Can Plant–Microbe–Insect Interactions Enhance Or Inhibit the Spread of Invasive Species?

Functional Ecology 2013, 27, 661–671 doi: 10.1111/1365-2435.12099

PLANT–MICROBE–INSECT INTERACTIONS Can plant–microbe–insect interactions enhance or inhibit the spread of invasive species?

Alison E. Bennett*

Ecological Sciences, James Hutton Institute, Errol Road, Invergowrie, Dundee DD2 5DA, UK

Summary 1. Invasive species are one of the great challenges facing the world leading to great economic losses. Increasing numbers of species introductions are also increasing the likelihood of new species interactions – particularly between plants, microbes and insects. 2. Frequently discovered interactions between plants, microbes and insects are giving rise to a new ﬁeld: plant–microbe–insect (PMI) interactions. This paper focuses on novel PMI interactions created from the introduction of new plant, insect and microbe species. In particular, this paper asks: Do novel PMI interactions promote or inhibit invasive plants, microbes and insects? And can we predict whether novel PMI interactions are likely to become invasive? 3. While we might predict that novel PMI interactions are likely to be simple additive interactions due to their relatively short period of interaction, instead this review demonstrates that most novel PMI interactions are actually nonadditive. This manuscript shows that there are a great number of instances where invasive species are promoted by novel PMI interactions. By contrast, the studied cases where PMI interactions limit invasive species are predominantly biocontrol PMI interactions. 4. Future research on novel PMI interactions should focus on predicting future novel PMI interactions that promote invasive species. Given that many novel PMI interactions involve plant pathogens and their insect vectors, this novel PMI interaction deserves more focus. New research should also focus on non-novel PMI interactions that could be manipulated to hinder the spread of invasive plant, microbe and insect species.

Key-words: biocontrol, endosymbionts, entomopathogens, herbivores, invasive species, mycorrhizal fungi, novel interactions, pathogens, plant–microbe–insect interactions, vectors

economic impacts are actually due to interactions between Introduction plants, insects and microbes. Invasive species are one of the greatest challenges for most Human transport of non-native species has likely ecosystems in the world. Alone, invasive fungi cost US occurred since the movement of humans across the globe agriculture $21 billion USD per year (Rossman 2009). began in Neolithic times (Webb 1985), but was not typi- Invasive plant species have similarly strong economic cally recorded until the age of European exploration impacts: in 2003, invasive plants were estimated to cost (approximately AD 1500) when the introduction of species Australia approximately $4 billion AUD per year (Sinden began to increase (di Castri, Hansen & Debussche 1990). et al. 2004), whereas Vila et al. (2010) estimated that the Today, however, as human movement and trade across the cost of eradicating only the 30 most common invasive globe becomes increasingly common, the introduction of plant species in Europe was greater than €150 million. In new species has increased in frequency (reviewed in Brad- addition, European crop losses to invasive insects are esti- ley et al. 2012). Seeds, eggs, spores and other living mate- mated at €2Á8 billion (Vila et al. 2010). These ﬁgures dem- rial are transported both knowingly and unknowingly. onstrate that plants, insects and microbes are having While most introductions fail, the increasing number of dramatic eﬀects on the world economy, and many of these introductions is leading to an increasing number of successful introductions (reviewed in Bradley et al. 2012). This *Correspondence author. E-mail: [email protected] paper will distinguish between two types of introduced

© 2013 The Author. Functional Ecology © 2013 British Ecological Society 662 A. E. Bennett species: ‘invasive’ species that dominate habitats causing which causes Pierce’s disease in grapevines. Here, the syn- changes to ecosystems and economic losses, and the ergistic interaction between the invasive insect and native broader category of ‘noninvasive’ introduced species that pathogen has promoted the range expansion of the patho- either have become naturalized in their new environment gen. In a second example of novel synergistic PMI interac- or have yet to become invasive. tions involving three novel interactions, the invasive shrub Multiple theories have been proposed to explain what Rosa multiflora is fed on by an invasive eriophyid mite that biotic factors influence invasive species success. The vast vectors a virus (Smith, de Lillo & Amrine 2010). Prior to majority of these theories have focused on or been devel- their introduction to North America, these organisms had oped for invasive plants. These theories include the Enemy never interacted before. Thus, despite their short associa- Release Hypothesis (invasives encounter fewer enemies in tion, novel PMI interactions containing invasive species new environments; Elton 1958; Keane & Crawley 2002; can be synergistic and have dramatic consequences for Liu & Stiling 2006), Evolution of Increased Competitive native and agricultural systems. Ability (invasives evolve to be better competitors in new These novel PMI interactions may be further promoted environments in the absence of enemies; Blossey & Notz- by climate change which is likely to influence novel PMI old 1995) or the Novel Weapons Hypothesis [in which interactions by increasing the introduction of novel spe- invasive species (primarily plants) exclude competitors cies (Hellmann et al. 2008), favouring invasive species using toxic compounds; Callaway & Ridenour 2004]. A over native species and promoting the range expansion of recent review revealed 29 different proposed hypotheses invasive species in their new environments (reviewed in for the success of invasive species, and the vast majority of Dukes 2011). We know increases in temperature often these hypotheses focused on traits of invasive plant species increase insect activity (reviewed in Bale et al. 2002), or two-way biotic interactions (Catford, Jansson & Nilsson while changes in CO2 and O3 alter both insect (Hillstrom 2009). For example, the Enemy Release Hypothesis applies & Lindroth 2008) and soil microbial mutualist communi- to the enemies of plants, regardless of whether they be ties (Andrew & Lilleskov 2009; but see Klironomos et al. insect or microbial, but does not consider the influence of 2005) as well as plant pathogens (Eastburn, McElrone & insect–microbe interactions on plants. Bilgin 2011). Climate changes have also been predicted to Greater numbers of introduced species can also increase promote species range shifts and the expansion of invasive the likelihood of novel species interactions (Richardson species globally (reviewed in Hellmann et al. 2008; Dukes et al. 2000), particularly between plants, microbes and 2011). All of these effects could lead to new encounters insects. The effects of microbes, insects and plants on between plants, microbes and insects. For example, beech each other can be additive or nonadditive. When effects bark disease, the result of an association between the are additive, the outcome of one interaction is not influ- beech scale insect (Cryptococcus fagisuga) and a fungus, is enced by a second or third interaction – all influences are moving northward in its introduced range (Kasson & Liv- independent allowing us to ‘add’ the influence of one ingston 2009). In addition, there are suggestions that the organism to the influence of a second organism. Non- invasive insect herbivore whitefly (Bemisia tabaci), a additive interactions between plants, microbes and insects vector of the economically devastating Gemini viruses, is are those in which the influence of multiple organisms is currently expanding its range in Europe in response to not equal to the sum of the individual influences of each warmer climates (E. Bejarano, pers. comm.). It can be dif- organism (Fournier et al. 2006). Nonadditive interactions ficult to make sweeping predictions about the influence of can be synergistic (in which the outcome is greater than climate changes on these interactions (Dukes et al. 2009), the additive effects) or antagonistic (in which partners but these examples also suggest that climate change could hinder each other and the outcome is less than the addi- increase the proportion and impact of novel PMI inter- tive effects; Fournier et al. 2006). In the new field of actions. plant–microbe–insect (PMI) interactions highlighted in The examples above highlight that interactions between this issue, research has identified additive, synergistic and plants, microbes and insects can create serious invasive antagonistic interactions between plants, insects and species problems. As demonstrated in this issue, PMI microbes (Table 1). interactions have far-reaching consequences in a wide This paper will focus on novel PMI interactions created variety of systems. Our increased knowledge of PMI from the introduction of new species. We would expect interactions in invasions has identified three major ques- that new interactions among species might be simple (or tions that need addressing: Will novel PMI interactions additive) in nature. However, there are several cases in promote invasive plants, insects and microbes? Can we which these novel interactions have nonadditive effects. use novel PMI interactions to inhibit new invasions? Can For example, the combination of a plant pathogen and a we predict whether novel PMI interactions are likely to novel insect vector of that pathogen has led to the loss or become invasive? damage of 1300 acres of grapevines in California (Gomes The aim of this paper is to address these three questions et al. 2000): the glassy winged sharpshooter (Homalodisca with our current knowledge of PMI interactions. In partic- vitripennis), an invasive insect introduced to California in ular, this paper will focus on whether PMI interactions 1989, has become a vector for the Xylella fastidiosa pathogen, promote or inhibit invasive plants, insects or microbes.

© 2013 The Author. Functional Ecology © 2013 British Ecological Society, Functional Ecology, 27, 661–671 © Table 1. Summary of all known (and some hypothesized) eﬀects of plant–microbe–insect (PMI) interactions on invasive plants, insects and microbes 03TeAto.Fntoa Ecology Functional Author. The 2013

Invasive PMI Interactions organism eﬀect type Functional group Examples Promote invasion?

Plant Additive Plant Plant Pathogens + Herbivores No (O’Brien et al. 2010; Rayamajhi et al. 2010) Plant Soil Plant Mutualists + Herbivores Variable (Kempel et al., unpublished) Plant Soil Plant Mutualists + Pollinators Yes (Gange & Smith 2005) Plant Pathogens + Pollinators No (Swope & Parker 2010) Plant Entomopathogen + Herbivore Yes (Smith, de Lillo & Amrine 2010) Synergistic Plant Pathogens + Herbivores No (Smith, de Lillo & Amrine 2010) Plant Herbivore + Herbivore Mutualist No (Wang, Wu & Ding 2010) Antagonistic Plant Endophyte + Herbivore Yes (Clay, Holah & Rudgers 2005; Rudgers & Clay 2008; Uchitel, Omacini & Chaneton 2011)

© Plant Soil Plant Mutualists + Herbivores Variable (Kempel et al., unpublished) 03BiihEooia Society, Ecological British 2013 Plant Insect vector + Pathogen No (Jiu et al. 2007; Guo et al. 2010; Kaiser et al. 2010) Plant Pathogens + Herbivores Unknown Insect Additive Herbivore Entomopathogens + Plant Host No (Hu et al. 2009; Hajek & Delalibera 2010) Synergistic Herbivore Endosymbionts + Plant Hosts Yes (Hansen et al. 2007; Gueguen et al. 2010; Kaiser et al. 2010; Himler et al. 2011; Giron et al., this issue) Pathogen Vector Pathogens + Plant Hosts Yes (Hubbes 1999; Gomes et al. 2000; Morse & Hoddle 2006; Hummel et al. 2009; Kaiser et al. 2010; Smith, de Lillo & Amrine 2010) Pathogen vector Pathogen + Endosymbiont + Plant Yes (Gottlieb et al. 2010) Host Antagonistic Pathogen Vector Pathogens + Plant Hosts Unknown Microbe Additive Entomopathogen Insect Host + Insect Plant Hosts Unknown ucinlEcology Functional Endophyte Plant Hosts + Herbivores Yes (Clay, Holah & Rudgers 2005; Rudgers & Clay 2008; Uchitel, invasives? inhibit or enhance interactions PMI Can Omacini & Chaneton 2011) Synergistic Plant Pathogen Plant Hosts + Insect Vectors Yes (Karnosky 1979; Hubbes 1999; Gomes et al. 2000; Morse & Hoddle 2006; De Barro et al. 2008; Hummel et al. 2009; Kaiser et al. 2010; Li et al. 2010; Smith, de Lillo & Amrine 2010; Giron et al., this issue) Entomopathogen Insect Host + Toxic Plant Yes (Keesing et al. 2011) + , Plant Pathogen Plant Hosts Herbivore Yes (Castlebury, Rossman & Hyten 2006) 27 Plant Pathogen + Plant Hosts + Insect Vector Yes (Gottlieb et al. 2010) 661–671 , Endosymbiont Plant Pathogen Herbivore + Plant Hosts Unknown Antagonistic Pathogen Herbivores + Plant Hosts Yes (Tack, Gripenberg & Roslin 2012)

The ﬁrst column lists the category of invasive organisms (plant, insect or microbe), and the second column lists the type of interaction (additive or nonadditive where nonadditive is broken down into synergistic or antagonistic). The remaining columns are divided based on the number of examples within each type of interaction. The third column lists the functional group of the invasive organism. In this table, all plants essentially fall into a common functional group, but insects and microbes can be divided into multiple functional groups based on the organisms with which they are interacting (e.g. plant pathogen vs. entomopathogen). All known (and some hypothesized) examples of PMI interactions involving an invasive organism are listed in column four, and whether these interactions are known to promote invasion of the focal organism (along with references supporting that conclusion) are listed in the ﬁnal column. In some cases (e.g. plant–endophyte interactions and insect vector and plant pathogen interactions), there were too many references, so examples have been provided instead. ‘Unknown’ listed in the ‘Promote Invasion?’ column refers to a potential interaction for which there are no published examples. 663 664 A. E. Bennett

two things: first, endophyte effects are independent of her- Invasive plants bivore species, and second, abiotic factors such as soil structure are not likely to hinder endophyte effects on her- CAN PMI INTERACTIONS PROMOTE INVASIVE PLANTS bivores. As a result, a plant species infected with an effec- IN THEIR NEW ENVIRONMENTS? tive antiherbivore endophyte could invade and be We might expect that novel PMI interactions with additive successful in almost any environment. or synergistic effects would be most likely to promote inva- Interactions between soil-dwelling plant mutualists, sive species in their new environment (Table 1). However, plants and insects are also a frequently studied combina- antagonistic PMI interactions that hinder a pathogen or tion of PMI interaction involving invasive plants, but the herbivore may also promote invasive species fitness. This effects are less consistent and can be either additive or non- section highlights cases where all three types of inter- additive. These plant mutualists include nitrogen-fixing actions promote invasive plants. bacteria that fix atmospheric nitrogen for their host plants Plant–endophyte interactions have been shown to pro- and mycorrhizal fungi that increase the uptake of limiting mote the spread of invasive relative to native plant species nutrients (e.g. N and P). All research in the area of PMI due to their antagonistic effects on herbivores (Clay, Holah influences on invasive plants has focused on arbuscular & Rudgers 2005; Rudgers & Clay 2008; Uchitel, Omacini mycorrhizal (AM) fungi. Recently, Kempel and colleagues & Chaneton 2011). Endophytes are commonly defined as examined the defence responses to herbivory of invasive microbes that live within host plant tissues without nega- and noninvasive introduced plant species associated with tively impacting their host fitness (Wilson 1995). Endo- AM fungi (Kempel et al., 2013) and found no overall phyte–plant interactions range from commensal through interaction between invasive status and mycorrhizal status to mutualistic and were first identified in grasses (Bacon on plant defence against herbivory. Instead, the influence et al. 1977) but are now also known to occur in a wide of AM fungi on induced defences was both plant and her- variety of other plant species including several herbaceous bivore species specific. In an antagonistic example, in the (Gange et al. 2007), noncereal crop (Hallmann & Sikora invasive Bidens frondosa AM fungi promoted induced 1994; Hallmann et al. 1997; Raps & Vidal 1998; Sturz, defences over constitutive defences for one, but not a sec- Christie & Nowak 2000; Garbeva et al. 2001; Jallow, Dug- ond, herbivore. In other cases, AM fungi suppressed assa-Gobena & Vidal 2004; Hashiba & Narisawa 2005) induced defences against herbivores (Bennett, Bever & and tree species (Arnold et al. 2000; Vega et al. 2008; Alb- Bowers 2009; Kempel et al., 2013). Thus, mutualistic soil rectsen et al. 2010; Newcombe, Martin & Kohler 2010). microbes can influence the fitness of herbivores of intro- Some endophytes have been shown to increase invasive duced plant species by manipulating plant defence systems, plant species fitness (Clay 1988; Rudgers, Koslow & Clay although we are a long way from making consistent 2004; Aschehoug et al. 2012). While endophytes can confer predictions about how soil mutualistic microbes are likely many different benefits, research has frequently shown neg- to influence plant defence in invasive species. ative effects of endophytes on mammalian and insect her- Soil mutualistic microbes may also have an additive bivores (Raps & Vidal 1998; Jallow, Dugassa-Gobena & influence on pollinating insects, although significantly less Vidal 2004; Clay, Holah & Rudgers 2005; Rudgers & Clay is known about the outcome of these pollinator interac- 2008; Vega et al. 2008; Newcombe, Martin & Kohler 2010; tions with invasive plant species in general (Stout & Mor- Menjivar et al. 2012; Zhang et al. 2012), although these ales 2009). AM fungi increased pollinator visitation rates effects can also be influenced by nutrients and other biotic to two noninvasive introduced species (Tagetes eracta and factors (Saikkonen et al. 2006; Eschen et al. 2010). In Tagetes patula; Gange & Smith 2005). Some authors have some cases, the negative effects of endophytes on herbi- proposed that if a plant species (invasive or otherwise) vores can be passed on to the second generation of responds positively to a mutualistic soil microbe, then that herbivores – even if they are not feeding on the endophyte- microbe will likely promote plant–pollinator interactions infected host plant (Jaber & Vidal 2010) – or onto preda- (Cahill et al. 2008), thereby promoting invasion. To date, tors or parasitoids of the herbivores (de Sassi, Muller & all studies of pollinator PMI interactions and invasive Krauss 2006; Harri, Krauss & Muller 2008b) or even plants have utilized AM fungi, and thus, the effects of hyperparasitoids (Harri, Krauss & Muller 2008a). The suc- other soil mutualistic microbes on pollination of invasive cessful discouragement of herbivores in many grass–endo- plant species is still an open question. phyte combinations has been shown to be due to the As demonstrated above, novel PMI interactions can production of highly toxic alkaloid compounds with uni- promote invasive plant species, but there are also several versal effects against both mammalian and insect herbi- examples of invasive plant species becoming successful vores (Bacon et al. 1977). The most striking aspect of because they reduce (or avoid) interactions with microbes these effects, however, is that they can be replicated in a or insects. Invasive species often have reduced responses to wide variety of geographically spatially distinct locations their soil communities (Kulmatiski 2006) and herbivores, (Uchitel, Omacini & Chaneton 2011). The lack of spatial although these effects may not be correlated (Morrien, specificity in some endophyte–herbivore effects suggests Engelkes & van der Putten 2011). This could be due to the

© 2013 The Author. Functional Ecology © 2013 British Ecological Society, Functional Ecology, 27, 661–671 Can PMI interactions enhance or inhibit invasives? 665 frequent ability of invasive plant species to alter their soil organism on tea trees is increased by the negative effect of community (reviewed in van der Putten, Klironomos & each additional insect or microbe (Rayamajhi et al. 2010). Wardle 2007; Raizada, Raghubanshi & Singh 2008; Sanon The effects of both insect herbivores (E. villosus and et al. 2009) and disrupt or diminish the mycorrhizal fun- C. succinea) and a fungal rust, P. jaceae var. solstitialis,on gal–plant mutualism (Vogelsang & Bever 2009). In addi- yellow starthistle (C. solstitialis) have also been shown to tion, the Enemy Release Hypothesis suggests that invasive be additive as there is no interaction between the presence plant species are successful due to a reduction in inter- of insects and fungi on starthistle fitness (O’Brien et al. actions with microbial pathogens and insect herbivores in 2010). In a study in the same system, P. jaceae increased their new environment (Elton 1958; Keane & Crawley adult feeding but reduced larval feeding by E. villosus, 2002; Liu & Stiling 2006), and there are several examples resulting in little net impact and no influence on visiting demonstrating this strategy (reviewed in Liu & Stiling insect pollinators (Swope & Parker 2010). 2006). There are also several examples of invasive species There are also cases where the presence of both insects that use allelopathy to limit both microbes and insects and microbes has nonadditive effects that limit invasive (Weidenhamer & Callaway 2010; Inderjit et al. 2011). For species. For example, fungal root pathogens (Fusarium and example, Vincetoxicum rossicum (Mogg et al. 2008), Allia- Rhizoctonia species) had the greatest effects on leafy spurge ria petiolata (Burke 2008; Wolfe et al. 2008; Barto et al. (Euphorbia esula-virgata) when roots experienced insect 2011; Cantor et al. 2011; Keesing et al. 2011) and Centau- herbivory (Kremer, Caesar & Souissi 2006). The negative rea maculosa (Mummey & Rillig 2006; Broz, Manter & effects of a leafhopper (Erythroneurini spp.) and the fungal Vivanco 2007) have been shown to limit microbial popula- pathogen Puccinia myrsiphylli on the invasive Asparagus tion growth using allelopathic chemicals and, in the case asparagoides are significantly greater than if their individ- of both A. petiolata (Stinson et al. 2006) and C. maculosa ual effects are added (Turner et al. 2010). Also, Rosa mul- (reviewed in Callaway & Ridenour 2004), have been shown tiflora is best controlled by the combination of an to limit microbial interactions in neighbouring plants. eriophyid mite that transmits a pathogenic virus (reviewed These influences on soil microbial communities can in Smith, de Lillo & Amrine 2010). A future goal of bio- directly (Keesing et al. 2011) or indirectly influence insect– control PMI interactions will be to identify insect–microbe plant interactions. As a result, we must consider that in interactions with additive and nonadditive effects like some cases the success of invasive species may be due to those above before release. reduced novel interactions with insects and microbes. There are some biocontrol candidates currently being explored that rely heavily on PMI interactions. One such case involves Japanese knotweed (Fallopia japonica). A ser- CAN PMI INTERACTIONS INHIBIT INVASIVE PLANTS IN ies of surveys have identified a weevil (Euops chinesis) with THEIR NEW ENVIRONMENTS? high specificity for F. japonica, and this specificity appears Most research efforts on understanding the inhibitory to be due to a particular fungus that occurs in the leaf rolls effects of PMI interactions on invasive plants have been produced by E. chinesis when feeding on F. japonica. This dedicated to finding herbivores and pathogens that could fungus does not occur in the leaf rolls of E. chinesis on act as biocontrol agents. In addition, most biocontrol any other host plant, and E. chinesis cannot survive on efforts have not identified microbial–insect interactions alternative host plants (Wang, Wu & Ding 2010). Thus, that inhibit invasive plants and then released them, but incorporating PMI interactions is opening a whole new instead have found microbial–insect interactions that have field of biocontrol exploration that may lead to the discov- formed after introduction. In addition, some biocontrol ery of biocontrol agents with greater host specificity and efforts introduced multiple insect and microbial agents efficacy. with the expectation that they act additively [e.g. biocontrol herbivores (Eustenopus villosus and Chaetorellia Invasive insects succinea) and a fungal rust (Puccinia jaceae var. solstitialis) on yellow starthistle (Centaurea solstitialis)]. However, CAN PMI INTERACTIONS PROMOTE INVASIVE INSECTS there are several possible PMI interactions that could inhi- IN THEIR NEW ENVIRONMENTS? bit invasive plant species that have rarely been explored, such as interactions between pollinators and pathogens Just like invasive plants, invasive insects can be subject to (Swope & Parker 2010; Table 1). additive, synergistic and antagonistic interactions with Microbes and insects introduced as biocontrol agents plants and microbes. Several examples of interactions can influence each other in additive (Paynter & Hennecke between invasive insects and plants and microbes have 2001), synergistic or antagonistic ways. In an example of been heavily explored (e.g. insects acting as vectors, endos- an additive inhibitive effect on an invasive species, the bio- ymbionts), but other interactions have never been exam- control weevil Oxyops vitosa, psyllid Boreioglycaspis mela- ined (e.g. influence of plant pathogens on invasive insect leucae and rust fungus Puccinia psidii all negatively herbivore fitness; Table 1). influence the invasive tea tree (Melaleuca quinquenervia)in A potential synergistic PMI interaction involves bacte- Florida. When combined, the negative effect of each rial endosymbionts which can help insects adapt to new

© 2013 The Author. Functional Ecology © 2013 British Ecological Society, Functional Ecology, 27, 661–671 666 A. E. Bennett environments quickly and can contribute to the invasive Antagonistic novel PMI interactions can also promote ability of insects. One of the major discoveries of the last invasive insects. While it has been shown, as discussed few decades is that a number of insects, not just aphids, above, that toxic and allelopathic plant compounds can host bacterial endosymbionts that confer traits that are negatively impact both insects and microbes, in some cases not present in the insect genome (reviewed in Feldhaar herbivores can benefit from these compounds due to a 2011). These endosymbionts fall into two categories: obli- reduced antagonistic microbial load. This could be due to gate (often called primary) and facultative (often called sequestration of toxic compounds [e.g. Junonia coenia her- secondary). Insects cannot survive without obligate/pri- bivores sequester toxins from a novel host plant P. lanceo- mary endosymbionts that typically perform a vital integra- lata (Bowers 1984)], the consumption of toxic compounds tive function within the insect. The most well-known that have stronger effects on microbes than on the host example of a primary endosymbiont is the Buchnera aphid- insect, or due to the influence of the toxic compounds in icola of aphids that synthesize tryptophan and other essen- the medium (e.g. soil) in which the insect lives. For exam- tial amino acids for their hosts (reviewed in Shigenobu & ple, allelochemicals from the invasive Allaria petiolata Wilson 2011; McCutcheon & Moran 2012). In an exten- plant released into the soil negatively influence the general- sion of PMI interactions, B. aphidicola have been shown to ist entomopathogenic fungus Beauveria bassiana, thereby produce a protein, GroEL, that binds to the economically reducing the load of B. bassiana hosted by waxworms and damaging plant pathogens luteo- and poleroviruses as they potentially promoting waxworm fitness in the presence of pass through the aphid and prevent the viruses from being Allaria petiolata (Keesing et al. 2011). This type of positive degraded (Ishikawa, Yamaji & Hashimoto 1985; Bau- influence on insects has rarely been explored in the context mann, Baumann & Clark 1996; Humphreys & Douglas of invasions, and it may be likely that in some cases insects 1997; Douglas 1998; Bouvaine, Boonham & Douglas benefit from associating with toxic plants (allelopathic, 2011), thereby increasing the negative influence of the virus endophytic or otherwise) which may promote their inva- on the host plant fed on by the aphid. sive ability in environments where other insects cannot By contrast, secondary symbionts are not obligate and survive. can confer benefits in certain environments (Oliver et al. One of the most disastrous synergistic effects invasive 2010). Secondary endosymbionts and their rapid evolution- insects can have on an ecosystem is to introduce new ary responses to environmental change have been suggested microbial pathogens or to increase the spread of native to contribute to the world-wide invasion of B. tabaci microbial pathogens. In some cases, invasive insect species (Gueguen et al. 2010; Himler et al. 2011). Another example act as partially co-evolved vectors, whereas in other cases of endosymbionts contributing to insect invasions involves invasive insects pick up new associations or incidentally a biocontrol parasitoid, Psyllaphaegus bliteus, introduced to transfer pathogens. There are several cases of invasive California to control the invasive herbivore, Glycaspis brim- insect vectors. For example, the introduction of the glassy blecombei, of the invasive Eucalyptus camaldulensis tree. A winged sharpshooter (H. vitripennis) is increasing the survey of the endosymbionts of G. brimblecombei revealed spread of the native bacterial pathogen Pierce’s disease that endosymbionts that conferred resistance to P. bliteus (X. fastidiosa) among grapevines in California (Gomes were present in higher frequencies in populations where et al. 2000). The invasive panicle rice mite has been P. bliteus was present, therefore reducing the efficacy of the spreading through the Caribbean and Central America biocontrol agent (Hansen et al. 2007). Given that research- where it devastates rice crops. However, much of the dam- ers are just beginning to identify the presence of secondary age caused by panicle rice mite may actually be due to the endosymbionts in many organisms and the function of interaction between the mite and two rice pathogens many of these endosymbionts has yet to be determined, it Sarocladium oryzae and Burkholderia glumae (reviewed in seems likely that future research will reveal a large role of Hummel et al. 2009). Thrips (insects of the order Thysa- endosymbionts in novel synergistic PMI interactions. noptera) vector a wide variety of viral pathogens, are com- In addition to carrying adaptive endosymbionts, herbi- mon invaders in agricultural systems and have received a vores can also host plant-attacking microbes as endo- great deal of attention due to the limited mechanisms symbionts that can have synergistic effects and increase available for controlling them or the diseases they spread herbivore fitness. For example, the leafmining moth, Phyl- (reviewed in Morse & Hoddle 2006). The combination of lonorycter blancardella, appears to host a Wolbachia bacte- invasive insects and their microbial associates can therefore rium that manipulates plant cytokinin levels (Kaiser et al. cause significant economic damage to agricultural systems. 2010). The manipulation of host plant physiology increases Like agricultural systems, forest systems are being hit P. blancardella fitness by preventing plants from senescing hard by combinations of insect pests and their associated attacked leaves and forcing the plant to continue to deliver microbes (Hulcr & Dunn 2011). Novel insect–microbe nutrients to areas where P. blancardella is feeding (Kaiser combinations are changing the composition of forests in et al. 2010, Giron et al., 2013). While this is so far a Europe and North America by eliminating trees which unique mechanism of action for an insect endosymbiont, it often act as keystone species (Loo 2009), and altering eco- seems likely that continued explorations of insect endo- system properties such as carbon cycling (Hicke et al. symbionts and plant pathogens will reveal similar cases. 2012). The effects of some of these novel insect–microbe

© 2013 The Author. Functional Ecology © 2013 British Ecological Society, Functional Ecology, 27, 661–671 Can PMI interactions enhance or inhibit invasives? 667 interactions are predicted to become more severe with the invasion of a forest tree pest, the Asian longhorned beetle onset of climate change (Dukes et al. 2009). For example, (Anoplophora glabripennis), in North America and Europe the Asian ascomycete pathogenic fungi, Ophiostoma ulmi, is partially controlled by entomopathogenic fungi (Hu Ophiostoma himal-ulmi and Ophiostoma novo-ulmi (Har- et al. 2009). It has been proposed that a combination of rington et al. 2001), the cause of Dutch elm disease in Eur- entomopathogenic fungi and manipulation of tree commu- ope and North America, have led to significant damage. nities to include preferred and nonpreferred host trees The spread of Dutch elm disease in North America was would provide the best control of A. glabripennis (Hu likely increased due to the introduction of European elm et al. 2009). As a result, entomopathogens, particularly bark beetle (Scolytus multistriatus), which along with the entomopathogenic fungi, are gaining increasing attention native elm bark beetle (Hylurgopinus rufipes) act as vectors as potential biocontrol agents of invasive insects. for Dutch elm disease (Karnosky 1979; Hubbes 1999). In Researchers are currently exploring the efficacy of entomo- this case, an invasive insect spreads an invasive pathogen pathogenic fungi for controlling the spread of B. tabaci in which the insect had never previously encountered before the UK (Cuthbertson et al. 2011). However, research also introduction. Beech bark disease is the result of another shows that nonadditive interactions with the plant can novel insect–microbe combination causing havoc in forest determine the efficacy of entomopathogenic fungi as plant systems. The introduction of the beech scale (C. fagisuga) chemistry can influence the success of fungal attack of into Europe and North America has led to the spread of insects (Cory & Ericsson 2010). This further demonstrates beech bark disease. Unlike S. multistriatus, which acts as a the need to incorporate all three organisms (plants, insects vector for fungal pathogens, beech scale does not vector and microbes) into biocontrol studies. the North American (Neonectria faginata) and European (Neonectria galligena) fungi (Castlebury, Rossman & Invasive microbes Hyten 2006) that produce beech bark disease. Instead, it simply creates the wounds in beech bark that are easily CAN PMI INTERACTIONS PROMOTE INVASIVE colonized by the fungi (Houston 1994). Although not a MICROBES IN THEIR NEW ENVIRONMENTS? tree, R. multiflora is a common invader of forest and other habitats. It also suffers from a novel invasive pathogen– There has been less research identifying novel additive, insect combination involving the introduced eriophyid mite synergistic and antagonistic interactions that influence the (Phyllocoptes fructiphilus) that transmits a pathogenic virus promotion of invasive microbes (Table 1). In particular, to R. multiflora while feeding. None of these organisms, there are no recorded cases of insect interactions helping plant, mite or virus, had previously encountered one invasive microbes overcome the influence of negative plant another before introduction; however, the combination is interactions, and there are no known examples of positive negatively impacting the invasive R. multiflora (reviewed in plant interactions allowing invasive microbes to overcome Smith, de Lillo & Amrine 2010). a negative interaction with an insect (Table 1). As a result, Awareness of the ability of introduced and invasive there is plenty of opportunity for exploring these interac- insects to spread disease has had impacts on the field of tions in future. biocontrol. Biocontrol insect candidates are now often Instead, the vast majority of our understanding of how being screened for their ability to spread native and inva- invasive microbes interact with insects and plants derives sive microbial pathogens, and rejected if they show the from the synergistic interaction of insect vectors of potential to do so (Lennox et al. 2009). Almost all of the microbes. In the previous section, we discussed several examples above are from agricultural or forestry systems examples of invasive microbes vectored by insects, includ- for which invasive insects spreading microbial pathogens ing panicle rice mite increasing the spread or effects of the cause significant economic impacts. However, it seems pathogens S. oryzae and B. glumae (reviewed in Hummel likely that invasive insects and their associated microbes et al. 2009), vectoring of the three invasive fungal Ophios- are impacting other systems as well; however, more toma spp. that cause Dutch elm disease (Karnosky 1979; research attention will need to be dedicated to determining Hubbes 1999; Harrington et al. 2001), and the spread of a those effects. number of microbial pathogens by thrips (reviewed in Morse & Hoddle 2006). Another concerning example is the case of the whitefly (B. tabaci) and the spread of Gem- CAN PMI INTERACTIONS INHIBIT INVASIVE INSECTS IN iniviruses. The invasive agricultural pest B. tabaci is THEIR NEW ENVIRONMENTS? spreading around the world, including sites as disparate as Research into PMI interactions that can limit invasive Indonesia (De Barro et al. 2008), Costa Rica (Guevara- insect plant pests has also focused on identifying bio- Coto et al. 2011) and La Reunion (Delatte et al. 2009). control agents from the original habitat of the invasive B. tabaci is an efficient vector of Geminiviruses, particu- insect that have additive or antagonistic interactions. In larly begomoviruses (De Barro et al. 2008; Li et al. 2010), particular, entomopathogenic microbes are often explored so wherever B. tabaci appears, diseases produced by Gem- as potential biocontrol agents of insect plant pests (Cory & iniviruses, such as lettuce infectious yellows virus, tobacco Ericsson 2010; Hajek & Delalibera 2010). For example, the curly shoot virus, tomato yellow leaf curl virus and

African cassava mosaic virus, appear or increase shortly plants described above may move in the opposite direction afterwards. In some cases, the interaction between viruses – herbivory may suppress microbial infection. The lack of such as tomato yellow leaf curl virus and B. tabaci research in this area opens up great opportunities for increases B. tabaci fecundity and fitness (Jiu et al. 2007; exploring how PMI interactions could suppress invasive Guo et al. 2010). The transmission of viruses by B. tabaci microbes. to plants requires a protein created by an endosymbiotic bacteria (Gottlieb et al. 2010), thereby increasing the com- What is the future of the study of invasive plexity of this novel synergistic PMI interaction. The intro- plants, microbes and insects involved in PMI duction of B. tabaci and its associated begomoviruses has interactions? caused complete crop losses, severe economic losses, and contributed to famines in some areas of the world Novel PMI interactions are likely to increase in future fol- (Thompson 2011). lowing increased introductions of species and the influence There is the potential for antagonistic PMI interactions of climate changes. In addition, the majority of docu- involving apparent trade-offs between plant defensive sys- mented successful novel PMI interactions are not additive, tems (such as the JA and SA pathways) to promote inva- but instead nonadditive (Table 1). As a result, the future sive pathogens. Although not a PMI interaction involving of the study of novel PMI interactions will need to involve an invasive species, on the Barbarea vulgaris plant in Den- both predictive and preventative components if we are to mark white rust is rarely observed – unless the plant has counter these new invasions. received herbivory (van Molken, unpublished). This sug- An obvious place to begin research on predicting inva- gests, as has been previously shown, that some plant sive novel PMI interactions is with insect vectors and the defensive activities can limit the activity of other plant microbial pathogens they promote. In this review, insects defensive activities (reviewed in Beckers & Spoel 2006). and the microbes they vector were the most common novel This is a potential mechanism for insect and microbe influ- PMI interaction and the group of novel PMI interactions ence that has rarely been explored in the context of causing the most economic damage. While their documen- invasive insects and microbes. tation and economic costs may not be independent factors, It may also be possible that invasive microbes can act their large impact does suggest they are among the most antagonistically towards plants and microbes. In Finland, frequent novel PMI interactions. In one pathogen–insect the presence of an invasive mildew on host trees decreases vector system, a secondary endosymbiont is credited both herbivore number and herbivore species number on with improving insect and pathogen matching (Gottlieb host plants (Tack, Gripenberg & Roslin 2012). In this case, et al. 2010). Therefore, utilizing techniques such as next- there may be unobserved direct effects between the mildew generation DNA sequencing, genomics, transcriptomics and insects, or the mildew may be able to manipulate host and metabolomics combined with traditional ecological defences to its advantage. Also, as discussed above, the experiments will likely identify whether endosymbionts are spread of endophyte-infected host plants increases the responsible for novel pathogen–insect vector interactions spread of their endophytes with potentially negative influ- or whether other mechanisms promote these novel interac- ences on insect herbivore communities (Rudgers & Clay tions in different systems. Researching the factors that 2008). As a result, there are still several potential unex- allow insects to vector a wide variety of microbes and the plored mechanisms describing the interactions between factors that allow pathogenic microbes to utilize novel vec- invasive microbes, insects and plants. tors is a first step to developing a predictive framework for identifying novel potentially invasive PMI interactions. Utilizing multiple synergistic and antagonistic interac- CAN PMI INTERACTIONS INHIBIT INVASIVE MICROBES tions to limit invasive species should also be a priority in IN THEIR NEW ENVIRONMENTS? the field of PMI interactions. In addition to identifying Relatively little research has identified examples where potential biocontrol PMI interactions (Wang, Wu & Ding PMI interactions inhibit invasive microbes within their 2010), there are common PMI interactions (e.g. soil mutu- new environments (Table 1). There are several possible alistic microbes associating with plants eaten by herbivores, avenues by which PMI interactions are likely to inhibit endophyte-infected plants that suppress herbivory) that invading microbes. For example, microbes that rely heavily occur in most systems that could possibly be manipulated on a vector are only likely to increase their spread if their to limit invasive species. In several cases, microbial plant vector increases their range or is introduced. As a result, mutualists have been shown to increase plant defences microbes that rely on vectors not present in the new envi- against herbivores (Clay, Holah & Rudgers 2005; Rudgers ronment could cause extensive plant diseases but are lim- & Clay 2008; Gehring & Bennett 2009; Uchitel, Omacini & ited by the lack of a synergistic interaction. As a result, Chaneton 2011). A second means of targeting invasive implementing measures that limit the spread of vectors insects could be to target their endosymbionts. Eliminating should also limit vectored invasive microbes. In addition, endosymbionts could limit invasive insect adaptation to it seems likely that in some cases, antagonistic interactions new host plants and even kill host insects. There is cur- like interactions between defensive strategies within host rently a developing field of research focused on community

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