Ecology, 84(9), 2003, pp.

22812291
q 2003 by the Ecological Society of America

GRASSROOTS ECOLOGY: PLANTMICROBESOIL INTERACTIONS AS

DRIVERS OF PLANT COMMUNITY STRUCTURE AND DYNAMICS
HEATHER L. REYNOLDS,1 ALISSA PACKER, JAMES D. BEVER, AND KEITH CLAY
Department of Biology, Indiana University, Bloomington, Indiana 47405 USA

Abstract. A growing body of research on plantmicrobe interactions in soil is con-

tributing to the development of a new, microbially based perspective on plant community
ecology. Soil-dwelling microorganisms are diverse, and interactions with plants vary with
respect to specificity, environmental heterogeneity, and fitness impact. Two microbial pro-
cesses that may exert key influences on plant community structure and dynamics are mi-
crobial mediation of niche differentiation in resource use and feedback dynamics between
the plant and soil community. The niche differentiation hypothesis is based on observations
that soil nutrients occur in different chemical forms, that different enzymes are required
for plant access to these nutrients, and that soil microorganisms are a major source of these
enzymes. We predict that plant nutrient partitioning arises from differential associations of
plant species with microbes able to access different nutrient pools. Feedback dynamics
result from changes in the soil community generated by the specificity of response in plant
microbe interactions. We suggest that positive feedback between plants and soil microbes
plays a central role in early successional communities, while negative feedback contributes
both to species replacements and to diversification in later successional communities. We
further suggest that plantmicrobe interactions in the soil are an important organizing force
for large-scale spatial gradients in species richness. The relative balance of positive feedback
(a homogenizing force) and negative feedback (a diversifying force) may contribute to

Special Feature
observed latitudinal (and altitudinal) diversity patterns. Empirical tests of these ideas are
needed, but a microbially based perspective for plant ecology promises to contribute to our
understanding of long-standing issues in ecology, and to reveal new areas of future research.
Key words: diversity; mycorrhizal fungi; N-fixing bacteria; niche partitioning; plant ecology;
soilborne pathogens; succession.

INTRODUCTION use of artificial soil mixes or soil amendments that

Ecological theory recognizes a variety of abiotic and result in depleted microbial communities.
biotic factors that shape the structure and dynamics of In recent years, however, a growing body of ecolog-
terrestrial plant communities. Climate, age, environ- ical research on plantmicrobe interactions in soil has
mental harshness, area, isolation, disturbance, environ- developed. A new, microbially based perspective on
mental heterogeneity, and biotic interactions may all plant community structure and dynamics is emerging
play key roles in determining plant community com- from this work. In this paper, we review the diversity
position and diversity in space and time (Tilman and of plantmicrobe interactions in soil and discuss the
Pacala 1993, Rosenzweig 1995). Much of plant eco- costs and benefits to each partner. We discuss the role
logical theory has been dominated by debate over the of environmental heterogeneity and host specificity in
relative importance of these factors, manifest in con- generating a continuum of positive and negative ef-
troversy over plant strategy theory and the relationships fects, both direct and indirect. Two processes, media-
between competition intensity, species diversity, and tion of niche differentiation in plant resource use and
habitat productivity (Reynolds 1999, Aarssen 2001). feedback dynamics between the plant and soil com-
Among the biological forces structuring plant com- munity, emerge from these fundamentals as key mi-
munities, plantmicrobe interactions have received lit- crobial influences on plant community structure and
tle attention (Thompson et al. 2001). This is not sur- dynamics. We discuss the evidence for these processes
prising, given the overwhelming diversity of soil mi- and their applications to understanding temporal and
crobes (Torsvik et al. 1994), the technical challenges spatial vegetation patterns. We conclude with a look
involved in their study, the tendency to view microbial toward how a microbial perspective can inform future
associates as simply extensions of the plant and their research directions in plant ecology.
outright exclusion from experimental designs through
BASICS OF PLANTMICROBE INTERACTIONS
Manuscript received 15 May 2002; revised 26 August 2002; Diversity and function
accepted 11 September 2002. Corresponding Editor: A. A. Agra-
wal. For reprints of this Special Feature, see footnote 1, p. 2256. Soil-dwelling microorganisms encompass a diversity
1 E-mail: [email protected]
of phylogenetic groups and all three major functional
2281
 2282 HEATHER L. REYNOLDS ET AL. Ecology, Vol. 84, No. 9

groups (producer, consumer, and decomposer). Genetic of association (i.e., the ability to form specific asso-
diversity can be exceptionalseveral thousand ge- ciations) and the specificity of the plant and microbe
nomes per gram of soil (Torsvik et al. 1990). Yet our responses to their association (i.e., the dependence of
knowledge of microbial species diversity is still in its relative fitness on specific associations, as estimated
infancy (Tate 1997). Interactions between soil microbes by specificity of growth responses). While these two
and plants span the range from mutualistic to patho- aspects of specificity are not completely independent,
genic. As decomposers, soil microbes are indirectly they are not necessarily collinear either. For example,
responsible for the bulk of terrestrial vegetations an- interactions that have relatively high specificity of as-
nual nutrient demand (Schlesinger 1991). In turn, plant sociation, such as the association between ectomycor-
matter is the major source of photosynthetically fixed rhizal host plants and ectomycorrhizal fungi, might also
carbon for decomposers. Yet microbes and plants also be expected to show relatively high specificity of re-
compete for soil nutrients (Hodge et al. 2000 a), making sponse. However, this does not imply that plant-mi-
their relationship simultaneously mutualistic and com- crobe interactions that show low specificity of asso-
petitive (Harte and Kinzig 1993). In contrast, nitrogen- ciation also show low specificity of response. The in-
fixing bacteria and mycorrhizal fungi enhance host teraction of plants and AM fungi shows relatively low
plant fitness by direct provisioning of mineral resources specificity of association, but the response of plants to
or by providing protection against other pests. Non- individual species of AM fungi can vary greatly de-
mycorrhizal fungi, various rhizosphere bacteria, pro- pending on the plantAM fungal combination (Van der
tozoa, and nematodes have also been shown to protect Heijden et al. 1998). Similarly, the relative growth rates
plants from soilborne enemies like fungi, bacteria, ac- of AM fungi also depend greatly on the identity of the
tinobacteria, protozoa, nematodes, and viruses (Lavelle plant with which they are associated (Eom et al. 2000;
and Spain 2001). Such pathogens are responsible for Bever 2002). Specificity of infection and of plant re-
damping-off diseases, vascular wilts, and root rots (Ka- sponse is also a well-known characteristic of soil path-
tan 1991). ogens (Bruehl 1987, Agrios 1997). In fact, when mea-
Special Feature

sured, soil microbes commonly show specificity of re-

Continuum of effects: environmental dependence sponse to plant species and specificity of growth effects
Many of the effects of microbes on plants are de- on those hosts. While the specificity of association is
pendent upon environmental conditions. For example, important for establishing the potential relationships,
the benefits that plants receive from nutritional mutu- the specificity of response determines the community
alisms with soil microbes (e.g., nitrogen-fixing bacteria dynamics resulting from these associations (Bever
and mycorrhizal fungi) depend upon the availability of 1999).
essential soil minerals. Available phosphorus (P) is of-
ten the primary determinant of plant dependence on MICROBIAL MECHANISMS FOR THE MAINTENANCE
OF DIVERSITY
arbuscular mycorrhizal (AM) fungi, such that the effect
of the interaction can be negative under high P con- Given a local species pool, the species diversity of
ditions (Bethlenfalvay et al. 1982). The benefit that a given area depends on the existence of mechanisms
plants receive from protective mutualisms is also en- that prevent a competitive dominant from excluding all
vironment dependent, as the benefit depends upon the other species. Recognizing that competition occurs
presence of enemies. A similar environmental depen- over resources, coexistence mechanisms may be cat-
dence is inherent in the interactions of plants and soil egorized on the basis of whether (Aarssen 1984) (1)
pathogens. Major groups of soil pathogens (e.g., Pyth- competition is avoided in the first place, through re-
ium) have high pathogenesis under a limited range of source partitioning (e.g., rooting depth differences), or
environmental conditions (e.g., wet and warm). The (2) competitive exclusion is avoided, despite overlap
ability of plants to tolerate or ward off pathogens is in resource use (e.g., competitive reversal). Here, we
also dependent upon environmental factors such as nu- discuss new facets to these coexistence mechanisms
trient and light availability. Thus, the impact of soil that emerge from a microbially based perspective.
communities on plant community processes will also
be a function of environmental factors, presenting a Microbial mediation of resource partitioning
particular challenge to investigations of the community We focus here on soil nitrogen (N) and P, the two
consequences of plantsoilmicrobe interactions. most common limiting nutrients in terrestrial ecosys-
tems (Chapin et al. 1986). These nutrients exist in a
Specificity of association vs. specificity of response variety of inorganic (e.g., ammonium, phosphate) and
Mutualistic and pathogenic associations between organic (e.g., amino acids, nucleic acids) pools made
plants and soil microbes are known to range in their available to plants through the action of soil enzymes
specificity from highly specific associations between (e.g., proteases, ribonucleases), the bulk of which are
orchids and their mycorrhizal fungal symbionts to the thought to come from bacteria and fungi (Tabatabai
cosmopolitan associations of plant roots with rhizo- and Dick 2002). If microbes or their enzymatic activ-
sphere bacteria. It is useful to distinguish the specificity ities are differentially associated with plant species, a
September 2003 UNDERGROUND PROCESSES 2283

Special Feature
FIG. 1. (a) N partitioning. Different plant species access different forms (e.g., NO32 vs. NH41 vs. amino acids) or sources
(e.g., NH41 from N2, proteins, urea or chitin) of N. (b) A similar model can be envisioned for P nutrition.

kind of resource partitioning may arise in which dif- species associate with different groups of microbes, so
ferent plant species access different pools, thus avoid- gaining differential access to nutrient pools. Confir-
ing competition for the same pools (Fig. 1). In this mation of this hypothesis would have the important
way, plants may experience a single nutrient axis (e.g., implication that plant species coexistence depends
N), as a diversity of axes, thereby vastly increasing the upon soil microbial diversity and microbial dynamics.
number of niches available for competing plant species. Evidence for microbially mediated resource parti-
On the surface, this is simply the standard niche-par- tioning.Evidence for less obvious forms of micro-
titioning model, but the niche partitioning is enabled bially mediated nutrient partitioning than that between
by soil microbes. plants with N-fixing symbionts and plants that rely on
Under the simplest form of the microbial mediation soil N awaits future studies. Evidence for partitioning
hypothesis, a single microorganism is able to produce of plant species into ammonium, nitrate, and amino
the entire range of enzymes and different plant species acid specialists is accumulating in a range of ecosys-
cause this super microbe to express different en- tems (McKane et al. 2002, Miller and Bowman 2002),
zymes. However, inevitable physiological trade-offs although a specific role for microbes has not been es-
and the diversity of microorganisms with distinct en- tablished. Nor do we know whether plant species, via
zymatic capabilities make this super microbe hypoth- microbial associations, differentially access complex
esis untenable. A more realistic hypothesis is that plant organic pools, such as protein, chitin, or nucleic acids.
 2284 HEATHER L. REYNOLDS ET AL. Ecology, Vol. 84, No. 9

We do know that microbial populations are highly Positive vs. negative feedback dynamics
elevated in the rhizospheres surrounding plant roots
A second, qualitatively distinct manner in which in-
(Paul and Clark 1996), where they may be influenced
teractions with soil microbes can contribute to the
by the quality and quantity of substances that plant
maintenance of diversity in plant communities is
roots continuously exude (Rovira 1969, Hamilton and
through feedbacks on plant growth resulting from
Frank 2001). Thus, the possibility arises that specific
changes in the composition of the soil community.
plantmicrobe and/or plantmicrobial-enzyme associ-
While feedbacks may be involved in microbially me-
ations could develop. Differential plantmicrobe as-
diated resource partitioning, we focus here on feedback
sociations have been observed (Grayston et al. 1998,
dynamics involving plants with overlapping resource
Westover and Bever 2001). Yet, with the obvious ex-
use. Feedbacks result from the community dynamics
ception of N fixation, the potential relevance of such
generated by the specificity of response in plantmi-
associations for plant N and P partitioning has not been
investigated. crobe interactions. Because growth rates of microbes
Mycorrhizal mediation of resource partitioning. are known to be host dependent, the composition of
Mycorrhizae are potentially key players in this model the soil community will likely change due to the iden-
of microbially mediated N and P partitioning. All forms tity of the local host plant. Moreover, as the growth
of mycorrhizal fungi exhibit phosphatase activity (Mar- promotion of soil microbes is also host-specific, the
schner 1995). In otherwise sterile soil, AM grasses change in the composition of the soil microbes will
showed increased growth and P uptake compared to likely alter the relative performance and local abun-
noninfected plants when supplied with such organic P dance of different plant species. The feedback then
sources as ribonucleic acid (RNA) (Jayachandran et al. represents the dynamics of the net direct effects of the
1992) and phytate (Jayachandran et al. 1992, Tarafdar microbial community on individual plant types.
and Marschner 1994). Ecto- and ericoid mycorrhizae Expected dynamics of feedback.The growth con-
are capable of breaking down complex organic N and sequences of soil community feedback can be positive
or negative. For example, if the presence of plant spe-
Special Feature

taking up dissolved organic N such as amino acids

(Ahmad and Hellebust 1991), allowing plants direct cies A causes an accumulation of microbes that spe-
access to organic N (Turnbull et al. 1995, 1996). A cifically benefit that host, then the relative performance
number of studies have now also demonstrated en- of plant A with its soil community will improve over
hanced acquisition of inorganic and organic N sources time. This positive feedback dynamic will be expected
by AM plants (Michelsen et al. 1996, Hawkins et al. to reinforce the initial abundance of plant A and lead
2000). A key issue is whether, like ecto- and ericoid to the loss of other plant types from the local com-
mycorrhizae, AM fungi are able to directly access com- munity, at least on a local scale (Bever et al. 1997,
plex organic N forms (e.g., chitin) or whether they Bever 1999).
simply enhance the ability of plants to compete with In the case of negative feedback, a given host per-
free-living heterotrophic microbes for the products of forms relatively worse with its own soil community
organic matter mineralization. Recent studies have over time. This can result from host-specific degra-
been conflicting (Hodge et al. 2000b, 2001). dation of the soil community, such as might result from
Might mycorrhizae facilitate differential access of the accumulation of species-specific pathogens. How-
plant species to different pools of N and P? Prior re- ever, negative feedback can also result from host-spe-
search with AM fungi has focused almost exclusively cific changes in the composition of the soil community
on a few AM fungal species in a single genus (Glomus). that improve the growth of a second plant species (i.e.,
Yet substantial host specificity of AM fungi with plant an indirect facilitation mediated by the change in the
hosts has been demonstrated (Bever et al. 1996, Van microbial community). The composition of the my-
der Heijden et al. 1998). This host specificity, in com- corrhizal fungal community, for example, might change
bination with AM fungal diversity, has been implicated in a manner that improves the growth of a competing
in the maintenance of plant community diversity (Van plant species (Bever 1999, 2002). Negative feedback
der Heijden et al. 1998, Bever et al. 2001), although will prevent any single plant species from dominating
the specific mechanism is not known. The potential for a site and thereby contribute to the coexistence of com-
microbially mediated niche partitioning may be even peting plant species (Bever et al. 1997).
greater in ecto- and ericoid mycorrhizae, which are Evidence for positive feedback.Positive feedback
thought to be more diverse than AM fungi and to ex- is known to play an important role in plantsoil com-
hibit greater host specificity. For example, isolates of munity interactions. Positive feedback dynamics are
four ectomycorrhizal species from northern Australian evident in the limited success of plant establishment
forests had different abilities to use a range of amino in the absence of particular symbionts, as illustrated
acids, protein and inorganic N sources and this was by the history of pine forests in the tropics. Attempts
affected by host plant identity (Turnbull et al. 1995). at growing pine failed until trees were inoculated with
More studies of this sort are needed for mycorrhizae compatible ectomycorrhizal fungi, and now these pines
in general. are increasingly perceived as a potentially invasive spe-
September 2003 UNDERGROUND PROCESSES 2285

cies (Rejmanek and Richardson 1996). A similar pat- working synergistically with pathogenic fungi to de-
tern has been found with invasive Russian olive crease plant growth (Van der Putten et al. 1990, Van
(Elaeagnus angustifolia) and its N-fixing Frankia sym- der Putten and Troelstra 1990). Soil communities have
biont (Richardson et al. 2000). Similarly, the success also been suggested as a driver of plant community
of plants that are dependent upon AM fungi or N-fixing dynamics in tallgrass prairies (Holah and Alexander
bacteria are dependent upon the initial abundance of 1999) and European grazed grasslands (Olff et al.
their symbionts (Medve 1984, Larson and Siemann 2000). In the latter system, the negative soil community
1998). Local-scale positive feedback is expected to feedbacks have been implicated as a cause of a shifting
maintain sharp boundaries between patches (Molofsky mosaic of grassland dominants (Olff et al. 2000), a
et al. 2001), and contribute to the maintenance of pattern predicted by spatial simulations of this process
boundaries between vegetation dominated by plants as- (Molofsky et al. 2002).
sociated with arbuscular vs. ectomycorrhizal fungi.
Evidence for negative feedback.There is accu- LARGE-SCALE VEGETATION PATTERNS
mulating evidence of negative feedbacks important In the previous section, we discussed how micro-
role in structuring plant communities. In agricultural bially mediated resource differentiation and feedback
settings, the accumulation of species-specific soil path- have implications for the maintenance of plant com-
ogens drives the rotation of crops. Much of the evi- munity diversity at a local scale. Here, we discuss how
dence for negative feedback in unmanaged communi- these processes may contribute to large-scale vegeta-
ties has come from efforts to test the Janzen-Connell tion patterns. We hypothesize that the relative impor-
hypothesis that high tropical forest tree diversity results tance of positive versus negative feedback processes
from negative density-dependent mortality resulting shifts over temporal and spatial gradients, with positive
from species-specific seed predation or herbivory (Jan- feedback processes dominating earlier in succession
zen 1970, Connell 1971). Seedling mortality in tropical and at high latitudes and altitudes and negative feed-
forests has been repeatedly found to increase with the back processes dominating later in succession and at

Special Feature
density of conspecifics (e.g., Wills et al. 1997, Harms low latitudes and altitudes. This hypothesis could be
et al. 2000) and with proximity to mature conspecifics tested in natural communities by examining plantsoil
(Augspurger 1992, Condit et al. 1994). Current evi- feedback over successional and spatial gradients.
dence suggests accumulation of soilborne pathogens as
the causal mechanism for these effects (Augspurger and Temporal patterns
Kelly 1984, Augspurger 1988). In temperate forests of Vegetation change over time, or succession, is char-
eastern North America, negative feedbacks may drive acterized by sequential species replacements, typically
the reciprocal replacement and coexistence of beech accompanied by changes in community diversity. Clas-
and maple codominants (Fox 1977, Woods 1979), al- sic successional models focus on vegetation-based
though the soil microbial mechanism has not been dem- mechanisms of species replacement, differing in em-
onstrated. The high mortality of black cherry (Prunus phasis on recruitment limitation, life history strategy,
serotina) seedlings near adult conspecifics and at high environmental modification, and competitive exclusion
seedling densities has been shown to result from ac- (Connell and Slatyer 1977, Tilman 1988). The role of
cumulation of soil pathogens in the genus Pythium plantmicrobe interactions in such models is princi-
(Packer and Clay 2000). pally limited to that of N-fixing associations in facil-
There is also accumulating evidence of negative soil itation. Yet evidence for microbial influences on suc-
community feedbacks playing an important role in cession can be found in early work, which established
grassland communities. In greenhouse assays of soil that many soil microbes vary predictably with vege-
community feedback within an old field community in tation through succession (Tresner et al. 1954, Wohlrab
North Carolina, negative feedback was found in nine et al. 1963). More recently, mycorrhizae (Janos 1980,
of the 14 pairwise comparisons tested (Bever 1994, Read 1991) and soil pathogens (Van der Putten et al.
Bever et al. 1997). In this system, several complemen- 1993, Clay and Van der Putten 1999) have been rec-
tary microbial mechanisms of negative feedback have ognized as potentially important drivers of succession.
been identified, including the accumulation of host- Here, we consider plant-microbe interactions in species
specific soil pathogens in the genus Pythium (Mills and replacements and changes in community diversity
Bever 1998, Westover and Bever 2001), host-specific through succession, using the context of feedback and
shifts in the composition of rhizosphere bacteria (Wes- resource differentiation.
tover and Bever 2001), and host-specific changes in the
composition of the AM fungal community (Bever Species replacements
2002). Negative feedbacks have also been found to Positive feedback.Soil mutualists and pathogens
drive plant community dynamics within sand dune can be limiting in the very beginning stages of both
communities (Van der Putten et al. 1993). Again, com- primary and secondary successions, favoring asym-
plementary microbial mechanisms have been identi- biotic, ruderal, life history strategies (Janos 1980,
fied, with accumulation of root feeding nematodes Sprent 1993), particularly in secondary successions,
 2286 HEATHER L. REYNOLDS ET AL. Ecology, Vol. 84, No. 9

FIG. 2. A conceptual model of how the rel-

ative strength of positive and negative feedback
changes over successional time and over lati-
tudinal gradients. The exact shape of the curves
does not matter. The important point is that there
is a switchover point at some intermediate suc-
cessional time or latitude where the strength of
negative feedback exceeds that of positive feed-
back.

where soil nutrient availability is comparatively higher. of succession, which is characterized by harsher con-
As mutualists and their plant hosts arrive at a site, ditions and lower host densities than are favorable to
positive feedback dynamics cause populations of both most disease organisms. As plant host densities build
to build (Fig. 2). and modify the abiotic environment, conditions should
The importance of positive feedback dynamics be- become more favorable to soil pathogens, leading to
tween plants and N-fixing microbes in primary suc- an increasing role for negative feedback in driving spe-
Special Feature

cessions is well recognized. In the classic example of cies replacements in succession (Fig. 2). Van der Putten
primary succession at Glacier Bay, N-fixers such as et al. (1993) showed that soilborne diseases can drive
Dryas are among the first vascular plants to colonize successional change in a foredune community; indi-
(Crocker and Major 1955). Similar dynamics are ex- viduals showed reduced biomass in the soil of their
pected between host plants and mycorrhizal fungi. Jan- successors, but not in the soil of their predecessors.
os (1980) envisioned a shift from nonmycorrhizal to The traits of early successional species themselves may
obligately mycorrhizal plants from early to late sec- make them particularly vulnerable to negative feedback
ondary succession, with low levels of facultatively my- by soil pathogens. Rapid growth is a well-known trait
corrhizal associations throughout. In sand dune and of ruderal species, and it is also established that rapid
many other successional communities there is also a growth trades off with allocation to herbivore defense
shift later in succession from herbaceous plant species (Coley et al. 1985, Poorter 1990). Given the assumption
involved in obligate symbioses with AM fungi to that belowground patterns of growth and defense mirror
woody species involved in obligate symbioses with aboveground patterns, ruderal species, by their own
ecto- or ericoid mycorrhizae (Smith and Read 1997), success, increase the likelihood that they will be re-
coincident with a shift in predominance of inorganic placed by slower growing species, better defended
versus organic N (Read 1993). against pathogens. Early and late successional species
In the case of N-fixing species, death and decom- differ in quality as well as quantity of antiherbivore
position of N-fixing species results in soil building over defense; defenses of ruderals tend to be against gen-
time. Thus, the benefits of N-fixation are not restricted eralist herbivores while defenses of climax species tend
to the plant host (Chapin et al. 1994), and a positive to be against specialists (Coley et al. 1985). Extrapo-
feedback dynamic transitions to facilitation of addi- lating belowground once again, this suggests that spe-
tional plant species. N-fixing associations may play a cialization of plant defenses against soil pathogens will
similar role in secondary successions on infertile soil. increase over successional time.
In contrast to N-fixing associations, mycorrhizal as- Microbially mediated resource differentiation.Mi-
sociations are relatively ubiquitous and act to increase crobially mediated resource partitioning might play a
access to rather than add nutrients to soil. The avail- role in species replacements if the forms of N or P
ability of P and other nutrients often decrease in late change through succession. Gorham et al. (1979) im-
succession (Walker and Syers 1976). The expectation plicated fungal symbionts in such sequential partition-
might therefore be of a strong role for mycorrhizae ing. Indeed, the example given above, of a shift from
throughout much of succession, after an initial recruit- arbuscular to ecto- or ericoid mycorrhizal plant species
ment-limited (and total N-limited, for primary succes- with a change in inorganic to organic forms of N is an
sion) phase. illustration of this process. Other shifts in forms of
Negative feedback.Negative feedback dynamics nutrients over succession (e.g., nitrate to ammonium,
are expected to be less important during the initial stage or protein to chitin) would provide the opportunity for
September 2003 UNDERGROUND PROCESSES 2287

additional species replacements on the basis of soil diating resource differentiation, then we would predict
resource specialization. greater opportunities for species coexistence (i.e.,
greater specialization of resource niches) as succession
Community diversity proceeds.
Feedback.Positive feedback, operating alone,
would be expected to lead to monocultures, or even, SPATIAL PATTERNS
in the absence of soil building or temporal shifts in Large-scale spatial patterns in the organization and
forms of nutrients (e.g., inorganic to organic N), ar- diversity of ecological communities are well known,
rested successions. It has been suggested, for example, and the underlying causes are much debated (Rosen-
that higher host specificity of ecto- compared to en- zweig 1995). Species diversity, primary productivity,
domycorrhizae leads to dominance by ectomycorrhizal and environmental equitability all tend to increase with
species, to the exclusion of endomycorrhizal species decreasing latitude (or altitude), corresponding to in-
(Connell and Lowman 1989). Even mycorrhizal net- creasing mean temperature and precipitation (Waide et
works (where benefits are shared by many hosts) can al. 1999, Mittelbach et al. 2001). Correlated changes
lead to lower diversity if one species in the network is in multiple environmental variables make the under-
the dominant sink for nutrients (Connell and Lowman lying mechanisms difficult to assign, but a variety of
1989, Allen and Allen 1990). In contrast, the process abiotic and biotic factors have been proposed as key
of negative feedback through the soil community can drivers (Waide et al. 1999). We suggest that plant
generate a pattern of increased species diversity over microbe interactions in the soil, particularly feedback
successional time. Plant life histories and pathogen col- processes, may also be an important driver of large-
onization opportunities vary with succession and offer scale spatial gradients. We predict that the relative bal-
two explanations for the increases in plant diversity ance of positive and negative feedback shifts towards
during early succession. As soil pathogens remove negative feedback as productivity increases with de-
weakly defended plants, only better defended plants creasing latitude or altitude (Fig. 2). Relatively few

Special Feature
remain. Later successional species with greater in- empirical studies have attempted to assess the relative
vestment in defense are less susceptible to generalist strength of positive and negative feedback in the soil
pathogens and only vulnerable to attack by more spe- over large-scale spatial gradients but there is a rich
cialized pathogens that are able to overcome their more conceptual and theoretical literature. Further, results
sophisticated plant defenses. Increased specialization from a number of studies indirectly contribute to our
of pathogens should lead to reciprocal negative feed- understanding of microbial interactions with plants
back that promotes plant species coexistence. Further- over large spatial scales.
more, opportunities for pathogen dispersal to a site
increase over succession, leading to greater pathogen Mutualism and positive feedback
diversity and increasing the chances for reciprocal neg- Positive interactions may be particularly advanta-
ative feedback. geous in extreme environments, such as those at high
Microbially mediated resource differentiation. latitude or altitude (Sanders 1968), and facilitation has
Community complexity increases during succession as been associated with habitats of high abiotic stress
plant, microbial, and animal species diversity increase, (Greenlee and Callaway 1996, Choler et al. 2001). Ad-
and this leads to increases in the quantity and kinds of aptations to physical stresses often arise from mutu-
nutrient pools. This is expected to be particularly true alistic symbioses with microbes, and these symbioses
for primary succession, but could also operate to a are often characterized by the host-specificity required
lesser extent in certain kinds of secondary succession, to generate positive feedback. It has been hypothesized
such as those initiating after severe fire, where much that as terrestrial productivity increases and light be-
of the above- and belowground resources may be vol- comes increasingly limiting, the high energetic costs
atilized and homogenized. We suggest that as the di- of N fixation may outweigh its benefits (Gutschick
versity of microbes and nutrient inputs increase over 1981). If this is generally true of mutualistic symbioses
succession, the opportunity for microbially mediated with microbes (at least those requiring significant car-
differentation in resource use increases, promoting in- bon inputs from the plant host) then it would promote
creased plant community diversity over succession. a gradient of increasing importance of positive feed-
Supporting this idea, ectomycorrhizal infectiveness and back between plants and soil microbes with increasing
diversity has been found to increase over a successional latitude or altitude (and decreasing primary productiv-
gradient (Boerner et al. 1996). ity).
Microbe-mediated niche diversification will also be
affected by the specificity of the associations between Pest pressure and negative feedback
plants and microbes. In the case of soil pathogens and Insofar as latitude and altitude are surrogates for tem-
mycorrhizal fungi, associations typically exhibit higher perature and precipitation, pest and pathogen pressure
levels of specificity as succession proceeds. If the same should increase as productivity increases with decreas-
pattern is true for the microorganisms involved in me- ing latitude or altitude (Weltzien 1972, Givnish 1999).
 2288 HEATHER L. REYNOLDS ET AL. Ecology, Vol. 84, No. 9

For example, damping-off fungi, which are major 2001). In temperate forests, host-specific soilborne
sources of seedling mortality for tropical tree species pathogens cause seedling mortality of black cherry
(Augspurger and Kelly 1984), thrive in warm, moist (Prunus serotina) in a distance and density-dependent
habitats. Levin (1975) concluded, based on a review manner (Packer and Clay 2000). Soilborne pathogens
of much evidence, that pathogen pressure is greater in may affect vegetation composition and dynamics in
the tropics. temperate grasslands as well (Mills and Bever 1998,
Additional evidence for a latitudinal gradient in path- Holah and Alexander 1999, Matthews and Clay 2000,
ogen pressure comes from agriculture. It is well estab- Olff et al. 2000).
lished that plant species diversity, which generally de- However, particular studies of positive or negative
creases with latitude, may reduce the incidence and feedback in any one habitat may not reflect large-scale
severity of disease (Elton 1958, Knops et al. 1999), geographical (or temporal) patterns of the relative
but, when diversity is held constant, a latitudinal effect strength of feedback processes. Appropriate empirical
is evident. For example, disease diversity of soybean, tests of the hypothesis illustrated in Fig. 2 could ma-
the United States second largest cash crop and grown nipulate microbial communities (i.e., the home vs.
over a wide latitudinal range, was shown to be signif- away culture approach of Bever [1994, 1997]) or their
icantly correlated with latitude, with the largest number presence or absence (i.e., the soil sterilization approach
of soybean diseases occurring further south (Yang and of Van der Putten et al. 1993) across latitudinal and
Feng 2001). On a worldwide basis Septoria tritici altitudinal (or successional) gradients. Plantsoil feed-
blotch of wheat decreased linearly with increasing dis- back, and plantmicrobe interactions in general, are
tance from the equator, although S. nodorum blotch likely to interact with other mechanisms, including oth-
increased with increasing latitude (Leath et al. 1993). er biotic interactions that are themselves correlated
In order to lead to diversity-maintaining negative with spatial or temporal gradients. Nonetheless, the
feedback, pest pressure must operate in a host-specific concept of plantsoil microbe interactions as drivers
way. There is evidence that soil pathogens generate of large-scale vegetation gradients deserves more at-
Special Feature

negative feedback in the tropics (Augspurger 1988). tention, and has the potential to enrich our understand-
Consistent with the mechanism of negative feedback, ing of vegetation diversity and succession.
density-dependence in the survival and growth of many
tropical tree species has also been reported (Wills et Microbially mediated resource partitioning
al. 1997, Harms et al. 2000), although a recent study It is difficult to imagine that the diversity of N, P,
found that similar proportions of tree species are af- or other soil nutrient pools changes much over large-
fected by density-dependent mortality in temperate vs. scale spatial gradients. However, we expect microbially
tropical forests (HilleRisLambers et al. 2002). mediated partitioning of soil nutrients to occur most
The correlation between latitude and outbreeding re- strongly in low productivity habitats, where soil re-
productive systems lends further support to the idea sources are relatively more limiting than light (Tilman
that negative feedback is greater at lower latitudes. 1988) and the benefits of partitioning correspondingly
Sexual reproduction is a mechanism by which host pop- higher. Unproductive habitats can occur anywhere, but
ulations can generate and regenerate rare host geno- the general trend of increasing productivity from poles
types favored in the face of pathogen attack (Clay and to equator or high to low altitude leads to the expec-
Kover 1996). Plants in tropical regions are more fre- tation that microbially-mediated resource partitioning
quently characterized by outbreeding mechanisms than will be relatively less important in the tropics or at low
plants in temperate areas, and increased pest pressure altitudes. Empirical tests of this hypothesis are needed.
in tropical systems may be responsible for this pattern
(Levin 1975). Results from animal systems also support CONCLUSIONS
this conclusion (Ghiselin 1974, Glesener and Tilman Plant interactions with soil microorganisms have be-
1978). come more central to a variety of ecological research
efforts, in spite of the fact that most ecologists lack
The case for feedback training in microbiology, the techniques of microbial
Positive feedback is certainly not limited to stressful ecology are challenging to apply in the field, and the
habitats, nor is negative feedback limited to the tropics. diversity of microbes and their interactions with plants
For example, ectomycorrhizal seedlings strongly ben- are to a large extent still unknown. In this paper, we
efit from proximity to parent trees in certain temperate have focused on microbial mediation of niche differ-
oak forests (Dickie et al. 2002). Positive feedback with entiation in resource use and feedback dynamics be-
ectomycorrhizae may also be responsible for anoma- tween the plant and soil community, but soil microbes
lous low-diversity tropical forests (Connell and Low- may influence many other important ecological pro-
man 1989, Torti and Coley 1999). Likewise, soilborne cesses.
plant pathogens create openings in high latitude co- We have posed hypotheses that are consistent with
niferous forests, affecting forest composition and suc- large bodies of existing data, but few studies have been
cessional patterns (Holah et al. 1993, McLaughlin conducted that explicitly test these ideas. With respect
September 2003 UNDERGROUND PROCESSES 2289

to microbial mediation of resource differentiation, Bethlenfalvay, G. J., M. S. Brown, and R. S. Pacovsky. 1982.
there is first a need to test the basic premise. Useful Relationships between host and endophyte development in
mycorrhizal soybean. New Phytologist 90:537543.
approaches range from observational studies of plant Bever, J. D. 1994. Feedback between plants and their soil
nutrient use and microbial associates in greenhouse or communities in an old field community. Ecology 75:1965
field to highly controlled greenhouse and field exper- 1977.
iments, where the identity of nutrient resources and the Bever, J. D. 1999. Dynamics within mutualism and the main-
composition of the microbial community are manipu- tenance of diversity: inference from a model of interguild
frequency dependence. Ecology Letters 2:5261.
lated, and host plant responses are monitored. Ad- Bever, J. D. 2002. Negative feedback within a mutualism:
vances in molecular and stable isotope techniques make Host-specific growth of mycorrhizal fungi reduces plant
these approaches feasible. Subsequent research might benefit. Proceedings of the Royal Society of London 269:
then focus on comparison of the phenomenon in early- 25952601.
vs. late-successional communities or in communities Bever, J. D., J. B. Morton, J. Antonovics, and P. A. Schultz.
1996. Host-dependent sporulation and species diversity of
along latitudinal or altitudinal gradients. arbuscular mycorrhizal fungi in a mown grassland. Journal
Such comparisons, using techniques of measuring of Ecology 84:7182.
plant growth in sterilized and cultured soil, are also Bever, J. D., P. Schultz, A. Pringle, and J. Morton. 2001.
needed to evaluate the relative balance of positive and Arbuscular mycorrhizal fungi: more diverse than meets the
negative feedback over temporal and spatial gradients. eye and the ecological tale of why. BioScience 51:923
931.
These relatively simple techniques have much to offer, Bever, J. D., K. M. Westover, and J. Antonovics. 1997. In-
although a disadvantage is that the microbial com- corporating the soil community into plant population dy-
munity is treated as a black box and only their net effect namics: the utility of the feedback approach. Journal of
on plant growth is revealed. The growing array of mo- Ecology 85:561573.
lecular techniques will enhance our perspective on Boerner, R. E. J., B. G. DeMars, and P. N. Leicht. 1996.
Spatial patterns of mycorrhizal infectiveness of soils long
plant-soil feedback by allowing the manipulation of a successional chronosequence. Mycorrhiza 6:7990.
individual microbial groups, as well as quantification Bruehl, G. W. 1987. Soilborne plant pathogens. Cambridge

Special Feature
of microbial populations and their individual effects on University Press, Cambridge, UK.
plants in diverse natural communities. Chapin, F. S., III, P. M. Vitousek, and K. van Cleve. 1986.
The nature of nutrient limitation in plant communities.
ACKNOWLEDGMENTS American Naturalist 127:4858.
Chapin, F. S., III, L. R. Walker, C. L. Fastie, and L. C. Sher-
Thanks to the Plant Interactions Group (PIG) at Indiana
man. 1994. Mechanisms of primary succession following
Universitys Department of Biology and two anonymous re-
deglaciation at Glacier Bay, Alaska. Ecological Mono-
viewers for helpful feedback. Partial financial support was
graphs 64:149175.
provided by NSF DEB-0090056 to K. Clay and A. Packer,
NSF DEB-0049080 to J. D. Bever, and an Andrew W. Mellon Choler, P., R. Michalet, and R. M. Callaway. 2001. Facili-
Foundation grant to H. L. Reynolds, J. D. Bever, and P. A. tation and competition on gradients in alpine plant com-
Schultz. munities. Ecology 82:32953308.
Clay, K., and P. Kover. 1996. The Red Queen hypothesis and
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