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Journal of Ecology 2013, 101, 607–613
doi: 10.1111/1365-2745.12078
ESSAY REVIEW
Pathogen accumulation and long-term dynamics of
plant invasions
S. Luke Flory1* and Keith Clay2
1
Agronomy Department, University of Florida, PO Box 110500, Gainesville, FL 32611, USA; and 2Department of
Biology, Indiana University, 1001 East 3rd Street, Bloomington, IN 47405, USA
Summary
1. The diversity of pathogens on highly abundant introduced hosts has been positively correlated
with time since introduction, geographical range of the introduced species and diversity of invaded
habitats. However, little is known about the ecological effects of pathogen accumulation on nonnative invasive plants.
2. Pathogen accumulation on invasive plant species may result from ecological processes such as
high plant densities, expanding geographical ranges and pathogen dispersal from the native range, or
evolutionary mechanisms such as host range shifts and adaptation of native pathogens to invasive
species.
3. Over time pathogen accumulation may cause decline in the density and distribution of invasive
plants and facilitate recovery of native species. Alternatively, pathogens might build up on invasive
species and then spill back onto co-occurring native species, further exacerbating the effects of invasions.
4. Synthesis. Research efforts should focus on determining the long-term outcomes of pathogen
accumulation on invasive species. Such research will require multifaceted approaches including comparative studies of diverse invasive species and habitats, experimental manipulations of hosts and
pathogens in nature and controlled environments, and predictive models of host-pathogen interactions within an invasion framework. Results of this research will improve our understanding and
ability to predict the outcomes of biological invasions.
Key-words: abundance, introduced species, invasion ecology, plant density, population decline,
species diversity, spillback
Introduction
A primary goal of ecological research has been to identify
mechanisms underlying biological invasions, which are key
drivers of global environmental change and require substantial
economic resources for management. Dozens of hypotheses
have been proposed to explain why some species become
invasive (Catford, Jansson & Nilsson 2009) and why some
habitats are vulnerable to invasion (Stohlgren et al. 2002).
However, abiotic and biotic factors affecting invasive species
are likely to change over time due to varying environmental
conditions, habitat disturbance, repeated introductions of distinct genotypes, expanding distributions leading to novel
interactions and evolution of invaders or co-occurring pathogens (e.g. Bossdorf et al. 2005; Gilbert & Parker 2010).
Research on post-introduction evolution (Maron et al. 2004)
*Correspondence author. E-mail: flory@ufl.edu
and the introduction of biological controls (reviewed by
Culliney 2005) suggests that interactions of invasive species
with enemies, competitors and mutualists can co-evolve and
feedback to affect the dynamics of invasive species over time.
Of the many hypotheses to explain biological invasions,
there is perhaps the greatest empirical support for the release
of invasive species from natural enemies when they are introduced into a new range, which then gain a competitive advantage over resident species (but see van Kleunen & Fischer
2009; Chun, van Kleunen & Dawson 2010). For example,
experimentally excluding pests from the shrub Clidemia hirta
promoted growth in its native, but not non-native, range
(DeWalt, Denslow & Ickes 2004). Similarly, black cherry
(Prunus serotina) seedling recruitment is suppressed near
adult trees in native U.S. habitats by below-ground Pythium
pathogens, but not in Europe where it invades forest understories (Reinhart et al. 2003). Although invasive species may
initially benefit from enemy escape, over the longer-term
© 2013 The Authors. Journal of Ecology © 2013 British Ecological Society
608 S. L. Flory & K. Clay
pathogens can accumulate, potentially reducing the effects of
invaders on native communities and ecosystems. For example,
in an analysis of 124 plant species, those that were introduced
400 years ago had six times more pathogens than those introduced only recently (Mitchell et al. 2010), but the effects of
those pathogens on hosts were not known. Alternatively,
pathogen accumulation may exacerbate the effects of invasions if pathogens spill back onto co-occurring native species
and reduce their performance and competitive inhibition of
invasive species (Kelly et al. 2009). The long-term dynamics
of plant invasions and their impacts on native communities
and ecosystems may be determined by interactions among
pathogens, invasive plants and co-occurring native species.
Here, we describe the patterns, mechanisms and potential outcomes of pathogen accumulation on invasive species with the
goal of generating discussion and research on how pathogens
alter the long-term dynamics of plant invasions. The results
of this research will improve our understanding and ability to
predict the outcomes of biological invasions.
time relative to rarer, less-dense species (Bever 1994; Olff
et al. 2000; Clay et al. 2008; Mitchell et al. 2010). However,
it is less apparent whether pathogen accumulation occurs
through ecological or evolutionary mechanisms, or by some
combination. Ecological mechanisms include spatiotemporal
dynamics, host density or abiotic conditions. For example, as
species invade wider geographical areas, there will be greater
encounter rates with native pathogens, and the number of
pathogens that accumulate may increase in the same or even
(a)
(b)
(c)
(d)
(e)
(f)
Patterns of pathogen accumulation
The limited research on pathogen accumulation in natural systems has demonstrated that the richness and diversity of
pathogens on introduced hosts are positively correlated with
time since introduction (Hawkes 2007), the geographical
range of the introduced species (Strong & Levin 1975; Clay
1995) and the diversity of invaded habitats (Mitchell et al.
2010). Many invasive plants, including grasses, forbs, trees
and ferns become infected by pathogens in their introduced
ranges (Fig. 1). For example, the invasive grass Microstegium
vimineum (stiltgrass) is infected by Bipolaris fungi (Fig. 1a,
Kleczewski & Flory 2010; Flory, Kleczewski & Clay 2011;
Kleczewski, Flory & Clay 2012), Alliaria petiolata (garlic
mustard) by powdery mildew (Fig. 1c, Enright & Cipollini
2007) and Pueraria lobata (kudzu) by soybean rust (Fig. 1f,
Harmon et al. 2006). Accumulation of below-ground pathogens, which are more difficult to identify, may also occur.
For example, the invasive tree Sapium sebiferum (Chinese tallow) survived more poorly and produced less biomass in
‘home’ compared with ‘away’ soils (Nijjer, Rogers &
Siemann 2007). Similarly, Diez et al. (2010) found that the
strength of negative plant–soil feedback increased with time
since introduction for 12 species in New Zealand. However,
neither study identified biological agents responsible for
decreased plant growth or excluded other potential mechanisms such as reduced benefit from soil mutualists or changes
in soil chemistry. Nevertheless, demonstrations of accumulation of above-ground pathogens and increasing negative plant
–soil feedbacks over time suggest that pathogen accumulation
on invasive species is widespread and potentially important
for regulating invasive plant populations.
Mechanisms of pathogen accumulation
Highly abundant species, such as invasive species, are
expected to exhibit greater accumulation of pathogens over
Fig 1. Examples of pathogen accumulation on invasive plants: (a)
Bipolaris sp. fungus causing leaf blight disease on Microstegium
vimineum (stiltgrass), (b) Pseudomonas syringae bacteria symptoms
on Cirsium arvense (Canada thistle), (c) powdery mildew Erysiphe
cruciferarum on Alliaria petiolata (garlic mustard), (d) Puccinia
lygodii rust on Lygodium japonicum (Japanese climbing fern), (e) rose
rosette disease symptoms on Rosa multiflora (multiflora rose) caused
by an unknown virus and (f) Phakopsora pachyrhizi (soybean rust)
on Pueraria lobata (kudzu). Photo credits: a: S. Luke Flory, b: Bob
Hartzler, c: Don Cipollini, d: Min Rayamajhi, e: Fred First, f: Albert
Tenuta.
© 2013 The Authors. Journal of Ecology © 2013 British Ecological Society, Journal of Ecology, 101, 607–613
Pathogen accumulation and invasive plants 609
higher levels than on native species (Strong & Levin 1975;
Clay 1995). Furthermore, the longer a species is present in its
new range, the more likely a pathogen from its home range
will be introduced (Mitchell et al. 2010). Invasive species
growing at high densities also have an increased probability
of intercepting inoculum, and shorter distances between hosts
can promote the spread of disease (Garrett & Mundt 1999).
High host density may also alter environmental conditions
such as humidity and temperature that affect pathogen transmission (Burdon & Chilvers 1982; Alexander 2010), and
intraspecific competition can increase the effects of infection
(Lively et al. 1995). Finally, larger, denser host populations
can more easily maintain pathogens that require a minimum
host population size (Carlsson & Elmqvist 1992; Holt et al.
2003).
Pathogen accumulation may also be mediated by evolutionary mechanisms. Most pathogens exhibit some level of specificity whereby they only infect certain genotypes, species,
genera or families (Keen & Staskawicz 1988; Gilbert &
Webb 2007). Hosts may vary in resistance to pathogens or in
tolerance to disease and pathogens may infect multiple hosts
but may have a more detrimental effect on a particular host
(Holah & Alexander 1999; Dobson 2004). In general, introduced species are more likely to accumulate pathogens in
habitats containing closely related species compared to habitats with more distantly related species (Agrawal & Kotanen
2003; Parker & Gilbert 2007). However, host–pathogen interactions can change over time; invasive plants may evolve
reduced resistance when enemies are lacking (Bossdorf et al.
2004), or pathogens may evolve the ability to attack widespread invasive hosts (Parker & Gilbert 2007). For example,
when plant species are introduced to new ranges and escape
their natural enemies, they may evolve greater competitive
ability at the expense of reduced defences and become more
susceptible to generalist pathogens (Evolution of Increased
Competitive Ability (EICA); Blossey & Notzold 1995; but
see van Kleunen & Schmid 2003; Gurevitch et al. 2011).
Identifying the ecological or evolutionary mechanisms underlying pathogen accumulation will help to determine the host
ranges and impacts of pathogens on invasive and native
species.
(Fig. 2). Disease epidemics in both wild and domesticated
plants (e.g. American chestnut) and control of invaders by
biocontrol agents (e.g. Australian Opuntia spp.) demonstrate
the potential of natural enemies to reduce or regulate host
populations. Recently, we showed that experimental fungicide
applications reduced infection of the invasive grass Microstegium vimineum by the fungal pathogen Bipolaris (Fig. 1a),
while simultaneously increasing Microstegium biomass by up
to 50% and seed production by up to 200% in natural populations (Flory, Kleczewski & Clay 2011). Similarly, Enright &
Cipollini (2007) found that infection of Alliaria petiolata
(garlic mustard) by a powdery mildew in the glasshouse significantly reduced plant growth and survival. In parallel,
experimental removals of Microstegium (Flory & Clay 2009)
and garlic mustard (Carlson & Gorchov 2004) in nature led
to recovery of co-occurring native species. However, we are
unaware of any system where the sequential pattern of pathogen accumulation, decline of invasive species and recovery of
native species has been documented.
Second, invasive species hosting abundant pathogens may
cause increased disease on co-occurring native hosts and
reduce their competitive suppression of invasive species
(Fig. 3). Such dynamics are termed ‘spillover’ when the
pathogens are non-native and introduced with the invader and
‘spillback’ when an invasive species hosts native pathogens.
The general phenomenon has also been called the ‘Enemy of
My Enemy Hypothesis’ (Colautti et al. 2004). For example,
spillover of barley yellow mosaic virus from a highly susceptible invasive grass decreased the abundance of two native
grasses through pathogen-mediated apparent competition
(Power & Mitchell 2004). Similarly, Mangla, Inderjit &
Callaway (2008) reported spillback where invasions of the
forb Chromolaena odorata resulted in a 25-fold increase in
Fusarium, a generalist soil pathogen, which strongly inhibited
native plant species, and the non-native invasive cheatgrass
(Bromus tectorum) serves as a reservoir for the native seed
pathogen Pyrenophora semeniperda, which causes significantly greater death of native seed in invaded areas
(Beckstead et al. 2010; see also Kotanen 2007 for seed pathogen effects on native tree species). Kelley et al. (2009)
reviewed a number of other potential examples of spillback
Possible outcomes of pathogen accumulation
(a)
Spatial distribution
While the process of pathogen accumulation has been of
longstanding interest (Strong & Levin 1975; Mitchell et al.
2010), there has been little research on the ecological consequences of pathogen accumulation for introduced hosts. We
hypothesize three possible outcomes of pathogen accumulation on invasive species. First, pathogen accumulation may
result in decreased density and extent of invasions and recovery of native species. We refer to this outcome as the Pathogen Accumulation and Invasive Decline (PAID) hypothesis.
Invasive species initially increase to high levels followed by
increasing pathogen density and species richness, which then
causes reductions in the density and distribution of the invasive species and potentially the recovery of native species
(b)
(c)
Local density
Invasive
species
Pathogen richness
Initial
introduction
Pathogen
Time since introduction
A. Rapid invasive species
population increase and
increasing spatial
distribution; low pathogen
prevalence.
B. Increasing pathogen
prevalence and richness;
lower invasive population
density, and declining
spatial distribution.
C. High pathogen
prevalence and species
richness; reduced local
density and spatial
distribution.
Fig 2. Conceptual model illustrating the pathogen accumulation and
invasive decline (PAID) hypothesis.
© 2013 The Authors. Journal of Ecology © 2013 British Ecological Society, Journal of Ecology, 101, 607–613
610 S. L. Flory & K. Clay
(a)
species (Clay et al. 2008; Mordecai 2011), we are unaware of
any documented cases of pathogen accumulation leading to
invasive species decline, and there are very few documented
cases of spillback. To determine the dynamics of pathogen
accumulation on invasive species and the outcomes for invasive and native species, a combination of literature reviews,
meta-analyses, comparative field surveys, population modelling and manipulative experiments in laboratories, glasshouses
and natural populations is required (Table 1). This information will help provide insights into the patterns and outcomes
of biological invasions and will help guide management
strategies.
Demonstrating pathogen accumulation requires evidence
that the diversity of pathogen species or prevalence of pathogen infection on invasive hosts increases over time. However,
many invasive species and pathogens were introduced accidentally and escaped evaluation for long periods, so there is
little information on changes in their historical distributions
and dynamics over time. To acquire better information, we
should target invasions of known ages, including new invasions, and gather data as the invasion progresses or, alternatively, substitute space for time by evaluating pathogen
richness and abundance at sites along a chronosequence of
invasion history (Lankau et al. 2009; Diez et al. 2010).
Observations of increasing disease and declining invasive host
populations and recovery of native hosts across a chronosequence of invasions would support PAID. Alternatively,
increasing disease and no effect or increasing invasive host
populations over time, along with increasing disease and
decline of native host populations, would suggest spillback
dynamics (Table 1).
Field surveys across the range of an invasive species can
be time-consuming and costly, but collaborations with natural
areas managers, invasive species working groups, cooperative
weed management areas and private land owners can significantly increase efficiency. For example, online resources
(e.g. Great Britain Non-native Species Secretariat, nonnativespecies.org; US Midwest Invasive Plant Network, mipn.org;
EPPO Lists of Invasive Alien Plants, eppo.int) can be utilized
to obtain information about invasive plant diversity and
distributions. Similarly, online data bases such as the USDA
Fungus-Host Distributions data base (nt.ars-grin.gov), the
(b)
Invasive
Spillback
PAID
Invasive
Native
No effect
Spatial distribution
Native
Time since introduction
A. Displacement of native by
invasive species prior to
pathogen colonization.
B. Three alternative outcomes of
pathogen accumulation on invasive
species.
Fig 3. Conceptual model illustrating three alternative outcomes of
pathogen accumulation over time: decline of invasive species (PAID
hypothesis) and recovery of native species, no effect of pathogens
through tolerance or compensation, or spillback of pathogens resulting
in further native species decline and release of invasive species from
competition.
and suggested that it is a widespread, but underappreciated,
component of biological invasions (see also Power et al.
2011). However, it is often unclear whether pathogens were
introduced with the invasive species or whether native pathogens accumulated on the invasive plant following its introduction. Further research is needed to determine how frequently
pathogen accumulation on invasive species results in spillback
to native species.
Finally, pathogen accumulation may have little or no effect
on invasive species due to tolerance, compensation or phenotypic plasticity (e.g. Gilbert & Parker 2006; Alexander 2010).
For example, many invasive species exhibit substantial phenotypic plasticity such that a reduction in population density
would have little effect on biomass or seed production per
unit area. Given the theoretical and empirical demonstrations
of the negative effects of pathogen build-up (e.g. Clay &
Kover 1996; Packer & Clay 2004; Mordecai 2011), this
outcome seems unlikely, although possible.
Research needs
Although theory predicts that abundant, high-density species
will be more heavily attacked by pathogens than less common
Table 1. Predicted outcomes for native and invasive host species for each of the three proposed hypotheses: Pathogen Accumulation and Invasive
Decline (PAID), Spillback and No effect. Outcomes of increasing (+), decreasing ( ) or no change (0) in disease and host population levels are
provided for three types of studies: observational across a chronosequence of young to old invasions, experimental suppression of disease in
invaded field areas and experimental addition of disease in glasshouse, growth chamber, common garden or field setting
PAID
Spillback
Type of study
Species
Disease
Host
Observations across chronosequence of invasions
Native
Invasive
Native
Invasive
Native
Invasive
0
+
0
+
+
0
+
+
+
Experimental suppression of pathogens
Experimental addition of pathogens
Disease
0 or +
+
+
0 or +
No effect
Host
Disease
Host
+
0
+
0
0
0
0
0
0
0
+
+
0
+
© 2013 The Authors. Journal of Ecology © 2013 British Ecological Society, Journal of Ecology, 101, 607–613
Pathogen accumulation and invasive plants 611
Virus Identification Data Exchange project (agls.uidaho.edu/
ebi/vdie) or the worldwide Distribution Maps of Plant Pests
and Diseases (cabi.org) can be extremely helpful for identifying pathogens on plant species. In addition, species-specific
reports of plant disease in the literature can be found using
tools such as Web of Science. In some cases, herbarium
records can help document spatial and temporal patterns of
disease (Hood & Antonovics 2003). Some types of pathogens
(e.g. foliar fungal pathogens) will be easier to identify and
quantify than other groups (e.g. root pathogens), but there is
no reason to expect that general patterns of pathogen accumulation and ecological impacts should differ among types of
pathogens. Beyond the existing data bases and literature,
determining the identity, source and distribution of pathogens
on invasive species will require collaborations among ecologists, plant pathologists and taxonomists, and the use of morphological, microbiological and molecular techniques.
Elucidating the host range of pathogens will help determine
whether spillback is possible and whether the pathogen likely
colonized from co-occurring native species or from in situ
evolution. Key questions include: Are pathogens specialists or
generalists? Do they only infect the invasive species or are
native species also susceptible? Do infection rates of pathogens vary among isolates, plant populations, habitats or
co-occurrence of host species? Determining whether pathogens are from the native or introduced range of the invasive
species, and whether they infect any other species, may help
to clarify their co-evolutionary history, which could explain
ongoing ecological and evolutionary dynamics. The first step
in evaluating pathogen host range is to collect symptomatic
samples during field surveys from functionally or phylogenetically related species that co-occur with the invasive species.
Then, following the identification and culture of isolated
pathogens, controlled laboratory and glasshouse inoculation
studies should be completed on native species found in
invaded habitats (Table 1; see also Charudattan & Dinoor
2000; Flory, Kleczewski & Clay 2011; Kleczewski, Flory &
Clay 2012). Such studies must be conducted with caution to
prevent the unintended spread of pathogens to uninfected
populations. Experimental inoculation studies can also determine whether pathogen genotypes attack certain invasive
plant genotypes or whether all invasive genotypes are susceptible (Schmid 1994), which may inform the potential for pathogen spread across the invasive host range. Field surveys in
the native range of the invasive species could provide further
information on pathogen diversity and prevalence. Further,
information on natural pathogen levels in the native range
would help inform the role of enemy release in the invasion
process and predict which pathogens are likely to attack the
host in the invasive range.
To determine how pathogen accumulation may affect the
survival, growth or fecundity of invasive species and cooccurring native species, field, glasshouse and laboratory
experiments manipulating the presence and density of pathogens, and the invasive and native plant species, are needed
(Table 1). The addition or removal of pathogens depends on
the feasibility of culturing and inoculating pathogens (while
minimizing the risk of pathogen escape), and the efficacy of
pesticides to reduce pathogen loads in nature. These types of
approaches can also help determine how the effects of pathogens on invasive and native species vary with climate, latitude, soils and other environmental factors. Simultaneous
infection by multiple pathogens will reveal whether their
combined effects on invasive and native plant species are
additive, synergistic or antagonistic.
Testing for spillback requires glasshouse or laboratory
experiments using native communities with and without the
invasive species in the presence and absence of pathogens.
Spillback may also be tested in the field by planting uninfected natives into infected and pathogen-removed (via pesticides) plots in invaded and uninvaded communities. If
invasive populations perform more poorly when pathogens
are experimentally added, or better when pathogens are experimentally decreased (Table 1), we can conclude support for
the PAID hypothesis. If increasing invasion density results in
greater pathogen loads on invasive species, but greater negative effects of disease on native species than on the invader,
then spillback may be occurring (Table 1; Kelly et al. 2009;
Diez et al. 2010). However, non-susceptible native species
could also be released from competition with other resident
species subject to spillback, leading to further indirect
changes in community structure and composition (Table 1).
Experimentally altering the presence of pathogens and
native species can help determine the immediate consequences of pathogen accumulation on populations and communities, but will not predict the effects of pathogen
accumulation over longer-time frames. Matrix population
models offer the opportunity to project population dynamics
beyond the shorter-term effects of pathogen accumulation
(Crone et al. 2011). Such models can compare population
growth rates under different environmental conditions or disease conditions and identify life history stages with the largest
impact on population growth. Data on each life history stage
could be collected from field or glasshouse experiments where
pathogens are manipulated and used to parameterize models
(Parker 2000; Davelos & Jarosz 2004). Matrix population
models would provide important information regarding the
longer-term effects of pathogen accumulation on invasive
hosts and resident native species, help determine whether
spillback or PAID is occurring and inform management decisions for plant invasions. However, we should recognize that
these models generally do not incorporate potential evolutionary changes in the pathogen, the invasive species or their
interaction.
Conclusions
Given the biological impacts of invasive species, there is an
urgent need for studies across diverse ecosystems that identify
pathogens on invasive species and quantify their distribution,
elucidate abiotic and biotic correlates of infection and evaluate the long-term ecological consequences for both invasive
and native species. Pathogen accumulation may lead to the
decline of invasive species and recovery of native species or
© 2013 The Authors. Journal of Ecology © 2013 British Ecological Society, Journal of Ecology, 101, 607–613
612 S. L. Flory & K. Clay
to spillback of pathogens onto native species and increased
ecological impacts of invasions. For example, if pathogen
accumulation causes invasive decline, the passage of time
may result in natural regulation of invasions and recovery of
native plant communities. But, if spillback is common, then
pathogen accumulation on invasive plants may suppress
native species and promote invasions. Pathogens that attack
and suppress invasive species (e.g. bioherbicides; Hallett
2005) also may be deliberately spread to help manage invasions once research is conducted to identify pathogens that do
not infect co-occurring native species. On the other hand, if
biological invasions result in spillback to native species (e.g.
Mangla, Inderjit & Callaway 2008), more urgent control
efforts may be warranted. Research efforts across diverse
plant–pathogen systems and habitats focused on understanding pathogen and host population dynamics, the source of
pathogens, and interactions among pathogens and invasive
and native plants, will help elucidate the long-term consequences of pathogen accumulation.
Acknowledgements
We thank Wim van der Putten and two anonymous reviewers for comments on
an earlier draft of this manuscript and acknowledge the past and current members of the Flory and Clay labs for helpful discussions. Funding was provided
in part by the Center for Research in Environmental Sciences at Indiana University and the Agronomy Department and the Institute of Food and Agricultural Sciences at the University of Florida.
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Received 10 September 2012; accepted 6 February 2013
Handling Editor: Peter Thrall
© 2013 The Authors. Journal of Ecology © 2013 British Ecological Society, Journal of Ecology, 101, 607–613