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Arbuscular mycorrhizas: drivers or passengers of alien plant invasion.

Introduction

Arbuscular mycorrhizal fungi are crucial to the functioning of ecosystems in view of their wide spread mutualistic association with more than 80% of known plant species (Smith & Read, 1997). While the below-ground 'dark half' of biodiversity still remains shrouded in mystery, yet the extent to which AMF mediate exotic species invasions needs to be urgently worked out in view of unprecedented increase in transport, introduction and spread of invasive plants in areas well outside their potential range as defined by their natural dispersal mechanisms and biogeographic barriers. Enhanced by increasing globalization of markets, explosive rise in world trade, travel, tourism, and exchange of goods, biological invasions are being increasingly implicated as the second most pervasive threat, after habitat degradation, to biodiversity at local, regional and global scales. Thus, elucidation of all the factors that facilitate and mediate such invasions is of paramount significance in formulating effective strategies for management of such invasions. Despite need for an urgently required unifying framework for understanding alien plant invasions, a number of partially overlapping hypotheses (reviewed by Hierro et al., 2005), to explain how alien species change from being minor components of their native communities to dominant components of invaded communities, have been advanced. While these hypotheses implicate one or the other attribute, trait or set of traits in promoting invasions, AM mutualism in relation to alien plant invasions needs more detailed examination. This is because the AM-plant relationship may possibly change from a completely mutualistic to one of parasitism during different stages of invasion. A meta-analysis of the several relevant studies by Levine et al. (2004) pointed out that soil microbes, particularly mycorrhizal mutualists, play a critical role in determining patterns of abundance and invasiveness of certain species. Despite such indications, carefully planned experimental studies that specifically and objectively examine the role of AMF in plant invasion are lacking, presumably due to their difficult cultivability on artificial media and apparent complexities in manipulations of mycorrhiza-plant interactions in field and laboratory experiments. Building upon the understanding of AM-host interaction, the present review brings out that the role of AM fungi in plant invasion needs to be investigated in light of following three paradigms: (a) is invasiveness of introduced species in non-native habitats due to their establishment of new symbiotic relationships with AM fungi that are native to the invaded region which contributes to fitness of alien species (b) do AM fungal symbionts get transported and introduced along with propagules of alien plant species and whether the AM fungi act as pathogens to native species or as superior mutualists in non-native habitats and confer additional benefits and (c) whether cessation of symbiotic associations in the non-native habitats decrease the invasiveness of introduced species.

The present review evaluates, in light of the recent findings, soil mycorrhizal mechanism behind plant invasion and changes in soil conditions created by dominance of a habitat by invasive plants in relation to growth and fitness of native plant species. Reviewing the positive and negative AM fungal feedbacks with invasive plants, we attempt to put in perspective the likely influence and implications of AM-mediated invasiveness on structure and diversity of native plant communities. The present contribution may have applications in conservation biology for habitat restoration after alien invasion through soil based management.

Possible Roles of Mycorrhizal Mutualism in Plant Invasion

The role of mycorrhizal symbiosis in plant invasions has been evaluated mainly in the light of Resistance Hypothesis (indirect effect of not having appropriate mutualists is that the invader is repelled from areas) [Mack, 1996], Enhanced Mutualisms Hypothesis (invasion at a biogeographical scale is facilitated by mutualists with strong beneficial effects) [Reinhart & Callaway, 2006], Mutualisms Hypothesis [Richardson et al., 2000] and Degraded Mutualisms Hypothesis (invasion by nonmycorrhizal species reduces the abundance of AMF thereby negatively affecting strongly mycorrhizal native plant species) [Vogelsang et al., 2004]. Several mechanisms by which AM fungi can facilitate or constrain the establishment and spread of alien plants in invaded communities can be identified from the published works. A critical analyses of the research work undertaken hitherto on different species in different ecosystems worldwide (Table 1) reveals a bias towards some life froms such as annual or perennial forbs in grasslands ecosystems in comparison to the other growth forms and habitats such as forests and wetlands. Besides, the evidence for invasive plant-AM feedback interactions comes more from greenhouse experiments and pot trials than from field studies (Table 1).

The alien invasive plants can potentially modify soil environment thereby influencing the AMF community composition and abundance, which in turn influences invasiveness of many alien plants in the introduced (Shah et al., 2008a, b). The possible interactive feedback between invasive plants, soil properties and AMF is presented in the form of a successional loop in Figs. 1 and 2. For the present review invasive plant-mycorrhizal feedback (Fig. 3) is considered as negative if performance of the plant species decreases relative to other native species and positive if the opposite is true. While most of the studies indicate by and large positive effect of AM fungi in plant invasions, some studies also suggest the opposite. The mutualistic facilitation of invasive plants by AM fungi is most likely through their influence on competitive interactions of these plants with native species. The altered interactions between native and invasive species are an outcome of differential impact of AMF on nutrient uptake and exchange, stage-specific spatio-temporal successional changes, or mediation of plant-herbivore interactions. Occasionally AM can suppress invasive plants to specially favour the native species. The invaders in turn may impact mycorrhizal community structure and functional dynamics in the invaded habitats in different ways. While critically evaluating evidences for different possible roles of AM in plant invasion (Fig. 1), their implications for prediction, prevention and management of plant invasions are also discussed. To begin with, we briefly highlight the importance of developing exhaustive checklists of mycorrhizal status of invasive plants to act as a baseline information for the subsequent studies.

Mycorrhizal Staus of Invasive Plants: Need of the Hour

In view of the recently reported multifarious role of arbuscular mycorrhizas (AM) in plant invasions, as documented below in this review, large scale exploration of invasive plants from diverse habitat types in different biogeographical regions needs to be undertaken for determining the extent and type of their AM association. Such baseline information would be of pivotal significance in further elucidating the role of AM F in alien plant invasions. Notwithstanding the importance of such studies, no major survey exploring the mycorrhizal status of alien invasive plants has yet been carried out except a recent attampt by Shah et al. (2009a, b). The study was conducted to evaluate the extent and type of AM occurrence in alien plant species at different stages of invasion in the Kashmir Himalaya and revealed high incidence of AM symbiosis both at species (92%) and family (96%) level. However, the extent and type of AM colonization was variable. In fact, about 78% of the species investigated by Shah et al. (2009a, b) belonged to the highest three frequency Classes C, D and E, based on percent root length colonized.

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As regards morphological AM types (Gallaud, 1905; and Dickson et al., 2007), Arum- type is more common in weedy plants (Yamoto, 2004) and decrease in the ratio of Arum to Paris type AM colonization from pioneer to late successional stages (Ahulu et al., 2005) is indicative of some functional differences between them. Of late, not only some invasive plants have been reported to harbour the Arum-type AM (Fumanal et al., 2006; Shah et al., 2009c) but also this morphological type has been linked to the rate of spread of some weedy plant species (Yamoto, 2004).

Since 80-90% of the land plant species and families are mycorrhizal (Wang and Qui, 2006), mere association of arbuscular mycorrhizal symbionts with alien plants cannot be taken as an indication of their role in promotion of alien plant invasions. But in view of promotion of invasiveness of some alien plant species by their associated AMF mutualists (Fumanal et al., 2006; Shah and Reshi, 2007; Shah et al., 2008a, b) information about the mycorrhizal status of invasive plants in different biogeographical regions and habitat types may help better understanding the role of AMF in alien plant invasions.

AM Fungi Influence Competitive Interactions through Nutrient Uptake

The critical importance of soil nutrients in plant invasions has been highlighted by many studies. With respect to invasive plants, some correlations have been reported to occur between nutrient availability and enemy release (Bluementhal, 2005), invasiveness and disturbance (Davis et al., 2000) and invasion facilitation upon experimental resource enrichment (Davis and Pelsor, 2001; Daehler, 2003). In view of the well established role of AMF in nutrient uptake for host plants in different forms and from different sources, plant-wide mycorhizal web is likely to influence competitive interactions of invasive and native plant species through differential exchange of nutrients between them. Recently competitive relationships of plants have been shown to be influenced by both the presence and identity of AMF (Scheublin et al., 2007) and also their geographical origin (Shah et al., 2008a, b). Besides, AMF are reported to regulate plant interactions (Casper and Castelli, 2007) and determine the structure, diversity and productivity of plant communities (van der Heijden et al., 1998; Scheublin et al., 2007; Shah, et al. 2009a, b).

Though the profound influence of soil biota on alien plant invasions has been recently reviewed (Reinhart & Callaway, 2006), the specific contribution of mycorrhizas in enhancing the competitive ability of invasive plants via uptake and transfer of nutrients still needs further investigation. The considerable impact of AMF in altering the competitive balance between species is discernible from both, observational field studies (Allen, 1991) and experimental studies in two species (Fitter, 1977) and multi-species (Grime et al., 1987) mixtures and attempts have been made to even quantify them (Watkinson & Freckleton, 1997). The role of mutualistic fungi in influencing competitive interactions of plants, though documented earlier also (Grime et al., 1987; Hetrick et al., 1990; Hartnett et al., 1993; Bever et al., 1996; Moora and Zobel, 1996, 1998), has seen a renewed interest in the context of plant invasions. This surge in the interest has been especially due to the potential of AM to acquire nutrients at a lower carbon cost than roots because of their smaller diameter and greater surface:volume ratio. In addition, extensive mycorrhizal colonization substitutes for the main root function of nutrient uptake thereby reducing resource allocation to roots (Berta et al., 1993; Vance et al., 2003). This helps most of the invasive plants to allocate the available resources more towards defence than growth, a strategy of particular significance for successful invasion as suggested by the Evolutionary Increased Competitive Ability (EICA) proposition (Blossey & Notzold, 1995). Whether such increased competitive ability due to AMF emerges only from the growth and defence tradeoff or due to differential response of native and invasive species to geographical source and taxonomic or functional identity of mycorrhizal species are still open questions.

Arbuscular mycorrhizas have been reported to indirectly enhance competitive effects of an invasive forb Centaurea maculosa over a native bunch grass Festuca idahoensis to invade native grasslands of western North America (Marler et al., 1999). While mycorrhizal mediated interplant carbon transfer was reported earlier by Francis and Read (1984), subsequently Carey et al. (2004) provided a direct isotopic and physiological evidence for transfer of carbon from the native species of F. idahoensis to invasive C. maculosa. The mycorrhizal mediated carbon theft by aliens from native neighbouring species thereby tilting the balance of competition in their favour is supported also by Giovannetti et al. (2006). However, Zabinski et al. (2002) showed that phosphorus uptake, not carbon transfer, is responsible for arbuscular mycorrhizal enhancement of C. maculosa in presence of native grassland species. The apparent contradiction of such studies, some showing C transfer and others P- uptake but not C transfer as the means of mycorrhizal favour to invasive plants, need comprehensive field studies and laboratory testing to elucidate whether they are the alternative mechanisms operating under different situations to favour invasives. Studying the role of AMF in facilitating neighbour recognition by invasive species in invaded ranges through altered resource availability and molecular cross talk would be quite interesting.

The findings that AMF facilitate N uptake by host plants (He et al., 2003) in different forms and even aid in N transfer from one plant to another (Govindarajalu et al., 2005) need to be put in the fight perspective in respect of invasive plants, the establishment and subsequent spread of which is usually nitrogen limited (Wolf et al., 2004). Mycorrhizal mediated enhanced invasiveness is discernible from a North American grassland invader, Centaurea diffusa, which competed best under low N conditions but lost its competitive ability under low P conditions (Kathrine et al., 2004) under which AM symbiosis might turn out of critical importance for this species. Arbuscular mycorrhizas may be especially important in regions with N[H4.sup.+] dominated soils (Ames et al., 1983; Johansen et al., 1996) due to the fact that some allelopathic compounds released by invasive plants inhibit nitrification (Lodhi & Killingbeck, 1980; Thibault et al., 1982) thus limiting growth of native plants by inducing nitrate deficiency. This hypothesis, however, needs to be validated by further investigations, which also need to determine the relative mycorrhizal dependency and species sensitivity of invasive vs. native plant species to determine the precise outcome of AM association in relation to invasiveness.

Invasive plants generally prefer disturbed habitats because disturbance promotes invasion by increasing resource availability and causing nutrient flushes. However, the way different disturbance regimes affect AM communities merit due attention in invasion ecology. It has been reported that the soil disturbance affects AM communities by breaking up AM extraradical mycelium both in pots (McGonigle & Miller, 1996, 2000) and in the field (Kabir et al., 1997). This may not only result in delayed root colonization but also reduced nutrient uptake. Yet paradoxically many invasive plant species have been reported to be highly mycorrhizal (Fumanal et al., 2006; Shah et al., 2008a, b). This indicates that the facilitative role of AM in plant invasions may not necessarily be through improved nutrient uptake but via some other mechanisms. Establishing the mycorrhizal responsiveness and mycorrhizal dependency of invasive plants, both in their invaded and home ranges, under different disturbance regimes is suggested as a useful approach in this direction.

Mutualistic Facilitation and Successional Dynamics of Invasive Plants

Plant invasion, being a multistage process like succession, is characterized by conspicuous spatio-temporal dynamics along introduction-establishment-naturalization-invasion continum. Mycorrhizal symbioses may contribute to plant invasiveness from the initial stage of their introduction to the final stage of widespread occurrence and abundance, possibly with changing roles during different stages along a mutualism-commensalism-parasistism gradient. AMF can potentially integrate the emerging seedlings in the introduced communities with the extensive hyphal networks to nourish them (van der Heijden, 2004) act as a symbiotic support system to overcome their recruitment limitation in the invaded habitats. Many introduced plant species have been shown to rely on mutualisms in their new habitats to overcome barriers to establishment and to become naturalized and, in some cases, invasive (Richardson et al., 2000).

Working out the invasion history of an alien plant, Solidago canadensis, on the Chinese Chongming Island, Liang et al. (2004) found a significant positive correlation between the time of invasion and rate of AM colonization. They showed that the total number of AM species increased with increasing invasion time and was positively related to the number of plant species occurring in plant communities. This suggests that invasion time and plant diversity can influence AM species diversity. Further studies, however, need to explore the spatiotemporal variations in AM communities as a function of invasive spread of alien species. Linking the process of invasion to the development pattern of mycorrhizal symbiosis during primary and secondary successions may give some insights into this complex relationship because the invasive plant species are often the primary colonizers in secondary succession. Such an approach of integrating habitat characteristics and invasive attributes into invasion dynamics may be helpful in the prediction and prevention of plant invasions.

AMF-mediated Differential Growth Performance of Native vs. Invasive Plants

The role of mycorrhizal fungi in plant invasions, though empirically tested hitherto by few studies only, needs to be viewed in light of the established ecological theories and principles in order to have restoration and management implications. Extensive field studies and subsequent greenhouse experiments (Fumanal et al., 2006) with Ambrosia artemisiifolia, a North American invader in Europe, showed positive impacts of AM on growth, development and spread of this invasive plant species thus underlining the need to integrate symbiotic interactions in future work on invasive plant processes. Earlier mycorhizas have been reported to be associated with invasion of Erechites glomerata on Californian San Miguel Island (Halvorson & Koske, 1987). In a recent greenhouse study (Nijjer et al., 2004) mycorrhizal inoculation unusually increased growth of Chinese Tallow (Sapium sebiferum), an invasive tree in the southeastern United States, but caused zero to negative growth changes of its five co-occuring native tree species (Liquidambar styraciflua, Nyssa sylvatica, Pinus taeda, Quercus alba, and Q. nigra). The study, however, indicated that the potential advantage Sapium gets from mycorrhizal associations may vary with native species and soil fertility. This is fully supported by our recent studies (Shah et al., 2008a, b) on the influence of resident and foreign AM on growth invasiveness of alien Anthemis cotula in Kashmir Himalaya vis-a-vis the effect of four common co-occurring neighbours, Conyza canadensis, Galinsoga parviflora, Sisymbrium loeselii and Daucus carota. The field studies revealed high incidence of Arum-type mycorrhizal colonization in natural populations of A. cotula and the pot trials confirmed reliance of its invasiveness on AM with more favourable effect of resident than foreign AMF. The mycorrhizal colonization intensity in field populations of A. cotula was, however, strongly influenced by neighbour identity with major reduction recorded in presence of Sisymbrium loeselii (a cruciferous non-host) in comparison to other con-familial neighbours. Pot experiments confirmed the differential effect of co-occurring species on A. cotula's invasive traits. Such studies on tripartite, invader-AM-neighbour, interactions provide a conceptual framework for future studies to analyze soil biota feedback and competition as interlinked processes influencing alien plant invasions. However, we suggest further studies to screen most effective native plant species that could deprive the invasive species of the benefits obtained from mycorrhizal association in invaded ranges and advocate use of such native species in ecological restoration of invaded habitats. Testing whether different AM taxa from native and invaded ranges of alien species differ in the rate, extent and location (root or soil) of colonization of invasive species and their non-native noninvasive congeners would help in determining the taxonomic and origin basis of AM functional diversity in relation to plant invasion. Native mycorrhizal isolates from invaded habitats also need to be screened for their comparative influence on growth promotion of invasive vs. native plant species. The AM isolates that favour growth of native species more than invasive species can be used as effective bio-inoculants to restore native plant communities in invaded habitats.

AM inoculation not only promotes growth of alien plants but can also influence plant and microbial community structure associated with them. The influence of Gmelina arborea, a potentially invasive tree in West Africa and native to India, on resident herbaceous plant community structure and microbial community function was shown to be significantly modified by the massive AM inoculation (Sanon et al., 2006). However, AM species identity may influence the invader's success and some invaders specifically increase abundance of their selectively cultivated AM species possibly to the detriment of native neighbors (Stampe & Daehler, 2003). Therefore, simple comparisons of plant growth with and without mycorrhizas, overlooking the identity of naturally associated AM species, may be of limited relevance from an invasion standpoint. Hence, the upcoming studies need to work out the effect of AM identity on invasive as well as co-occurring native species and compare the mycorrhizal status of invasive species in their native and invaded ranges to correlate AMF with invasiveness. More importantly, attention to the effects of native soil mycorrhizas on nonnative plants that do not successfully invade will be crucial if we are to assess the relative importance of AMF in invasions. Furthermore, the role of AM in plant invasion needs to be viewed in light of the often overlooked Biotic Indirect Effect, how one species alters the effect that another species has on third (White et al., 2006). Moreover, the complexity of biotic interactions, influencing or getting influenced by plant invasion, underlines the need for further studies to shift from a single factor- to multi-factorial approach to be truly reflective of natural communities. Better understanding of mycorrhizology through cross fertilization of empirical data with the concepts of ecology, mycology and plant pathology will help us not only to predict but possibly prevent alien invasions.

Mycorrhiza-invasive Plant-herbivore Tripartite Interactions

Mycorrhizae and herbivores both have been shown to influence plant invasions at different ecological scales. Whilst their effect has been hitherto studied independently, interactions between herbivores and mycorrhizal fungi are expected because both depend upon and influence important plant resources. Herbivores, being aboveground foliage consumers, may reduce photosynthate translocated to the root system and available to mycorrhizal fungi, resulting in a reduction in mycorrhizal colonization and reduced development of the symbiosis (Gehring et al., 1997; Hetrick et al., 1988; Trent et al., 1988). Mycorrhizas, in turn, can have many potential effects on plant herbivore interactions. Under certain conditions, up to 40-50% of a plant's net production may be allocated to its fungal symbiont (Fogel & Hunt, 1979; Harris & Paul, 1987). Because mycorrhizal fungi both consume photosynthate and at the same time enhance mineral nutrient acquisition and growth capacity, the cost--benefit relationships among mycorrhizal fungi, herbivores and host plants are likely to be complex. Mycorrhizas may affect herbivores through alteration of plant growth or foliar chemistry (e.g., Goverde et al., 2000; Koide, 2000), and they may have large effects on plant responses to herbivores by influencing anti-herbivore defenses and/or herbivory tolerance (regrowth capacity). Klironomos et al. (2004) while studying the response of AMF to stimulated herbivory suggested that it is difficult to generalize on the effects of herbivory on plant and fungal responses, even when dealing with the same plant species.

In view of the significance of enemy release and biotic resistance in plant invasions (Mitchell & Power, 2003; Klironomos, 2003; Shah & Reshi, 2007), developing AM association in the invaded ranges might help invasives overcome this biotic resistance. Reinhart et al. (2003) provided experimental evidence for escape from specific pathogens by Prunus serotinus, a native to North America and invasive in Europe, where it harvests the maximum benefits of interacting with generalist mutualists such as AMF. This is in concurrence with our findings of alien A. cotula, an annual herbaceous plant native to southern Europe-west Siberia, where the species is attacked by about 68 insect pathogens, and invasive in Kashmir Himalaya where it has escaped all the native herbivores and pathogens (Shah & Reshi, 2007) due to characteristically very high (>84%) AM root length colonization. The indirect role of high mycorrhizal colonization in keeping herbivores at bay by alien invasives in their invaded areas is of specific significance because it is too costly for plants in terms of carbon economy to harbor mycorrhizal association at home where their foliage is under intense insect herbivory. A path breaking study supporting this case (Abigail et al., 2005) showed that mycorrhizas, to a great extent may benefit plants subjected to herbivory by stimulating compensatory growth, and herbivores, in turn, may increase the development of the mycorrizal symbiosis. However, their results indicate strong interspecific differences among tallgrass prairie plant species in their responses to the interaction of aboveground herbivores and mycorrhizal symbionts. More studies on AM mediated invasive plant-herbivore interactions need to be specifically carried out with invasive plants to draw robust conclusions. Furthermore, AMF can induce insect specialism in host plants by altering their chemistry (Gange et al., 2002) thereby preventing the generalist insects from attacking the host plants (Gange et al., 2005). Thus, if fewer specialist insects are absent in invaded habitats, the mutualism can be drawn to the best advantage by the invaders to avoid generalist insects. In order to have an inclusive picture of the outcome of plant-herbivore interactions, developing comprehensive mycorrihizal status wise checklists of invasive plants, as reported recently by Shah et al., 2009a, b, together with associated specific herbivores, parasites and pathogens on a local, regional and global scale is important. Despite the fact that invasiveness can be affected both by mycorrhizal fungi and herbivores, very few studies have hitherto examined the interactive effects of these factors on alien plants. While most of the available data suggest reduction in AM root colonization by severe herbivory (Gehring and Whitham, 1994), the reverse interactions have also been documented. Although consistent patterns and mechanistic explanations are yet to emerge, it is likely that herbivore-AM interactions have important implications for plant invasions.

Negative Feedback between AM Fungi and Invasive Plants

Mycorrhiza-plant interactions may vary along a mutualism-commensalism-parasitism gradient depending upon several factors such as the host species, soil fertility status and other environmental conditions (Lovelock et al., 2003). Arbuscular mycorrhizas may not always confer benefits to their host species but may also reduce their competitive abilities due to high carbon costs (Walling & Zabinski, 2006). A negative mycorrhizal feedback on plant growth can be attributed to asymmetries in the delivery of benefit between plants and AM species (Bever, 2002) and this may result in community dynamics where competing plant species can coexist. This reduces the possibility of competitive exclusion of native species by invasives. Landis et al. (2004, 2005) corroborated their field data with controlled experimentations to show that AM can induce parasitism on susceptible hosts and non-mycorrhizal plants may not only persist in and successfully compete with mycorrhizal plants in well established species-rich communities but can even invade and dominate them. However, studies on variation in plant response to native and exotic AMF (Klironomos, 2003) have shown that extreme responses are more common in case of locally adapted plants and fungi. Though exotic AM may not function any differently from native AM, the former offer less variation in plant response than later (Klironomos, 2003) thus having relatively lesser positive or negative feedback with aliens than native plant species. In addition, a negative correlation between AM density and invasive plant (knapweed) cover was recorded (Lutgen & Rillig, 2004) by demonstrating that areas with high knapweed density generally had lower glomalin concentration and AM hyphal length compared with areas having no or less knapweed cover. Through floral examinations and experimental tests, naturalized plants are reported not only to be less dependent on and poor hosts of AMF but also their initial establishment and dominance of invaded habitats can inhibit the reestablishment of effective mycorrhizal mutualists (Bever et al., 2003). Alteration of soil biotic characteristics in such a way by invasive species may negatively feedback to change their performance relative to co-occurring native plant species. On the other hand even a small increase in growth of native species from mycorrhizal mutualists has been shown to help them to compete effectively with exotic species (Gillespie & Allen, 2005) despite the fact the alien invasion may cause changes in the mycorrhizal community. Whilst Goodwin (1992) indicated a negative role of fungal mutualisms in maximizing fitness of invasive species, Bever et al. (2003) suggested that dominance of naturalized plant species in Southern California is facilitated by degradation of mycorrhizal mutualisms. It appears from such findings that communities with rich AM diversity may be more resistant to invasion by alien plants. Also because of their low host specificity AMF may not necessarily play a major role to specifically facilitate or hinder the growth of alien plants. The potential of alien invasive species to improve phosphorus dynamics and bioavailability (Chapuis-Lardy et al., 2006) indicate their pervasive influence on AM communities. However, exhaustive field observations and controlled experiment, including different permutations and combinations to incorporate most of the variables affecting or getting affected by invasive plant-AM interactions, need to firmly establish whether alien invaders out-compete more easily the mycorrhizal or non-mycorrhizal native plants and which of them can resist invasion more strongly. These findings will be most useful in identification and selection of the effective native mycorrhizal species/isolates conferring more benefits to native than alien plants that can be used to restore invaded habitats. In situations where aliens rely more on mycorrhizal symbiosis, the non-mycorrhizal native plants with suppressive influence on AM inocula could be used for restoration purposes.

A basic ecological attribute of successful invaders is to be least or non dependent on mutualists such as AMF, which if indispensable or obligate, may hamper their introduction and successful colonization in usually disturbed and AM poor habitats in their invaded range. Whether invasive plants have obligate or facultative dependence on AMF in invaded communities need to be ascertained through convincing evidence. Although development of negative plant-soil feedback in the root zone of invasive plants has been reported (van der Stoel et al., 2002), yet there can be a shift in the organisms causing this feedback during subsequent stages of invasion. The mycorrhizal association may turn from mutualistic to parasitic during subsequent stages in the life cycle of invasive host species or even during different stages of invasion. Detecting these stage-specific changes in the nature of AM-invasive plant interaction along introduction-establishment-naturalization_invasion continuum may help in devising effective soil-based management strategies for some plant invasions.

Impact of Plant Invasions on Structure and Function of AMF Communities

How alien plants affect the soil microbial communities in their invaded habitats is an exciting aspect of contemporary invasion biological studies. A recent study (Hong-bang et al., 2007) elucidated that soil biota alteration after Ageratina adenophora establishment may be an important part of its invasion process in Chinese forest understories to facilitate it and inhibit native plants. Furthermore, invasion by A. adenophora was found to strongly increase the abundance of soil AMF and the fungi/bacteria ratio. Mummey and Rillig (2006) indicated significant AM community alterations and considerable reduction in their diversity in response to invasion by Centaurea maculosa invasion. A major shift in composition and function of soil microbial community, of which AMF comprise an important part, due to alien invasion in numerous ecosystems has been reported (reviewed by Wolfe & Klironomos, 2005). Allelochemistry of invasive plants, depending upon whether they are mycorrhizal or non-mycorrhizal, may differently influence AMF communities in native soils of the introduced range. For instance, Alliaria petiolata (a noxious invader of eastern North American hardwood forests), is non-mycorrhizal, but produces allelochemicals that directly degrade AM fungi (Roberts & Anderson, 2001; Stinson et al., 2006). Through such positive feedback mechanisms, A. petiolata alters the mycorrhizal soil environment to one that is more conducive to its own growth and development rather than mycorrhizal-dependent native plants. Such degradation of local mycorrhizal fungi has also been noted for a variety of other invasive plants of disturbed ecosystems (although through other indirect mechanisms), leading to a new hypothesis for alien plant invasion--the Mycorrhizal Degradation Hypothesis (Vogelsang et al., 2004). Nevertheless some allelochemicals secreted by some plants like sesquiterpenes may induce proliferation of hyphal branching in AMF (Akiyama et al., 2005) and cause improved germination of seeds of such invasive plants. While reviewing recently the role of allelopathy and mycorrhizas in plant invasions, Weir (2007) pointed out that allelochemicals play a much larger role in plant invasion than reflected by current literature. In fact alien plants may alter soil chemistry and soil ecology, probably creating conditions that favour their invasion at the cost of native species, as reported in case of Halogeton glomeratus (Duda et al., 2003). Species shift and significant reduction in abundance of soil biota, which may include AMF, has been attributed to the response of native species to soil nutrients like N, P, K present before invasion which were elevated in the soils that produced the greatest native species biomass (Belnap et al., 2005). Allsopp and Holmes (2001) also showed that following a single cycle of dense alien vegetation, mycorrhizal plant species are not negatively affected but other effects of alien vegetation on nutrient cycling may change the balance between different mycorrhizal-plant guilds. Exotic invasion through their profound influence on soil properties and elemental cycling (Blank & Young, 2002) may indirectly impact AM diversity and distribution which in turn can translate into the success or failure of invasive species. This can be related to altered soil quality and textural properties due to plant invasions as indicated in case of invasion by Parthenium hysterophorus (Annapuma & Singh, 2003). The self altered soil conditions by this alien species may potentially promote its invasiveness over a broad range of habitat conditions. Since AM can notably influence soil quality and texture (Landis et al., 2004), their role in plant invasion needs further investigations in light of this perspective as well. The differential abilities of plants to influence their abundance by changing the structure of their soil communities (Klironomos, 2002), is considered to regulate plant community structure which in turn determines community invasibility. We argue that soil aggregation should be included in a more complete 'multifunctional' perspective and that in-depth understanding of tripartite, mycorrhizasoil process-invasion, relationships will require analyses emphasizing feedbacks between soil structure and mycorrhizas vis-a-vis plant invasion, rather than a unidirectional approach simply addressing mycorrhizal effects on soils.

Stinson et al. (2006) presented a novel evidence that antifungal phytochemistry of the invasive plant, Alliaria petiolata, a European invader of North American forests, suppresses native plant growth by disrupting mutualistic associations between native canopy tree seedlings and belowground AM. The pervasive influence of an invasive plant (Centaurea maculosa) on AM communities in roots of its competitors such as Dactylis glomerata was indeed an interesting proposition (Mummey et al., 2005) adding a biological spatial component to controls on root colonization. An insight into the possible mechanism of how invasive plants drive mycorrhizal symbionts to their advantage is discernible from Pamiske (2005) and Akiyama et al. (2005). Their studies showed that roots of some parasitic weeds release potent molecules such as strigolactones that activate symbiotic fungi at very low concentrations by providing cue for the hyphal branching connections and triggering seed germination, thus facilitating plant roots to enter into symbiosis with AM. However, it is currently unclear precisely which phytochemicals produced by invasive plants have the antifungal properties, whether and how they interact with other functionally important soil microbes. In addition, within the home range, it is important to know if evolutionary natural resistance of co-occurring native plant species buffers the effects of invasive plant's anti-mycorrhizal properties. Further research in these directions is needed to better understand the effects of invasives on natural ecosystems and the mechanisms involved.

Conclusion

While many studies suggest driving influence of AM fungi on plant invasiveness (Table 1) by facilitating competitive dominance of alien plants over the native species (positive feedback), some studies also indicate the opposite showing that AM may contribute to the coexistence of competing plant species (negative feedback). Reciprocally, the alien plant species may impact mycorrhizal community structure and function in the invaded habitats in different ways (Fig. 3). Elucidating the facilitative as well as suppressive role of AM fungi in plant invasions, the gaps and limitations in the field studies and experimental designs of complex AM-invasive plant interactions research identified hereby call for alternative strategies in future studies (Fig. 2). Understanding the stage-specific transition of mycorrhizal associations, from mutualism to parasitism or vice-versa, along introduction-establishment-naturalization-invasion continuum would be an interesting discourse for future research. This, however, needs a unified top-down and bottom-up approach targeting both biotic and abiotic factors under field and laboratory conditions.

DOI 10.1007/s12229-009-9039-7

Acknowledgement The senior author acknowledges the internship program supported by the Department of Foreign Affairs and International Trade (DFAIT) through the Canadian Bureau for International Education (CBIE) at the University Laval, Quebec, Canada. We are grateful to various mycorrhizal ecologists for providing access to their research works. We also thank anonymous reviewers for their useful comments and suggestions.

Published online: 13 November 2009

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Manzoor A. Shah (1,3) * Zafar A. Reshi (1) * Damase P. Khasa (2)

(1) Department of Botany, University of Kashmir, Srinagar, J&K 190 006, India

(2) Forest Research and Institute of Integrative Biology and Systems, University Laval, Quebec GIVOA6, Canada

(3) Author for Correspondence; e-mail: mashah75@yahoo.com
Table 1 Major Studies Depicting the Role of AM in Plant Invasions

  Alien invasive       Growth form           Invaded Habitat/Region
      species

Ageratina adenophor    Annual herb           Forest understories,
                                             China
Anthemis cotula        Annual herb           Disturbed ecosystems-
                                             Kashmir Himalaya
Ambrosia               Annual or perennial   Disturbed areas and
  artemisiifolia       herb                  crop fields--France
Cantaurea maculosa     Annual forb           Grasslands--North
                                             American
C. maculosa            Annual forb           Grassland -USA.
C. maculosa            Annual forb           Grassland -USA
Alliaria petiolata     Biennial herb         Hardwood Forest,
                                             North America
Oenothera panciniata   Annual herb           Coastal sand dune-Japan
Sapium sebiferum       Perennial tree        Hyric forest-USA
Solidago canadensis    Perennial herb        Chongming Island, China.
Acer negundo + Acer    Tree                  Riparian sites and mesic
  platanoides                                forests-North America.
Centaureamaculosa      Annual forb           Grassland-USA.
Centaurea melitensis   Annual forb +         Grassland-USA
  + Avena barbata      Annual grass.
Ardisia crenata        Shrub                 Forest--Japan
Prunus seroti          Tree                  Forest--north-western
                                             Europe
Bidens pilosa L.       Annual herb           Natural ecosystems-
                                             Hawaii USA
Cantaeurea maculosa    Perennial forb.       Grassland-USA
Centaurea melitensis   Annual forb           Grassland-USA
Brumus medrisensis     Annual grass          Coastal scrub-southern
                                             California
Pinus elliotti         Tree                  Fynbos-Africa
C. maculosa            Annual forb           Grassland--U.S.A
Andropogon gerardii    Grass                 Grassland/Prairies--
                                             North America

  Alien invasive       Study type              AM effect/Response
      species                                  variable

Ageratina adenophor    Greenhouse experiment   Invasive plant
                                               increased AM
                                               abundance
Anthemis cotula        Field studies and       Positive effect on
                       pot experiments         growth, fitness and
                                               enemy release
Ambrosia               Field studies and       Positive on invasive
  artemisiifolia       green house             spread
                       experiment
Cantaurea maculosa     Defoliation effects     Negative on
                       on AM in competition    competitive ability.
C. maculosa            Using field inocula     Positive on biomass
                       in greenhouse
                       experiments
C. maculosa            Using field inocula     Positive overall
                       in greenhouse
                       experiments
Alliaria petiolata     Field studies and       Native AM suppressed
                       pot trials              by the invader
Oenothera panciniata   Field and culture       Non significant
                       experiments.            effect on
                                               establishment.
Sapium sebiferum       AM inoculation of       Positive on growth
                       invasive in             of invasive and
                       competition with        negative on native
                       five native species     species
                       in greenhouse
                       experiments
Solidago canadensis    Evaluating              Positive on
                       mycorrhizal             colonization in
                       association as a        reclaimed lands.
                       function of time.
Acer negundo + Acer    Field studies and       Positive on height
  platanoides          greenhouse              and biomass.
                       experiments.
Centaureamaculosa      Grown with native       Positive on C
                       neighbours with and     transfer
                       without AM inoculum.
Centaurea melitensis   Grown with native       Positive on biomass.
  + Avena barbata      neighbours with and
                       without AM inocula.
Ardisia crenata        Field inocula in        Differential effect
                       greenhouse house        on growth,
                       experiments.            physiology and
                                               competitive ability.
Prunus seroti          Field studies and       Positive on
                       greenhouse              neighboring
                       experiments.            conspecific
                                               establishment and
                                               seedling performance
Bidens pilosa L.       Microcosm study.        Positive or negative
                                               depending upon AM
                                               species identity m.
Cantaeurea maculosa    Field trials.           Positive on P
                                               uptake.
Centaurea melitensis     Green house           Positive on
                         experiments in        compensatory growth
                         inter-and intra-      and competitive
                         specific              ability
                         competition.
Brumus medrisensis       Field inoculum in     Positive on number
                         green house           of leaves.
                         experiments.
Pinus elliotti           Mycorrhizal           Positive or
                         distribution and &    negative.
                         competitive
                         interactions.
C. maculosa              Grown with various    Positive on biomass
                         neighbors using
                         field inocula in
                         green house
                         experiments.
Andropogon gerardii      Radio-labeled P-      Positive on P-
                         transfer              transfer

  Alien invasive       Reference
      species

Ageratina adenophor    Hong-bang et al., 2007
Anthemis cotula        Shah and Reshi, 2007,
                       Shah et al., 2008a, b.
Ambrosia               Fumanal et al., 2006
  artemisiifolia
Cantaurea maculosa     Walling and Zabinski,
                       2006.00
C. maculosa            Callaway et al., 2004a
C. maculosa            Callaway et al., 20046
Alliaria petiolata     Stinson et al., 2006
Oenothera panciniata   Funatsu et al., 2005
Sapium sebiferum       Nijjer et al., 2004
Solidago canadensis    Liang et al., 2004
Acer negundo + Acer    Reinhart and Callaway,
  platanoides          2004
Centaureamaculosa      Carey et al., 2004
Centaurea melitensis   Callaway et al., 2003
  + Avena barbata
Ardisia crenata        Bray et al., 2003
Prunus seroti          Reinhart et al., 2003
Bidens pilosa L.       Stampe and Daehler,
                       2003
Cantaeurea maculosa    Zabinski et al., 2002
Centaurea melitensis   Callaway et al., 2005
Brumus medrisensis     Yoshida and Allen,
                       2001
Pinus elliotti         Allsopp and Holmes,
                       2001
C. maculosa            Marler et al., 1999
Andropogon gerardii    Francis and Read, 1994
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Author:Shah, Manzoor A.; Reshi, Zafar A.; Khasa, Damase P.
Publication:The Botanical Review
Article Type:Report
Geographic Code:1CANA
Date:Dec 1, 2009
Words:9440
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