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Ecological Monographs, 81(3), 2011, pp. 429–441
Ó 2011 by the Ecological Society of America
Pathogen impacts on plant communities:
unifying theory, concepts, and empirical work
ERIN A. MORDECAI1
Department of Ecology, Evolution and Marine Biology, University of California, Santa Barbara, California 93106 USA
Abstract. Pathogens, like other consumers, mediate the outcome of competitive
interactions between their host species. Ongoing efforts to integrate pathogens into plant
community ecology could be accelerated by greater conceptual unification. Research on plant
pathogens has mainly focused on a variety of disparate mechanisms—the Janzen-Connell
hypothesis, plant–soil feedbacks, competition–defense trade-offs, escape of invasive plants
from their enemies, and epidemic-driven community shifts—with limited recognition of how
these mechanisms fit into the broader context of plant coexistence. Here, I extend an emerging
theoretical framework for understanding species coexistence to include various pathogen
impacts on plant communities. Pathogens can promote coexistence by regulating relative
abundance or by reducing the disparities between species in fitness that make coexistence more
difficult. Conversely, pathogens may undermine coexistence by creating positive feedbacks or
by increasing between-species fitness differences. I review the evidence for these pathogenmediated mechanisms, and I reframe the major hypotheses in a community ecology context in
order to understand how the mechanisms are related. This approach generates predictions
about how various modes of pathogen attack affect plant coexistence, even when direct
impacts on host relative abundance are difficult to measure. Surprisingly, no study gives direct
empirical evidence for pathogen effects on mutual invasibility, a key criterion for coexistence.
Future studies should investigate the relationship between pathogen attack and host relative
abundance, in order to distinguish between mechanisms.
Key words: coexistence; density dependence; disease; enemy release; epidemic; Janzen-Connell;
pathogen impacts; plant; plant–soil feedback.
INTRODUCTION
While ecologists increasingly recognize that the
interaction between competition and consumer pressure
regulates plant populations and communities (Chesson
and Kuang 2008), comparatively few studies have
focused on how pathogens affect plant species composition in natural communities (Gilbert 2002). Pathogens
are well known to reduce growth, survival, and
productivity of cultivated plants, resulting in a huge
literature on the control and spread of crop diseases
(Weller 1988, Matson et al. 1997, Brown and Hovmoller
2002). Despite the enormous potential for pathogens to
regulate natural plant populations (van der Heijden et
al. 2008), these interactions are often overlooked in field
studies. Plant–pathogen interactions are complex, inManuscript received 19 November 2010; revised 17
December 2010; accepted 23 December 2010. Corresponding
Editor: E. T. Borer.
1
E-mail: [email protected]
volving many modes of infection with fitness consequences that are difficult to discern. For example,
fungal, bacterial, and viral pathogens may be transmitted between parent and offspring or both within and
across species via soil, air, water, or insect vectors. These
pathogens may be specialists or generalists with host
ranges from several to hundreds of species. Once they
infect their plant hosts, microorganisms can modify
growth, survival, and reproduction positively, negatively, or negligibly, with the direction and strength of these
effects not always fixed (Jarosz and Davelos 1995,
Klironomos 2003). Highly virulent pathogens may
regulate their host populations even when infection
prevalence is low (Anderson and May 1981, Dinoor and
Eshed 1984). An important question remains: how do
plant pathogens modify the dynamics of host communities in nature?
Pathogens can mediate plant diversity when their
impacts on growth, reproduction, or survival modify
plant competition within and between species (Dinoor
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ERIN A. MORDECAI
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FIG. 1. The theoretical framework describing how interactions with pathogens can influence plant community dynamics
(Chesson 2000); the figure is adapted and substantially modified
from Adler et al. (2007). The x-axis measures the strength of
stabilization or destabilization (per capita growth rates that
respond negatively or positively to relative abundance, respectively). The y-axis measures the fitness differences between
species. Coexistence occurs in the dark shaded region, where
stabilization is strong enough to overcome fitness differences.
Priority effects, in which one species excludes the other and the
outcome depends on initial conditions, occur in the light shaded
region. Competitive exclusion occurs in the white region to the
left and right of the y-axis.
and Eshed 1984, Holt and Pickering 1985, Alexander
and Holt 1998). Plant species can indirectly suppress
each other by promoting a shared pathogen, resulting in
apparent competition that may either weaken or
exacerbate resource competition (Holt 1977, Hatcher
et al. 2006). Pathogens that attack a single species in a
community can reduce the dominance of that species
(Clay et al. 2008), or eliminate already rare or
competitively inferior hosts from the community. The
variety of mechanisms of transmission within and
between species as well as the differential impacts of
pathogens on plants makes predicting the effect of
pathogens on plant diversity in any particular system
difficult (Alexander and Holt 1998, Hatcher et al. 2006).
Although many pathogen-mediated mechanisms have
been examined theoretically and empirically, there is
currently no comprehensive review of the diversity of
pathogen impacts on plant species coexistence. The goal
of this review is to place pathogen dynamics into a
broader community ecology framework by reviewing the
empirical evidence for mechanisms by which pathogens
impact the outcome of plant competition.
Coexistence framework
Recent theoretical work emphasizes that the interaction between competition and predation or parasitism
determines the impact of consumers on the coexistence
of their prey species (Chesson and Kuang 2008).
Contrary to the notion that consumers should increase
diversity by reducing competition, theory emphasizes
that consumers may have positive, negative, or neutral
effects on resource species diversity depending on their
differential impacts across species (Chesson 2000, Chase
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et al. 2002, Chesson and Kuang 2008). Previous models
of two host species and a shared pathogen found that
when transmission within a species exceeds transmission
between species, pathogen attack can promote coexistence (Holt and Pickering 1985, Bowers and Begon 1991,
Begon et al. 1992, Begon and Bowers 1994). These
models highlight a helpful analogy between pathogen
attack and other regulatory processes such as competition, one that I extend here.
To clarify the specific ways in which pathogens can
affect the outcome of competition, I place plant–
pathogen interactions into a community ecology context. In Chesson’s (2000) coexistence framework, niche
differences (species differences in resource use, hostspecific pathogen loads, and other processes that cause
intraspecific limitation to exceed interspecific limitation)
promote coexistence. Niche differences generate negative feedbacks between relative abundance and per
capita growth rates (negative frequency dependence;
see Box 1), which force species to achieve their highest
per capita growth rates at low relative abundance. In
this paper, I will refer to ‘‘stabilization’’ as the processes
that increase self-regulation or niche differences, and to
‘‘destabilization’’ as the processes that increase positive
feedbacks between relative abundance and per capita
growth rates (the positive and negative x-axis of Fig. 1,
respectively). By contrast, differences in competitive
ability, or ‘‘fitness differences,’’ promote exclusion (the
y-axis of Fig. 1). The negative effects of these differences
in overall performance persist even when the inferior
species drops to low density, promoting species dominance. Coexistence requires strong enough stabilization
to overcome the fitness differences between species
(Chesson 2000). Processes can thus promote coexistence
either by increasing stabilization or by decreasing fitness
differences.
Interactions with pathogens, like other processes, can
modify both stabilization and fitness differences. Pathogens influence stabilization when their effect on plant
population growth rates depends on host relative
abundance. For example, host-specific pathogens tend
to increase in prevalence as their preferred hosts become
more abundant, limiting further growth (Fig. 2a). This
general mechanism underlies both the Janzen-Connell
hypothesis (Janzen 1970, Connell 1971) and negative
plant–soil feedbacks (Bever 2003), as discussed in
Stabilizing Effects of Pathogens. Conversely, pathogen
attack can generate destabilizing positive feedbacks
when plants promote the spread of pathogens that harm
competitors more strongly than themselves (pathogen
spillover; Fig. 2b; see Power and Mitchell 2004). This
theoretical framework provides the key insight that
Janzen-Connell effects and pathogen spillover are
opposing extremes of the same process: pathogen attack
that responds to host relative abundance (the stabilization axis in Fig. 1).
In contrast, some pathogens do not respond strongly
to community composition; they apply approximately
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PATHOGEN IMPACTS ON PLANT COMMUNITIES
431
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FIG. 2. Four mechanisms by which pathogens and parasites affect plant communities. (a) Host-specific pathogens reduced
survival in Prunus serotina tree seedlings at high density but not at low density, and this effect disappeared when the soil was
sterilized; data are from Packer and Clay (2000). (b) Hypothetical relationship between survival and relative abundance, for
example, in the spillover of Sudden Oak Death from tolerant bay laurels to susceptible oaks and tanoaks; pathogen-induced
mortality at low relative abundance disappears under sterilization. (c) The plant parasite Cuscuta salina reduces the fitness of the
dominant salt marsh competitor, Plantago maritima, and indirectly increases the fitness of the rare hemiparasitic plant Cordylanthus
maritimus ssp. palustris; Shannon diversity (H 0 ) drops from 2.16 with the parasite present to 1.74 with the parasite removed; data
are from Grewell (2008). (d) Hypothetical infection that increases fitness differences between species, for example, a pathogen that
differentially harms the inferior competitor; removal of this pathogen increases diversity and evenness.
even pressure regardless of host relative abundance,
often due to their broad host ranges or environmental
reservoirs. When these pathogens are more costly to
some species than others, they modify fitness differences
between species. These fitness difference changes may
promote or undermine coexistence, depending on the
strength and relative impacts of pathogens on different
plant species (Fig. 2c, d). Note that many pathogens
may affect both stabilization and fitness differences. In
each of the examples that follow, I highlight the
dominant effect.
Based on this community ecology framework, I
survey the literature on plant–pathogen interactions in
natural systems to assess evidence for pathogen-mediat-
ed community dynamics. In each section, I provide
several illustrative examples; further examples and
references, following the organization of the sections,
can be found in Table 1. These references are not
intended to be exhaustive, but instead provide a broad
survey of known pathogen impacts on natural communities. Incorporating empirical studies into this theoretical framework provides intuition for how particular
classes of pathogens are likely to affect communities. At
the same time, this framework clarifies the relationship
between a range of pathogen-mediated mechanisms such
as Janzen-Connell effects, plant–soil feedbacks, pathogen spillover, enemy escape of invasive plants, and
competition–defense trade-offs.
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Vol. 81, No. 3
ERIN A. MORDECAI
TABLE 1. Mechanisms by which pathogens affect plant community dynamics.
Mechanism
Systems
A) Density-dependent pathogens
1) Stabilization: disease transmission and/or cost
increases as a species becomes common
Janzen-Connell/host-specific pathogens
Negative plant–soil feedbacks
old fields (15); tropical trees (16); reviews (17–19)
Density-dependent attack
grazed clover (20); Ustilago violacea and its hosts (21–23);
herbivore-vectored diseases (24–26); reviews (27, 28)
Density-dependent cost of infection
sterilizing pathogens (29–32); rust infections in Impatiens capensis
(33); agricultural weeds (34); generalist root rot (35)
Disease responds to host diversity
agriculture: crop rotation (36); mixed genotype plantings (37–39);
mixed crop plantings (40); grasslands (41, 42); Solidago altissima
genotypes (43); review (44)
2) Destabilization: disease transmission and/or cost
increases as a species becomes rare
Pathogen spillover
Positive plant–soil feedbacks
sudden oak death (45–47); invaded annual grasslands (48);
review (48)
grasslands (49, 50); review (27)
B) Density-independent pathogens
1) Reduced fitness differences: competitively dominant
species experience the greatest cost of pathogens
Equalizing trade-offs
Enemy release of invading plants
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tropical trees (1–8); temperate trees (9, 10); grasslands (11);
Australian eucalypt forests (12); reviews (8, 9, 13, 14)
Agriculture and biocontrol
salt marsh plants (51, 52); weedy perennials (53); grasslands
(54–57); fast-cycling Brassica species (58); root rot in eucalypt
forests (35) and Douglas-fir forests (59)
tropical shrub (60); reviews (61–66)
soybean fields (67, 68); cultivated clover (69); reviews (27, 70–73)
2) Fitness hierarchy reversal/increased fitness differences:
susceptible hosts face extreme fitness costs
Pathogen-driven succession
dune grasses (74–76); coniferous forests (77); old fields (78)
Highly virulent epidemics
chestnut blight (79–81); Phytophthora cinnamomi in Australian
forests (77, 82); Dutch elm disease (83); review (84)
Notes: The table is divided into systems in which pathogens respond to host density or relative abundance and those in which
they do not: (A) density-dependent pathogens; (B) density-independent pathogens. Systems are the community type or the specific
plant or pathogen in which these interactions have been studied, reported with corresponding numbered references: (1) Augspurger
1983; (2) Augspurger 1984; (3) Augspurger 1988; (4) Augspurger and Kelly 1984; (5) Bagchi et al. 2010; (6) Bell et al. 2006; (7)
Gilbert et al. 1994; (8) Wright 2002; (9) HilleRisLambers et al. 2002; (10) Packer and Clay 2000; (11) Petermann et al. 2008; (12)
Burdon and Chilvers 1974; (13) Freckleton and Lewis 2006; (14) Gilbert 2005; (15) Mills and Bever 1998; (16) Mangan et al. 2010;
(17) Bever 2003; (18) Ehrenfeld et al. 2005; (19) Kulmatiski et al. 2008; (20) Bowers and Sacchi 1991; (21) Burdon 1987; (22)
Jennersten et al. 1983; (23) Gibson et al. 2010; (24) Christiansen (1991); (25) Okland and Berryman 2004; (26) Silliman and Newell
2003; (27) Antonovics and Levin 1980; (28) Burdon and Chilvers 1982; (29) Bradshaw 1959; (30) Roy 1993; (31) Roy 1994; (32)
Wennström and Ericson 1991; (33) Lively et al. 1995; (34) Paul and Ayres 1987; (35) Jarosz and Davelos 1995; (36) Peters 2003; (37)
Jeger 2000; (38) Wolfe 1985; (39) Zhu et al. 2000; (40) Van Rheenen et al. 1981; (41) Schnitzer et al., in press; (42) Maron et al. 2010;
(43) Schmid 1994; (44) Keesing et al. 2006; (45) Davidson et al. 2003; (46) Meentemeyer et al. 2004; (47) Rizzo and Garbelotto 2003;
(48) Power and Mitchell 2004; (49) Batten et al. 2008; (50) Olff et al. 2000; (51) Callaway and Pennings 1998; (52) Grewell 2008; (53)
Orrock and Damschen 2005; (54) Allan et al. 2010; (55) Peters and Shaw 1996; (56) Malmstrom et al. 2005; (57) Borer et al. 2007;
(58) Bradley et al. 2008; (59) Holah et al. 1993; (60) DeWalt et al. 2004; (61) Blumenthal et al. 2009; (62) Colautti et al. 2004; (63)
Keane and Crawley 2002; (64) Klironomos 2002; (65) Mitchell and Power 2003; (66) Mitchell et al. 2006; (67) Chen et al. 1995; (68)
Ditommaso and Watson 1995; (69) Groves and Williams 1975; (70) Charudattan and Dinoor 2000; (71) McFadyen 1998; (72)
Smith and Holt 1997; (73) Te Beest et al. 1992; (74) De Rooij-Van der Goes 1995; (75) Van der Putten et al. 1993; (76) Van der
Putten and Peters 1997; (77) Dickman 1992; (78) Kardol et al. 2007; (79) Day and Monk 1974; (80) Nelson 1955; (81) Woods and
Shanks 1959; (82) Weste 1981; (83) Gibbs 1978; (84) Burdon 1993.
STABILIZING EFFECTS
OF
PATHOGENS
Pathogens stabilize plant communities when their per
capita costs increase with plant species frequency in the
community (Fig. 2a). Gillett (1962) hypothesized that
pathogens and other pests were responsible for the
‘‘apparently pointless multiplicity of species,’’ by constantly adapting to build up on the most common
species and thereby favoring rarer species that were less
attacked. Clay et al. (2008) refer to this stabilizing
mechanism as frequency-dependent selection against
common species, in a community-level analogy to the
Red Queen hypothesis from population genetics. Frequency-dependent reductions in population growth
encompass the Janzen-Connell hypothesis (Janzen
1970, Connell 1971), negative plant–soil feedbacks
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PATHOGEN IMPACTS ON PLANT COMMUNITIES
433
BOX 1. More on the coexistence framework
driven by soil biota (Mills and Bever 1998, Bever 2003),
and other plant–pathogen interactions that intensify as
plants become abundant (Gillett 1962). The demographic cost of stabilizing pathogens increases with host
species relative abundance in the community, rather
than with overall plant density. Studies demonstrating
that pathogen-induced mortality depends on the density
of conspecifics but not heterospecifics provide strong
evidence for stabilization.
Janzen (1970) and Connell (1971) hypothesized that
tree diversity in tropical forests was maintained by
specialist herbivores and seed predators that build up on
common species, affording rare, relatively enemy-free
species an advantage. The hypothesis postulates that
seed and/or seedling survival increases with distance
from the parent tree, due to escape from host-specific
enemies. This distance- or density-dependent mortality
leads to advantages for seeds dispersing outside the
range of their host-specific enemies and into areas
currently occupied by trees of another species (Nathan
and Casagrandi 2004). More recently, the hypothesis has
been extended to include specialist pathogen attack
(Gilbert 2005) and has been applied to a range of plant
communities (Table 1). For example, Gilbert and
colleagues (1994) showed that seedlings of the tropical
tree Ocotea whitei were more likely to die of canker
disease when densely clustered near a parent tree, while
healthy seedlings were more likely to grow near adult
trees that were not susceptible to the disease. In this and
other examples, distance dependence and density dependence are inextricably linked (Nathan and Casagrandi 2004). As reviewed elsewhere (Lieberman 1996),
many empirical studies have demonstrated a negative
relationship between the survival or growth of seedlings
and the density of seedlings or their proximity to a
conspecific adult, but most do not explicitly investigate
the biological processes responsible (Freckleton and
Lewis 2006). While a few studies clearly demonstrate the
role of host-specific pathogens in stabilizing communities, other systems with density- and distance-dependent
mortality of seedlings may be driven by interactions with
soil pathogens as well.
Negative feedbacks between plants and the soil biota
are a closely related stabilizing mechanism in which
specialist pathogens accumulate in the soil of abundant
species, benefiting rare individuals that invade soil
cultured by other species (Bever 2003). For example,
Pythium fungi isolated from two old-field plant species
differentially reduced the growth of those species over
two competitor species, contributing to negative plant–
soil feedbacks that may stabilize coexistence (Mills and
Bever 1998). Negative plant–soil feedbacks have been
reviewed in several publications (Table 1), though few of
these studies test for the role of pathogens in generating
negative feedbacks.
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Stable coexistence requires that each species in a community be able to increase when invading a system
filled with its competitors: the mutual invasibility criterion (Turelli 1978, Chesson 2000). This requires all
species to have greater per capita growth rates when rare than when common. These rare-species advantages
generate a negative correlation between per capita growth rates and relative abundance, sometimes called
‘‘negative frequency dependence.’’ Note that in this context, frequency dependence refers to the response of
per capita growth rates to relative abundance, rather than the response of disease transmission to the
proportion of infected individuals, as in epidemiology (Antonovics and Alexander 1992). Following Chesson
(2000), I refer to processes that increase negative frequency dependence as ‘‘stabilizing,’’ because they promote
stable coexistence. Stabilizing processes can also be thought of as self-regulation or negative feedbacks because
they slow down the growth of common species and favor the growth of rare species. These processes include
partitioning of resources or natural enemies, temporal or spatial segregation, and differential responses to
environmental fluctuations (Chesson 2000).
Although stabilizing processes require growth rates to decline with relative abundance in the community,
the underlying mechanism may involve a response to the density of a particular host, rather than its relative
abundance per se. For example, host-specific disease transmission may increase with the density of a
susceptible host. But as a host species increases, this changes relative abundance in a way that mirrors changes
in density.
In contrast to frequency-dependent processes, ‘‘fitness differences’’ generated by differences between species
in factors such as competitive ability, disease resistance or tolerance, or fecundity, do not change with relative
abundance. These fitness differences can be thought of as overall differences in competitive ability because
they predict the outcome of competition if stabilizing processes were removed. The special case in which
species in a community have no fitness differences (nor stabilizing processes) forms the basis of Hubbell’s
(2001) neutral theory of biodiversity. Life-history trade-offs can reduce fitness differences and promote
coexistence, equalizing processes sensu Chesson (2000). These trade-offs may also have stabilizing components
because a species with a particular strategy is favored when a species with the opposite strategy is abundant.
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ERIN A. MORDECAI
The reversal of plant–soil feedbacks has recently been
suggested to explain the success of invasive species
(Callaway et al. 2004, Van der Putten et al. 2007, but see
Turnbull et al. 2010). The soil biota inhibits the growth
of Centaurea maculosa in its native range in France, but
promotes growth in sites in Montana where it is exotic
(Callaway et al. 2004). More generally, Klironomos
(2002) found that five highly invasive species in
Canadian meadows each had positive or neutral plant–
soil feedbacks, while five rare native annuals had strong
negative feedbacks driven by pathogens. The strength
and direction of the feedback predicted relative abundance in the field for 61 species in an old-field site
(Klironomos 2002). These studies suggest that release
from negative feedbacks promotes invader dominance.
By contrast, strong negative plant–soil feedbacks for the
successful tree invader Sapium sebiferum due to rapid
accumulation of host-specific soil pathogens in its exotic
range have likely prevented the invader from forming
dense monocultures (Nijjer et al. 2007).
Perhaps due to the focus on the Janzen-Connell
hypothesis and, more recently, the development of
theory on plant–soil feedbacks, other plant–pathogen
stabilizing mechanisms remain largely unexplored.
When the risk or cost of pathogen attack increases with
the density of a particular species, this attack is
stabilizing because pathogen impacts increase as a
species becomes abundant. A study of mixed-species
eucalyptus stands in Australia found considerable
evidence for host-specific pathogen attack on saplings,
which helps to stabilize the coexistence of closely related
and ecologically similar species (Burdon and Chilvers
1974). In a cross-species comparison of Silene species,
rare species were significantly less likely to sustain
anther-smut disease than nonthreatened species, even
though all species were susceptible to infection (Gibson
et al. 2010). More generally, Burdon and Chilvers (1982)
found that most plant diseases showed a positive
correlation between plant population density and
disease incidence, and that the majority of systems in
which incidence declined with plant density were aphidvectored viruses. Indeed, endangered plant species tend
to have fewer fungal pathogens than their nonthreatened
relatives (Gibson et al. 2010).
When herbivore pressure increases with host relative
abundance, herbivore-vectored diseases should also
exert stabilization. No studies have drawn direct links
between host density, herbivore outbreaks, and disease
pressure. However, Littorina snails and the fungus they
farm on the salt marsh grass Spartina alterniflora
synergistically reduce plant growth in southeastern
U.S. salt marshes (Silliman and Newell 2003), and snail
populations likely respond behaviorally and numerically
to plant density (B. Silliman, personal communication).
Similarly, the spruce bud beetle, which transmits the
lethal blue-stain fungus as it feeds on spruce trees in
Norway, may also respond to tree density (Christiansen
1991, Okland and Berryman 2004). In both of these
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cases, if herbivores aggregate in dense host stands, the
resulting increase in disease transmission may regulate
host plant populations.
Pathogens that inflict density-dependent costs are also
strong regulators of host populations (Anderson and
May 1981). Density-dependent costs of infection can
arise when pathogens benefit vegetative growth at the
expense of sexual reproduction (Bradshaw 1959, Roy
1994). For example, a castrating endophyte infection
benefits its Agrostis grass hosts at low host density
(under heavy livestock grazing) by promoting vegetative
growth, but this infection is costly at high density due to
reduced seed production (Bradshaw 1959). Infections
that are more costly under dense, highly competitive
conditions have been observed in several natural and
agricultural systems (Table 1). Alternatively, in eucalypt
forests in southern Australia, the root rot Armillaria
luteobubalina creates infected patches in which all woody
vegetation is killed, but these open patches then provide
habitat for colonizer species (Jarosz and Davelos 1995).
These secondary succession species may not be able to
establish in closed canopy, but the 3–5% of the forest
infected at a time provides open space that allows these
species to persist. When increased competition at high
density reduces the capacity of plants to resist,
compensate for, or tolerate disease, these pathogens
are also stabilizing. In each of the mechanisms discussed
in this section, stabilizing effects need not involve
multispecies interactions with pathogens, as long as the
pathogen regulates its host population as a function of
density.
Disease responds to host diversity
Research in agricultural systems has produced a
convincing body of indirect evidence for the importance
of frequency-dependent pathogen attack. Farmers control disease in their crops by increasing plant diversity in
order to reduce transmission. These disease-control
tactics imply that disease transmission increases with
relative abundance, indicating stabilizing impacts of
disease. Three widely used disease control methods are
crop rotation, which increases diversity temporally to
prevent disease buildup (Peters et al. 2003), mixed
plantings of genetically diverse varieties that vary in
disease resistance (Wolfe 1985, Jeger 2000, Zhu et al.
2000), and planting multiple crops within a field (Van
Rheenen et al. 1981). These diversity treatments reduce
disease because per capita pathogen transmission
decreases as a particular crop variety declines in relative
abundance. The fact that methods for controlling crop
disease by increasing diversity are so widespread is
indirect evidence for the stabilizing nature of many
pathogens.
In natural communities, disease transmission often
increases in low-diversity stands where individual species
reach high relative abundance. Schnitzer et al. (2011)
found that disease decreased with increasing diversity in
grassland communities. Release from disease increased
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PATHOGEN IMPACTS ON PLANT COMMUNITIES
plant productivity in high-diversity stands; at low
diversity, productivity was reduced by 500% due to
host-specific disease. Maron et al. (2010) found similar
results: pathogens generate a positive relationship
between plant diversity and productivity by dramatically
decreasing productivity in low-diversity stands. A study
of the interaction between pathogen pressure and
genetic diversity in Solidago altissima found that
pathogen levels were initially higher in high-diversity
stands, but over time the pattern reversed as specific
pathogen strains became abundant on common genotypes in low-diversity plots (Schmid 1994). This study
provides evidence that pathogen specialization on a few
common genotypes can develop over time, a mechanism
that may also promote diversity in multispecies mixtures. More broadly, several studies highlight a variety
of mechanisms by which host diversity can decrease or
increase disease transmission, implying stabilization or
destabilization, respectively (Dobson 2004, Keesing et
al. 2006, 2010).
DESTABILIZING EFFECTS
OF
PATHOGENS
spillover is likely in many plant communities, especially
those in contact with agricultural populations.
Pathogens that generate positive plant–soil feedbacks
can also destabilize plant species interactions. Olff and
colleagues (2000) found that the grasses Festuca rubra
and Carex arenaria both grew better in soil cultured by
conspecifics, leading to shifting mosaics of patches
dominated by a single species. In contrast to negative
plant–soil feedbacks, which give species advantages
when invading soil cultured by other species, positive
plant–soil feedbacks are highly destabilizing and drive
single-species dominance. In these systems with positive
feedbacks, larger-scale community composition depends
on initial conditions.
Stabilization and destabilization arise when pathogens
generate feedbacks between host relative abundance and
population growth rates. Specialist pathogens that
preferentially harm common species stabilize species
interactions and improve conditions for coexistence. On
the other hand, generalist pathogens with tolerant
reservoir hosts destabilize by creating positive feedbacks.
PATHOGENS
AND
FITNESS DIFFERENCES
When pathogen effects do not depend strongly on
host density or relative abundance, these pathogens
cannot stabilize coexistence but can alter fitness differences between species. Fitness differences are the
characteristics that give species population growth rate
advantages over others, independent of density—for
example, differences in competitive ability, seed production, or susceptibility to pathogens. Without stabilization, these fitness differences lead to the exclusion of the
inferior species. Pathogens can decrease fitness differences by differentially harming the competitive dominant (Fig. 2c), increase fitness differences by attacking
already inferior competitors (Fig. 2d), or shift community composition altogether by altering the competitive
hierarchy of species. However, the majority of research
has focused on (1) pathogens that reduce the fitness of
competitive dominant species, promoting coexistence,
and (2) pathogens that reduce the fitness of resident
species, promoting invasion. Of course these two
categories are not mutually exclusive. In fact, resident
species that face invasion following pathogen-induced
reductions in fitness may also be the competitive
dominant species in the absence of pathogen attack.
However, pathogen-driven fitness costs to competitively
dominant species and resident species are two major
routes by which previous research has shown that
pathogen attack modifies fitness differences.
Pathogens that reduce the fitness
of otherwise dominant competitors
Pathogens can reduce fitness differences by keeping
competitive dominant hosts in check, promoting diversity via competition–defense trade-offs in which strong
competitors are most susceptible to pathogens (Holt and
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Pathogens that differentially harm rare species are
destabilizing because they create positive feedbacks
between relative abundance and population growth.
Pathogen spillover is a well-recognized destabilizing
mechanism in which a tolerant or highly competent host
species sustains a large pathogen population that harms
competing species more than the tolerant host (Dobson
2004, Power and Mitchell 2004). Destabilizing spillover
occurs when the transmission a species promotes is
disproportionate to the costs it suffers. When a tolerant
species becomes common in a community, it promotes
pathogen attack that reduces its competitors’ population
growth rates, further benefiting the tolerant species (Fig.
2b). For example, the Sudden Oak Death (SOD)
epidemic that has decimated populations of oaks and
tanoaks in the United States is largely driven by the bay
laurel and other tolerant trees, which can harbor dense
foliar infections that produce many spores without
killing the tolerant hosts (Rizzo and Garbelotto 2003,
Cobb et al. 2010). The SOD pathogen infects host
species by multiple pathways: nonlethal foliar infections
like those found on the bay laurel produce the majority
of spores and drive transmission, while lethal cankers
that develop on oaks and tanoaks kill the host but
produce few spores (Cobb et al. 2010). Tolerant
reservoir hosts for other diseases include the invasive
grasses Avena fatua, which substantially increases the
prevalence of barley yellow dwarf virus (BYDV) in other
annual grasses (Power and Mitchell 2004), and Bromus
tectorum, which creates dense seed beds that foster the
growth of a fungus that kills native seeds (Beckstead et
al. 2010). While broader evidence of pathogen spillover
destabilizing natural plant communities is lacking,
Power and Mitchell (2004) highlight the importance of
spillover in animal and human diseases and suggest that
435
REVIEWS
436
ERIN A. MORDECAI
Dobson 2006). When competitive dominant species are
more suppressed by pathogens, inferior species benefit
indirectly from reduced competition (Fig. 2c). For
example, the parasitic plant Cuscuta salina preferentially
attacks the competitive dominant pickleweed species in
northern and southern California salt marsh systems,
promoting the coexistence of inferior competitors (Callaway and Pennings 1998, Grewell 2008). Similarly, the
barley yellow dwarf viruses (BYDV) have reversed the
competitive dominance of native grasses in California,
facilitating the invasion and spread of European annual
grasses (Malmstrom et al. 2005, Borer et al. 2007).
Pathogens that directly benefit rare species also reduce
fitness differences. Pathogens increased diversity in
mesocosm experiments with four Brassica species
because infected individuals of two rare species produced more seed than uninfected individuals, in an
overcompensation response (Bradley et al. 2008). In
other systems, pathogens infect all species but impose
differential costs. Although equalizing competition–
defense trade-offs are widely invoked as a mechanism
underlying coexistence (see Viola et al. 2010), relatively
few studies implicate the role of pathogens in these
trade-offs (Table 1).
Large-scale epidemics are dramatic examples of
pathogens that reduce dominant species fitness and alter
community composition. Epidemics can increase fitness
differences and thereby exclude susceptible species. A
well-known example is chestnut blight, which swept
through North American forests and decimated the
dominant chestnut, leading to replacement by nonsusceptible oak, maple, poplar, and hickory species
(Nelson 1955, Woods and Shanks 1959). Similarly, the
outbreak of the generalist fungus Phytophthora cinnamomi in Australian sclerophyll woodlands caused
wholesale shifts in vegetation from trees and shrubs to
a resistant sedge species, Lepidosperma concavum (Weste
1981, Dickman 1992). When highly virulent pathogens
decimate populations, the indirect fitness advantage to
unsusceptible species can completely restructure the
community (Table 1).
Epidemic pathogens are variable in space and time.
Following outbreaks, transmission subsides when susceptible individuals become too scarce. If the susceptible
population is able to reestablish after an epidemic, these
diseases may also play a stabilizing, if sporadic, role in
the community over time. The nonspecialist Australian
root rot case discussed in Stabilizing Effects of
Pathogens is one example of the stabilizing effect of
spatial and temporal variation in pathogen attack
(Jarosz and Davelos 1995; Table 1).
Finally, numerous studies of pathogen or parasite
effects on fitness differences between crops and weeds
have been performed in agricultural systems, due to the
financial importance of maximizing crop yield (i.e.,
maximizing the fitness of crop plants relative to weeds).
An excellent example is provided by two complementary
studies examining the interaction between soybeans,
Ecological Monographs
Vol. 81, No. 3
weed plants (Abutilon theophrasti and Chenopodium
album), and their pathogens and parasites (Chen et al.
1995, Ditommaso and Watson 1995). One study found
that both crop plant infection with the soybean cyst
nematode and interspecific competition with Chenopodium reduced soybean plant biomass (Chen et al. 1995).
Nematode infection reduced the competitive ability of
the soybean, and may thereby promote Chenopodium
coexistence in agricultural fields. On the other hand,
when the weed Abutilon theophrasti is inoculated with a
fungal pathogen that does not infect soybeans, the
biomass of the weed is reduced and soybean biomass
increases (Ditommaso and Watson 1995). The fungal
pathogen reduces the fitness of Abutilon relative to the
soybean, and is thus a candidate for biocontrol of the
weed. These agricultural studies provide clear examples
of how pathogen-driven reductions in crop fitness
promote the persistence of weeds, while decreasing the
fitness of the weed speeds its exclusion (Table 1).
Agricultural studies that test the effects of pathogens
on fitness differences are good models for designing
experiments in natural communities.
Pathogens that harm residents and benefit newly
colonizing species
When pathogens reduce the fitness of resident species,
they increase the probability of colonization and
establishment by species not limited by pathogens. This
is perhaps the most well-known route by which
pathogens are thought to modify fitness differences:
invasive plants leave behind their natural enemies and
thereby achieve higher fitness that allows them to
establish and spread in exotic ranges (Elton 1958, Keane
and Crawley 2002). This natural enemies hypothesis
posits that release from pathogen limitation favors
invaders over natives and, importantly, it implies that
natural enemies are a strong regulatory force for plants
in their native ranges. In a review of fungal and viral
pathogens of 473 plant species naturalized in the United
States from Europe, Mitchell and Power found that
these plants had on average 84% fewer fungal species
and 24% fewer viruses in their introduced range than in
their home range (Mitchell and Power 2003). Furthermore, the more complete the release from pathogens, the
more ‘‘invasive’’ and ‘‘noxious’’ the plants tended to be,
based on economic cost and environmental impact
(Mitchell and Power 2003). While many invasive species
have escaped most of their enemies, few studies have
shown that this release actually improves the fitness of
introduced species, or in particular that escape from
pathogens gives invaders the competitive benefit over
enemy-regulated natives that promotes invasion (Keane
and Crawley 2002, Hierro et al. 2005). Further, other
studies have found that evidence for release from
enemies is equivocal (Blaney and Kotanen 2001,
Beckstead and Parker 2003, Parker and Gilbert 2007),
as reviewed by Gilbert and Parker (2006). Indeed, the
BYDV example discussed in the previous section,
August 2011
PATHOGEN IMPACTS ON PLANT COMMUNITIES
Pathogens and fitness differences: Pathogens that reduce
. . . , is a case in which the gain, rather than loss, of
natural enemies promotes invasion. Experiments that
directly manipulate pathogen load on exotic and native
species or on populations from invasive vs. native ranges
would provide clear evidence on the role of pathogens in
the invasion process (Keane and Crawley 2002, Mitchell
et al. 2006).
In successional communities, pathogens can accelerate species replacement by building up on early
colonizers. In dunes in The Netherlands, each species
along the successional sequence tolerates soil cultured by
its predecessors better than soil from conspecifics and
later-successional species (Van der Putten et al. 1993).
More mechanistically, each species suffers from the
accumulation of soil enemies until it is replaced by the
next successor. Because species cannot tolerate the soil
of these successors, community composition shifts in a
single direction until fresh wind-blown sand replaces
plant-cultured soil. Soil feedbacks such as these provide
a fitness advantage for late successional species rather
than stabilizing coexistence. Pathogens have also been
found to drive succession and create historical contingency effects in other systems (Table 1).
SYNTHESIS
Directions for future research
Experiments can demonstrate stabilizing effects of
pathogens in natural communities by measuring the
effect of pathogen removal or addition on per capita
growth rates, over a range of relative abundances. Such
an experiment would follow the approach of Adler et al.
(2007) and Levine and HilleRisLambers (2009) to
measure per capita growth rates as a function of relative
abundance, when pathogens are either present (naturally
or due to inoculation) or absent (naturally or due to
fungicide application or soil sterilization). In this
approach, species relative abundance is experimentally
varied from low to high frequency, and per capita
growth rates are calculated. If disease stabilizes community dynamics, species will experience high growth
rates when rare due to low pathogen pressure, and
decreased growth rates when common resulting from
high pathogen pressure. Importantly, the stabilizing
effect of pathogens will be demonstrated by the degree
to which the slope between per capita growth rate and
relative abundance becomes more negative in the
presence of pathogens.
Models fit to field data make similar predictions for
less easily manipulated species, such as long-lived trees,
rare plants, and highly destructive epidemic pathogens
(Nathan and Casagrandi 2004). Models can also aid in
extending single-species or local-scale effects to community-level implications. In fact, several studies have
already used data-driven modeling to extrapolate from
local demographic effects to community-level coexistence mechanisms. In the barley yellow dwarf virus
(BYDV) study discussed in Pathogens and Fitness
Differences, Borer and colleagues (2007) used a parameterized model to show that the virus reverses the
competitive hierarchy, and that native grasses should
exclude the invasive grass in the absence of BYDV.
Petermann et al. (2008) also used a field-parameterized
model to show that negative plant–soil feedbacks
observed in European grasslands were strong enough
to stabilize coexistence of three plant functional groups
(Table 1).
Theoretical models predict that vector transmission,
free-living infective stages, multiple forms of infection,
and other modes that deviate from direct transmission can
affect coexistence mechanisms, but many of these
predictions have not been empirically tested (Anderson
and May 1981, Holt and Pickering 1985, Bowers and
Begon 1991, Begon et al. 1992, Begon and Bowers 1994,
Rudolf and Antonovics 2005). Broadly, these models
predict that pathogen attack is stabilizing when withinspecies transmission exceeds between-species transmission, while when the reverse is true, the species best able to
tolerate or recover from disease can exclude the others
(Holt and Pickering 1985, Begon and Bowers 1994,
Dobson 2004). The present review, by comparing the
pathogens largely transmitted within species (e.g., the
Janzen-Connell studies) to the cases of pathogen spillover,
has given broad evidence in support of this prediction.
However, no empirical study has shown that variation in
within- vs. between-species transmission within the same
plant–pathogen system can affect the outcome of the
interaction. Similarly, the prediction that one host species
REVIEWS
Coexistence requires that each species be able to
invade the community when it is rare and its competitors
are common (Chesson 2000). Such mutual invasibility
requires species to have greater per capita growth rates
when rare than when common, generating frequency
dependence (Siepielski and McPeek 2010). Surprisingly,
pathogen effects on frequency dependence or mutual
invasibility were not demonstrated in any study
reviewed here. Instead, most studies inferred community-level coexistence mechanisms from single-species
interactions. Even studies on Janzen-Connell effects
and plant–soil feedbacks (two of the best-studied
pathogen-driven coexistence mechanisms) have not
shown direct evidence that pathogens generate frequency dependence. Janzen-Connell studies usually measure
pathogen effects on seedling survival as a function of
population density or distance from conspecifics, without showing that these effects generate rare-species
advantages and without reference to other species in the
community. This single-species focus is also true for a
model of distance-dependent seed dispersal and predation, based on the Janzen-Connell mechanism (Nathan
and Casagrandi 2004). Plant–soil feedback studies focus
on a specific pairwise interaction pathway without
demonstrating that these local-scale interactions generate frequency dependence in population growth rates
(but see Mangan et al. 2010).
437
438
ERIN A. MORDECAI
can exclude another via a shared pathogen, even when
each species alone can persist with the pathogen (Holt and
Pickering 1985), has not been borne out empirically.
Finally, more empirical work is needed to evaluate the
prediction that vector-transmitted shared diseases should
decline with increasing host diversity, a stabilizing effect
(Dobson 2004, Rudolf and Antonovics 2005). Here, I
evaluate only two examples of two vector-transmitted
diseases, but of these, BYDV is destabilizing while
Ustilago violacea is stabilizing (Table 1).
In this review, I have qualitatively identified the most
likely effect of pathogens in a variety of plant
communities (Table 1). While this provides some useful
guidelines for understanding the importance of pathogens for plant community dynamics, an important next
step is to quantitatively compare the strength of
pathogen-mediated mechanisms with other processes
that regulate community dynamics. Further knowledge
of the role that pathogens play in mediating community
dynamics is critical in light of species introductions,
habitat loss and fragmentation, climate change, and
other anthropogenic changes that will likely affect the
intensity and diversity of plant–pathogen interactions in
the future (Thompson et al. 2010).
REVIEWS
ACKNOWLEDGMENTS
I thank Jonathan Levine, Kevin Lafferty, David Viola, Ben
Gilbert, Jennifer Williams, Jarrett Byrnes, and Greg Gilbert for
helpful comments on this manuscript. This work was supported
by graduate research grants from the Department of Ecology,
Evolution, and Marine Biology at the University of California–
Santa Barbara.
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