ESSAY REVIEW

Pathogen accumulation and long-term dynamics ofplant invasionsS. Luke Flory1* and Keith Clay2

1Agronomy Department, University of Florida, PO Box 110500, Gainesville, FL 32611, USA; and 2Department ofBiology, Indiana University, 1001 East 3rd Street, Bloomington, IN 47405, USA

Summary

1. The diversity of pathogens on highly abundant introduced hosts has been positively correlatedwith time since introduction, geographical range of the introduced species and diversity of invadedhabitats. However, little is known about the ecological effects of pathogen accumulation on non-native invasive plants.2. Pathogen accumulation on invasive plant species may result from ecological processes such ashigh plant densities, expanding geographical ranges and pathogen dispersal from the native range, orevolutionary mechanisms such as host range shifts and adaptation of native pathogens to invasivespecies.3. Over time pathogen accumulation may cause decline in the density and distribution of invasiveplants and facilitate recovery of native species. Alternatively, pathogens might build up on invasivespecies and then spill back onto co-occurring native species, further exacerbating the effects of inva-sions.4. Synthesis. Research efforts should focus on determining the long-term outcomes of pathogenaccumulation on invasive species. Such research will require multifaceted approaches including com-parative studies of diverse invasive species and habitats, experimental manipulations of hosts andpathogens in nature and controlled environments, and predictive models of host-pathogen interac-tions within an invasion framework. Results of this research will improve our understanding andability 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 identifymechanisms underlying biological invasions, which are keydrivers of global environmental change and require substantialeconomic resources for management. Dozens of hypotheseshave been proposed to explain why some species becomeinvasive (Catford, Jansson & Nilsson 2009) and why somehabitats are vulnerable to invasion (Stohlgren et al. 2002).However, abiotic and biotic factors affecting invasive speciesare likely to change over time due to varying environmentalconditions, habitat disturbance, repeated introductions of dis-tinct genotypes, expanding distributions leading to novelinteractions and evolution of invaders or co-occurring patho-gens (e.g. Bossdorf et al. 2005; Gilbert & Parker 2010).Research on post-introduction evolution (Maron et al. 2004)

and the introduction of biological controls (reviewed byCulliney 2005) suggests that interactions of invasive specieswith enemies, competitors and mutualists can co-evolve andfeedback 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 releaseof invasive species from natural enemies when they are intro-duced into a new range, which then gain a competitive advan-tage over resident species (but see van Kleunen & Fischer2009; Chun, van Kleunen & Dawson 2010). For example,experimentally excluding pests from the shrub Clidemia hirtapromoted growth in its native, but not non-native, range(DeWalt, Denslow & Ickes 2004). Similarly, black cherry(Prunus serotina) seedling recruitment is suppressed nearadult trees in native U.S. habitats by below-ground Pythiumpathogens, but not in Europe where it invades forest understo-ries (Reinhart et al. 2003). Although invasive species mayinitially benefit from enemy escape, over the longer-term*Correspondence author. E-mail: flory@ufl.edu

© 2013 The Authors. Journal of Ecology © 2013 British Ecological Society

Journal of Ecology doi: 10.1111/1365-2745.12078

pathogens can accumulate, potentially reducing the effects ofinvaders on native communities and ecosystems. For example,in an analysis of 124 plant species, those that were introduced400 years ago had six times more pathogens than those intro-duced only recently (Mitchell et al. 2010), but the effects ofthose pathogens on hosts were not known. Alternatively,pathogen accumulation may exacerbate the effects of inva-sions if pathogens spill back onto co-occurring native speciesand reduce their performance and competitive inhibition ofinvasive species (Kelly et al. 2009). The long-term dynamicsof plant invasions and their impacts on native communitiesand ecosystems may be determined by interactions amongpathogens, invasive plants and co-occurring native species.Here, we describe the patterns, mechanisms and potential out-comes of pathogen accumulation on invasive species with thegoal of generating discussion and research on how pathogensalter the long-term dynamics of plant invasions. The resultsof this research will improve our understanding and ability topredict the outcomes of biological invasions.

Patterns of pathogen accumulation

The limited research on pathogen accumulation in natural sys-tems has demonstrated that the richness and diversity ofpathogens on introduced hosts are positively correlated withtime since introduction (Hawkes 2007), the geographicalrange of the introduced species (Strong & Levin 1975; Clay1995) and the diversity of invaded habitats (Mitchell et al.2010). Many invasive plants, including grasses, forbs, treesand ferns become infected by pathogens in their introducedranges (Fig. 1). For example, the invasive grass Microstegiumvimineum (stiltgrass) is infected by Bipolaris fungi (Fig. 1a,Kleczewski & Flory 2010; Flory, Kleczewski & Clay 2011;Kleczewski, Flory & Clay 2012), Alliaria petiolata (garlicmustard) by powdery mildew (Fig. 1c, Enright & Cipollini2007) and Pueraria lobata (kudzu) by soybean rust (Fig. 1f,Harmon et al. 2006). Accumulation of below-ground patho-gens, which are more difficult to identify, may also occur.For example, the invasive tree Sapium sebiferum (Chinese tal-low) survived more poorly and produced less biomass in‘home’ compared with ‘away’ soils (Nijjer, Rogers &Siemann 2007). Similarly, Diez et al. (2010) found that thestrength of negative plant–soil feedback increased with timesince introduction for 12 species in New Zealand. However,neither study identified biological agents responsible fordecreased plant growth or excluded other potential mecha-nisms such as reduced benefit from soil mutualists or changesin soil chemistry. Nevertheless, demonstrations of accumula-tion of above-ground pathogens and increasing negative plant–soil feedbacks over time suggest that pathogen accumulationon invasive species is widespread and potentially importantfor regulating invasive plant populations.

Mechanisms of pathogen accumulation

Highly abundant species, such as invasive species, areexpected to exhibit greater accumulation of pathogens over

time relative to rarer, less-dense species (Bever 1994; Olffet al. 2000; Clay et al. 2008; Mitchell et al. 2010). However,it is less apparent whether pathogen accumulation occursthrough ecological or evolutionary mechanisms, or by somecombination. Ecological mechanisms include spatiotemporaldynamics, host density or abiotic conditions. For example, asspecies invade wider geographical areas, there will be greaterencounter rates with native pathogens, and the number ofpathogens that accumulate may increase in the same or even

(a) (b)

(c) (d)

(e) (f)

Fig 1. Examples of pathogen accumulation on invasive plants: (a)Bipolaris sp. fungus causing leaf blight disease on Microstegiumvimineum (stiltgrass), (b) Pseudomonas syringae bacteria symptomson Cirsium arvense (Canada thistle), (c) powdery mildew Erysiphecruciferarum on Alliaria petiolata (garlic mustard), (d) Puccinialygodii rust on Lygodium japonicum (Japanese climbing fern), (e) roserosette disease symptoms on Rosa multiflora (multiflora rose) causedby an unknown virus and (f) Phakopsora pachyrhizi (soybean rust)on Pueraria lobata (kudzu). Photo credits: a: S. Luke Flory, b: BobHartzler, c: Don Cipollini, d: Min Rayamajhi, e: Fred First, f: AlbertTenuta.

© 2013 The Authors. Journal of Ecology © 2013 British Ecological Society, Journal of Ecology

2 S. L. Flory & K. Clay

higher levels than on native species (Strong & Levin 1975;Clay 1995). Furthermore, the longer a species is present in itsnew range, the more likely a pathogen from its home rangewill be introduced (Mitchell et al. 2010). Invasive speciesgrowing at high densities also have an increased probabilityof intercepting inoculum, and shorter distances between hostscan promote the spread of disease (Garrett & Mundt 1999).High host density may also alter environmental conditionssuch as humidity and temperature that affect pathogen trans-mission (Burdon & Chilvers 1982; Alexander 2010), andintraspecific competition can increase the effects of infection(Lively et al. 1995). Finally, larger, denser host populationscan more easily maintain pathogens that require a minimumhost population size (Carlsson & Elmqvist 1992; Holt et al.2003).Pathogen accumulation may also be mediated by evolution-

ary mechanisms. Most pathogens exhibit some level of speci-ficity whereby they only infect certain genotypes, species,genera or families (Keen & Staskawicz 1988; Gilbert &Webb 2007). Hosts may vary in resistance to pathogens or intolerance to disease and pathogens may infect multiple hostsbut may have a more detrimental effect on a particular host(Holah & Alexander 1999; Dobson 2004). In general, intro-duced species are more likely to accumulate pathogens inhabitats containing closely related species compared to habi-tats with more distantly related species (Agrawal & Kotanen2003; Parker & Gilbert 2007). However, host–pathogen inter-actions can change over time; invasive plants may evolvereduced resistance when enemies are lacking (Bossdorf et al.2004), or pathogens may evolve the ability to attack wide-spread invasive hosts (Parker & Gilbert 2007). For example,when plant species are introduced to new ranges and escapetheir natural enemies, they may evolve greater competitiveability at the expense of reduced defences and become moresusceptible to generalist pathogens (Evolution of IncreasedCompetitive Ability (EICA); Blossey & Notzold 1995; butsee van Kleunen & Schmid 2003; Gurevitch et al. 2011).Identifying the ecological or evolutionary mechanisms under-lying pathogen accumulation will help to determine the hostranges and impacts of pathogens on invasive and nativespecies.

Possible outcomes of pathogen accumulation

While the process of pathogen accumulation has been oflongstanding interest (Strong & Levin 1975; Mitchell et al.2010), there has been little research on the ecological conse-quences of pathogen accumulation for introduced hosts. Wehypothesize three possible outcomes of pathogen accumula-tion on invasive species. First, pathogen accumulation mayresult in decreased density and extent of invasions and recov-ery of native species. We refer to this outcome as the Patho-gen Accumulation and Invasive Decline (PAID) hypothesis.Invasive species initially increase to high levels followed byincreasing pathogen density and species richness, which thencauses reductions in the density and distribution of the inva-sive species and potentially the recovery of native species

(Fig. 2). Disease epidemics in both wild and domesticatedplants (e.g. American chestnut) and control of invaders bybiocontrol agents (e.g. Australian Opuntia spp.) demonstratethe potential of natural enemies to reduce or regulate hostpopulations. Recently, we showed that experimental fungicideapplications reduced infection of the invasive grass Microste-gium vimineum by the fungal pathogen Bipolaris (Fig. 1a),while simultaneously increasing Microstegium biomass by upto 50% and seed production by up to 200% in natural popula-tions (Flory, Kleczewski & Clay 2011). Similarly, Enright &Cipollini (2007) found that infection of Alliaria petiolata(garlic mustard) by a powdery mildew in the glasshouse sig-nificantly reduced plant growth and survival. In parallel,experimental removals of Microstegium (Flory & Clay 2009)and garlic mustard (Carlson & Gorchov 2004) in nature ledto recovery of co-occurring native species. However, we areunaware of any system where the sequential pattern of patho-gen accumulation, decline of invasive species and recovery ofnative species has been documented.Second, invasive species hosting abundant pathogens may

cause increased disease on co-occurring native hosts andreduce their competitive suppression of invasive species(Fig. 3). Such dynamics are termed ‘spillover’ when thepathogens 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 ofMy Enemy Hypothesis’ (Colautti et al. 2004). For example,spillover of barley yellow mosaic virus from a highly suscep-tible invasive grass decreased the abundance of two nativegrasses through pathogen-mediated apparent competition(Power & Mitchell 2004). Similarly, Mangla, Inderjit &Callaway (2008) reported spillback where invasions of theforb Chromolaena odorata resulted in a 25-fold increase inFusarium, a generalist soil pathogen, which strongly inhibitednative plant species, and the non-native invasive cheatgrass(Bromus tectorum) serves as a reservoir for the native seedpathogen Pyrenophora semeniperda, which causes signifi-cantly greater death of native seed in invaded areas(Beckstead et al. 2010; see also Kotanen 2007 for seed patho-gen effects on native tree species). Kelley et al. (2009)reviewed a number of other potential examples of spillback

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.

Spa

tial d

istri

butio

n

Initial introduction

Invasive species

Pathogen

Time since introduction

Local density

Pathogen richness

(c)(a) (b)

Fig 2. Conceptual model illustrating the pathogen accumulation andinvasive decline (PAID) hypothesis.

© 2013 The Authors. Journal of Ecology © 2013 British Ecological Society, Journal of Ecology

Pathogen accumulation and invasive plants 3

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 wereintroduced with the invasive species or whether native patho-gens accumulated on the invasive plant following its introduc-tion. Further research is needed to determine how frequentlypathogen accumulation on invasive species results in spillbackto native species.Finally, pathogen accumulation may have little or no effect

on invasive species due to tolerance, compensation or pheno-typic plasticity (e.g. Gilbert & Parker 2006; Alexander 2010).For example, many invasive species exhibit substantial pheno-typic plasticity such that a reduction in population densitywould have little effect on biomass or seed production perunit area. Given the theoretical and empirical demonstrationsof the negative effects of pathogen build-up (e.g. Clay &Kover 1996; Packer & Clay 2004; Mordecai 2011), thisoutcome seems unlikely, although possible.

Research needs

Although theory predicts that abundant, high-density specieswill be more heavily attacked by pathogens than less common

species (Clay et al. 2008; Mordecai 2011), we are unaware ofany documented cases of pathogen accumulation leading toinvasive species decline, and there are very few documentedcases of spillback. To determine the dynamics of pathogenaccumulation on invasive species and the outcomes for inva-sive and native species, a combination of literature reviews,meta-analyses, comparative field surveys, population model-ling and manipulative experiments in laboratories, glasshousesand natural populations is required (Table 1). This informa-tion will help provide insights into the patterns and outcomesof biological invasions and will help guide managementstrategies.Demonstrating pathogen accumulation requires evidence

that the diversity of pathogen species or prevalence of patho-gen infection on invasive hosts increases over time. However,many invasive species and pathogens were introduced acci-dentally and escaped evaluation for long periods, so there islittle information on changes in their historical distributionsand dynamics over time. To acquire better information, weshould target invasions of known ages, including new inva-sions, and gather data as the invasion progresses or, alterna-tively, substitute space for time by evaluating pathogenrichness and abundance at sites along a chronosequence ofinvasion history (Lankau et al. 2009; Diez et al. 2010).Observations of increasing disease and declining invasive hostpopulations and recovery of native hosts across a chronose-quence of invasions would support PAID. Alternatively,increasing disease and no effect or increasing invasive hostpopulations over time, along with increasing disease anddecline of native host populations, would suggest spillbackdynamics (Table 1).Field surveys across the range of an invasive species can

be time-consuming and costly, but collaborations with naturalareas managers, invasive species working groups, cooperativeweed management areas and private land owners can signifi-cantly increase efficiency. For example, online resources(e.g. Great Britain Non-native Species Secretariat, nonnative-species.org; US Midwest Invasive Plant Network, mipn.org;EPPO Lists of Invasive Alien Plants, eppo.int) can be utilizedto obtain information about invasive plant diversity anddistributions. Similarly, online data bases such as the USDAFungus-Host Distributions data base (nt.ars-grin.gov), the

A. Displacement of native by invasive species prior to pathogen colonization.

B. Three alternative outcomes of pathogen accumulation on invasive species.

Spa

tial d

istri

butio

n

Native

Invasive

PA

ID

No

effe

ct

Spi

llbac

k

Native Invasive

Time since introduction

(b)(a)

Fig 3. Conceptual model illustrating three alternative outcomes ofpathogen accumulation over time: decline of invasive species (PAIDhypothesis) and recovery of native species, no effect of pathogensthrough tolerance or compensation, or spillback of pathogens resultingin further native species decline and release of invasive species fromcompetition.

Table 1. Predicted outcomes for native and invasive host species for each of the three proposed hypotheses: Pathogen Accumulation and InvasiveDecline (PAID), Spillback and No effect. Outcomes of increasing (+), decreasing (�) or no change (0) in disease and host population levels areprovided for three types of studies: observational across a chronosequence of young to old invasions, experimental suppression of disease ininvaded field areas and experimental addition of disease in glasshouse, growth chamber, common garden or field setting

Type of study Species

PAID Spillback No effect

Disease Host Disease Host Disease Host

Observations across chronosequence of invasions Native 0 + � + 0 0Invasive + + 0 or + � + 0

Experimental suppression of pathogens Native 0 � + � 0 0Invasive � � + + � 0

Experimental addition of pathogens Native 0 + � + 0 0Invasive + + 0 or + � + 0

© 2013 The Authors. Journal of Ecology © 2013 British Ecological Society, Journal of Ecology

4 S. L. Flory & K. Clay

Virus Identification Data Exchange project (agls.uidaho.edu/ebi/vdie) or the worldwide Distribution Maps of Plant Pestsand Diseases (cabi.org) can be extremely helpful for identify-ing pathogens on plant species. In addition, species-specificreports of plant disease in the literature can be found usingtools such as Web of Science. In some cases, herbariumrecords can help document spatial and temporal patterns ofdisease (Hood & Antonovics 2003). Some types of pathogens(e.g. foliar fungal pathogens) will be easier to identify andquantify than other groups (e.g. root pathogens), but there isno reason to expect that general patterns of pathogen accumu-lation and ecological impacts should differ among types ofpathogens. Beyond the existing data bases and literature,determining the identity, source and distribution of pathogenson invasive species will require collaborations among ecolo-gists, plant pathologists and taxonomists, and the use of mor-phological, microbiological and molecular techniques.Elucidating the host range of pathogens will help determine

whether spillback is possible and whether the pathogen likelycolonized from co-occurring native species or from in situevolution. Key questions include: Are pathogens specialists orgeneralists? Do they only infect the invasive species or arenative species also susceptible? Do infection rates of patho-gens vary among isolates, plant populations, habitats orco-occurrence of host species? Determining whether patho-gens are from the native or introduced range of the invasivespecies, and whether they infect any other species, may helpto clarify their co-evolutionary history, which could explainongoing ecological and evolutionary dynamics. The first stepin evaluating pathogen host range is to collect symptomaticsamples during field surveys from functionally or phylogeneti-cally related species that co-occur with the invasive species.Then, following the identification and culture of isolatedpathogens, controlled laboratory and glasshouse inoculationstudies should be completed on native species found ininvaded habitats (Table 1; see also Charudattan & Dinoor2000; Flory, Kleczewski & Clay 2011; Kleczewski, Flory &Clay 2012). Such studies must be conducted with caution toprevent the unintended spread of pathogens to uninfectedpopulations. Experimental inoculation studies can also deter-mine whether pathogen genotypes attack certain invasiveplant genotypes or whether all invasive genotypes are suscep-tible (Schmid 1994), which may inform the potential for path-ogen spread across the invasive host range. Field surveys inthe native range of the invasive species could provide furtherinformation on pathogen diversity and prevalence. Further,information on natural pathogen levels in the native rangewould help inform the role of enemy release in the invasionprocess and predict which pathogens are likely to attack thehost in the invasive range.To determine how pathogen accumulation may affect the

survival, growth or fecundity of invasive species and co-occurring native species, field, glasshouse and laboratoryexperiments manipulating the presence and density of patho-gens, and the invasive and native plant species, are needed(Table 1). The addition or removal of pathogens depends onthe feasibility of culturing and inoculating pathogens (while

minimizing the risk of pathogen escape), and the efficacy ofpesticides to reduce pathogen loads in nature. These types ofapproaches can also help determine how the effects of patho-gens on invasive and native species vary with climate, lati-tude, soils and other environmental factors. Simultaneousinfection by multiple pathogens will reveal whether theircombined effects on invasive and native plant species areadditive, synergistic or antagonistic.Testing for spillback requires glasshouse or laboratory

experiments using native communities with and without theinvasive species in the presence and absence of pathogens.Spillback may also be tested in the field by planting unin-fected natives into infected and pathogen-removed (via pesti-cides) plots in invaded and uninvaded communities. Ifinvasive populations perform more poorly when pathogensare experimentally added, or better when pathogens are exper-imentally decreased (Table 1), we can conclude support forthe PAID hypothesis. If increasing invasion density results ingreater pathogen loads on invasive species, but greater nega-tive 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 speciescould also be released from competition with other residentspecies subject to spillback, leading to further indirectchanges in community structure and composition (Table 1).Experimentally altering the presence of pathogens and

native species can help determine the immediate conse-quences of pathogen accumulation on populations and com-munities, but will not predict the effects of pathogenaccumulation over longer-time frames. Matrix populationmodels offer the opportunity to project population dynamicsbeyond the shorter-term effects of pathogen accumulation(Crone et al. 2011). Such models can compare populationgrowth rates under different environmental conditions or dis-ease conditions and identify life history stages with the largestimpact on population growth. Data on each life history stagecould be collected from field or glasshouse experiments wherepathogens are manipulated and used to parameterize models(Parker 2000; Davelos & Jarosz 2004). Matrix populationmodels would provide important information regarding thelonger-term effects of pathogen accumulation on invasivehosts and resident native species, help determine whetherspillback or PAID is occurring and inform management deci-sions for plant invasions. However, we should recognize thatthese models generally do not incorporate potential evolution-ary changes in the pathogen, the invasive species or theirinteraction.

Conclusions

Given the biological impacts of invasive species, there is anurgent need for studies across diverse ecosystems that identifypathogens on invasive species and quantify their distribution,elucidate abiotic and biotic correlates of infection and evalu-ate the long-term ecological consequences for both invasiveand native species. Pathogen accumulation may lead to thedecline of invasive species and recovery of native species or

© 2013 The Authors. Journal of Ecology © 2013 British Ecological Society, Journal of Ecology

Pathogen accumulation and invasive plants 5

to spillback of pathogens onto native species and increasedecological impacts of invasions. For example, if pathogenaccumulation causes invasive decline, the passage of timemay result in natural regulation of invasions and recovery ofnative plant communities. But, if spillback is common, thenpathogen accumulation on invasive plants may suppressnative species and promote invasions. Pathogens that attackand suppress invasive species (e.g. bioherbicides; Hallett2005) also may be deliberately spread to help manage inva-sions once research is conducted to identify pathogens that donot infect co-occurring native species. On the other hand, ifbiological invasions result in spillback to native species (e.g.Mangla, Inderjit & Callaway 2008), more urgent controlefforts may be warranted. Research efforts across diverseplant–pathogen systems and habitats focused on understand-ing pathogen and host population dynamics, the source ofpathogens, and interactions among pathogens and invasiveand native plants, will help elucidate the long-term conse-quences of pathogen accumulation.

Acknowledgements

We thank Wim van der Putten and two anonymous reviewers for comments onan earlier draft of this manuscript and acknowledge the past and current mem-bers of the Flory and Clay labs for helpful discussions. Funding was providedin part by the Center for Research in Environmental Sciences at Indiana Uni-versity and the Agronomy Department and the Institute of Food and Agricul-tural Sciences at the University of Florida.

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Received 10 September 2012; accepted 6 February 2013Handling Editor: Peter Thrall

© 2013 The Authors. Journal of Ecology © 2013 British Ecological Society, Journal of Ecology

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