This file was created by scanning the printed publication. Errors identified by the software have been corrected; however, some errors may remain. RHIZOSPHERE BIOLOGY: ECOLOGICAL LINKAGES BETWEEN SOIL PROCESSES, PLANT GROWTH, AND COMMUNITY DYNAMICS Randy Molina Michael Amaranthus

ABSTRACT that roots of the same or dissimilar plants can be connected by commonly shared symbiotic root fungi, the mycorrhizal Productivity of the forest plant community results from fungi; carbon (sugars) and other nutrients can actually flow interactions of shoots and roots with the environment. One between connected plants (Read and others 1985). Increas­ of the more important and least understood biotic zones of ing attention has been focused on the food web dynamics of interaction is the soil immediately surrounding and influ­ soil organisms, particularly their relations to the vitality of enced by roots, known as the rhizosphere. Microorganisms highly visible aboveground organisms (Ingham and others and processes in the rhizosphere profoundly influence plant 1985). An increasingly sophisticated and knowledgeable growth through effects on uptake, storage, and cycling of public is becoming aware of these tight ecosystem linkages. nutrients, suppression ofpathogens, and development of Such heightened awareness and demand for sustaining soil structure. Rhizosphere organisms are affected by and total ecosystems requires that forest managers stay cur­ contribute to the successional dynamics offorest communi­ rent on the latest developments in the many disciplines ties. Protecting the functional biodiversity ofrhizosphere of forest research. organisms through proper management practices is essen­ Our previous research has concentrated on mycorrhizal tial to maintaining ecosystem health and resiliency. fungi of forest trees, with emphasis on selection ofbenefi­ cial fungus strains for inoculation of nursery seedlings. INTRODUCTION We tried to enhance seedling survival and growth on hard­ to-regenerate sites by tailoring root systems with fungi Today's forest management decisions integrate increas­ adapted to the planting site. In addition to successfully ingly complex and changing social, economic, and ecological developing this technology (see Castellano and Molina values. Foresters not only are concerned with the basic 1989), we encountered ecological concepts relevant to man­ silvicultural goals of harvesting and regeneration but also aging forest sites and protecting soil organisms. We found, seek to sustain long-term productivity of forest sites, pro­ for example, that the tremendous biological diversity of tect nontimber resources such as water and scenery, and mycorrhizal fungi represents a similarly wide range of maintain biodiversity. All this requires understanding of physiological diversity providing a wide range of benefits how forest ecosystems function. Today, forestry and forest to plants in diverse habitats. Different site disturbances sciences are shifting dramatically from basing decisions and patterns of reforestation affect the survival potential on how trees operate to a holistic integration of how all of mycorrhizal fungus propagules in the soil. Enhancement the parts of a forest work together, how they are linked of seedling performance by mycorrhizal inoculation was and interdependent. most successful on drought-stressed sites with low popula­ The study of soil biology also has shifted fundamentally. tion levels of residual mycorrhizal fungi. Such findings Over the last decade, research has shown the critical link­ allowed development of testable hypotheses on how forest age of soil microorganisms to forest productivity and com­ practices degrade the soil biological community in ways munity dynamics. Ecosystem studies quantified the tre­ requiring inoculation. Our major goal now is to achieve mendous energy invested by trees in fine root production better understanding of the natural forest processes that and organisms growing in the immediate vicinity of these maintain viable populations of soil microoganisms after roots, known as the rhizosphere. As much as 80 percent natural disturbance and thus contribute to forest recovery; of the photosynthate of trees is used to support fine roots that is, natural soil biological mechanisms of resiliency and associated microorganisms (Fogel and Hunt 1983; Vogt (see Perry and others 1987). and others 1982). Laboratory and field studies have shown The objectives of this paper are to (1) overview funda­ mental concepts in forest soil biology, including key organ­ isms and processes; (2) discuss rhizosphere ecology in the context of interactions and interdependencies of above­ Paper presented at the Symposium on Management and Productivity ground and belowground biotic communities; (3) emphasize of Westem-Montane Forest Soils, Boise, ID, April 10-12, 1990. Randy Molina is Research Botanist, Pacific Northwest Research Sta­ protection of the soil biological community through wise tion, Forest Service, U.S. Department of Agriculture, Corvallis, OR 97331; resource management; and (4) update forest managers Michael Amaranthus is Soil Scientist, Siskiyou National Forest, Forest Service, U.S. Department of Agriculture, Grants Pass, OR 97526. on research directions in forest soil biology.

51 THE RHIZOSPHERE OF FOREST Rhizosphere organisms receive nutrients primarily from root exudates, and nonrhizosphere organisms use organic PLANTS residues in varying stages of decomposition (Rambelli Productivity of plant communities results from interac­ 1973). The different microbial compositions of bulk and tions of shoots and roots with the environment. One of the rhizosphere soils reflect these nutritional modes. The more important and least understood biotic zones of inter­ rhizosphere microenvironment also differs strongly from action is the soil immediately surrounding and influenced that of the bulk soil. Organic substrates and compounds by roots-the "rhizosphere." Depending on site quality, of all kinds are more abundant in the rhizosphere than in forests can divert 50 to 80 percent or more of the net car­ bulk soil. This includes humic compounds, polysaccharides, bon fixed by photosynthesis to belowground processes hormones, chelators, and enzymes (Perry and others 1987). (Fogel and Hunt 1983; Vogt and others 1982). Although The supply of other nutrients such as N, P, Mn, and Fe much goes to root growth, a relatively high proportion may may limit plant growth because of intense utilization and be used to feed soil microorganisms and fuel processes in competition (Foster 1988). the rhizosphere. This is not energy lost from the plant. Rhizosphere organisms experience large fluctuations in These organisms and processes in the rhizosphere influ­ pH as different ions are removed from the soil by roots and ence plant growth positively by enhancing nutrient uptake, replaced by balancing ions. Similarly, rhizosphere organ­ storage, and cycling, moisture storage, pathogen suppres­ isms may experience very low water potentials as water is sion, development of soil structure, and protection against removed by high transpiration rates. High osmotic poten­ environmental extremes. The specialized rhizosphere tial can also occur from the accumulation of calcium at the microorganisms include mycorrhizal fungi, saprophytes, root surfaces. Local microaerophyllic or anaerobic condi­ microfauna, pathogens, and growth-promoting and delete­ tions can develop in the rhizosphere due to high respiration rious bacteria (see Curl and Truelove 1986; Linderman rates by roots and microorganisms (Foster and Bowen 1986 for more detail). 1982), further influencing microbial composition and pro­ Factors that influence rhizosphere organisms include cesses. Rhizosphere organisms can also be buffered from the age and kinds of plant, soil physical conditions, tem­ unfavorable environmental changes by gels and poly­ perature, moisture, interactions with other soil microbes, saccharides secreted by roots and microorganisms. and cultural practices (Katznelson 1965). Rhizosphere activities fluctuate in response to changes in plant, micro­ MYCORRHIZAE AND THE bial community, edaphic, and environmental factors. Unfortunately, except for mycorrhizal fungi offorest MYCORRHIZOSPHERE trees and nitrogen fIXation in forests, most of our knowl­ Mycorrhiza literally means "fungus root" and represents edge ofrhizosphere dynamics comes from agricultural soils the intimate association between the fine roots of plants and crop research. Forest soils and processes differ funda­ and specialized symbiotic fungi. Readers are referred mentally from agricultural soils; we are just beginning to to recent reviews of the tremendous body ofli terature on probe the complex interactions within the rhizospheres of this mutualistic symbiosis for greater detail (Castellano forest plants and their impacts on forest health and pro­ and Molina 1989; Harley and Smith 1983; Perry and others ductivity. The following sections discuss key rhizosphere 1987). We emphasize mycorrhizae in this section and oth­ organisms and processes and their importance at forest ers because most land plants depend on mycorrhizae for community and ecosystem levels. nutrient uptake, and mycorrhizae perform far-reaching ecosystem functions in our forests. RHIZOSPHERE VERSUS BULK SOIL Mycorrhizae come in several types and involve thousands offungus species. Understanding the overall variety of Biological activity and function is not distributed homo­ mycorrhizal types, differences between groups of plants geneously across the soil environment. Intense biological in their mycorrhizal association, and physiological and activity typically extends about 2 mm out from fine roots ecological differences among the fungi is key t.O under­ and differs significantly from that in the bulk soil in num­ standing their biotic diversity and impact on ecosystem bers, types, and functions of organisms. Fine roots maneu­ function and community development. Ectomycorrhizae, vering through the soil exude amino acids, carbohydrates, vesicular-arbuscular mycorrhizae (V AM), and ericaceous and other compounds that stimulate growth of bacteria, mycorrhizae prevail in temperate forests. actinomycetes, and fungi. These, in tum, produce com­ Ectomycorrhizae predominate in temperate forests pounds that repel or stimulate other soil organisms. The of the Pacific Northwest because species of the Pinaceae, microflora is a prime food for "grazer" herbivores such as Betulaceae, and Fagaceae all form this type. Ectomycor­ mites, nematodes, and springtails, which, in tum, fall prey rhizal fungi form an often colorful sheath or mantle around to carnivores such as centipedes and spiders. Saprophytes feeder roots and penetrate the root cortex to form the decay the dead remains of microbes and roots in the rhi­ "Hartig net," a zone of nutrient exchange between fungus zosphere and decompose complex organic molecules into and host (see figs. 1-5). These fungi also extensively colo­ basic components. Nutrients and waste released through nize the soil, often to form visible, persistent mats in the decomposition are captured and returned to the host plant upper soil and humus. Most fleshy mushrooms that fruit via mycorrhizal fungi. The fine roots of forest plants and on the forest floor as well as the hidden subterranean their associated mycorrhizal fungi form an often contiguous truffies are fruiting bodies of the ectomycorrhizal fungus network in the upper soil profile. This rooting zone is colonies in the soil. A walk through the woods during the essentially a rhizosphere zone in which the vast majority mushroom season reveals the abundance and diversity of of soil nutrients are recycled and retained. 52 these fungi; thousands of ectomycorrhizal fungus species modify root morphology; they ramify in fine roots to form associate with trees in the Pacific Northwest. specialized structures (arbuscules and vesicles). Although The VAM are also widespread in our forests but have they do not form the showy mycelia of the ectomycorrhizal received less attention because they primarily occur on fungi in the soil, they, too, extensively colonize the soil and understory species and herbaceous plants. They are typi­ bring in nutrients to the plants. The VAM fungi only num­ cal on cedars (Thuja, Chamaecyparis, and Libocedrus) and ber in the hundreds, and most can form mycorrhizae with redwoods (Sequoia and Sequoiadendron), however. Unlike a wide range of plant species. the ectomycorrhizal fungi, VAM fungi do not strikingly Ericaceous mycorrhizae, as the name implies, are formed exclusively with members of the Ericales; for example, Gaultheria, Rhododendron, and Vaccinium. Although this seems a narrow grouping, the Ericaceae are wide­ spread understory components in coastal and mountain forests. Similarly to VAM, the ericaceous mycorrhizal fungi ramify through the fine, hairlike rootlets, to form dense hyphal coils but not to modify the root structure as do ectomycorrhizal fungi. Relatively few fungus species form this type of mycorrhizae, but they seem to be wide­ spread in the soil. Benefits ofmycorrhizae to plants include enhanced up­ take of nutrients and water, protection against pathogens, improved resistance to drought, enlarged root systems, and tolerance of heavy metal. The uptake of immobile ions such as phosphorus, typically benefiting growth of hosts, is mostly due to the ability of the fungus hyphae to explore a soil volume for nutrients far beyond the capabilities of the roots. Ectomycorrhizal fungi also produce hormones that promote branching of feeder roots, increasing not only the absorbing root surface but also the contact and exchange zone between fungus and plant. A recent study (Read 1987) also shows an important role for nitrogen uptake Figure 1-Scanning electron micrograph of pine ectomycorrhiza showing the typically forked branching by mycorrhizal fungi, particularly from organic nitrogen pattern. Note the numerous hyphae radiating out from sources. For exam pIe, ericaceous mycorrhizal fungi can the fungus mantle. (Magnification =93x.) (Photo degrade protein as well as other organic nitrogen sources courtesy of Drs. H. B. Massicotte and R. L. Peterson, (Read 1987). Such an ability may be critically important University of Guelph, Ontario, Canada.) in organic substrates such as rotting logs or buried wood, common niches for ericaceous plants.

Figure 2-Scanning electron micrograph of a Figure 3-Scanning electron micrograph of an eucalypt ectomycorrhiza showing a pinnate branch­ ectomycorrhizal mantle showing the complex ing pattern and a well-developed mantle. (Magni­ development of interwoven hyphal strands and fication = 77x.) (Photo courtesy of Drs. H. B. individual hyphae. (Magnification = 1310x.) Massicotte and R. L. Peterson, University of (Photo courtesy of Drs. H. B. Massicotte and R. L. Guelph, Ontario, Canada.) Peterson, University of Guelph, Ontario, Canada.)

53 The plants pay for such benefits in photosynthate essence then, mycorrhizae extend rhizosphere to a zone shuttled to roots. Indeed, mycorrhizal fungi are strongly termed the "mycorrhizosphere" (Rambelli 1973). dependent on a continuous supply of plant sugars and Most plant benefits noted here were discovered in com­ other organic compounds such as vitamins. The fungus parisons of mycorrhizal with nonmycorrhizal seedlings. functions as a structure of the root system supported by We are only beginning to understand the role of mycor­ plant energy. The mycorrhizal fungi produce organic rhizal fungi and other rhizosphere organisms in forest exudates and undergo rapid turnover, thereby attracting community development and ecosystem function. other microorganisms that feed in the hyphal zone. In NITROGEN FIXATION Nitrogen is typically the most limiting nutrient in Pacific Northwest forests. Natural inputs of nitrogen through the process of nitrogen gas fixation are essential to maintain long-term forest productivity in much of the Western United States. Symbiotic nitrogen fixation can add substantial nitrogen continuously to Pacific Northwest forests (Wollum and Youngberg 1964). Common nodulated plants such as lupine, alder, and snowbrush (Lupinus, Alnus, and Ceano­ thus) species form a mutually beneficial relationship with certain bacteria or actinomycetes that convert atmospheric nitrogen into ammonium nitrogen (see fig. 6). This fixed nitrogen is released into the roots of host plants, thereby increasing nitrogen concentrations in living tissue (Tarrant and Trappe 1971). As nitrogen is returned to the soil by litterfall and washing ofleaves by rain, other species ben­ efit, such as commercially important conifer species. "Free-living" nitrogen fixation by bacteria living in close association with roots and mycorrhizae was first Figure 4-Transverse section through an suggested by Richards and Voigt (1964), and the phenom­ ectomycorrhiza of red alder. Note the well­ enon is now well established (Chartarpaul and Carlisle developed fungal sheath or mantle. (Magni­ 1983; Dawson 1983; Florence and Cook 1984; Li and Hung fication = 154x.) (Photo courtesy of Drs. H. B. 1987). Nitrogen-fixing bacteria were observed in close asso­ Massicotte and R. L. Peterson, University of ciation with the mycorrhizosphere of Pinus radiata D. Don Guelph, Ontario, Canada.) (Rambelli 1973). We have also found nitrogen-fixing bacte­ ria to associate with ectomycorrhizae of forest trees in the Pacific Northwest (Li and Hung 1987). Bacteria in the genera Azotobacter, Azospirillum, and Clostridium fix nitrogen under conditions characteristic of the rhizosphere, where oxygen concentrations are low (Giller and Day 1985). The amount ofrhizosphere nitrogen fixation differs by my­ corrhiza type, host plant, and plant community. For ex­ ample, Amaranthus and others (1989) found significantly higher nitrogenase activity in Douglas-fir rhizospheres associated with cleared areas of Arctostaphylos viscida shrubs compared to Douglas-fir grown in adjacent cleared areas of annual grass. Nitrogen is fixed by free-living bac­ teria in buried wood (Jurgensen and others 1984), an im­ portant niche for mycorrhizal development (Harvey and others 1987). Although the amount of nitrogen added to forest sites by free-living microoganisms is small compared to symbiotic sources, steady accretions especially in the immediate root zone can contribute significantly to the overall long-term nitrogen budget. Thus, silvicuItural use ofrhizosphere organisms to improve nitrogen levels deserves continuing research. Figure 5-High-magnification transverse section of red alder ectomycorrhiza showing fungal penetration into the epidermis to form SOIL FAUNA the Hartig net. (Magnification = 655x.) (Photo courtesy of Drs. H. B. Massicotte and R. L. Many soil animals interact in the rhizosphere. Recent Peterson, University of Guelph, Ontario, attention has been devoted to soil animals that influence Canada.) nutrient cycling by acting as microbial grazers in the rhizosphere (Coleman and others 1984; Elliot and others 54 other rhizosphere organisms that inhibit pathogens, and (5) inducing biochemical changes in root cortical cells that inhibit pathogen infection and spread (Marx 1972; Zak 1964). How do these mechanisms work in forest soils? In Australia, Malajczuk and McComb (1979) found signifi­ cant differences between rhizosphere populations around mycorrhizal and nonmycorrhizal Eucalyptus seedlings in soils suppressive or conducive to the fungal pathogen Phytophthora cinnamoni Rands. High counts of bacteria were present throughout the fungal mantle within and between root cortical cells of mycorrhizal seedlings but were not present in nonmycorrhizal seedlings; in culture, many of the bacteria strongly antagonized root pathogens (Phytophthora and Pythium spp.). In the Pacific North­ west, Rose and others (1980) found that a free-living Streptomycete species from the rhizosphere of snowbrush (Ceanothus velutinus Doug1.) antagonized three common Figure 6-Scanning electron micrograph of root pathogens: Phellinus weirii (Murr.) Gilb., Fomes nitrogen-fixing nodules formed on Alnus sinuata annosus (Fries) Karst., and Phytophthora cinnamoni. In roots. (Magnification = 7.7x.) (Photo courtesy of bareroot nurseries, the ectomycorrhizal fungus Laccaria Drs. H. B. Massicotte and R. L. Peterson, Univer­ laccata (Scop.:Fr.) Berk. and Br. can reduce incidence of sity of Guelph, Ontario, Canada.) Fusarium root rot (Sinclair and others 1982). Nonmycor­ rhizal fungi can also inhibit pathogens. Common soil fungi in the genus Trichoderma can reduce the incidence of root rot in pine seedlings (Kelly 1976). Root-protecting 1980; Ingham and others 1985). Nematodes, protozoa, organisms, such as symbionts and nitrogen fixers, are amoebae, and microarthopods graze on fungi and bacteria important components of "forest health." A research focus in the rhizosphere and release nitrogen in a form available on the organisms involved and the effect of management to plants. Nutrient fluxes due to grazing can be significant. practices on their survival and function is much needed. Persson (1983) estimated that 10 to 50 percent of total nitrogen mineralization in a Swedish pine forest is medi­ ated by soil invertebrates. Louisier and Parkinson (1984) SOIL STRUCTURE estimated that testate amoebae alone consume more than An often-overlooked function of soil organisms is their 13,000 kg/ha/yr in an aspen woodland soil; 85 percent of dynamic contribution to soil structure, particularly aggre­ that consumption was released or respired. This would gate formation and stability (Perry and others 1987). The release from 25 to 50 kilograms ofN/ha/yr from bacterial resulting porosity, essential for movement of air and water biomass, an amount roughly equivalent to the amount required by roots and microorganisms, greatly influences annually taken up by trees. Invertebrates, particularly forest productivity. Mycorrhizal fungi and other rhizo­ arthropods, may also move fungi, bacteria, and other mi­ sphere microbes influence soil structure by producing crobes from rhizosphere to rhizosphere. humic compounds (Tan and others 1978), accelerating the decomposition of primary minerals (Cromack and others PATHOGENS AND RHIZOSPHERE 1979), and secreting organic "glues" called extracellular polysaccharides (Sutton and Shepard 1976; Tisdale and INTERACTIONS Oades 1979). Extracellular polysaccharides are especially The ecology of soil pathogens and pathogen protection by efficient at stabilizing soil structure and act by linking rhizosphere organisms is poorly understood in forest soils; mineral grains, homogenous clays, and humus into stable most research has concentrated on the root rot fungi in the aggregates that maintain porosity (Toogood and Lynch genera Phellinus, Armillaria, and Fomes, which infect and 1959). persist in large structural roots and stumps. Feeder root Because extracellular polysaccharides are also degraded pathogens are less well known. Soil biologists hypothesize by microbial activity, maintenance of soil structure depends that a "healthy" forest soil supports populations of micro­ on the relatively continuous flow ofphotosynthate into the organisms that compete or otherwise antagonize fine-root rhizosphere. Without energy flowing from plants to rhizo­ pathogens. For example, common pathogens in tree nurs­ spheres, soil structure may be altered. Borchers and Perry ery soils are rarely isolated from forest soils. This phenom­ (1989) found that the proportion oflarge aggregates was enon of naturally "suppressive soil" is a subject of consider­ significantly reduced in two unreforested southern Oregon able research. Ectomycorrhizal fungi can protect trees clearcuts. The management implications of this impor­ against fine-root pathogens by (1) providing a physical tant soil biological function are clear: rapid tree regenera­ barrier (fungal mantle) against penetration, (2) depriving tion or recolonization by pioneering vegetation are essen­ root pathogens of carbohydrates, (3) secreting inhibitory tial to supply soil organisms with the energy needed to antibiotic substances against pathogens, (4) promoting maintain a functioning soil structure.

55 NUTRIENT CYCLING the "hyphal bridge" (Read and others 1985); if one of the plants is shaded, carbon may move from the strongly pho­ We typically consider the saprophytic microflora, the tosynthesizing plant in full light to the shaded plant. The decomposers, as the primary soil organisms controlling implication of this to interactions between plants and nu­ nutrient cycling. Recent studies, however, show rhizo­ trient cycling is enormous. For example, understory plants sphere organisms also to be important in nutrient cycling, or late successional plants may be able to receive carbon even though they receive energy primarily from root exu­ from overstory plants. Seedlings may survive in the shady dates; for example, ericaceous mycorrhizal fungi and ecto­ understory due to overs tory carbon support. But another mycorrhizal fungi can possess enzymes capable of degrad­ more important mechanism likely occurs in these rhizo­ ing organic nitrogen into usable forms (Read 1987). Some sphere relationships between plants, a phenomenon termed ectomycorrhizal fungi can also degrade organic carbon rhizosphere "legacy" (see Perry and others 1987). A plant sources, albeit at rates typically lower than saprophytic species entering in the later stages of succession can grow fungi. Under some circumstances, mycorrhizal fungi may into a community ofrhizosphere organisms that has been compete with saprophytes to slow down overall rates of developed and maintained by earlier plant species. The decomposition (Gadgil and Gadgil 1975). Other direct later successional plants can utilize a fully functional rhi­ physiological mechanisms suggest further roles of mycor­ zosphere community developed at the expense (that is, rhizal fungi in nutrient cycling. For example, ectomycor­ photosynthates) of early successional plant species. Such rhizal fungi release enzymes that increase the availability a functional rhizosphere connection in "successional time" of phosphorus to higher plants (Alexander and Hardy is an important but poorly understood component of com­ 1981; Ho and Zak 1979; Williamson and Alexander 1975). munity development. This extraction process extends to other nutrients, espe­ One should not suppose, however, that all plants are cially immobile heavy metals, and enters them into the connected by mycorrhizal fungi or exchange nutrients forest nutrient cycle. Many ectomycorrhizal fungi and through such fungi. Trees that form only ectomycorrhizae rhizosphere bacteria produce chelating agents called cannot associate with VA or ericaceous mycorrhizal fungi, siderophores that are especially important for iron uptake and so plants that exclusively form these different types by plants (Graustein and others 1977; Perry and others of mycorrhizae would not be directly linked. Also, several 1982; Powell and others 1980). Still other fungi produce ectomycorrhizal fungi form mycorrhizae only with a par­ oxalic acid that enhances the primary weathering of soil ticular genus of trees. For example, many fungus species particles (Cromack and others 1979). are "host-specific" to Douglas-fir (Pseudotsuga menziesii) Maintenance of forest productivity requires not only the or the genus Pinus. The important point is that such a steady cycling of nutrients but also the conservation of rich assemblage ofrhizosphere organisms with different nutrient capital. The living microbial biomass in the rhizo­ plant compatibilIties enables the soil organisms to "parti­ sphere is exceedingly large, especially when one considers tion" use of the soil by the plants. In essence then, when the extensive mats of ectomycorrhizal fungi composed of there is a variety of plants in a forest a related mosaic of ropelike hyphal aggregations that tenaciously store nutri­ belowground rhizosphere organisms partition the soil re­ ents. Thus, few nutrients leach out when populations of source, at times influencing plant-plant interactions and rhizosphere organisms are healthy and active. This is at other times not. We believe that compatible and com­ particularly important for soluble forms of nitrogen such petitive interactions between plants as mediated by rhizo­ as nitrate, which is susceptible to leaching. As a primary sphere organisms contribute significantly to community ecosystem function, rhizosphere organisms form a web to development (Perry and others 1989). capture and assimilate nitrogen and other nutrients into One final concept ofrhizosphere development is impor­ complex organic compounds and then slowly release them tant to forest community succession. Studies in birch into the forest ecosystem. (Betula) stands in Great Britain reveal that certain mycor­ rhizal fungi dominate tree root systems of young birch RHIZOSPHERE DYNAMICS trees, and other fungi are common in older stands (Mason and others 1987). Such fungi have been termed "early and AND FOREST COMMUNITY late-stage" fungi, respectively. These two groups offungi DEVELOPMENT differ physiologically, with the late group generally better adapted to deal with soils high in organic matter. We are Several exciting directions ofrhizosphere research em­ only beginning to eval uate such phenomena among mycor­ phasize that the successional dynamics of plant communi­ rhizal associations in Pacific Northwest forests, where tree ties and rhizosphere microorganisms are intricately related and habitat diversity is greater than in Great Britain. We and interdependent. Because tree harvest and site prepa­ hypothesize, however, that the species composition ofrhi­ ration set the stage for forest community succession, they zosphere organisms shifts tremendously as forests mature, likewise impact the belowground successional dynamics. reflecting changes in soil characters as well as forest com­ We expect that major management implications on forest position (Amaranthus and Perry 1987). Manyectomycor­ recovery will develop from soil biological investigations. rhizal fungi show strong preference for specific soil micro­ Most leads on rhizosphere-plant community dynamics niches. For example, some fungus species predominate deal primarily with mycorrhizal relationships, so we em­ in highly organic substrates such as buried wood; others phasize those here. Many different host species can form proliferate in exposed mineral soils. In addition to improv­ mycorrhizae with the same fungi. Laboratory studies ing our knowledge on the dynamics of belowground bio­ indicate that plants connected by a shared fungus can logical succession, understanding such fundamentally exchange nutrients, including carbon and minerals, via

56 different ecological strategies of mycorrhizal fungi and growth of conifer seedlings on old, nonreforested clear­ other rhizosphere microorganisms will allow us to main­ cuts. Canadian Journal of Forest Research. 17: 944-950. tain or, if necessary, reestablish viable populations of ben­ Amaranthus, M. P.; Perry, D. 1989. Interaction effects of eficial soil organisms on degraded sites. vegetation type and Pacific madrone soil inoculum on Our studies in the Siskiyou Mountains of southwestern survival, growth, and mycorrhiza formation of Douglas­ Oregon and northern California provide invaluable leads fir. Canadian Journal of Forest Research. 19: 550-556. in testing community-level hypotheses of interactions be­ Amaranthus, M. P.; Molina, R.; Trappe, J. 1989. Long­ tween plants and soil organisms. Many of the pioneering term forest productivity and the living soil. In: Perry, hardwood shrubs and trees of these forests form mycor­ D. A.; Meurisse, R.; Thomas, B.; Miller, R.; Boyle, J.; rhizae with the same fungi as do the timber tree species. Means, J.; Perry, C. R.; Powers, R. F., eds. Maintaining Amaranthus and Perry (1989) show the lasting beneficial long-term productivity of Pacific Northwest ecosystems. "legacy" effect of rhizosphere organisms in the soil beneath Portland, OR: Timber Press: 36-52. pioneering hardwoods. They hypothesize that the diverse Borchers, J. G.; Perry, D. A. 1989. Organic matter content plant species in these typically harsh forest habitats have and aggregation offorest soils with different textures evolved mutual compatibilities between rhizosphere organ­ in southwest Oregon clearcuts. In: Perry, D. A.; isms. This ensures not only rapid occupancy of the sites Meurisse, R.; Thomas, B.; Miller, R.; Boyle, J.; Means, by pioneering plants but also maintenance of soil organ­ J.; Perry, C. R.; Powers, R. F., eds. Maintaining long­ isms that will benefit later successional stages. Such a term productivity of Pacific Northwest ecosystems. legacy may also operate under the proposed system of Portland, OR: Timber Press: 245. green tree retention; the ramifications of such rhizosphere Castellano, M. A.; Molina, R. 1989. Mycorrhizae. In: mechanisms may be important in other forest areas in the Landis, T. D.; Tinus, R. W.; McDonald, S. E.; Barnett, Pacific Northwest. J. P. The container tree nursery manual. Vol. 5. Agric. Handb. 674. Washington, DC: U.S. Department of Agri­ culture, Forest Service: 101-167. CONCLUSIONS AND FUTURE Chatarpaul, L.; Carlisle, A. 1983. Nitrogen fixation: a DIRECTIONS biotechnological opportunity for Canadian forestry. Forestry Chronicle. 59: 249-250. As we develop holistic approaches to understanding Coleman, D. C.; Anderson, R. V.; Cole, C. V.; McClellan, forest ecosystems and integrated, ecologically based man­ J. F.; Woods, L. E.; Trofymow, J. A.; Elliot, E. T. 1984. agement tools, we must factor in the inseparable connec­ Roles of protozoa and nematodes in nutrient cycling. tions to soil organisms. Just as forests invest tremendous In: Microbial-plant interactions. Madison, WI: Soil capital in the form of photosynthates to fuel beneficial soil Science Society of America: 17-28. organisms, so too must we protect this unseen and over­ Cromack, K.; Sollins, P.; Graustein, W. C.; Seidel, K.; looked ecosystem. We need to better understand its "func­ Todd, A.; Spycher, W. G.; Ching, Y. L.; Todd, R. L. 1979. tional biodiversity." Calcium oxialate accumulation and soil weathering in The number of species of microorganisms in the soil is mats of the hypogeous fungus Hysterangeum crassum. far greater than aboveground plants and animals, but it Soil Biology and Biochemistry. 11: 463-468. is difficult to quantify. Also, although many soil organisms Curl, E. A.; Truelove, B. 1986. The rhizosphere. New perform similar processes, reflecting a "redundancy in York: Springer-Verlag. 288 p. function," they may have different ecologies; for example, Dawson, J. O. 1983. Dinitrogen fixation in forest ecosys­ different functions during the year or over successional tems. Canadian Journal of Microbiology. 29: 979-992. time. Our goal was to define and characterize viable popu­ Elliot, E. T.; Anderson, R. V.; Coleman, D. D.; Cole, C. V. lation levels of critical functional groups in a diversity of 1980. Habitable pore space and microbial trophic inter­ forest types and age classes so that we can predict when actions. Oikos. 35: 327-335. forest systems are becoming degraded. Understanding Florence, L. Z.; Cook, F. D. 1984. Asymbiotic N-fixing how the functional biodiversity of the soil biota acts as bacteria associated with three boreal conifers. Canadian a biological "buffer" to forest disturbance and contributes Journal of Forest Research. 14: 595-597. to recovery will be an area of intense investigation. Fogel, R.; Hunt, G. 1983. Contribution ofmycorrhizae and Other challenges involve linking soil biological science soil fungi to nutrient cycling in a Douglas-fir ecosystem. to the complex issues oflong-term site productivity and Canadian Journal of Forest Research. 13: 219-232. vegetation shifts during rapid global climate change. Foster, R. C. 1988. Microenvironments of soil microorgan­ Sharpened understanding of soil biology, particularly isms. Biology and Fertility of Soils. 6: 189-203. the tight linkages in the rhizosphere, is paramount to Foster, R. C.; Bowen, G. D. 1982. Plant surfaces and developing sound ecological guidelines to protect the living bacterial growth: the rhizosphere and rhizoplane. In: resource of the soil. Mount, M. S.; Lacy, G. H., eds. Phytopathogenic pro­ karyotes. Vol. I. 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