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Keywords:

  • alien plant;
  • butterfly;
  • disruption;
  • exotic plant;
  • heterogeneity;
  • multitrophic interactions

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Going up: from two to three trophic levels and higher
  5. Structural and chemical characteristics of plants as they affect the foraging and dispersal behavior of herbivores, parasitoids, and hyperparasitoids
  6. How invasive plants affect structural heterogeneity in native habitats
  7. How invasive plants may affect chemical heterogeneity in native habitats
  8. The effects of invasive plants on native insect communities via associational resistance and susceptibility
  9. The potential benefits of invasive plants on native insects
  10. Conclusions and future directions
  11. Acknowledgements
  12. References

The introduction and/or spread of exotic organisms into new habitats is considered a major threat to biodiversity. Invasive plants have been shown to negatively affect native communities, competing with and excluding other plants and disrupting a wide range of trophic interactions associated with them. In spite of this, thus far, few studies have explicitly studied the mechanisms underlying the displacement and potential local extinction of native herbivores and their natural enemies up to the third trophic level and even higher. Here, we formulate hypotheses on how structural and chemical characteristics of invasive plants may affect the plant-finding abilities of herbivores and the host- or prey-finding behavior of predators and parasitoids. The sudden incursion of an invasive plant into a native plant community may fragment native habitats and thus create structural barriers that impede dispersal and plant-finding ability for herbivores and prey- or host-finding ability for predators and parasitoids. At the same time, invasive plants may produce odors that are attractive to native insects and thus interfere with interactions on native plants. If invasive plants are both attractive and toxic to native insects, they may constitute ‘traps’ that are possibly beneficial against insect pests in agro-ecosystems, but have conservation implications for native herbivores and their natural enemies. However, we also suggest that some herbivores, and by association their parasitoids, may benefit from the establishment and spread of exotic plants because they increase the amount of available resources for them to exploit.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Going up: from two to three trophic levels and higher
  5. Structural and chemical characteristics of plants as they affect the foraging and dispersal behavior of herbivores, parasitoids, and hyperparasitoids
  6. How invasive plants affect structural heterogeneity in native habitats
  7. How invasive plants may affect chemical heterogeneity in native habitats
  8. The effects of invasive plants on native insect communities via associational resistance and susceptibility
  9. The potential benefits of invasive plants on native insects
  10. Conclusions and future directions
  11. Acknowledgements
  12. References

Over the past century, an increasing number of anthropogenic processes have combined to threaten ecological communities, ecosystems, and biomes across the biosphere. These processes include habitat loss and fragmentation, various forms of pollution, climate change, and biological homogenization through the introduction of exotic species into non-native ecosystems (Kappelle et al., 1999; Novacek & Cleland, 2001; van der Putten et al., 2004; Thuiller, 2007; McGeoch et al., 2010). The scale of these threats has increased in recent years, especially with concomitant increases in population and per capita impacts on nature due to increases in technology. For example, the integration of the global economy, combined with habitat destruction, has accelerated the introduction and/or spread of plants and animals into new habitats. Once they occupy new habitats, a small number of invasive organisms flourish and are capable of displacing native biota, driving local extinctions and ultimately threatening the functioning of ecosystems and interfering with a range of important services that emerge from them (Vitousek et al., 1996; Pejchar & Mooney, 2009; Ehrenfeld, 2010).

Predicting the impacts of invasive species on food webs and communities is one of the biggest contemporary challenges facing ecologists. Because they occur at the basal end of the food chain, invasive plants have the capacity to seriously disrupt native communities from the bottom up, competing with and excluding other plants and interfering with a wide range of trophic interactions associated with them (Cronin & Haynes, 2004; Harvey & Gols, 2011; Paine et al., 2011). Some invasive plants are able to colonize a broad range of native ecosystems and to displace native vegetation, quickly transforming these ecosystems into ones that are profoundly different in structure and composition.

Several hypotheses have been proposed to describe the factors that help promote the success of invasive plants. Two of these deal exclusively with the effects of the second trophic level (e.g., herbivores and plant pathogens) on the plants and vice versa. For example, the ‘enemy-release hypothesis’ (ERH) posits that invasive plants have escaped from a wide range of co-evolved specialist natural enemies in their native range and thus experience less damage from native generalist enemies in their new range (Keane & Crawley, 2002; Agrawal et al., 2005; Jogesh et al., 2008). Several studies, for example, have indeed reported that invasive plants have lower herbivore loads than related native plants (Wolfe et al., 2004). Furthermore, it has also been shown that some of the most successful invaders posses certain characteristics, such as novel secondary compounds, that are not found amongst native plants in the new range (Cappuccino & Arnason, 2006). The ‘novel-weapons hypothesis’ (NWH) describes plants, which produce unique morphological or chemical traits that confer protection for the invader against potentially new enemies in the native range that are not evolutionarily adapted to the new traits (Callaway & Maron, 2006; Callaway et al., 2008). The garlic mustard, Alliaria petiolata (M. Bieb.) Cavara & Grande, is native to Eurasia where it is locally common, but rarely dominant. By contrast, this species is highly invasive in North America, where it aggressively out-competes native vegetation, including other forbs and even trees (Stinson et al., 2006). Alliaria petiolata produces a cocktail of toxins in its leaf tissues, including the glucopyranoside alliarinoside and cyanide, which are absent or rare in other North American plant taxa (Cappuccino & Arnason, 2006; Cipollini & Gruner, 2007). The plant is highly toxic to the caterpillars of native white butterflies, including Pieris oleracea Harris and Pieris virginiensis Edwards, whose adult females readily oviposit onto the plant. This has been cited as a major factor in the regional decline of these insects over the past 20 years (Keeler et al., 2006; Keeler & Chew, 2008).

Going up: from two to three trophic levels and higher

  1. Top of page
  2. Abstract
  3. Introduction
  4. Going up: from two to three trophic levels and higher
  5. Structural and chemical characteristics of plants as they affect the foraging and dispersal behavior of herbivores, parasitoids, and hyperparasitoids
  6. How invasive plants affect structural heterogeneity in native habitats
  7. How invasive plants may affect chemical heterogeneity in native habitats
  8. The effects of invasive plants on native insect communities via associational resistance and susceptibility
  9. The potential benefits of invasive plants on native insects
  10. Conclusions and future directions
  11. Acknowledgements
  12. References

One of the biggest shortcomings of current studies with invasive plants is that they have primarily focused on interactions involving only two directly interacting trophic levels, i.e., the first and second. Moreover, the vast majority of these studies have been based on unraveling the various factors that enable a small minority of exotic plant species to become invasive pests in their new range (e.g., Keane & Crawley, 2002; Thomas & Reid, 2007). However, it has long been known that a more complete appreciation of the factors that regulate the structure and functioning of terrestrial communities must include natural enemies of herbivores, such as pathogens, predators, and parasitoids, as well as antagonistic interactions even further up the food chain (Hairston et al., 1960; Price et al., 1980; Hunter & Price, 1992; Hunter, 2003).

Recent meta-analyses have shown that top-down as well as bottom-up forces are involved in regulating terrestrial biomass (Schmitz et al., 2000; Halaj & Wise, 2001; Romero & Koricheva, 2011). If this is true, studies exploring the various factors that determine the success or failure of a plant to become an invasive pest in a new habitat should include natural enemies of herbivores, although this has rarely been done (but see Cronin & Haynes, 2004). Thus far, current knowledge of invasive plants on native food webs (including natural enemies) is largely descriptive, for instance, based on quantitative food web analyses (Memmott & Waser, 2002; Heleno et al., 2009). By contrast, few studies with invasive plants have thus far explored a range of eco-physiological mechanisms that determine: (1) the effects of primary and secondary plant compounds (nutrients and toxins) on the development and survival of herbivores and their natural enemies; and (2) structural and chemical aspects of invasive plants that affect foraging and host location behavior in herbivorous insects, and thus might lead to differential consequences on various members of an interacting food chain. The first area has recently been discussed by Harvey et al. (2010a,b). This article addresses the second aspect. Our main hypothesis is that changes in the structural and chemical environment at small and medium spatial scales will affect interactions between native herbivores and their antagonists. These effects may lead to the local loss in insect abundance and/or diversity, and have consequences for the structuring of food webs. Although many of these effects will be negative through either the disruption of foraging behavior of herbivores, parasitoids, and/or predators, or through variable responses exhibited by the organisms across different trophic levels, we argue that alien plants may also benefit some native insects.

Structural and chemical characteristics of plants as they affect the foraging and dispersal behavior of herbivores, parasitoids, and hyperparasitoids

  1. Top of page
  2. Abstract
  3. Introduction
  4. Going up: from two to three trophic levels and higher
  5. Structural and chemical characteristics of plants as they affect the foraging and dispersal behavior of herbivores, parasitoids, and hyperparasitoids
  6. How invasive plants affect structural heterogeneity in native habitats
  7. How invasive plants may affect chemical heterogeneity in native habitats
  8. The effects of invasive plants on native insect communities via associational resistance and susceptibility
  9. The potential benefits of invasive plants on native insects
  10. Conclusions and future directions
  11. Acknowledgements
  12. References

Vegetation complexity is characterized by two main trait-mediated aspects: structural and chemical complexity. These traits are often species-specific and diversity within and between habitat patches will strongly affect the expression of these traits. Chemical and structural complexity of plants will affect flight, host-finding, orientation, and oviposition behavior in insects and both may act synergistically in affecting these parameters. It should also be stressed that habitats in which invasive plants establish themselves are never in stasis, but exhibit dynamic patterns of growth, biomass, and species diversity that may vary considerably even over the course of a single growing season (Figure 1). This may mean that the phenology of seasonal invaders and the life-cycles of arthropods in their habitats may overlap to varying degrees. Furthermore, many insect herbivores and their natural enemies that are found in habitat patches may have more than a single generation per year, and thus different generations of insects may be exposed to a structural and chemical milieu that differs profoundly according to the composition of the plant community (Gols et al., 2011). For example, there is a high seasonal fluctuation in the toxicity of the invasive crucifer, A. petiolata, in North America (Haribal & Renwick, 2001). The theoretical and empirical literature is replete with studies that have examined the effects of structural and chemical complexity of the plant community on the biology and ecology of herbivorous insects and their natural enemies (Root, 1973; Kareiva, 1985; Andow, 1991; Grez & Gonzalez, 1995; Renwick, 2002; Meiners & Obermaier, 2004; Tscharntke & Brandl, 2004; Gols et al., 2005; Hambäck et al., 2006; Randlkofer et al., 2010). However, thus far, this has rarely been done in exploring the potential community-related effects of invasive plants. In the following section, we separately examine each of these areas in more detail.

image

Figure 1.  Phenology of the exotic plant Bunias orientalis across a single growing season in a natural population in The Netherlands. This species, which is native to central and western Asia, has recently become a highly invasive pest weed over much of central and northern Europe. The plant is a perennial that can live up to 15 years, although every winter it dies back to the root–soil interface. In early spring, rosette leaves begin to grow and flowering shoots appear in May when the plant begins to flower. Following the production of seeds (which are ripe by late July), the first rosette temporarily dies back; however, a second set of rosette leaves begin to grow soon thereafter, and remain apparent until the end of October, when the first frosts kill the plant above the soil surface. In the peak of the summer, B. orientalis plants grow several flowering stems and can dominate extensive areas along disturbed habitats, such as roadsides as shown on the picture above taken in June 2010 in Drempt, province Gelderland, The Netherlands.

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How invasive plants affect structural heterogeneity in native habitats

  1. Top of page
  2. Abstract
  3. Introduction
  4. Going up: from two to three trophic levels and higher
  5. Structural and chemical characteristics of plants as they affect the foraging and dispersal behavior of herbivores, parasitoids, and hyperparasitoids
  6. How invasive plants affect structural heterogeneity in native habitats
  7. How invasive plants may affect chemical heterogeneity in native habitats
  8. The effects of invasive plants on native insect communities via associational resistance and susceptibility
  9. The potential benefits of invasive plants on native insects
  10. Conclusions and future directions
  11. Acknowledgements
  12. References

After they have become well established in a native community, invasive plants may displace native plants and end up occupying much of the latter’s habitat, thereafter much smaller patches of native vegetation. This in turn may significantly affect insect herbivores and their natural enemies which are associated with the native plants. A large body of evidence has shown that the physical characteristics of habitats can affect intra- and inter-patch dispersal movements of insects that are associated with plants within the patches [Roland et al., 2000; Goodwin & Fahrig, 2002; Cronin, 2004; Cronin & Haynes, 2004; Bukovinszky et al., 2005; Gols et al., 2005; Bezemer et al., 2010; reviewed by Andow (1991) and Randlkofer et al. (2010)]. In theory at least, the disruption of dispersal and foraging behavior in herbivores and their natural enemies could deleteriously affect the population dynamics of predator–prey or host–parasitoid associations and, if serious enough, eventually lead to the local extinctions of species or species interactions.

The effects of invasive plants on native consumer-based interactions are also likely to vary at the spatial and temporal scales in which they occur. Early in the season, when annual plants have only begun to grow, the structure of the plant community is likely to be much simpler than later in the season after which there has been a dramatic increase in biomass. However, even in simple landscapes and at smaller scales, the architecture of the plant stem, young shoots, and leaves can either facilitate or impede insect movement amongst vegetation. If the invasive plant is taller than its native neighbors, or else produces much more densely packed foliage, then this may prove to be a major impediment in the efficiency of insects to cross habitat patches, to locate suitable food plants, or to disperse to adjacent habitat patches (Figure 2B). In one of the few studies to explicitly test the effects of an invasive plant on a native tri-trophic interaction, Cronin & Haynes (2004) examined landscape-level interactions involving prairie cordgrass, Spartina pectinata Link, an obligate specialist herbivore, the plant-hopper Prokelisia crocea Van Duzee, and its specialist egg parasitoid, Anagrus columbi Perkins in mudflat plots with and without an invasive grass, smooth brome, Bromus inervis Leyss. The authors found that the presence of brome facilitated dispersal of the insects much more rapidly through habitat matrices and negatively affected the abundance and persistence of both species. They also found that the presence of brome resulted in a four- to five-fold increase in local extinction rates of the insects, with the parasitoid being more adversely affected than its herbivore host. It is not known if the invasive plant impeded trophic interactions through structural or chemical (or a combination of both) traits.

image

Figure 2.  Conceptual diagram showing the potential effects of invasive plants on a four-trophic-level interaction involving plants, herbivores, a parasitoid, and hyperparasitoid. (A) A native plant species grows in patches where it is dominant. A specialist herbivore (in this case a moth) oviposits on the plant which, through feeding damage from the caterpillar, releases volatiles (blue plumes) that attracts one of its specialist natural enemies, a primary endoparastioid. In turn, plant-related cues attract a primary hyperparasitoid of the primary endoparasitoid. (B) A larger unrelated invasive plant species fragments patches in which the native plant grows. The plant provides structural and perhaps chemical barriers, such as repellents (red plumes) that interfere with the foraging behavior of the moth, its primary parasitoid and hyperparasitoid. (C) The invasive plant species is a close relative of the native plant species, and invades the same patches where the native plant normally occurs. The invasive plant produces volatiles that are attractive to the herbivore and its parasitoid, but the plant tissues are toxic to both of them and the plant thus represents a potential evolutionary ‘trap’ for these consumers. Another generalist herbivore readily feeds on both plants, increasing the level of volatiles emitted that are attractive to the herbivore and its parasitoid. This may increase the detection or ‘associational susceptibility’ of the invasive plant to the specialist herbivore and its parasitoid. Ultimately, the effects of structural and chemical impediments imposed by invasive plants on native insects will critically depend on how different species and trophic levels respond to them.

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A number of studies with either natural or artificial plant assemblages have begun to disentangle the effects of structural barriers on the foraging behavior of insects. Gols et al. (2005) found that the parasitoid Diadegma semiclausum Hellén took longer to find larvae of its host, Plutella xylostella L., on the host food plant, cabbage, when the wasps were released into cages containing barley and cabbage as opposed to cabbage alone. Barley plants were taller than cabbage plants and the wasps were physically impeded during foraging flights by the presence of barley. However, some insects may forage more efficiently in complex habitats. For instance, White & Andow (2006) found that parasitism of the European corn borer, Ostrinia nubilalis Hübner, by its specialist parasitoid Macrocentrus grandii Goindanich was reduced by almost 100% when roots of host plants were infested with larvae of the corn rootworm, Diabrotica virgifera virgifera LeConte. The authors revealed that root-infested plants were much smaller and grew in patches that were less dense than plants growing in the absence of rootworms, and that the parasitoids preferred to forage in structurally complex, dense habitats, avoiding more open habitats. These results reveal that the effects of changes in the composition structure of the plant community, potentially mediated by the presence of invasive plants, are likely to be association-specific depending on biological and life-history characteristics of species in the trophic chain under investigation.

At smaller scales, characteristics of plants, such as the shape and size of the leaves, the density in which leaf tissues grow, and the surface structure of leaf tissues can affect interactions between herbivores and their natural enemies (Grevstad & Klepetka, 1992; Mulatu et al., 2006; Olson & Andow, 2008). Sticky glands or trichomes, for instance, that are present on the leaf surfaces or undersides of a novel invader may either trap native insects that are not adapted to them or else impede the movement of insects on the leaf surface (Romeis et al., 1998; Lovinger et al., 2000). Additionally, the structure of the host plant may shape the odor plumes and the way that the chemical cues are perceived by insects when searching for host plants or prey (Chapman, 1988). Plant structural traits (e.g., vegetation height, density, plant connectivity) can also affect microclimatic conditions, such as air flow and turbulence, which affect the emission and spread of plant volatiles within the host habitat (Randlkofer et al., 2010). These parameters will come into play if native insects must navigate through stands of invasive plants to find a native plant that is embedded in the same habitat. However, thus far, studies of these plant characteristics have been restricted to native-plant insect interactions or research involving cultivars. There is clearly an urgent need for studies exploring the importance of similar mechanisms in invasive plants and how these may affect the local demographics of native insect assemblages.

How invasive plants may affect chemical heterogeneity in native habitats

  1. Top of page
  2. Abstract
  3. Introduction
  4. Going up: from two to three trophic levels and higher
  5. Structural and chemical characteristics of plants as they affect the foraging and dispersal behavior of herbivores, parasitoids, and hyperparasitoids
  6. How invasive plants affect structural heterogeneity in native habitats
  7. How invasive plants may affect chemical heterogeneity in native habitats
  8. The effects of invasive plants on native insect communities via associational resistance and susceptibility
  9. The potential benefits of invasive plants on native insects
  10. Conclusions and future directions
  11. Acknowledgements
  12. References

Invasive plants may play an important role by interfering with the chemical heterogeneity of the introduced community. Plant volatiles, as part of this chemical complexity, are known to influence arthropod movements and plant orientation in the native host habitat (Schoonhoven et al., 2005; Figure 2A). Therefore, the foraging behavior and fitness success of herbivores and carnivores might be influenced by novel odor blends emitted by invading plants, and this in turn may have repercussions on community composition and functioning. Although plant volatiles belong mainly to three chemical groups (e.g., terpenoids, phenylpropanoids, fatty acid derivates) and some compounds are common to most of the plants (e.g., green leaf volatiles), there is still enormous inter-specific variation in the types of plant volatiles released in nature. The specificity is expressed in the qualitative and quantitative composition of the different odor blends and on the arthropod response to the volatile bouquet (Bruce et al., 2005; Baldwin, 2010). For instance, specific volatile compounds such as the breakdown products of glucosinolates, such as iso-thiocyanates, which are characteristic of plants in the order Brassicales (e.g., Brassicaceae), may vary profoundly amongst different species in this order and may therefore influence the plant preference behavior of different crucifer specialists in a wide range of ways (Hopkins et al., 2009; Müller, 2009). In addition, plant volatiles can vary amongst cultivated strains of wild plants (Poelman et al., 2008; Gols et al., 2011).

The chemical complexity of specific habitats is closely related to the vegetation structure and diversity within the habitat. Odor plumes in adjacent habitats may differ significantly because of differences in the species richness, abundance, and structure of these habitats. Therefore, when an invasive plant colonizes a native habitat, the effect on the arthropod community will depend on several factors, including the response of native plants in the habitat and the higher trophic levels associated with them. In this context, if the invasive plant is introduced into a native plant community where there are few or no related plant species present, the odor blend emitted by the invasive plant may overwhelm volatile blends from the native plants. In this way, it might dilute or mask the detection of volatiles released by the native plants by native arthropods. Odor masking has been shown to affect the foraging behavior of parasitoids, and has even been suggested as a factor in reducing population levels of herbivorous insects in mixed cropping systems (Bukovinszky et al., 2005; Schoonhoven et al., 2005). In an even more extreme scenario, novel volatile cues released by the non-host plant may act as repellents for herbivore and carnivores within their host plant-host patch, decreasing their fitness success (Soler et al., 2007; Figure 2B). On the other hand, if the invasive plant colonizes habitats containing related native plants and shares a similar secondary chemistry with them it might attract herbivores and carnivores associated with the natives because of their similar volatile cues (Renwick, 2002; Randlkofer et al., 2010 and references therein; Figure 2C). Furthermore, plant volatiles can also indirectly influence arthropod populations through the attraction of mutualists such as ants and many species of pollinators (Heil & Bueno, 2007). Some volatile compounds can also act as repellents to both plant enemies and mutualists, including herbivores, parasitoids, and pollinators (Soler et al., 2007; Kessler et al., 2008; Figure 2B). In addition, volatile metabolites (e.g., phytohormones) can also be emitted in sufficient quantities to adversely affect the growth of neighboring plants through their effects on microbes associated with their rhizo- and phyllo-spheres. These compounds can indirectly mediate interactions between native and invasive plants, altering the plant community through plant–microbe associations (Baldwin, 2010). At the other end of the spectrum, novel volatiles that are not recognized by herbivores or their natural enemies may actually benefit these consumers by making it easier to recognize cues that are attractive. Clearly, there is a wide array of potential effects that may be only disentangled at the level of individual associations.

Chemical heterogeneity in native habitats is strongly influenced by plant community diversity (Randlkofer et al., 2010). Different scenarios may occur according to the diversity of the plant community where the exotic plant is introduced and how arthropods respond to the volatiles emitted by the invader (Figure 3). In a species-rich habitat, the odors of an exotic plant may attract more arthropods to the patch than would be the case when it is absent (Gohole et al., 2005). The exotic plant may be considered an evolutionary ‘trap’, however, if its odors are attractive to herbivores for oviposition, but which are not suitable for the development of their offspring (Keeler et al., 2006; Keeler & Chew, 2008; Harvey et al., 2010a; TM Fortuna, J Woelke, CA Hordijk, J Janssen, NM van Dam, LEM Vet & JA Harvey, unpublished data). On the other hand, if plant volatiles emitted by the invader have a repellent effect on arthropod foraging behavior, this might negatively affect the ability of herbivores and natural enemies to locate suitable plants within their habitat and changes in the strength of food web interactions might be expected (Cronin & Haynes, 2004; Cronin & Reeve, 2005) (Figure 3). In disturbed habitats, fast growing invaders (e.g., early successional species) may find optimal conditions in which to spread rapidly, creating large stands where the invading species eventually becomes dominant (Anderson et al., 1996; Woitke & Dietz, 2002). In this scenario, patch colonization by arthropods may be enhanced if the volatile blend emitted by the novel plant is attractive. Consequently, native herbivores may rapidly switch to the invasive plant. Louda & Rand (2002) found that native herbivores of the bull thistle, Cirsium altissimum (L.) Spreng, readily attacked an invasive thistle, Cirsium vulgare (Savi) Ten., suppressing establishment and spread of the latter species. This rapid switch may have been because the volatile blends emitted from both the native and exotic thistles were both attractive to the native herbivores, although no mechanism was explored. On the other hand, if chemical cues emitted by an invasive plant are repellent to many native herbivores, even when the plant may be nutritionally suitable, then this may allow the plant to escape from its antagonists in support of the ERH.

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Figure 3.  Flow diagram showing various scenarios describing the potential effects of plant volatiles on arthropod communities based on the diversity of the native (N) plant communities where the invasive (I) plant is introduced. Attractive volatiles emitted by the invaded plant community may lead to a plant shift by local fauna if the invasive plant is suitable or to an evolutionary trap if the invasive plant is not suitable. Alternatively, if invasive plant volatiles trigger a repellent response on local arthropods, the patch will hold few or no plant enemies, and the invasive plant may find a time window that enables it to spread and eventually become dominant, supporting the Enemy Release Hypothesis.

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The majority of plants in the field are attacked by a wide array of herbivores, including species that exploit the plant in quite different ways. Hence, the chemical heterogeneity of a given habitat will change according to the herbivore-induced plant volatiles emitted by the native plant community where the exotic is introduced. In addition, the amount of volatile compounds released by plants under herbivore attack varies with the herbivore species and such differences might be detected by natural enemies (Schoonhoven et al., 2005). Herbivore-damaged plants may increase their production of secondary metabolites that are involved in direct and indirect defense, which will contribute to an increase in volatile emission in the habitat as a whole. These qualitative and quantitative changes of the odor plumes might alter the foraging behavior of herbivores and their natural enemies. For instance, Soler et al. (2007) showed that the foraging behavior of Cotesia glomerata L., a parasitoid of an aboveground herbivore, can be influenced by belowground herbivory through changes in plant volatile blends. Additionally, plants do not only react to herbivore feeding, but they can adjust their metabolism upon egg deposition by insects (Hilker & Meiners, 2002, 2006). Studies have shown that herbivore oviposition can suppress constitutive and herbivore-induced volatiles (Bruce et al., 2010; Peñaflor et al., 2010), which may influence a plant’s response to herbivory and affect the interactions with associated organisms, such as egg parasitoids (Fatouros et al., 2005). Assuming that an exotic plant introduced in similar systems might be initially less susceptible to herbivore attack than its native neighbors, we might predict that host preference of herbivores and parasitoids might change based on qualitative and quantitative differences in the chemical induction of the invader compared with the more heavily damaged natives. Moreover, natural enemies will often have to choose between plants containing host and non-host herbivores and plants infested with only non-host species (Figure 2C). It has been reported that some parasitoid species are attracted to infochemicals emitted from the leaves of plants containing non-host herbivores (Vos et al., 2001; Snoeren et al., 2010). In extreme cases, parasitoids are as equally attracted to certain species of ‘clean’ (e.g., host-non-infested) plants as they are too closely related plants infested with hosts (Bukovinszky et al., 2005). Chemical signals from exotic plants and how the insects perceive them may therefore affect local diversity by differentially affecting the behavior of various species in food chains.

The perception of volatiles in the invaded habitat is restricted to the sensorial capacity of arthropods to distinguish the various compounds in the odor plumes. For host plant recognition, the insect requires a highly sophisticated detection mechanism enabling it to identify the correct volatile blend against a heterogeneous background of compounds that are constantly being emitted by non-host plants. A host plant is recognized if the herbivore is attracted by the correct combination of sensory inputs. In contrast, a plant is considered as a non-host plant when wrong chemical cues are detected or there is a repellent response by the insect. Several studies have shown that the majority of chemical receptors found on the antennae of herbivores and parasitoids do not only respond to the volatiles of a single host plant. Instead, they rely on the recognition of particular blends of volatiles distributed generally among a range of plant species found in their habitat (Rojas, 1999; Bruce et al., 2005; Gouinguené et al., 2005; Jönsson & Anderson, 2008; Ngumbi et al., 2009). Behavioral studies suggest that the blend composition of plant volatiles is crucial because specific mixtures are more attractive than individual compounds (Fraser et al., 2003; Natale et al., 2003). For instance, blends of ubiquitous compounds have been found to attract the specialist wheat midge, Sitodiplosis mosellana Géhin. The midge is highly sensitive to subtle changes in the ratios of host-plant volatiles, and exhibits no response when the incorrect ratio of ubiquitous compounds is presented (Birkett et al., 2004). The presence of an invasive plant may similarly alter the blend ratio of volatile compounds in native plant communities which will have repercussions on the host plant-host recognition behavior of herbivores and their natural enemies.

The effects of invasive plants on native insect communities via associational resistance and susceptibility

  1. Top of page
  2. Abstract
  3. Introduction
  4. Going up: from two to three trophic levels and higher
  5. Structural and chemical characteristics of plants as they affect the foraging and dispersal behavior of herbivores, parasitoids, and hyperparasitoids
  6. How invasive plants affect structural heterogeneity in native habitats
  7. How invasive plants may affect chemical heterogeneity in native habitats
  8. The effects of invasive plants on native insect communities via associational resistance and susceptibility
  9. The potential benefits of invasive plants on native insects
  10. Conclusions and future directions
  11. Acknowledgements
  12. References

Characteristics of plants and habitat patches have long been known to strongly influence the demographics of insect herbivores and their natural enemies through differences in structural and chemical properties amongst the plants and their neighbors. Several hypotheses have been proposed to explain the relationship between vegetation complexity in a habitat and the diversity of herbivorous and carnivorous arthropods. The ‘resource concentration hypothesis’ (Root, 1973) posits that plants growing in more diverse habitats harbor fewer herbivores than plants growing in less diverse habitats. This is because herbivores are able to locate and colonize larger patches of suitable food plants more easily. The ‘natural enemy hypothesis’ (Root, 1973) predicts that natural enemies will be more abundant (and thus reduce herbivore populations more effectively) in structurally complex habitats, because these will contain more micro-niches where the insects can hide as well as larger numbers of potential hosts or prey. One of the shortcomings of these hypotheses is that they were originally postulated on the basis of crop plants (e.g., cultivated cabbage) growing in agricultural landscapes. However, agricultural fields are generally simple environments, where interstitial vegetation has been removed. This makes them often much more susceptible to herbivores, or else population ‘sinks’ where insect populations become saturated.

The species diversity and structural and chemical complexity of natural and semi-natural plant communities is often many times greater than that found in agro-ecosystems. In these communities, interactions between plant species may act in synergy in effecting the behavior of herbivores and their natural enemies. For instance, specific plant associations may enhance (known as ‘associational susceptibility’) or decrease (known as ‘associational resistance’) the attractiveness of focal plants to herbivores, predators, or parasitoids (Barbosa et al., 2009). Thus far, this area of research has focused almost exclusively on interactions involving native plants and their insect communities. Associational resistance or susceptibility may be mediated by chemical or structural traits in plants that influence the behavior of insects within habitat patches (Andow, 1991; Stiling et al., 2003; Hambäck et al., 2006; White & Andow, 2006; Adati et al., 2011; Jactel et al., 2011). Recent studies have suggested that increased plant floral diversity around the perimeter of cropping systems may even enhance the abundance of hyperparasitoids, thus negating the benefits of attracting primary parasitoids through associational susceptibility (Araj et al., 2009). It is almost inevitable that novel, invasive plants will also facilitate the resistance and/or susceptibility of native plants to interactions with higher trophic levels, although thus far this area has received little attention.

Invasive plants may also act as chemical lures and traps for native insects, with potential benefits as well as costs in terms of biological control and conservation (Renwick, 2002). In the vicinity of agricultural systems, for example, invasive plants that become established may attract native herbivores that may not be able to detoxify or excrete their toxic allelochemicals. For instance, Harvey et al. (2010b) found that larvae of the small and large cabbage white butterflies, Pieris rapae L. and Pieris brassicae L., which are major pests in collard crops, performed very poorly when fed on leaves of the invasive crucifer, Bunias orientalis L. In spite of this, adult female butterflies of both species, and especially P. rapae, oviposit onto leaves of this plant.

Over time, invasive plants may serve as food plants for a diverse range of native insect herbivores (Louda & Rand, 2002). If an invasive plant is of high nutritional quality for a certain herbivore species, then over time this might facilitate a plant shift, whereby that herbivore becomes locally (or more widely) adapted to the novel plant (Grosman et al., 2009). This may reduce pressure from this herbivore on other native food plants with which it has long been associated. At the same time, strongly co-evolved natural enemies of the herbivore may ‘follow’ their host/prey and also develop a new and intimate relationship with it and its new food plant over time. In reducing herbivore pressure because of the presence of the invader, native plants may develop associational resistance as a result of herbivore switching (Andow, 1991; Barbosa et al., 2009).

The potential benefits of invasive plants on native insects

  1. Top of page
  2. Abstract
  3. Introduction
  4. Going up: from two to three trophic levels and higher
  5. Structural and chemical characteristics of plants as they affect the foraging and dispersal behavior of herbivores, parasitoids, and hyperparasitoids
  6. How invasive plants affect structural heterogeneity in native habitats
  7. How invasive plants may affect chemical heterogeneity in native habitats
  8. The effects of invasive plants on native insect communities via associational resistance and susceptibility
  9. The potential benefits of invasive plants on native insects
  10. Conclusions and future directions
  11. Acknowledgements
  12. References

The effects of invasive plant species on native insects, at least in terms of their demographics and populations dynamics, are poorly understood, but the effects are not necessarily always negative. In particular, if the invasive plant possesses traits, such as allelochemistry, that are also found in potentially less common native plant species, then the presence of a more common invasive plant may benefit native insect communities. Native plants may decline due to a range of anthropogenic stresses including habitat loss and climate change, meaning that successful exotics may ultimately substitute as food plants. Indeed, several studies have reported host-plant switches by native generalist and specialist herbivores to invasives. For instance, larvae of the southern white butterfly, Pontia protodice Boisduval & Leconte which is native to the southeastern USA, feed on a range of well-established exotic cruciferous plants (Brassicaceae) that originate from Eurasia (Kingsolver, 1985). Similarly, Chew (1981) found that P. oleracea, which occurs over much of the USA and southern Canada, oviposits and feeds on several exotic crucifers including Brassica rapa L., B. nigra L., Sisymbrium altissimum L., and Raphanus raphanistrum L. In California (USA), 34% of the state’s native specialist butterfly species were found to feed on exotic plants (Graves & Shapiro, 2003). Urban butterflies in California were even found to be dependent on alien plants for their survival (Shapiro, 2002). A specialist herbivore, the Baltimore checkerspot butterfly, Euphydryas phaeton Drury has recently expanded its dietary breath from feeding exclusively on turtlehead, Chelone glabra L., to also feeding on the introduced weed, ribwort plantain Plantago lanceolata L. (Bowers et al., 1992). However, herbivores performed less well on the alien plant, in terms of reduced pupal mass and relative growth rate on plantain, suggesting that there may be a trade-off between plant quality and accessibility. Generalist herbivores, such as woolley bear caterpillars, Pyrrharctia isabella JE Smith, also feed on a wide variety of abundant alien plants in North America, including P. lanceolata and dandelion, Taraxacum officinale Weber (Dethier, 1980).

By association, natural enemies may follow their herbivore prey or hosts to the novel plant, although this is not always the case (Grosman et al., 2009). The ability of predators and parasitoids to adapt to novel plants and to enjoy realized fitness is dependent on the completion of several hierarchal steps involving the location of suitable habitat, plant location, prey/host acceptance, and palatability (Vinson, 1976). Although these processes have been well studied with insect herbivores and their natural enemies in native communities, little is known about shifts involving several trophic levels from native to alien plants. Several studies have shown that the buckeye butterfly, Junonia coenia Hübner, and several of its predators are now intimately associated with the alien plant, P. lanceolata, in western North America (Stamp & Bowers, 1992, 1993, 1996). However, the time scales over which shifts occur, and the degree of success up to the terminal end of the food chain has been little studied.

Conclusions and future directions

  1. Top of page
  2. Abstract
  3. Introduction
  4. Going up: from two to three trophic levels and higher
  5. Structural and chemical characteristics of plants as they affect the foraging and dispersal behavior of herbivores, parasitoids, and hyperparasitoids
  6. How invasive plants affect structural heterogeneity in native habitats
  7. How invasive plants may affect chemical heterogeneity in native habitats
  8. The effects of invasive plants on native insect communities via associational resistance and susceptibility
  9. The potential benefits of invasive plants on native insects
  10. Conclusions and future directions
  11. Acknowledgements
  12. References

It is evident that there are many gaps in our understanding of invasive plants on the population ecology of multitrophic level interactions involving insect herbivores, their natural enemies such as parasitoids and predators, and even higher up in the food chain (e.g., hyperparasitoids). To fill in these gaps, we need many more studies combining various interdisciplinary approaches and that are carried out over a wide range of scales to better elucidate the local and broader effects of invasive plants on native communities. Cronin & Reeve (2005) argued that most predator–prey models are inadequate in predicting the dynamics of trophic interactions because they generally ignore landscape-level processes. For instance, predator–prey models are spatially unrealistic, ignoring the size and structure of habitat patches and their edges and how these parameters affect dispersal, foraging, and mate-finding behavior in insects. At the same time, the models usually focus on only two-trophic levels (e.g., host and parasitoid), whilst ignoring the role of plant-related traits such as stem and shoot architecture on host location and nutritional quality on herbivore and parasitoid development. Additionally, given the potential importance of carnivores in regulating prey numbers and how plant volatile cues are crucial in the foraging behavior of carnivores (Vet & Dicke, 1992; Steidle & van Loon, 2003; Bukovinszky et al., 2005), studies with invasive plants should include a larger number of interactions that include higher trophic levels, such as parasitoids and hyperparasitoids (Harvey et al., 2010a).

Importantly, most studies with invasive plants have focused their effects on native communities long past the establishment phase when they are already dominant. Patterns of weed spread show that many exotic species have long ‘sleeper’ or ‘lag’ phases after their introduction before they begin to dominate local ecosystems. Hobbs & Humphries (1995) argued that early detection and treatment of invasions before the rapid spread occurs may enable the development of more effective management strategies. Thus far, little is still known about the impact of invasive species on native communities during the establishment and lag phases. Many intra-continental plant invasions are now occurring as result of anthropogenic processes, such as climate warming, whereby plants are colonizing more poleward biomes from their natural ranges in lower latitudes (Engelkes et al., 2008). A challenging way to understand how species responses change from the lag phase to later stages of invasion is to study the ecology of these species along environmental and/or geographical gradients. Studies comparing changes in population patterns and effects of exotic species on local communities across spatial gradients can help reconstruct how the invasion occurred and which factors favored or limited its spread at different phases of invasion (Dietz & Edwards, 2006).

Thus far, the effects of differences in habitat structure on multitrophic interactions have been primarily based on population-related studies, whilst often ignoring traits and characters of the species involved. For instance, the effects of invasive plants on native arthropod communities may be contingent on certain life-history and morphological traits exhibited by higher trophic levels. These may include differences in feeding strategies, degree of dietary specialization, morphological traits like the presence or absence of wings, reproductive biology, and in parasitoids, the stage of host attacked. To be honest, the importance of these parameters has even rarely been investigated in native communities, where differences in habitat characteristics have only considered herbivores and their natural enemies on their trophic status, ignoring more intimate aspects of multitrophic interactions. However, a better understanding of results such as those generated by Cronin & Haynes (2004) may be obtained by incorporating an evolutionary perspective of the interactions between different trophic levels.

In addition, although several studies have focused on insect orientation based on host-plant volatile emissions, most of these are based on behavioral essays in Y-tubes or flight tunnels where the insect response is measured toward a single plant or a small group of plants. Future research should include a more realistic picture of invaded communities by measuring their structural and chemical complexity under field conditions. There is a clear need to develop a better understanding of the species composition of communities with invasive plants and to compare them with less disturbed native communities. Furthermore, experiments measuring insect preference and performance in both the laboratory and in the field can tell us much about the impact of invasive plants in native communities. These studies should be combined with the measurement of allelochemicals in plant tissues and headspace analyses to measure volatile emissions. Additionally, conceptual models of odor plume diffusion under different conditions, including air turbulence, light intensity, and species composition, may help understand better the effect of novel community assemblages on insect foraging behavior.

Although the field of invasion ecology has grown immensely over the past 20 years, there are still large gaps in the empirical literature, particularly with respect to the effects of invasive plants on native communities. We suggest that this gap can be filled by addressing some of the following questions:

  • 1
     How do alien, invasive plants affect the foraging and dispersal behavior and development of native insects?
  • 2
     Are these effects mediated by primary and secondary chemistry or by structural and architectural characteristics of the plant or are the factors inter-related?
  • 3
     Do these effects differ for different members of an interacting trophic chain?
  • 4
     If the effects of invasive plants are disproportionate amongst herbivores and their parasitoids, can invasive plants create stronger trophic cascades or, alternatively, reduce the strength of top-down control?
  • 5
     How do the spatial and temporal dynamics of the spread of invading populations affect native multitrophic interactions?
  • 6
     What are the longer term implications of invasive plants on native food webs and their persistence?

Addressing these questions will require a multidisciplinary approach integrating population and evolutionary ecology as well as ecophysiology. However, by doing so, we will be able to better appreciate both large- and small-scale effects of invaders on multitrophic interactions in native plant-arthropod communities.

References

  1. Top of page
  2. Abstract
  3. Introduction
  4. Going up: from two to three trophic levels and higher
  5. Structural and chemical characteristics of plants as they affect the foraging and dispersal behavior of herbivores, parasitoids, and hyperparasitoids
  6. How invasive plants affect structural heterogeneity in native habitats
  7. How invasive plants may affect chemical heterogeneity in native habitats
  8. The effects of invasive plants on native insect communities via associational resistance and susceptibility
  9. The potential benefits of invasive plants on native insects
  10. Conclusions and future directions
  11. Acknowledgements
  12. References