Invasive species are one of the greatest challenges for most ecosystems in the world. Alone, invasive fungi cost US agriculture $21 billion USD per year (Rossman 2009). Invasive plant species have similarly strong economic impacts: in 2003, invasive plants were estimated to cost Australia approximately $4 billion AUD per year (Sinden et al. 2004), whereas Vila et al. (2010) estimated that the cost of eradicating only the 30 most common invasive plant species in Europe was greater than €150 million. In addition, European crop losses to invasive insects are estimated at €2·8 billion (Vila et al. 2010). These figures demonstrate that plants, insects and microbes are having dramatic effects on the world economy, and many of these economic impacts are actually due to interactions between plants, insects and microbes.
Human transport of non-native species has likely occurred since the movement of humans across the globe began in Neolithic times (Webb 1985), but was not typically recorded until the age of European exploration (approximately AD 1500) when the introduction of species began to increase (di Castri, Hansen & Debussche 1990). Today, however, as human movement and trade across the globe becomes increasingly common, the introduction of new species has increased in frequency (reviewed in Bradley et al. 2012). Seeds, eggs, spores and other living material are transported both knowingly and unknowingly. While most introductions fail, the increasing number of introductions is leading to an increasing number of successful introductions (reviewed in Bradley et al. 2012). This paper will distinguish between two types of introduced species: ‘invasive’ species that dominate habitats causing changes to ecosystems and economic losses, and the broader category of ‘noninvasive’ introduced species that either have become naturalized in their new environment or have yet to become invasive.
Multiple theories have been proposed to explain what biotic factors influence invasive species success. The vast majority of these theories have focused on or been developed for invasive plants. These theories include the Enemy Release Hypothesis (invasives encounter fewer enemies in new environments; Elton 1958; Keane & Crawley 2002; Liu & Stiling 2006), Evolution of Increased Competitive Ability (invasives evolve to be better competitors in new environments in the absence of enemies; Blossey & Notzold 1995) or the Novel Weapons Hypothesis [in which invasive species (primarily plants) exclude competitors using toxic compounds; Callaway & Ridenour 2004]. A recent review revealed 29 different proposed hypotheses for the success of invasive species, and the vast majority of these hypotheses focused on traits of invasive plant species or two-way biotic interactions (Catford, Jansson & Nilsson 2009). For example, the Enemy Release Hypothesis applies to the enemies of plants, regardless of whether they be insect or microbial, but does not consider the influence of insect–microbe interactions on plants.
Greater numbers of introduced species can also increase the likelihood of novel species interactions (Richardson et al. 2000), particularly between plants, microbes and insects. The effects of microbes, insects and plants on each other can be additive or nonadditive. When effects are additive, the outcome of one interaction is not influenced by a second or third interaction – all influences are independent allowing us to ‘add’ the influence of one organism to the influence of a second organism. Nonadditive interactions between plants, microbes and insects are those in which the influence of multiple organisms is not equal to the sum of the individual influences of each organism (Fournier et al. 2006). Nonadditive interactions can be synergistic (in which the outcome is greater than the additive effects) or antagonistic (in which partners hinder each other and the outcome is less than the additive effects; Fournier et al. 2006). In the new field of plant–microbe–insect (PMI) interactions highlighted in this issue, research has identified additive, synergistic and antagonistic interactions between plants, insects and microbes (Table 1).
|Invasive organism||PMI Interactions 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)|
|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 Host||Yes (Gottlieb et al. 2010)|
|Antagonistic||Pathogen Vector||Pathogens + Plant Hosts||Unknown|
|Microbe||Additive||Entomopathogen||Insect Host + Insect Plant Hosts||Unknown|
|Endophyte||Plant Hosts + Herbivores||Yes (Clay, Holah & Rudgers 2005; Rudgers & Clay 2008; Uchitel, 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)|
|Plant Pathogen + Endosymbiont||Plant Hosts + Insect Vector||Yes (Gottlieb et al. 2010)|
|Plant Pathogen||Herbivore + Plant Hosts||Unknown|
|Antagonistic||Pathogen||Herbivores + Plant Hosts||Yes (Tack, Gripenberg & Roslin 2012)|
This paper will focus on novel PMI interactions created from the introduction of new species. We would expect that new interactions among species might be simple (or additive) in nature. However, there are several cases in which these novel interactions have nonadditive effects. For example, the combination of a plant pathogen and a novel insect vector of that pathogen has led to the loss or damage of 1300 acres of grapevines in California (Gomes et al. 2000): the glassy winged sharpshooter (Homalodisca vitripennis), an invasive insect introduced to California in 1989, has become a vector for the Xylella fastidiosa pathogen, which causes Pierce's disease in grapevines. Here, the synergistic interaction between the invasive insect and native pathogen has promoted the range expansion of the pathogen. In a second example of novel synergistic PMI interactions involving three novel interactions, the invasive shrub Rosa multiflora is fed on by an invasive eriophyid mite that vectors a virus (Smith, de Lillo & Amrine 2010). Prior to their introduction to North America, these organisms had never interacted before. Thus, despite their short association, novel PMI interactions containing invasive species can be synergistic and have dramatic consequences for native and agricultural systems.
These novel PMI interactions may be further promoted by climate change which is likely to influence novel PMI interactions by increasing the introduction of novel species (Hellmann et al. 2008), favouring invasive species over native species and promoting the range expansion of invasive species in their new environments (reviewed in Dukes 2011). We know increases in temperature often increase insect activity (reviewed in Bale et al. 2002), while changes in CO2 and O3 alter both insect (Hillstrom & Lindroth 2008) and soil microbial mutualist communities (Andrew & Lilleskov 2009; but see Klironomos et al. 2005) as well as plant pathogens (Eastburn, McElrone & Bilgin 2011). Climate changes have also been predicted to promote species range shifts and the expansion of invasive species globally (reviewed in Hellmann et al. 2008; Dukes 2011). All of these effects could lead to new encounters between plants, microbes and insects. For example, beech bark disease, the result of an association between the beech scale insect (Cryptococcus fagisuga) and a fungus, is moving northward in its introduced range (Kasson & Livingston 2009). In addition, there are suggestions that the invasive insect herbivore whitefly (Bemisia tabaci), a vector of the economically devastating Gemini viruses, is currently expanding its range in Europe in response to warmer climates (E. Bejarano, pers. comm.). It can be difficult to make sweeping predictions about the influence of climate changes on these interactions (Dukes et al. 2009), but these examples also suggest that climate change could increase the proportion and impact of novel PMI interactions.
The examples above highlight that interactions between plants, microbes and insects can create serious invasive species problems. As demonstrated in this issue, PMI interactions have far-reaching consequences in a wide variety of systems. Our increased knowledge of PMI interactions in invasions has identified three major questions that need addressing: Will novel PMI interactions promote invasive plants, insects and microbes? Can we use novel PMI interactions to inhibit new invasions? Can we predict whether novel PMI interactions are likely to become invasive?
The aim of this paper is to address these three questions with our current knowledge of PMI interactions. In particular, this paper will focus on whether PMI interactions promote or inhibit invasive plants, insects or microbes.