Arbuscular mycorrhizae and terrestrial ecosystem processes

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 ‘pools and flux’ paradigm of ecosystem ecology); I finish with an assessment of the tools (experimental designs, response variables) available for studying mycorrhizae at the ecosystem scale.

[1]  M. Allen,et al.  Direct nocturnal water transfer from oaks to their mycorrhizal symbionts during severe soil drying , 2002, Oecologia.

[2]  J. Cairney,et al.  Co-evolution of Mycorrhizal Symbionts and their Hosts to Metal-contaminated Environments , 1999 .

[3]  E. Schulze,et al.  THE ROLE OF PLANT DIVERSITY AND COMPOSITION FOR NITRATE LEACHING IN GRASSLANDS , 2003 .

[4]  M. Rillig Arbuscular mycorrhizae, glomalin, and soil aggregation , 2004 .

[5]  D. Rowland,et al.  Nitrogen enrichment alters mycorrhizal allocation at five mesic to semiarid grasslands , 2003 .

[6]  R. Miller,et al.  Mycorrhizal Fungi Influence Soil Structure , 2000 .

[7]  D. van Tuinen,et al.  Isolation from the Sorghum bicolorMycorrhizosphere of a Bacterium Compatible with Arbuscular Mycorrhiza Development and Antagonistic towards Soilborne Fungal Pathogens , 1999, Applied and Environmental Microbiology.

[8]  D. Read Towards Ecological Relevance — Progress and Pitfalls in the Path Towards an Understanding of Mycorrhizal Functions in Nature , 2003 .

[9]  Melanie D. Jones,et al.  Carbon and Nutrient Fluxes Within and Between Mycorrhizal Plants , 2003 .

[10]  T. Boller,et al.  Clonal growth traits of two Prunella species are determined by co-occurring arbuscular mycorrhizal fungi from a calcareous grassland. , 1997 .

[11]  M. Allen Mycorrhizal functioning: an integrative plant-fungal process. , 1994 .

[12]  D. Read,et al.  Mycorrhizal sink strength influences whole plant carbon balance of Trifolium repens L , 1998 .

[13]  K. Treseder,et al.  Direct nitrogen and phosphorus limitation of arbuscular mycorrhizal fungi: a model and field test. , 2002, The New phytologist.

[14]  Daniel Schwarzott,et al.  A new fungal phylum, the Glomeromycota: phylogeny and evolution * * Dedicated to Manfred Kluge (Tech , 2001 .

[15]  E. Paul,et al.  Carbon flow, photosynthesis, and N2 fixation in mycorrhizal and nodulated faba beans (Vicia faba L.) , 1982 .

[16]  T. Anken,et al.  SOIL TILLAGE AFFECTS THE COMMUNITY STRUCTURE OF MYCORRHIZAL FUNGI IN MAIZE ROOTS , 2003 .

[17]  C. Lovelock,et al.  Using glomalin as an indicator for arbuscular mycorrhizal hyphal growth: an example from a tropical rain forest soil , 2004 .

[18]  M. Hart,et al.  Ergosterol and mycorrhizal fungi - the way forward. , 2003, The New phytologist.

[19]  J. Graham,et al.  Functioning of mycorrhizal associations along the mutualism–parasitism continuum* , 1997 .

[20]  C. Ramsey,et al.  Rapid Turnover of Hyphae of Mycorrhizal Fungi Determined by AMS Microanalysis of 14C , 2003, Science.

[21]  F. Chapin,et al.  Biotic Control over the Functioning of Ecosystems , 1997 .

[22]  C. R. Johnson,et al.  Carbon Cost of the Fungal Symbiont Relative to Net Leaf P Accumulation in a Split-Root VA Mycorrhizal Symbiosis. , 1988, Plant physiology.

[23]  W. Parton,et al.  Analysis of factors controlling soil organic matter levels in Great Plains grasslands , 1987 .

[24]  A. Varma,et al.  Mycorrhiza : structure, function, molecular biology, and biotechnology , 1996 .

[25]  D. Clark,et al.  Soil stocks of glomalin produced by arbuscular mycorrhizal fungi across a tropical rain forest landscape , 2004 .

[26]  I. Jakobsen,et al.  Function and Diversity of Arbuscular Mycorrhizae in Carbon and Mineral Nutrition , 2003 .

[27]  R V O'Neill,et al.  Hierarchy theory as a guide to mycorrhizal research on large-scale problems. , 1991, Environmental pollution.

[28]  S. Sørensen,et al.  Ecosystem response of pasture soil communities to fumigation-induced microbial diversity reductions: an examination of the biodiversity-ecosystem function relationship , 2000 .

[29]  V. Borowicz A fungal root symbiont modifies plant resistance to an insect herbivore , 1997, Oecologia.

[30]  P. Marschner,et al.  Changes in bacterial community structure induced by mycorrhizal colonisation in split-root maize , 2003, Plant and Soil.

[31]  C. Rice,et al.  Effects of long-term fungicide applications on microbial properties in tallgrass prairie soil , 2000 .

[32]  J. Knops,et al.  Mechanisms of plant species impacts on ecosystem nitrogen cycling , 2002 .

[33]  J. Tisdall,et al.  Organic matter and water‐stable aggregates in soils , 1982 .

[34]  S. Barker,et al.  A mutant in Lycopersicon esculentum Mill. with highly reduced VA mycorrhizal colonization: isolation and preliminary characterisation. , 1998, The Plant journal : for cell and molecular biology.

[35]  E. Bååth,et al.  The use of phospholipid and neutral lipid fatty-acids to estimate biomass of arbuscular mycorrhizal fungi in soil , 1995 .

[36]  D. Coleman,et al.  Carbon partitioning patterns of mycorrhizal versus non-mycorrhizal plants: real-time dynamic measurements using 11 CO2. , 1989, The New phytologist.

[37]  R. Miller,et al.  External hyphal production of vesicular-arbuscular mycorrhizal fungi in pasture and tallgrass prairie communities , 1995, Oecologia.

[38]  J. Bever,et al.  Divergent phenologies may facilitate the coexistence of arbuscular mycorrhizal fungi in a North Carolina grassland. , 2002, American journal of botany.

[39]  Ian R. Sanders,et al.  Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity , 1998, Nature.

[40]  A. Hodge Arbuscular mycorrhizal fungi influence decomposition of, but not plant nutrient capture from, glycine patches in soil. , 2001, The New phytologist.

[41]  R. Koide Nutrient supply, nutrient demand and plant response to mycorrhizal infection. , 1991, The New phytologist.

[42]  D. Read The ecophysiology of mycorrhizal symbioses with special reference to impacts upon plant fitness , 1999 .

[43]  D. Tilman,et al.  Productivity and sustainability influenced by biodiversity in grassland ecosystems , 1996, Nature.

[44]  V. Brown,et al.  Vesicular-Arbuscular Mycorrhizal Fungi: A Determinant of Plant Community Structure in Early Succession , 1993 .

[45]  M. V. D. van der Heijden,et al.  Arbuscular mycorrhizal fungi influence life history traits of a lepidopteran herbivore , 2000, Oecologia.

[46]  R. Peterson,et al.  The Use of Plant Mutants to Study Regulation of Colonization by AM Fungi , 2000 .

[47]  T. L. Lyon,et al.  The Nature and Properties of Soils , 1930 .

[48]  J. Fyles,et al.  Seasonal changes of arbuscular mycorrhizal fungi as affected by tillage practices and fertilization : Hyphal density and mycorrhizal root colonization , 1997, Plant and Soil.

[49]  J. P. Grime,et al.  Biodiversity and Ecosystem Functioning: Current Knowledge and Future Challenges , 2001, Science.

[50]  L. Larsson,et al.  Ergosterol and fatty acids for biomass estimation of mycorrhizal fungi. , 2003, The New phytologist.

[51]  Sally E. Smith,et al.  Arbuscular mycorrhizas influence plant diversity and community structure in a semiarid herbland , 2002 .

[52]  C. Mitchell Trophic control of grassland production and biomass by pathogens , 2003 .

[53]  P. Olsson,et al.  Fungal Lipid Accumulation and Development of Mycelial Structures by Two Arbuscular Mycorrhizal Fungi , 2003, Applied and Environmental Microbiology.

[54]  R. Miller,et al.  Carbon cycling by arbuscular mycorrhizal fungi in soil-plant systems. , 2003, Trends in plant science.

[55]  G. Galili,et al.  Identification of a novel genetically controlled step in mycorrhizal colonization: plant resistance to infection by fungal spores but not extra-radical hyphae. , 2001, The Plant journal : for cell and molecular biology.

[56]  S. Ogle,et al.  Soil organic matter, biota and aggregation in temperate and tropical soils - Effects of no-tillage , 2002 .

[57]  Alastair H. Fitter,et al.  Arbuscular Mycorrhiza Protect an Annual Grass from Root Pathogenic Fungi in the Field , 1995 .

[58]  H. Marschner Mineral Nutrition of Higher Plants , 1988 .

[59]  S. Hobbie Effects of plant species on nutrient cycling. , 1992, Trends in ecology & evolution.

[60]  J. Garbaye Tansley Review No. 76 Helper bacteria: a new dimension to the mycorrhizal symbiosis. , 1994, The New phytologist.

[61]  Klironomos,et al.  Host-specificity and functional diversity among arbuscular mycorrhizal fungi , 1999 .

[62]  B. Schmid,et al.  Diversity-dependent production can decrease the stability of ecosystem functioning , 2002, Nature.

[63]  J. P. Grime,et al.  FLORISTIC DIVERSITY IN A MODEL SYSTEM USING EXPERIMENTAL MICROCOSMA , 1988 .

[64]  M Díaz-Zorita Disruptive methods for assessing soil structure , 2002 .

[65]  Sally E Smith and David J Read Mycorrhizal Symbiosis 2nd ed , 1997 .

[66]  G. Bethlenfalvay,et al.  Bacteria from rhizosphere and hyphosphere soils of different arbuscular-mycorrhizal fungi , 1997, Plant and Soil.

[67]  R. Finlay,et al.  Microbial interactions in the mycorrhizosphere and their significance for sustainable agriculture. , 2004, FEMS microbiology ecology.

[68]  M. V. D. Heijden Arbuscular mycorrhizal fungi as support systems for seedling establishment in grassland , 2004 .

[69]  R. Augé Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis , 2001, Mycorrhiza.

[70]  R. Miller,et al.  The importance of integration and scale in the arbuscular mycorrhizal symbiosis , 2004, Plant and Soil.

[71]  C. Hamel Prospects and problems pertaining to the management of arbuscular mycorrhizae in agriculture , 1996 .

[72]  J. Barea,et al.  Mycorrhizosphere interactions to improve plant fitness and soil quality , 2002, Antonie van Leeuwenhoek.

[73]  W. Holben,et al.  GC Fractionation Enhances Microbial Community Diversity Assessment and Detection of Minority Populations of Bacteria by Denaturing Gradient Gel Electrophoresis , 2004, Applied and Environmental Microbiology.

[74]  E. Allen,et al.  SHIFTS IN ARBUSCULAR MYCORRHIZAL COMMUNITIES ALONG AN ANTHROPOGENIC NITROGEN DEPOSITION GRADIENT , 2000 .

[75]  S. Wright,et al.  EXTRACTION OF AN ABUNDANT AND UNUSUAL PROTEIN FROM SOIL AND COMPARISON WITH HYPHAL PROTEIN OF ARBUSCULAR MYCORRHIZAL FUNGI , 1996 .

[76]  J. Bever,et al.  Host-Dependent Sporulation and Species Diversity of Arbuscular Mycorrhizal Fungi in a Mown Grassland , 1996 .

[77]  D. Redecker,et al.  Glomalean fungi from the Ordovician. , 2000, Science.

[78]  M. Allen,et al.  Mycorrhizae and the integration of scales: from molecules to ecosystems , 1992 .

[79]  J. Larsen,et al.  Bacterial populations associated with mycelium of the arbuscular mycorrhizal fungus Glomus intraradices. , 2002, FEMS microbiology ecology.

[80]  J. Klironomos,et al.  VARIATION IN PLANT RESPONSE TO NATIVE AND EXOTIC ARBUSCULAR MYCORRHIZAL FUNGI , 2003 .

[81]  A. Hodge,et al.  An arbuscular mycorrhizal fungus accelerates decomposition and acquires nitrogen directly from organic material , 2001, Nature.

[82]  J. Pérez‐Moreno,et al.  Mycorrhizas and nutrient cycling in ecosystems - a journey towards relevance? , 2003, The New phytologist.

[83]  H. Bothe,et al.  Towards Growth of Arbuscular Mycorrhizal Fungi Independent of a Plant Host , 2002, Applied and Environmental Microbiology.

[84]  Michael G. Booth Mycorrhizal networks mediate overstorey‐understorey competition in a temperate forest , 2004 .

[85]  K. Treseder,et al.  Mycorrhizal fungi have a potential role in soil carbon storage under elevated CO2 and nitrogen deposition , 2000 .

[86]  M. St-Arnaud,et al.  Direct interaction between the arbuscular mycorrhizal fungus Glomus intraradices and different rhizosphere microorganisms , 1999 .

[87]  H. West,et al.  Interactions between arbuscular mycorrhizal fungi and foliar-feeding insects in Plantago lanceolata L. , 1994, The New phytologist.

[88]  J. P. Grime,et al.  Plant community composition affects the biomass, activity and diversity of microorganisms in limestone grassland soil , 2003 .

[89]  R. Miller,et al.  Mycorrhizal mediated feedbacks influence net carbon gain and nutrient uptake in Andropogon gerardii. , 2002, The New phytologist.

[90]  D. Hartnett,et al.  MYCORRHIZAE INFLUENCE PLANT COMMUNITY STRUCTURE AND DIVERSITY IN TALLGRASS PRAIRIE , 1999 .

[91]  F. Chapin,et al.  Principles of Terrestrial Ecosystem Ecology , 2002, Springer New York.

[92]  P. Reich,et al.  The Influence of Functional Diversity and Composition on Ecosystem Processes , 1997 .

[93]  M. Rillig,et al.  Glomalin, an arbuscular-mycorrhizal fungal soil protein, responds to land-use change , 2003, Plant and Soil.

[94]  F. S. Chapin,et al.  The Mineral Nutrition of Wild Plants , 1980 .

[95]  M. Hart,et al.  Life-history strategies of arbuscular mycorrhizal fungi in relation to their successional dynamics , 2001 .

[96]  C. Bandi,et al.  An obligately endosymbiotic mycorrhizal fungus itself harbors obligately intracellular bacteria , 1996, Applied and environmental microbiology.

[97]  James H Graham,et al.  What do root pathogens see in mycorrhizas? , 2001, The New phytologist.

[98]  C. Daehler,et al.  Mycorrhizal species identity affects plant community structure and invasion: a microcosm study , 2003 .

[99]  G. Galili,et al.  Isolation of a premycorrhizal infection (pmi2) mutant of tomato, resistant to arbuscular mycorrhizal fungal colonization. , 2003, Molecular plant-microbe interactions : MPMI.

[100]  Peter M. Vitousek,et al.  Effects of plant composition and diversity on nutrient cycling , 1998 .

[101]  K. Treseder,et al.  Global Change and Mycorrhizal Fungi , 2002 .

[102]  J. Goudet,et al.  High genetic variability and low local diversity in a population of arbuscular mycorrhizal fungi. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[103]  Mycorrhizas and global environmental change: research at different scales , 2002 .

[104]  A. Gange Species‐specific responses of a root‐ and shoot‐feeding insect to arbuscular mycorrhizal colonization of its host plant , 2001 .

[105]  H. W. Hunt,et al.  Relationships at the aboveground-belowground interface: plants, soil biota and soil processes , 2003 .

[106]  M. Rillig,et al.  Glomalin production by an arbuscular mycorrhizal fungus: a mechanism of habitat modification? , 2002 .

[107]  M. Hart,et al.  Taxonomic basis for variation in the colonization strategy of arbuscular mycorrhizal fungi , 2002 .

[108]  A. Kent,et al.  Microbial communities and their interactions in soil and rhizosphere ecosystems. , 2002, Annual review of microbiology.

[109]  J. Downing,et al.  Biodiversity and stability in grasslands , 1996, Nature.

[110]  Jenny L. McCune,et al.  The influence of arbuscular mycorrhizae on the relationship between plant diversity and productivity , 2000 .

[111]  I. Hiscock Communities and Ecosystems , 1970, The Yale Journal of Biology and Medicine.

[112]  G. Samson,et al.  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 , 1999 .

[113]  M. V. D. Heijden Arbuscular Mycorrhizal Fungi as a Determinant of Plant Diversity: in Search of Underlying Mechanisms and General Principles , 2002 .

[114]  J. P. Grime,et al.  Plant communities affect arbuscular mycorrhizal fungal diversity and community composition in grassland microcosms. , 2004, The New phytologist.

[115]  Y. Kapulnik,et al.  Arbuscular mycorrhizas : physiology and function , 2000 .

[116]  M. Rillig,et al.  Differential decomposition of arbuscular mycorrhizal fungal hyphae and glomalin , 2003 .

[117]  Hodge,et al.  Microbial ecology of the arbuscular mycorrhiza. , 2000, FEMS microbiology ecology.

[118]  D. Read,et al.  Novel in-growth core system enables functional studies of grassland mycorrhizal mycelial networks. , 2001, The New phytologist.

[119]  M. Torn,et al.  Large contribution of arbuscular mycorrhizal fungi to soil carbon pools in tropical forest soils , 2001, Plant and Soil.

[120]  J. C. Moore,et al.  The detrital food web in a shortgrass prairie , 1987, Biology and Fertility of Soils.

[121]  C. Field,et al.  Rise in carbon dioxide changes soil structure , 1999, Nature.

[122]  M. Rillig,et al.  What is the role of arbuscular mycorrhizal fungi in plant-to-ecosystem responses to Elevated atmospheric CO2? , 1999, Mycorrhiza.

[123]  T. Boller,et al.  Impact of Land Use Intensity on the Species Diversity of Arbuscular Mycorrhizal Fungi in Agroecosystems of Central Europe , 2003, Applied and Environmental Microbiology.

[124]  S. Wright,et al.  A survey of soils for aggregate stability and glomalin, a glycoprotein produced by hyphae of arbuscular mycorrhizal fungi , 2004, Plant and Soil.

[125]  R. Callaway,et al.  MYCORRHIZAE INDIRECTLY ENHANCE COMPETITIVE EFFECTS OF AN INVASIVE FORB ON A NATIVE BUNCHGRASS , 1999 .

[126]  A. Fitter FUNCTIONING OF VESICULAR–ARBUSCULAR MYCORRHIZAS UNDER FIELD CONDITIONS , 1985 .

[127]  P. Staddon Carbon isotopes in functional soil ecology. , 2004, Trends in ecology & evolution.

[128]  E. Kandeler,et al.  Six years of in situ CO2 enrichment evoke changes in soil structure and soil biota of nutrient‐poor grassland , 2003 .

[129]  Ji‐Hyung Park,et al.  Controls on the dynamics of dissolved organic matter in soils: a review. , 2000 .

[130]  D. Read,et al.  Mycorrhizas in ecosystems , 1991, Experientia.

[131]  F. Stuart Chapin,et al.  Functional Matrix: A Conceptual Framework for Predicting Multiple Plant Effects on Ecosystem Processes , 2003 .

[132]  J. Wolf,et al.  Interactions among mycorrhizae, atmospheric CO2 and soil N impact plant community composition , 2003 .

[133]  David Johnson,et al.  In situ13CO2 pulse-labelling of upland grassland demonstrates a rapid pathway of carbon flux from arbuscular mycorrhizal mycelia to the soil , 2002 .

[134]  S. Aymerich,et al.  Disruption of the Paenibacillus polymyxa levansucrase gene impairs its ability to aggregate soil in the wheat rhizosphere. , 2000, Environmental microbiology.

[135]  Michael F. Allen,et al.  The Spread of Va Mycorrhizal Fungal Hyphae in the Soil: Inoculum Types and External Hyphal Architecture , 1991 .

[136]  R. Linderman Mycorrhizal interactions with the rhizosphere microflora: the mycorrhizosphere effect , 1988 .

[137]  A. Heinemeyer,et al.  The impact of elevated CO2 and global climate change on arbuscular mycorrhizas: a mycocentric approach , 2000 .

[138]  A. Fitter,et al.  Co‐existing grass species have distinctive arbuscular mycorrhizal communities , 2003, Molecular ecology.

[139]  Sandra Díaz,et al.  The mycorrhizal dependence of subordinates determines the effect of arbuscular mycorrhizal fungi on plant diversity , 2003 .

[140]  P. Högberg,et al.  Extramatrical ectomycorrhizal mycelium contributes one-third of microbial biomass and produces, together with associated roots, half the dissolved organic carbon in a forest soil. , 2002, The New phytologist.