequently diverge (Kent & Triplett 2002). For example, Johnson et al. (2003) have shown that microbial communities differ significantly with plant community composition and AMF abundance. Likewise, host resource capture could be influenced by soil microbial communities (e.g. nitrogen fixing bacteria). Additionally, causality does not only run in one direction. There is, for example, evidence that plant community composition can impact AMF community composition (Johnson et al. 2004). Likewise, soil microbial communities can provide positive (e.g. mycorrhization helper bacteria (bacteria that promote AMF root colonization); Garbaye 1994) or negative (resource competition, fungal parasites) effects on AMF. Finally, although not further considered here, temporal changes may occur in the AMF community on a variety of scales from seasonal (Pringle & Bever 2002) to successional (Hart et al. 2001). This suggests that, insofar as AMF communities are influential on ecosystem processes, feedbacks and effects outlined above may be highly dynamic. In the following sections, I will discuss each of the four general mechanisms outlined above. Then, I will examine the case of C cycling to illustrate how AMF, via these different mechanisms, may act to affect carbon sequestration. Mycorrhizal fungi can influence ecosystem properties indirectly by affecting plant community composition Several studies, using mesocosms and in the field, have shown that presence or diversity of mycorrhizal fungi can have strong influences on plant community composition (Grime et al. 1987; Gange et al. 1993; van der Heijden et al. 1998; Hartnett & Wilson 1999, 2002; Klironomos et al. 2000; O’Connor et al. 2002; van der Heijden 2002; Stampe & Daehler 2003; Johnson et al. 2003a). Effects of AMF on plant species diversity (mostly evenness) range from positive to negative. The direction and magnitude of the effect is hypothesized to be related to the relative mycorrhizal dependency of the dominant and subordinate plant species of a community (Urcelay & Dı´az 2003). Mycorrhizal dependency is defined as the dry matter yield of a species in the mycorrhizal compared to the non-mycorrhizal

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condition. For example, if the competitively dominant plant species in a community is highly mycorrhizal dependent, then loss of mycorrhizae can actually increase diversity (evenness), because of competitive release of subordinates. In addition, AMF presence can alter competitive interaction (in pairs of interacting plant species) even if AMF do not have any effects on the involved plant hosts in isolation (Marler et al. 1999); this points to the presence of mechanisms that may be difficult to predict from individual host responses in a community. In the plant ecology literature, there is a rich database and theoretical framework for the role of plant species traits in influencing ecosystem properties (e.g. Hobbie 1992; Chapin et al. 1997; Cornelissen et al. 2001; Knops et al. 2002; Wardle 2002; Eviner & Chapin 2003). Plant species properties that have the potential to influence ecosystem processes include traits that affect use of resources (e.g. association with nitrogen fixing bacteria, litter quality, rhizodeposition, access to certain forms of nutrients [e.g. via mycorrhizae; Cornelissen et al. 2001]), that affect trophic structure in an ecosystem (e.g. palatability), and that influence disturbance regimes (e.g. soil erosion, fire). There are a number of empirical studies that provide direct evidence for effects of plant species composition or diversity (mechanisms underlying the latter being controversial; see Wardle 2002) on ecosystem processes. The dominant ecosystem process examined is primary productivity (e.g. Tilman et al. 1997; Loreau et al. 2001; Pfisterer & Schmid 2002; Wardle 2002), which is an important driver for other processes. Other ecosystem processes affected by experimental manipulations of plant species diversity include soil nutrient depletion and reduced potential leaching losses (e.g. nitrate: Tilman et al. 1996), light penetration (Tilman et al. 1997), immobilization of N (using plant functional group diversity: Hooper & Vitousek 1998), and resistance and resilience of biomass production to perturbation (Tilman & Downing 1994; Pfisterer & Schmid 2002). There is only limited empirical evidence to support that AMF-mediated changes in plant community composition are of a magnitude to cause changes in ecosystem processes. Van der Heijden et al. (1998) have provided direct evidence that AMF (diversity) can change plant community composition; importantly, the same study also showed that the AMF-altered plant community had significantly different primary production and soil phosphate depletion. Of course, in this study, both AMF and plant communities changed concomitantly – in fact, AMF and plant communities, as interdependent entities, have a natural tendency to co-vary (Hart et al. 2001). Hence, it is difficult to partition influence on the observed changes in ecosystem properties between AMF and plant communi-

AM fungi and terrestrial ecosystem processes 743

ties, and it will, in the field, always be difficult to separate these influences. However, using microcosm studies this is possible (at the cost of loss of realism): for example, Klironomos et al. (2000) have grown plant communities (richness from 0 to 15 species) with or without a single AMF isolate. The plant species richness – primary production relationship was strongly influenced by AMF presence (and identity). This indicates that presence of AMF can alter primary production of a starting plant community independently of changes in AMF community composition. In summary, AMF can influence ecosystem process rates through altering plant community composition, and this likely is a dominant pathway. Future research in this area should also examine processes beyond primary production. For example, plant community composition can also influence processes such as nutrient leaching (e.g. nitrate: Scherer-Lorenzen et al. 2003; dissolved organic carbon (DOC): Kalbitz et al. 2000). AMF can affect ecosystem processes by modifying soil microbial community structure One potential way for AMF to influence soil microbial community structure is by influencing the plant community with indirect ripple-on effects on soil microbiota (e.g. Kent & Triplett 2002; Porazinska et al. 2003; Johnson et al. 2003); however, this section will focus on direct influences of AMF on the microbial community at the scale of the individual host (by necessity, given the available literature). Although our understanding of the microbial ecology of AMF-associations is still in its infancy, there is little doubt that AMF presence can alter microbial community composition in the rhizosphere and mycorrhizosphere of a given host plant (Hodge 2000; Johansson et al. 2004). There are two main avenues by which AMF can affect changes in soil microbial community composition: there can be direct effects of the mycelium and its products (e.g. Andrade et al. 1997; Filion et al. 1999; Marschner & Baumann 2003), and AMF can modify rhizodeposition (Linderman 1988), thereby indirectly affecting soil microbiota (e.g. Marschner & Baumann 2003). The former can be called ÔhyphosphereÕ effects, the latter are rhizosphere effects. In addition, AMF hyphae also harbour endosymbiotic bacteria (e.g. Bianciotto et al. 1996). It thus seems evident that AMF can influence soil microbial communities. It is less clear what the functional significance of these population/community changes for ecosystem processes is. It is often difficult to empirically relate overall soil microbial community composition to function (e.g. Griffiths et al. 2000); this is perhaps in part due to relatively high ÔredundancyÕ in highly species-rich soil communities (Wardle 2002). An alternative explanation could be that molecular-based surveys may miss minority

populations that are functionally important (Holben et al. 2004). Nevertheless, in an agricultural context, AMF influences on selected populations of functionally circumscribed microbiota have been found. These include effects on phosphate-solubilizing bacteria (Barea et al. 2002), mycorrhization-helper bacteria (Garbaye 1994), nitrogentransforming microbes (autotrophic ammonium oxidizers: Amora-Lazcano et al. 1998; saprobes: Hodge et al. 2001; Hodge 2001), bacteria involved in soil aggregation (see Case Study), and fungal root pathogens (e.g. Newsham et al. 1995; Filion et al. 1999; Graham 2001). While this information is mainly available from controlled environment studies, it is likely that similar interactions take place in the field. Separating effects and quantifying the relative importance of AMF and AMF-caused changes in soil microbial communities will be an area of intense interest in mycorrhizal ecology. AMF influences on the individual host plant AMF influences on the individual plant host have been the focal point of most of AMF ecological and eco-physiological research, and general reviews on this topic are available from Allen (1991), Koide (1991), Allen (1992), Marschner (1995), Smith & Read (1997), Varma & Hock (1999), Kapulnik & Douds (2000) and van der Heijden & Sanders (2002). By far, most research has been devoted to the role of AMF in host mineral nutrient acquisition (mostly phosphate); however, there is a disconnect between mechanistic studies of nutrient translocation and quantification of relative importance of AMF contributions to this process in the field (Fitter 1985; Jakobsen et al. 2002; Read & PerezMoreno 2003), which would be more important from the ecosystem perspective. In addition to their roles in plant nutrition, AMF are also involved in protection against root pathogens (Newsham et al. 1995), provision of carbon sink strength to their host (e.g. Miller et al. 2002), improvement of host water relations including drought tolerance (Auge´ 2001), mediation of pollutant effects (Meharg & Cairney 2000), resulting often, but not always (Johnson et al. 1997; Klironomos 2003), in improved host plant growth and fitness (Read 1999). An important development in the area of individual host physiology is the recognition of the importance of AMF species/isolate differences. It is tempting to assume that AMF are not host-specific (given the large number of potential hosts and the comparatively small number of described AMF species, for example) and hence perhaps functionally equivalent. However, there is ample evidence, more recently also using molecular microbial ecology approaches, that co-occurring hosts associate with a nonrandom subset of the soil AMF community (e.g. Bever et al. 1996; Vandenkoornhuyse et al. 2003), that AMF Ó2004 Blackwell Publishing Ltd/CNRS

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species/isolates differ in a number of ecophysiological traits (e.g. Hart & Reader 2002), and as a consequence in their effects on host physiology and growth (e.g. Klironomos 2003). Realization of the multitude of AMF influences on host physiology and the potential division of labor within AMF species/isolates (Klironomos 2000; Koch et al. 2004) gives rise to an important lesson in the ecosystem context: it is dangerous to extrapolate from results on any given AMF effect obtained from a ÔrepresentativeÕ AMF isolate to conditions in the field. Direct effects of the AMF mycelium and its products on ecosystem processes In this section, I am discussing the effects of the extraradical mycelium only; the intraradical mycelium will likely only have indirect effects (for example, by modifying host physiology) on ecosystem processes. The AMF extraradical mycelium can also influence soil microbial community structure, as discussed above. Effects of the AMF mycelium on nutrient uptake were mentioned in the section headed AMF influences on the individual host plant. The extraradical AMF mycelium is a crucial contributor to the formation and maintenance of soil structure (Tisdall & Oades 1982; Miller & Jastrow 1994, 2000; Rillig 2004). Soil structure is an ecosystem variable that influences virtually all nutrient cycling processes and soil biota (Diaz-Zorita et al. 2002). Soil structure, the arrangement of primary particles and organic material into aggregates and pore spaces, is not generally considered in ecosystem models, which are parameterized using soil texture (the size distribution of primary particles). There certainly are strong links between texture and structure, but structure can deteriorate (or form) on ecological time scales, without change in texture. It is also clear that soil aggregation can be changed by a variety of treatments in agroecosystems (e.g. tillage, crop rotations), as well as in natural ecosystems (for example, global change factors: Rillig et al. 1999; Niklaus et al. 2003). The mechanisms by which AMF extraradical hyphae help stabilize soil aggregates are still not clearly understood. AMF are thought to have most important contributions to the stabilization of macroaggregates (>250 lm), where they are hypothesized to help stabilize aggregates via hyphal enmeshment (Ôstring-bagÕ mechanism; Miller & Jastrow 2000) and by deposition of organic material. An important component of the organic material contained in or released by AMF hyphae is glomalin, a putative protein produced by AMF (Wright & Upadhyaya 1996; Rillig 2004). The biochemical nature of glomalin is still unknown; aspects of this substance are currently quantified by measuring several glomalin-related soil-protein (GRSP) pools (Rillig 2004), including immunoreactive proteins using a monoclonal antibody (MAb32B11; originally created against crushed spores of the AMF Glomus Ó2004 Blackwell Publishing Ltd/CNRS

intraradices). GRSP concentrations are highly positive, but curvilinearly correlated (ÔsaturationÕ-type response curve) with soil aggregate water stability (Wright & Upadhyaya 1998). A significant portion of GRSP (e.g. 50%; Rillig et al. 2003) has slow turnover in soil, highlighting its utility in soil structural ÔengineeringÕ roles. GRSP production appears to be controlled by environmental factors (including aspects of physical growing space; Rillig & Steinberg 2002); numerous phenomenological studies are available that document GRSP pool changes, and frequently concomitant changes in soil aggregation, in response to a variety of ecosystem disturbances (reviewed in Rillig 2004). While research on GRSP and glomalin is still in its infancy, it is clear that this pathway of AMF influence on ecosystem processes is a particularly remarkable one; this is the case because GRSP, at least partially controlled by AMF, has direct consequences at the ecosystem scale (see also Table 1). Hence, any factor applied at the ecosystem scale that can potentially impinge on AMF functioning, has the propensity to cause down-stream effects on soil structure; these soil structure effects could often be ÔhiddenÕ treatment effects in ecosystem studies (hidden, since soil structure is not part of the usual ecosystem response variable repertoire, except in agroecosystems). CASE STUDY: CARBON CYCLING AND STORAGE

Clearly, AMF can influence ecosystem processes other than carbon and nutrient cycling (see previous discussion and Table 1). However, carbon storage in ecosystems is currently of societal and scientific interest, and hence I will focus on this aspect of AMF influences. The net carbon accumulation (storage) by an ecosystem over a certain time step is termed net ecosystem production (NEP; Chapin et al. 2002), currently mostly approximated as net ecosystem exchange. Conceptually, NEP has several main components: change in plant biomass, change in soil organic matter (SOM) and change in animal biomass (the latter not considered further here) (Fig. 2). In this section, I examine how the different pathways of AMF influence on ecosystem processes (Fig. 1) apply to carbon cycling (Fig. 2). I propose that the influence of AMF on plant community composition and individual plants will be of greatest importance in determining net primary production (NPP), while the other two mechanisms, soil microbial community impacts and direct mycelium effects, will be most important in the processing of SOM (Fig. 2). Change in plant biomass

The sum of all net photosynthesis in an ecosystem is called gross primary production (GPP); clearly, as AMF can influence leaf-level (and whole-plant) photosynthesis (Allen

(H) Surface roughness; boundary layer resistance (H) Partitioning between runoff and infiltration (H) Albedo change (affecting absorption of Kin) by leaf surfaces (H) Latent heat flux (O) Plant macro- and micronutrient, pollutant uptake (H) Leaching of dissolved organic matter (DOM) (H) Leaching of inorganic nutrients Hyphal production of DOM; soil aggregation; AMF effects on net primary production Hyphal nutrient uptake; effects on soil microbial community

AMF influence on soil hydrophobicity (via glomalin production?) Increased chlorophyll content in mycorrhizal leaves AMF influences on transpiration AMF hypha-mediated uptake

1,3

Passive water movement along W gradient provided by AMF (and EM) soil hyphae Hormonal involvement; scavenging of soil water, etc. Canopy architecture changes

Kalbitz et al. (2000); Rillig (2004) Smith & Read (1997); Johansson et al. (2004)

1,2,3

Auge´ (2001) Smith & Read (1997)

3 3 1,3,4

Louche-Tessandier et al. (1999)

Rillig, unpublished observation

Streitwolf-Engel et al. (1997)

Auge´ (2001)

Querejeta et al. (2003)

Reference

3

4

1,3

3

Pathway 

Mechanism

*O, observed effect; H, hypothesized effect based on mechanism.  Refers to the four pathways depicted in Fig. 1 (1, plant community; 2, soil microbial community; 3, host plant; 4, direct mycelium effect).

Element/nutrient cycling

Energy balance

(O) Hydraulic lift

Water balance

(O) Plant water uptake

Process*

Context

Table 1 Additional ecosystem processes mediated or potentially influenced by arbuscular mycorrhizal fungi (AMF) that are not explicitly discussed in this review. For carbon cycle effects, see Fig. 2

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Figure 2 Simplified representation of carbon fluxes in a terrestrial ecosystem, highlighting potential contributions of arbuscular mycorrhizal

fungi (AMF). Numbers in circles refer to pathway of influences (see Fig. 1): 1, plant community composition; 2, soil microbial community composition; 3, host level effects, 4, direct mycelium effects. NPP, net primary production (gross primary production minus autotrophic respiration); NEP, net ecosystem production; VOC, volatile organic carbon (generally a negligible effect).

1991; Smith & Read 1997), an influence on GPP seems indisputable. Additional influences on GPP relate to the role of AMF in altering plant community composition (see section Plant community effects). Not all GPP is transferred into plant production. Plant respiration fluxes (typically 50% of GPP) need to be subtracted to obtain NPP, or the production of plant biomass. AMF can influence plant respiration rates, and hence also affect the NPP through this mechanism. For example, even when Trifolium repens L. plants of similar foliar N and P content were compared (to reduce impact of AMF on respiration via plant nutritional and growth changes), root respiration and dark shoot respiration were higher in mycorrhizal than non-mycorrhizal plants (on a per plant basis in diurnal C budgets; Wright et al. 1998). Other studies have also found that the percentage of C assimilated by plants which is respired by mycorrhizal roots (compared with nonmycorrhizal) is about 15% (e.g. Kucey & Paul 1982; Douds et al. 1988; Wang et al. 1989); however, this also includes mycorrhizal fungal respiration. As will be the case for much of this discussion, few of these rates appear to have been measured or estimated for the ecosystem scale, but rather at the scale of the individual plant (the latter may not scale up, for example as a result of plant and fungal species differences). Nevertheless, we will assume that Ó2004 Blackwell Publishing Ltd/CNRS

similar patterns will hold at the ecosystem scale (e.g. a recent study by Johnson et al. 2002) confirmed in the field that lab-based estimates of respiration of plant carbon by AMF were realistic). Not all NPP will translate to plant biomass change; important pathways here include losses due to herbivory, litter production, support of symbionts (including AMF), and rhizodeposition (Fig. 2; other losses not further considered here include volatile organic carbon, and losses due to disturbances and fire). AMF can potentially also influence these fluxes; for example, AMF root colonization can reduce rhizodeposition (Linderman 1988). AMF also can potentially influence the rate of herbivory at the level of the individual host plant, for example through increasing foliar or root nutritional quality (Borowicz 1997), or by altering concentrations of plant defense compounds (Gange & West 1994). Effects on herbivory can even depend on the identity of the AMF species/isolate (Goverde et al. 2000; Gange 2001), suggesting that not only presence but also AMF community composition may be able to exert control over plant herbivory. It follows that effects of AMF on plant biomass change are pervasive, and that factors other than photosynthetic carbon gain have to be taken into account to adequately represent AMF contributions.

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Change in SOM

Pathways of carbon loss

One of the most important components of ecosystem C storage is net change in SOM because of the large soil C pool (Chapin et al. 2002). At this level, direct hyphal contributions, and influences on soil microbial communities could be most important (Fig. 2). First, AMF-derived carbon in itself may be a significant component of SOM. AMF mycelium is frequently a dominant fraction of soil microbial biomass (Allen 1991; Miller et al. 1995; Rillig & Allen 1999; Treseder & Allen 2000; Zhu & Miller 2003). GRSP, to the extent that its origin can be traced back to AMF, can constitute additional C inputs, typically greatly exceeding mycelial mass (Rillig et al. 2001, 2003; Lovelock et al. 2004a; Rillig 2004). For example, in lowland tropical forest, levels of GRSP were 3.94 ± 0.16 mg cm)3 (1.45 Mg C ha)1), corresponding to 3.2% of total soil C and 5% of soil nitrogen in the top 10 cm of soil. At least some of the GRSP is in the slow soil C pool (Rillig et al. 2001, 2003). Turnover of some of the mycelial C pool appears to be on the order of weeks (Friese & Allen 1991; Staddon et al. 2003; Steinberg & Rillig 2003). Other aspects of the mycelium, runner hyphae (Friese & Allen 1991), may turn over much slower. Miller & Kling (2000) estimated AMF mycelium turnover using a prairie chronosequence from 2.56 to 3.84 years. AMF also contribute residual hyphal/spore wall material (including GRSP and chitin), which may be substantially more recalcitrant in soil (Treseder & Allen 2000; Rillig et al. 2003; Zhu & Miller 2003). In addition to direct contributions to soil C, AMF also make significant indirect contributions via their effects on soil aggregation. Physical protection of otherwise labile C inside of stable soil aggregates plays a crucial role in soil C sequestration (reviewed in Six et al. 2002). With AMF mycelium and its products (e.g. GRSP) positively correlated with soil aggregate stability, this is a highly significant effect. However, AMF also influence soil bacterial communities (see above). Recently, bacteria have been isolated from individual AMF mycelia which can be important in soil aggregation, such as Paenibacillus spp. (Budi et al. 1999; Hildebrandt et al. 2002; Mansfeld-Giese et al. 2002). Bezzate et al. (2000) have shown, through deletion of the Paenibacillus polymyxa levansucrase gene, that these bacteria and their fructosyl polymers have a role in soil aggregation. This introduces the interesting possibility that AMF-ÕculturedÕ bacteria are a significant factor in the soil aggregation effectiveness of AMF, or that AMF have even more farreaching effects on this ecosystem parameter than previously realized. AMF, in affecting other saprobic soil microbiota, could also alter SOM processing in a more direct way (e.g. Hodge et al. 2001).

Carbon fluxes leaving an ecosystem include leaching and erosion (Fig. 2). Carbon can be lost in leachate in organic (DOC) or inorganic form (Kalbitz et al. 2000). DOC originates from several sources, including plant litter, soil humus, and microbial biomass. While field estimates of the contribution of ectomycorrhizal fungi to DOC have recently become available (Ho¨gberg & Ho¨gberg 2002), no such data exist for AMF. Clearly, AMF-produced carbon may be lost directly as DOC (e.g. in the form of GRSP; Rillig et al. unpublished); or AMF-induced changes at the level of NPP, and hence plant litter amount and/or quality, could be important for DOC production and losses. Additionally, AMF influences on soil microbes could alter DOC processing. Carbon can be removed from an ecosystem via soil erosion. Stable soil structural units provide resistance against erosion caused by water and wind (Brady & Weil 1999); with AMF positively influencing soil aggregate stability (see Direct mycelium effects section), a negative effect of AMF on soil erosion follows. However, to date no empirical data is available to substantiate this hypothesis. When are AMF effects most crucial?

From the discussion above, it would appear that AMF have a positive net effect on soil carbon storage, via all four pathways of influence. Under what conditions will it then be most important for ecologists to study AMF influences on soil carbon storage? Clearly, a mechanism or organism group is most critical to study if it becomes limiting to the ecosystem process of interest (O’Neill et al. 1991). While it will still be important to study mycorrhizae under Ônon-limitingÕ conditions in order to understand mechanisms, and to define their maximum functional capacities, the question becomes: what conditions may render AMF limiting to carbon storage? Disturbances, such as tillage or other forms of soil disruption (e.g. by mining, stock-piling, compaction, etc.), have been indicated as a negative influence on AMF biomass in soil (e.g. Kabir et al. 1997). Toxic compounds also limit AMF biomass, as do certain conditions of nutrient enrichment, particularly those affecting ambient soil N : P ratio (Treseder & Allen 2002; Johnson et al. 2003b); in the latter case largely as a consequence of decreased plant C allocation to the symbiont. Limited AMF biomass may translate more directly into function in the context of soil aggregation, but abundance of AMF in the field does not straightforwardly translate into other functions. However, a more important question here is: are the effects of such treatments and disturbances on AMF more important than

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the effects on ecosystem components other than AMF? In other words, are AMF more severely affected by certain disturbances compared with other key biota/processes involved in soil C storage? Species losses of AMF, such as induced by disturbances, have consequences for NPP (e.g. van der Heijden et al. 1998), but what level of disturbance is required to lower AMF species richness beyond a threshold level where function is impaired; and what relative effect would the severity of disturbance required to achieve this reduction have on other processes? I believe these are critical questions to address in mycorrhizal and ecosystem ecology. Another useful conceptual framework for addressing the question of relative importance of AMF in soil C storage may be given by ecosystem state factors; these are: time, parent material, potential biota, topography, and climate (Chapin et al. 2002). Not all ecosystems in state factor ÔspaceÕ will be occupied chiefly by AMF, as other mycorrhizal types become dominant with increasing latitude or altitude (Read 1991). Hence, a first answer is to focus on ecosystems in which AMF form the dominant mycorrhizal association (e.g. grasslands, many tropical forests). However, when these state factors are examined individually, it becomes clear that AMF research has not been aimed at addressing questions at this scale; hence no conclusive generalizations can emerge. However, important studies are beginning to become available. For example, Johnson et al. (2003b) examined N fertilization effects on AMF over a wide range of grasslands in North America. Reanalyzing data from this paper (control values only, Kellogg Agricultural site excluded), there is a correlation (r2 ¼ 0.97; P ¼ 0.01; n ¼ 4) of precipitation (mm year)1) with AMF extraradical hyphal lengths (cm g)1 soil). This suggests that larger patterns in state factors, e.g. climate, may emerge as important drivers of AMF biomass, independent of a plethora of other potential controllers (like host plants, nutrients). This is a potentially fruitful area for research in mycorrhizal and ecosystem ecology; patterns like this could be useful in framing conditions under which AMF are most important in key processes of carbon storage, such as soil aggregation. THE TOOL BOX FOR MYCORRHIZAL RESEARCH AT THE ECOSYSTEM SCALE

In this section, I point out key problem areas with measuring aspects of AMF at the ecosystem scale, and I introduce two promising, novel experimental designs that can be used to enhance our ability to study AMF in an ecosystem context. When experimenting with mycorrhizae in general it is useful to consider a combination of approaches, some of which maximize experimental control and others that provide a maximum of realism.

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Problems with studying mycorrhizae at the ecosystem scale

There are a number of difficulties in quantifying AMF contributions to ecosystem processes. Part of the reason why there are large gaps in this knowledge is that certain processes appear to have rarely ever been measured in the first place, e.g. leaching of nutrients and organic matter, etc. This could be alleviated by a shift in research focus. Other problems, some of which are highlighted below, are more difficult to address. Problems with scaling up from pot studies It is often difficult to scale up from individual host level responses to higher levels of biological organization because of certain properties ÔemergingÕ only at the higher level (e.g. leaf-level processes and canopy-level controls). For mycorrhizae this problem is particularly serious, since experiments in pots and greenhouses are mostly carried out with a subset of culturable AMF isolates that perform well under the chosen conditions, and typically with a disturbed mycelial network. Other problems include nonrepresentative growth substrates, reconstruction of other soil biota in the experimental units, or ecologically irrelevant plant–AMF species combinations (reviewed in Read 2002). Additionally, in the field AMF and plant communities likely form common mycelial networks (Simard et al. 2002; Booth 2004; van der Heijden 2004); these networks, providing linkages between roots of different plant species, representing pathways of nutrient exchange, and meditating competitive interactions among plants, would not be represented in individual host scale studies. Inability to specifically eliminate AMF in the field (or mesocosms) The inability to specifically eliminate or inhibit AMF fungi from a soil or ecosystem (combined with the ubiquity and abundance of these fungi) lies at the heart of the difficulties of experimenting with AMF at the ecosystem scale. Larger scale, i.e. field-plot size reductions of AMF are currently only feasible with the application of nonAMF specific fungicides, such as benomyl. Non-target effects of such fungicides may impact other soil biota (e.g. other soil fungi) and processes. Smith et al. (2000) and Hartnett & Wilson (2002) defend the use of benomyl, stating that it is possible to control for non-target effects. It is also worth pointing out that the alternative approaches (albeit not suitable for field experimentation) of sterilizing field soil (by a variety of means) and reinoculation with a subset of the AMF community to selected experimental units are also confounded with nontarget effects.

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Shortage of response variables The most commonly measured response variable in mycorrhizal research, percent root colonization, is illmatched to answering questions at the ecosystem scale, since it neither represents a pool or a flux (it is essentially a measure of the relative growth of fungus and root; Allen 1991). Functional measures are often not correlated with percent root colonization (Smith & Read 1997), in part due to the fact that life history strategies among AMF species/ isolates differ significantly (Hart & Reader 2002). Hyphal lengths, which are much more difficult to adequately quantify (Miller et al. 1995), are an additional representation of AMF biomass, but also do not always directly relate to a process rate (with the possible exception of soil aggregation; Miller & Jastrow 2000). Other ÔmarkersÕ for AMF biomass may also not be universally applicable to field soils, as opposed to controlled environment studies, such as phospholipid or neutral fatty acid markers (e.g. the fatty acid 16:1x5: Olsson et al. 1995; van Aarle & Olsson 2003), or ergosterol (Hart & Reader 2002, 2003; Olsson et al. 2003), because they occur in other soil biota as well, or their production is also subject to physiological conditions, or both. GRSP is likely not directly useful in this context due to its long residence time (Rillig 2004), but certain fractions of this pool may prove valuable as indicators of AMF biomass inside the root and in the soil (Lovelock et al. 2004b). Isotopic tracer methods, applied more frequently to ectomycorrhizal systems than to AMF, may prove to become valuable tools for tracing carbon fluxes through AMF biomass in soil (e.g. Johnson et al. 2002; Staddon et al. 2003; Staddon 2004). The inability to adequately quantify AMF in most instances (both inside and outside of roots) may represent an impediment to integrating AMF into process level Ôpool and fluxÕ models. Novel and emerging experimental designs

What are recent developments that can aid in bridging the interface between mycorrhizal research and ecosystem ecology? In the following I highlight two novel experimental approaches (rotated in-growth cores and use of nonmycorrhizal host mutants). Rotated in-growth cores A very noteworthy innovation is the rotated core design developed by Johnson et al. (2001, 2002). It exploits the obligately biotrophic nature of AMF and their dependence, as a consequence, on a non-interrupted link with the host plant for carbon supply. In the elegantly simple design used by Johnson and co-workers, these hyphal links with the host plant are severed by rotating a core containing the experimental soil on a regular basis (while a non-rotated set of control cores permits hyphal re-colonization). The

advantage of this method is clearly that it can be applied in the field, where effects on ecosystem processes can be studied under conditions where carbon supply to the AMF mycelium has essentially been Ôswitched offÕ. This design likely avoids problems associated with non-target effects of toxic compounds, such as benomyl. However, the design somewhat limits the volume of soil to be examined, since the cores are relatively small in diameter, and since mycelium effects, in the absence of roots, may be overestimated. Additionally, the design is not completely disturbance-free, since cores are introduced into soils. Nevertheless, this design, not least due to its simplicity, will open the door to a number of studies aimed at understanding the contribution of AMF mycelium to process rates and organism interactions in the field. Use of non-mycorrhizal host mutants The increasing availability of colonization-defective AMF (Myc)) plant mutants (reviewed by Petersen & Guinel 2000), derived from the study of plant–AMF recognition processes, may present novel opportunities for the study of AMF contributions to ecosystems processes. While these mutants will not be practical for addressing problems at the stand/watershed scale itself, experimental approaches in mesocosms could be used to test relative strength and elucidate mechanistic pathways of mycorrhizal contributions to processes such as nutrient cycling. The clear advantage of this approach is that soils can be studied noninvasively, since AMF populations do not need to be eliminated (using fungicides or by heat, irradiation). This will hence be an approach useful for exploring the pathway of AMF influence on ecosystem processes via alteration of soil microbial communities (Fig. 1), since other soil biota will be minimally impacted by this experimental design. Myc) mutants have mostly been available for leguminous plant species (e.g. Lotus, Medicago, Pisum), which also are also host for rhizobial microorganisms. These non-AMF interactions could be a confounding factor in isolating AMF contributions to process rates. However, the recent identification of Myc) mutants in tomato (Barker et al. 1998; David-Schwartz et al. 2001, 2003), a non-legume, has opened up exciting possibilities of using these mutants as model systems to study ecosystem processes. Limitations of this approach include restriction to plant hosts for which suitable Myc) mutants are available, constraint to mostly a mesocosm scale of investigation, and potential non-target effects of mutants. In terms of non-target effects, studies to date have not found any deleterious effect(s) associated with the Myc) phenotype compared to the wildtype phenotype. For example, comparison of phenotypic characters like rate of growth, efficiency of elemental uptake, susceptibility to infection by non-AMF species etc., of the pmi tomato mutants, did not reveal any difference when compared with Ó2004 Blackwell Publishing Ltd/CNRS

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non-mutagenized wildtype plants (David-Schwartz et al. 2001). This observation could be best explained by the fact that evolutionary the Myc) phenotype in the host is a highly recessive trait. Any induced defect to the gene(s) controlling AMF signaling/colonization thus does not lead to any measurable phenotypic change(s). In other words, interfering with host perception of AMF does not lead to measurable losses of gene function; nevertheless, furthers comparison of the mutant and wildtype could solidify the usefulness of this approach for addressing the functional ecology of AMF. CONCLUSIONS

One goal of this overview is to highlight the pervasive influence AMF on ecosystem processes via a number of different mechanisms; another goal is to point out areas in need of further work. There are a number of impediments to progress in the endeavor to incorporate AMF into ecosystem processes and models. Shifts in research focus are a solution to some issues, but others require the creative development of new experimental approaches and the systematic improvement of currently available AMF-related response variables that are of relevance to the ecosystem scale. The issues brought up in this review are not only of purely academic interest, but may also have applied relevance. For example, the role of AMF in ecosystem processes may actually be clearest in severely disturbed ecosystems in need of restoration (Allen 1991), and clearly extends beyond interactions at the individual plant scale that often tend to be the focus. In fact under conditions of disturbance (e.g. nitrogen deposition, pollution, CO2 exposure, tillage, deforestation, invasive plant species) AMF may become significantly limiting to ecosystem processes (for example through AMF species losses); under those conditions ecosystem ecologists may profit most from knowing about AMF and incorporating their influence into empirical research and models. ACKNOWLEDGEMENTS

I thank the National Science Foundation and the US Department of Agriculture for funding during the writing of this review. Thanks to Dr Vijay Gadkar for help with the non-mycorrhizal mutant section, and three reviewers and the editor for helpful comments that improved the paper. REFERENCES van Aarle, I.M. & Olsson, P.A. (2003). Fungal lipid accumulation and development of mycelial structures by two arbuscular mycorrhizal fungi. Appl. Environ. Microbiol., 69, 6762–6767.

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Allen, M.F. (1991). The Ecology of Mycorrhizae. Cambridge University Press, Cambridge, UK. Allen, M.F. (ed.) (1992). Mycorrhizal Functioning: An Integrative Plant– Fungal Process. Chapman & Hall, New York. Allen, M.F., Clouse, S.D., Weinbaum, B.S., Jeakins, S.L., Friese, C.F. & Allen, E.B. (1992). Mycorrhizae and the integration of scales: from molecules to ecosystems. In: Mycorrhizal Functioning (ed. Allen, M.F.). Chapman & Hall, Inc., New York, pp. 488– 515. Amora-Lazcano, R., Vazquez, M.M. & Azcon, R. (1998). Response of nitrogen-transforming microorganisms to arbuscular mycorrhizal fungi. Biol. Fert. Soils, 27, 65–70. Andrade, G., Mihara, K.L., Linderman, R.G. & Bethlenfalvay, G.J. (1997). Bacteria from rhizosphere and hyphosphere of different arbuscular mycorrhizal fungi. Plant Soil, 192, 71–79. Auge´, R.M. (2001). Water relations, drought and vesicular arbuscular mycorrhizal symbiosis. Mycorrhiza, 11, 3–42. Barea, J.M., Azcon, R. & Azcon-Aguilar, C. (2002). Mycorrhizosphere interactions to improve plant fitness and soil quality. Antonie van Leeuwenhoek, 81, 343–351. Barker, S.J., Stummer, B., Gao, L.L., Dispain, I., O’Connor, P.J. & Smith, S.E. (1998). A mutant in Lycopersicon esculentum Mill. with highly reduced VA mycorrhizal colonization: isolation and preliminary characterization. Plant J., 15, 791–797. Bever, J.D., Morton, J.B., Antonovics, J. & Schultz, P.A. (1996). Host-dependent sporulation and species diversity of arbuscular mycorrhizal fungi in a mown grassland. J. Ecol., 84, 71–82. Bezzate, S., Aymerich, S., Chambert, R., Czarnes, S., Berge, O. & Heulin, T. (2000). Disruption of the Paenibacillus polymyxa levansucare gene impairs its ability to aggregate soil in the wheat rhizosphere. Env. Microbiol., 2, 333–342. Bianciotto, V., Bandi, C., Minerdi, D., Sironi, M., Tichy, H.V. & Bonfante, P. (1996). An obligately endosymbiotic mycorrhizal fungus itself harbors obligately intracellular bacteria. Appl. Environ. Microbiol., 62, 3005–3010. Booth, M.G. (2004). Mycorrhizal networks mediate overstorey– understorey competition in a temperate forest. Ecol. Lett., 7, 538–546. Borowicz, V. (1997). A fungal root symbiont modifies plant resistance to an insect herbivore. Oecologia, 112, 534–542. Brady, N.C. & Weil, R.R. (1999). The Nature and Properties of Soils, 12th edn. Prentice Hall, Upper Saddle Rive, NJ. Budi, S.W., van Tuinen, D., Martinotti, G. & Gianinazzi, S. (1999). Isolation from the Sorghum bicolor mycorrhizosphere of a bacterium compatible with arbuscular mycorrhiza development and antagonistic towards soil-borne fungal pathogens. Appl. Environ. Microbiol., 65, 5148–5150. Chapin, F.S. (1980). The mineral nutrition of wild plant. Annu. Rev. Ecol. Syst., 11, 233–260. Chapin, F.S., Walker, B.H., Hobbs, R.J., Hooper, D.U., Lawton, J.H., Sala, O.E. et al. (1997). Biotic control over the functioning of ecosystems. Science, 277, 500–504. Chapin, F.S., Matson, P.A. & Mooney, H.A. (2002). Principles of Terrestrial Ecosystem Ecology. Springer Verlag, New York. Cornelissen, J.H.C., Aerts, R., Cerabolini, B., Werger, M.J.A. & van der Heijden, M.G.A. (2001). Carbon cycling traits of plant species are linked with mycorrhizal strategy. Oecologia, 129, 611– 619. David-Schwartz, R., Badani, H., Wininger, S., Levy, A.A., Galili, G. & Kapulnik, Y. (2001). Identification of a novel genetically

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controlled step in mycorrhizal colonization: plant resistance to infection by fungal spores but not to extraradical hyphae. Plant J., 27, 561–569. David-Schwartz, R., Gadkar, V., Wininger, S., Bendov, R., Galili, G., Levy, A.A. et al. (2003). Isolation of a pre-mycorrhizal infection (pmi 2) mutant of Tomato, resistant to Arbuscular Mycorrhizal Fungal Colonization. Mol. Plant Microbe Interact., 16, 382–388. Diaz-Zorita, M., Perfect, E. & Grove, J.H. (2002). Disruptive methods for assessing soil structure. Soil Tillage Res., 64, 3–22. Douds, D.D., Johnson, C.R. & Koch, K.E. (1988). Carbon cost of the fungal symbiont relative to net leaf P accumulation in a split-root VA mycorrhizal symbiosis. Plant Physiol., 86, 491– 496. Egerton-Warburton, L.M. & Allen, E.B. (2000). Shifts in arbuscular mycorrhizal fungal communities along an anthropogenic nitrogen deposition gradient. Ecol. Appl., 10, 484–496. Eviner, V.T. & Chapin, F.S. (2003). Functional matrix: a conceptual framework for predicting multiple plant effects on ecosystem processes. Annu. Rev. Ecol. Evol. Syst., 34, 455–485. Filion, M., St-Arnaud, M. & Fortin, J.A. (1999). Direct interaction between the arbuscular mycorrhizal fungus Glomus intraradices and different rhizosphere micro-organisms. New Phytol., 141, 525–533. Fitter, A.H. (1985). Functioning of vesicular-arbuscular mycorrhizas under field conditions. New Phytol., 99, 257–265. Fitter, A.H., Heinemeyer, A. & Staddon, P.L. (2000). The impact of elevated CO2 and global climate change on arbuscular mycorrhizas: a mycocentric approach. New Phytol., 147, 179– 187. Friese, C.F. & Allen, M.F. (1991). The spread of VA mycorrhizal fungal hyphae in the soil: inoculum types and external hyphal architecture. Mycologia, 83, 409–418. Gange, A.C. (2001). Species-specific responses of a root- and shoot-feeding insect to arbuscular mycorrhizal colonization of its host plant. New Phytol., 150, 611–618. Gange, A.C. & West, H.M. (1994). Interactions between arbuscular-mycorrhizal fungi and foliar-feeding insects in Plantago lanceolata L. New Phytol., 128, 79–87. Gange, A.C., Brown, V.K. & Sinclair, G.S. (1993). Vesiculararbuscular mycorrhizal fungi: a determinant of plant community structure in early succession. Functional Ecology, 7, 616–622. Garbaye, J. (1994). Helper bacteria: a new dimension to the mycorrhizal symbiosis. New Phytol., 128, 197–210. Goverde, M., van der Heijden, M.G.A. & Wiemken, A. (2000). Arbuscular mycorrhizal fungi influence life history traits of a lepidopteran herbivore. Oecologia, 125, 362–369. Graham, J.H. (2001). What do root pathogens see in mycorrhizas? New Phytol., 149, 357–359. Griffiths, B.S., Ritz, K., Bardgett, R.D., Cook, R., Christensen, S., Ekelund, F. 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. Grime, J.P., Mackey, J.M., Miller, S.H. & Read, D.J. (1987). Floristic diversity in a model system using experimental microcosm. Nature, 328, 420–422. Hamel, C. (1996). Prospects and problems pertaining to the management of arbuscular mycorrhizae in agriculture. Agric. Ecosyst. Environ., 60, 197–210.

Hart, M.M. & Reader, R.J. (2002). Taxonomic basis for variation in the colonization strategy of arbuscular mycorrhizal fungi. New Phytol., 153, 335–344. Hart, M.M. & Reader, R.J. (2003). Ergosterol and mycorrhizal fungi, the way forward. New Phytol., 159, 536–537. Hart, M.M., Reader, R.J. & Klironomos, J.N. (2001). Life-history strategies of arbuscular mycorrhizal fungi in relation to their successional dynamics. Mycologia, 93, 1186–1194. Hartnett, D.C. & Wilson, G.W.T. (1999). Mycorrhizae influence plant community structure and diversity in tallgrass praire. Ecology, 80, 1187–1195. Hartnett, D.C. & Wilson, G.W.T. (2002). The role of mycorrhizas in plant community structure and dynamics: lessons from grasslands. Plant Soil, 244, 319–331. van der Heijden, M.G.A. (2002). Arbuscular mycorrhizal fungi as a determinant of plant diversity: in search of underlying mechanisms and general principles. In: Mycorrhizal Ecology (eds van der Heijden, M.G.A. & Sanders, I.), Ecological Studies, Vol. 157. Springer-Verlag, Berlin, pp. 243–265. van der Heijden, M.G.A. (2004). Arbuscular mycorrhizal fungi as support systems for seedling establishment in grassland. Ecol. Lett., 7, 293–303. van der Heijden, M.G.A. & Sanders, I.R. (eds) (2002). Mycorrhizal Ecology. Ecological Studies, Vol. 157. Springer-Verlag, Berlin. van der Heijden, M.G.A., Klironomos, J.N., Ursic, M., Moutoglis, P., Streitwolf-Engel, R., Boller, T. et al. (1998). Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature, 396, 69–72. Hildebrandt, U., Janetta, K. & Bothe, H. (2002). Towards growth of arbuscular mycorrhizal fungi independent of a plant host. Appl. Env. Microbiol., 68, 1919–1924. Hobbie, S.E. (1992). Effects of plant species on nutrient cycling. Trends Ecol. Evol., 7, 336–339. Hodge, A. (2000). Microbial ecology of the arbuscular mycorrhiza. FEMS Microbiol. Ecol., 32, 91–96. Hodge, A. (2001). Arbuscular mycorrhizal fungi influence decomposition of, but not plant nutrient capture from, glycine patches in soil. New Phytol., 151, 725–734. Hodge, A., Campbell, C.D. & Fitter, A.H. (2001). An arbuscular mycorrhizal fungus accelerates decomposition and acquires nitrogen directly from organic material. Nature, 413, 297–299. Ho¨gberg, M.N. & Ho¨gberg, P. (2002). Extramatrical ectomycorrhizal mycelium contributes one-third of microbial biomass and produces, together with associated roots, half the dissolved organic carbon in a forest soil. New Phytol., 154, 791– 795. Holben, W.E., Feris, K.P., Kettunen, A. & Apajalahti, J.H.A. (2004). GC fractionation enhances microbial community diversity assessment and detection of minority populations of bacteria by denaturing gradient gel electrophoresis. Appl. Environ. Microbiol., 70, 2263–2270. Hooper, D.U. & Vitousek, P.M. (1998). Effects of plant composition and diversity on nutrient cycling. Ecol. Monogr., 68, 121– 149. Hunt, H.W., Coleman, D.C., Ingham, E.R., Ingham, R.E., Elliott, E.T., Moore, J.C. et al. (1987). The detrital food web in a shortgrass prairie. Biol. Fert. Soils, 3, 57–68. Jakobsen, I., Smith, S.E. & Smith, F.A. (2002). Function and diversity of arbuscular mycorrhizae in carbon and mineral nutrition. In: Mycorrhizal Ecology (eds van der Heijden, M.G.A. &

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752 M. C. Rillig

Sanders, I.), Ecological Studies, Vol. 157. Springer-Verlag, Berlin, pp. 75–92. Jansa, J., Mozafar, A., Kuhn, G., Anken, T., Ruh, R., Sanders, I.R. et al. (2003). Soil tillage affects the community structure of mycorrhizal fungi in maize roots. Ecol. Appl., 13, 1164–1176. Johansson, J.F., Paul, L.R. & Finlay, R.D. (2004). Microbial interactions in the mycorrhizosphere and their significance for sustainable agriculture. FEMS Microbiol. Ecol., 48, 1–13. Johnson, N.C., Graham, J.H. & Smith, F.A. (1997). Functioning of mycorrhizal associations along the mutualism-parasitism continuum. New Phytol., 135, 575–585. Johnson, D., Leake, J.R. & Read, D.J. (2001). Novel in growth core system enables functional studies of grassland mycorrhizal mycelial networks. New Phytol., 152, 555–562. Johnson, D., Leake, J.R., Ostle, N., Ineson, P. & Read, D.J. (2002). In situ 13CO2 pulse-labelling of upland grassland demonstrates a rapid pathway of carbon flux from arbuscular mycorrhizal mycelia to the soil. New Phytol., 153, 327–334. Johnson, D., Booth, R.E., Whiteley, A.S., Bailey, M.J., Read, D.J., Grime, J.P. et al. (2003). Plant community composition affects the biomass, activity and diversity of microorganisms in limestone grassland soil. Europ. J. Soil Sc., 54, 671–677. Johnson, N.C., Wolf, J. & Koch, G.W. (2003a). Interactions among mycorrhizae, atmospheric CO2 and soil N impact plant community composition. Ecology Lett., 6, 532–540. Johnson, N.C., Rowland, D.L., Corkidi, L., Egerton-Warburton, L.M. & Allen, E.B. (2003b). Nitrogen enrichment alters mycorrhizal allocation at five mesic to semiarid grasslands. Ecology, 84, 1895–1908. Johnson, D., Vandenkoornhuyse, P.J., Leake, J.R., Gilbert, L., Booth, R.E., Grime, J.P. et al. (2004). Plant communities affect arbuscular mycorrhizal fungal diversity and community composition in grassland microcosms. New Phytol., 161, 503–515. Kabir, Z., O’Halloran, I.P., Fyles, J.W. & Hamel, C. (1997). Seasonal changes of arbuscular mycorrhizal fungi as affected by tillage practices and fertilization: Hyphal density and mycorrhizal root colonization. Plant Soil, 192, 285–293. Kalbitz, K., Solinger, S., Park, J.H., Michalzik, B. & Matzner, E. (2000). Controls on the dynamics of dissolved organic matter in soils: a review. Soil Sci., 165, 277–304. Kapulnik, Y. & Douds, D.D. (eds) (2000). Arbuscular Mycorrhizas: Physiology and Function. Kluwer Academic Publishers, Dordrecht, The Netherlands. Kent, A.D. & Triplett, E.W. (2002). Microbial communities and their interactions in soil and rhizosphere ecosystems. Annu. Rev. Microbiol., 56, 211–236. Klironomos, J.N. (2000). Host specificity and functional diversity among arbuscular mycorrhizal fungi. In: Microbial Biosystems: New Frontiers. Proceedings of the 8th International Symposium of Microbial Ecology (eds Bell, C.R., Brylinski, M. & Johnson-Green, P.). Atlantic Canada Society for Microbial Ecology, Halifax, pp. 845– 851. Klironomos, J.N. (2003). Variation in plant response to native and exotic arbuscular mycorrhizal fungi. Ecology, 84, 2292–2301. Klironomos, J.N., McCune, J., Hart, M. & Neville, J. (2000). The influence of arbuscular mycorrhizae on the relationship between plant diversity and productivity. Ecol. Lett., 3, 137–141. Knops, J.M., Bradley, K.L. & Wedin, D.A. (2002). Mechanisms of plant species impacts on ecosystem nitrogen cycling. Ecol. Lett., 5, 454–466.

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Koch, A.M., Kuhn, G., Fontanillas, P., Fumagalli, L., Goudet, J. & Sanders, I.R. (2004). High genetic variability and low local diversity in a population of arbuscular mycorrhizal fungi. Proc. Natl. Acad. Sci. USA, 101, 2369–2374. Koide, R.T. (1991). Nutrient supply, nutrient demand and plant response to mycorrhizal infection. New Phytol., 117, 365–386. Kucey, R.M.N. & Paul, E.A. (1982). Carbon flow, photosynthesis, and N2 fixation in mycorrhizal and nodulated faba beans (Vicia faba L.). Soil Biol. Biochem., 14, 407–412. Linderman, R.G. (1988). Mycorrhizal interactions with the rhizosphere microflora: the mycorrhizosphere effect. Phytopathol., 78, 366–371. Loreau, M., Naeem, S., Inchausti, P., Bengtsson, J., Grime, J.P., Hector, A. et al. (2001). Biodiversity and ecosystem functioning: current knowledge and future challenges. Science, 294, 804– 808. Louche-Tessandier, D., Samson, G., Hernandez-Sebastia, C., Chagvardieff, P. & Desjardins, Y. (1999). Importance of light and CO2 on the effects of endomycorrhizal colonization on growth and photosynthesis of potato plantlets (Solanum tuberosum) in an in vitro tripartite system. New Phytol., 142, 539– 550. Lovelock, C.E., Wright, S.F., Clark, D.A. & Ruess, R.W. (2004a). Soil stocks of glomalin produced by arbuscular mycorrhizal fungi across a tropical rain forest landscape. J. Ecol., 92, 278– 287. Lovelock, C.E., Wright, S.F. & Nichols, K.A. (2004b). Using glomalin as an indicator for arbuscular mycorrhizal hyphal growth: an example from a tropical rain forest soil. Soil Biol. Biochem., 36, 1009–1012. Mansfeld-Giese, K., Larsen, J. & Bodker, L. (2002). Bacterial populations associated with mycelium of the arbuscular mycorrhizal fungus Glomus intraradices. FEMS Microbiol. Ecol., 41, 133–140. Marler, M.J., Zabinski, C.A. & Callaway, R.M. (1999). Mycorrhizae indirectly enhance competitive effects of an invasive forb on a native bunchgrass. Ecology, 80, 1180–1186. Marschner, H. (1995). Mineral Nutrition of Higher Plants, 2nd edn. Academic Press, London. Marschner, P. & Baumann, K. (2003). Changes in bacterial community structure induced by mycorrhizal colonisation in splitroot maize. Plant Soil, 251, 279–289. Meharg, A.A. & Cairney, J.W.G. (2000). Co-evolution of mycorrhizal symbionts and their hosts to metal-contaminated environments. Adv. Ecol. Res., 30, 70–102. Miller, R.M. & Jastrow, J.D. (1994). Vesicular-arbuscular mycorrhizae and biogeochemical cycling. In: Mycorrhizae and Plant Health (eds Pfleger, F.L. & Linderman, R.G.). APS Press, St. Paul, pp. 189–212. Miller, R.M. & Jastrow, J.D. (2000). Mycorrhizal fungi influence soil structure. In: Arbuscular Mycorrhizas: Molecular Biology and Physiology (eds Kapulnik, Y. & Douds, D.D.). Kluwer Academic, Dordrecht, The Netherlands, pp. 3–18. Miller, R.M. & Kling, M. (2000). The importance of integration and scale in the arbuscular mycorrhizal symbiosis. Plant Soil, 226, 295–309. Miller, R.M., Reinhardt, D.R. & Jastrow, J.D. (1995). External hyphal production of vesicular-arbuscular mycorrhizal fungi in pasture and tallgrass prairie communities. Oecologia, 103, 17–23.

AM fungi and terrestrial ecosystem processes 753

Miller, R.M., Miller, S.P., Jastrow, J.D. & Rivetta, C.B. (2002). Mycorrhizal mediated feedbacks influence net carbon gain and nutrient uptake in Andropogon gerardii. New Phytol., 155, 149–162. Mitchell, C.E. (2003). Trophic control of grassland production and biomass by pathogens. Ecol. Lett., 6, 147–155. Newsham, K.K., Fitter, A.H. & Watkinson, A.R. (1995). Arbuscular mycorrhiza protect an annual grass from root pathogenic fungi in the field. J. Ecol., 83, 991–1000. Niklaus, P.A., Alphei, J., Ebersberger, D., Kampichler, C., Kandeler, E. & Tscherko, D. (2003). Six years of in situ CO2 enrichment evoke changes in soil structure and biota of nutrientpoor grassland. Global Change Biol., 9, 585–600. O’Connor, P.J., Smith, S.E. & Smith, F.A. (2002). Arbuscular mycorrhizas influence plant diversity and community structure in a semiarid herbland. New Phytol., 154, 209–218. O’Neill, E.G., O’Neill, R.V. & Norby, R.J. (1991). Hierarchy theory as a guide to mycorrhizal research on large-scale problems. Environ. Pollut., 73, 271–284. Oehl, F., Sieverding, E., Ineichen, K., Ma¨der, P., Boller, T. & Wiemken, A. (2003). Impact of land use intensity on the species diversity of arbuscular mycorrhizal fungi in agroecosystems of central Europe. Appl. Environ. Microbiol., 69, 2816– 2824. Olsson, P.A., Ba˚a˚th, E., Jakobsen, I. & Soderstrom, B. (1995). The use of phospholipid and neutral lipid fatty acids to estimate biomass of arbuscular mycorrhizal fungi in soil. Mycol. Res., 99, 623–629. Olsson, P.A., Larsson, L., Bago, B., Wallander, H. & van Aarle, I.M. (2003). Ergosterol and fatty acids for biomass estimation of mycorrhizal fungi. New Phytol., 159, 7–10. Parton, W.J., Schimel, D.S., Cole, C.V. & Ojima, D.S. (1987). Analysis of factors controlling soil organic matter levels in Great Plains grasslands. Soil Sci. Soc. Am. J., 51, 1173–1179. Petersen, R.L. & Guinel, F.C. (2000). The use of plant mutants to study regulation of colonization by AM fungi. In: Arbuscular Mycorrhizas: Physiology and Function (eds Kapulnik, Y. & Douds, D.D.). Kluwer Academic Press, Dordrecht, The Netherlands, pp. 147–172. Pfisterer, A.B. & Schmid, B. (2002). Diversity-dependent production can decrease the stability of ecosystem functioning. Nature, 416, 84–86. Porazinska, D.L., Bardgett, R.D., Blaauw, M.B., Hunt, H., William, H.W., Parsons, A.N. et al. (2003). Relationships at the aboveground-belowground interface: Plants, soil biota, and soil processes. Ecol. Monogr., 73, 377–395. Pringle, A. & Bever, J.D. (2002). Divergent phenologies may facilitate the coexistence of arbuscular mycorrhizal fungi in a North Carolina grassland. Am. J. Bot., 89, 1439–1446. Querejeta, J.F., Egerton-Warburton, L.M. & Allen, M.F. (2003). Direct nocturnal water transfer from oaks to their mycorrhizal symbionts during severe soil drying. Oecologia, 134, 55–64. Read, D.J. (1991). Mycorrhizas in ecosystems. Experientia, 47, 376– 391. Read, D.J. (1999). The ecophysiology of mycorrhizal symbioses with special reference to impacts upon plant fitness. In: Physiological Plant Ecology (eds Press, M.C., Scholes, J.D. & Barker, M.G.), Blackwell Science, Oxford. Read, D.J. (2002). Towards ecological relevance – progress and pitfalls in the path towards an understanding of mycorrhizal

functions in nature. In: Mycorrhizal Ecology (eds van der Heijden, M.G.A. & Sanders, I.), Ecological Studies, Vol. 157. SpringerVerlag, Berlin, pp. 3–29. Read, D.J. & Perez-Moreno, J. (2003). Mycorrhizas and nutrient cycling in ecosystems – a journey towards relevance? New Phytol., 157. 475–492. Redecker, D., Kodner, R. & Graham, L.E. (2000). Glomalean fungi from the Ordovician. Science, 289, 1920–1921. Rillig, M.C. (2004). Arbuscular mycorrhizae, glomalin and soil aggregation. Can. J. Soil Sci., in press. Rillig, M.C. & Allen, M.F. (1999). What is the role of arbuscular mycorrhizal fungi in plant-to-ecosystem responses to elevated atmospheric CO2? Mycorrhiza, 9, 1–8. Rillig, M.C. & Steinberg, P.D. (2002). Glomalin production by an arbuscular mycorrhizal fungus: a mechanism of habitat modification. Soil Biol. Biochem., 34, 1371–1374. Rillig, M.C., Wright, S.F., Allen, M.F. & Field, C.B. (1999). Rise in carbon dioxide changes soil structure. Nature, 400, 628. Rillig, M.C., Wright, S.F., Nichols, K.A., Schmidt, W.F. & Torn, M.S. (2001). Large contribution of arbuscular mycorrhizal fungi to soil carbon pools in tropical forest soils. Plant Soil, 233, 167–177. Rillig, M.C., Treseder, K.K. & Allen, M.F. (2002). Global change and mycorrhizal fungi. In: Mycorrhizal Ecology (eds vander Heijden, M.G.A. & Sanders, I.), Ecological Studies, Vol. 157. Springer-Verlag, Berlin, pp. 135–160. Rillig, M.C., Ramsey, P.W., Morris, S. & Paul, E.A. (2003). Glomalin, an arbuscular-mycorrhizal fungal soil protein, responds to land-use change. Plant Soil, 253, 293–299. Scherer-Lorenzen, M., Palmborg, C., Prinz, A. & Schulze, E.D. (2003). The role of plant diversity and composition for nitrate leaching in grasslands. Ecology, 84, 1539–1552. Schu¨ßler, A., Schwarzott, D. & Walker, C. (2001). A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycol. Research, 105, 1413–1421. Simard, S.W., Jones, M.D. & Durall, D.M. (2002). Carbon and nutrient fluxes within and between mycorrhizal plants. In: Mycorrhizal Ecology (eds van der Heijden, M.G.A. & Sanders, I.), Ecological Studies, Vol. 157. Springer-Verlag, Berlin, pp. 33– 74. Six, J., Feller, C., Denef, K., Ogle, S.M., de Moraes, J.C. & Albrecht, A. (2002). Soil organic matter, biota and aggregation in temperate and tropical soils – effects of no-tillage. Agronomie, 22, 755–775. Smith, S.E. & Read, D.J. (1997). Mycorrhizal symbiosis, 2nd edn. Academic Press, New York. Smith, M.D., Hartnett, D.C. & Rice, C.W. (2000). Effects of longterm fungicide applications on microbial properties in tallgrass prairie soil. Soil Biol. Biochem., 32, 935–946. Staddon, P.L. (2004). Carbon isotopes in functional soil ecology. Trends Ecol Evol., 19, 148–154. Staddon, P.L., Heinemeyer, A. & Fitter, A.H. (2002). Mycorrhizas and global environmental change: research at different scales. Plant Soil, 244, 253–261. Staddon, P.L., Ramsey, C.B., Ostle, N., Ineson, P. & Fitter, A.H. (2003). Rapid turnover of hyphae of mycorrhizal fungi determined by AMS microanalysis of 14C. Science, 300, 1138– 1140. Stampe, E.D. & Daehler, C.C. (2003). Mycorrhizal species identity affects plant community structure and invasion: a microcosm study. Oikos, 100, 362–372.

Ó2004 Blackwell Publishing Ltd/CNRS

754 M. C. Rillig

Steinberg, P.D. & Rillig, M.C. (2003). Differential decomposition of arbuscular mycorrhizal fungal hyphae and glomalin. Soil Biol. Biochem., 35, 191–194. Streitwolf-Engel, R., Boller, T., Wiemkem, A. & Sanders, I.R. (1997). Clonal growth traits of two Prunella species are determined by co-occurring arbuscular mycorrhizal fungi from a calcareous grassland. J. Ecol., 85, 181–191. Tilman, D. & Downing, J.A. (1994). Biodiversity and stability in grasslands. Nature, 367, 363–365. Tilman, D., Wedin, D. & Knops, J. (1996). Productivity and sustainability influenced by biodiversity in grassland ecosystems. Nature, 379, 718–720. Tilman, D., Knops, J., Wedin, D., Reich, P., Ritchie, M. & Siemann, E. (1997). The influence of functional diversity and composition on ecosystem processes. Science, 277, 1300–1302. Tisdall, J.M. & Oades, J.M. (1982). Organic matter and water-stable aggregates in soils. J. Soil Sc., 33, 141–163. Treseder, K.K. & Allen, M.F. (2000). Mycorrhizal fungi have a potential role in soil carbon storage under elevated CO2 and nitrogen deposition. New Phytol., 147, 189–200. Treseder, K.K. & Allen, M.F. (2002). Direct nitrogen and phosphorus limitation of arbuscular mycorrhizal fungi: a model and field test. New Phytol., 155, 507–515. Urcelay, C. & Dı´az, S. (2003). The mycorrhizal dependence of subordinates determines the effect of arbuscular mycorrhizal fungi on plant diversity. Ecol. Lett., 6, 388–391. Vandenkoornhuyse, P., Ridgway, K.P., Watson, I.J., Fitter, A.H. & Young, J.P. (2003). Co-existing grass species have distinctive arbuscular mycorrhizal communities. Mol. Ecol., 12, 3085–3095.

Ó2004 Blackwell Publishing Ltd/CNRS

Varma, A. & Hock, B. (eds) (1999). Mycorrhiza: Structure, Function, Molecular Biology and Biotechnology. Springer Verlag, Berlin. Wang, G.M., Coleman, D.C., Freckman, D.W., Dyer, M.I., McNaughton, S.J., Acra, M.A. et al. (1989). Carbon partitioning patterns of mycorrhizal versus non-mycorrhizal plants: real-time dynamic measurements using 11CO2. New Phytol., 112, 489–493. Wardle, D.A. (2002). Communities and Ecosystems. Princeton University Press, Princeton. Wright, S.F. & Upadhyaya, A. (1996). Extraction of an abundant and unusual protein from soil and comparison with hyphal protein of arbuscular mycorrhizal fungi. Soil Sci., 161, 575–586. Wright, S.F. & Upadhyaya, A. (1998). A survey of soils for aggregate stability and glomalin, a glycoprotein produced by hyphae of arbuscular mycorrhizal fungi. Plant Soil, 198, 97– 107. Wright, D.P., Read, D.J. & Scholes, J.D. (1998). Mycorrhizal sink strength influences whole plant carbon balance of Trifolium repens L. Plant Cell Environ., 21, 881–891. Zhu, Y.G. & Miller, R.M. (2003). Carbon cycling by arbuscular mycorrhizal fungi in soil-plant systems. Trends Plant Sci., 8, 407– 409.

Editor, John Klironomos Manuscript received 30 March 2004 First decision made 5 May 2004 Manuscript accepted 14 May 2004

Arbuscular mycorrhizae and terrestrial ecosystem ...

exchange between the symbionts. Intraradical structures, such as arbuscules, vesicles (lipid storage structures), coils, and the hyphae growing within the root ...

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