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The endophyte-enemy release hypothesis: implications for classical biological control and plant invasions H.C. Evans Summary Fungal endophytes are asymptomless colonizers of higher plants for all, or a part, of their life cycles. They range from latent pathogens to symbionts. There is increasing evidence that some form mutually beneficial, highly specialized or co-evolved associations with their hosts and that they provide the plant with an additional armoury to combat abiotic and biotic stresses, including pests and diseases. Thus, there may be a trade-off between reduced growth (in the short term), as nutrients are sequestered by the fungal mutualist, but increased overall long-term fitness as natural-enemy pressure is decreased. This tripartite balance may be lost when plants arrive in exotic ecosystems with incomplete guilds of both co-evolved endophytes and natural enemies. The enemy release hypothesis (ERH) explains why alien plants can become invasive. It is now hypothesized that another, more cryptic but still significant factor could also be involved: the presence or absence of mutualistic endophytes. Those neophytes arriving without co-evolved natural enemies but with mutualistic co-evolved endophytes would have a double advantage over local competitors. Such endophytic-enriched, alien-invasive weeds and those that form mutualistic associations with indigenous endophytes could help to explain the inconsistencies of some classical biological control introductions. Similarly, those alien plants that arrive and remain endophyte-free and without co-evolved natural enemies would have a distinct competitive advantage because they would have more resources to allocate to growth and reproduction, given, of course, that there are no significant pressures from indigenous natural enemies or that sufficient auto-defences are retained to overcome them. Such endophyte-depauperate alien-invasive weeds, however, remain highly susceptible to co-evolved natural enemies. This may explain the ‘silver bullet’ phenomenon, whereby the introduction of a single classical biological control agent can achieve complete control. This endophyte-enemy release hypothesis (E-ERH) is discussed with examples. Keywords: coevolution, fungal mutualists, plant fitness. Introduction partnerships with fungi, which enabled them to survive the stresses of life on dry land, where water and nutrients were the main constraints to colonization: ‘Once an endosymbiotic relationship of a fungus with an alga was achieved, a blueprint for a terrestrial plant was drawn’ (Pirozynski and Malloch, 1975). Here, the form and function of mutualistic endophytic fungi is reassessed in the light of recent studies, and their possible significance in plant ecology is explored, leading to the hypothesis that their presence or absence may explain, at least in part, why some alien plants become invasive and why classical biological control can be so unpredictable as a management strategy. There is now overwhelming evidence that all plants in natural ecosystems have developed symbiotic relationships with fungi (Rodriguez et al., 2004) and that the mutualistic ones, especially those involving vesicular– arbuscular mycorrhizae (VAM), are ancient in origin (Brundrett, 2002). Indeed, it has been suggested that such associations were pivotal to the colonization of land by plants (Simon et al., 1993; Blackwell, 2000; Brundrett, 2002). However, this mycotrophic theory had been discussed much earlier by Pirozynski and Malloch (1975), who hypothesized that the evolution of plants was made possible only through mutualistic Definitions and concepts CABI, E-UK, Bakeham Lane, Egham, Surrey TW20 9TY, UK <[email protected]>. © CAB International 2008 There has been considerable debate and controversy as to the correct usage of the term endophyte, origi20 The endophyte-enemy release hypothesis nally coined by the founder of modern mycology, Heinrich de Bary in 1866 (Wilson, 1995). The ambiguities and confusion have been such (Wilson, 1993, 1995; Wennstrom, 1994) that it has been recommended the term should be defined according to context (Kirk et al., 2001). Here, and specifically in relation to the proposed hypothesis, the use is restricted to fungi that invade living plants and colonize them without causing visible or immediate symptoms. Mycorrhizal fungi are excluded because, as dual plant–soil inhabitants, they are restricted to root systems in which there is synchronized plant–fungus development with nutrient transfer at specialized interfaces (Schulz and Boyle, 2005). In contrast, endophytic fungi lack the means of acquiring nutrients from soil but have evolved mechanisms that enable them to survive and live asymptomatically, at least initially, within the roots, stems and leaves of healthy plants (Brundrett, 2002). Fungal endophyte associations with their host plants have been described as a continuum (Saikkonen et al., 1998; Schulz and Boyle, 2005), ranging from parasitism (amensalism) through commensalism to mutualism (Lewis, 1985). This paper concentrates on the mutualists, those that form intimate associations with their plant hosts that are beneficial to both, providing protection from environmental stresses and microbial competition, as well as nutrients, for the fungus and increased resistance or tolerance to both abiotic and biotic stresses for the plant. Most evidence for this increased fitness comes from studies of forage and turf grasses, particularly from plant associations in the subfamily Pooideae, with balansiaceous fungi belonging to the genus Neotyphodium (Clavicipitaceae: Hypocreales) because of their ecological and economic importance (Schardl and Phillips, 1997; Clay and Schardl, 2002; Bouton and Hopkins, 2003). Neotyphodium is a genus of highly specialized or obligate endophytic species that live systemically and intercellularly in all the aerial parts of their hosts and that are transmitted vertically in the grass seeds. There is increasing evidence, however, that similar benefits and increased plant fitness are also conferred to both non-woody and woody dicot hosts by horizontally transmitted, facultative endophytic fungi (Narisawa et al., 2000; Wilson, 2000; Arnold et al., 2003; Clay, 2004). Obviously, there is a price to pay by the host plant for harbouring beneficial endophytes; although, as yet, quantitative data are lacking. Nevertheless, there is circumstantial evidence from field trials with turf grasses (Poa spp.) that shows that there is a significant cost involved because endophyte-free plants were notably more vigorous early in the season than those inoculated with endophytes. In contrast, later in the season, those with endophytes had markedly outperformed the plants lacking endophytes, as pests, diseases and drought stress took their toll (author, Rutgers University Experimental Station, 2001, personal observation). Moreover, there is indirect evidence of trade-offs in mycorrhizal fungi, where the carbon costs to the plant of supporting these mutualists have been found to be significant (Douds et al., 1988). Background to the hypothesis Mutualistic endophytic fungi offer a variety of potential benefits to their host plants including growth enhancement, tolerance to abiotic factors (including drought, heat and heavy metals) and resistance to pests and diseases (Redman et al., 2001; Rudgers et al., 2004; Schulz and Boyle, 2005). The mechanisms involved may be wide-ranging and complex, the result of an ancient association (coevolution). In the case of conferring protection against plant pathogens, for example, these could range from antagonism, mycoparasitism, competitive displacement, to induced resistance (Evans et al., 2003). It has now been established that anti-fungal, as well as anti-herbivore, secondary metabolites are produced by many endophytes (Latch, 1993; Christensen, 1996; Clay, 1997; Schardl and Phillips, 1997; Stone et al., 2000). In addition, some produce novel growth-enhancement compounds (Varma et al., 1999), whereas endophyte-free plants have been shown to activate defence mechanisms much more slowly than those with mutualistic endophytes (Rodriguez et al., 2004), suggesting that they are also involved in inducing host resistance to pests and diseases. Finally, more recent studies have revealed unique trophic interrelationships between endophytes and their plant hosts, which enhance tolerance to both drought and heat (Rodriguez and Redman, 2005; Marquez et al., 2007). The endophyte-enemy release hypothesis Plants in their centres of origin live in mutualistic relationships with a guild of specialized or co-evolved endophytic fungi that increase their tolerance of, or resistance to, both abiotic and biotic pressures, including co-evolved natural enemies. This protection comes at a price, with a trade-off in plant resources. Alien plants, especially dicot hosts, arriving in exotic ecosystems would have a depauperate endophytic mycobiota, freeing up resources for increased growth and reproduction. This, together with the absence of co-evolved natural enemies (enemy release hypothesis, ERH; Keane and Crawley, 2002), would enhance significantly their fitness. Given that these endophyte-free aliens have sufficient auto-defence mechanisms to overcome the pressure from indigenous natural enemies, they then would have increased competitive advantage. The result would be a dominance of these enhanced or favoured species that would increase over successive generations. Thus, neophytes with weedy traits would tend to become dominant and invasive. However, such plants would be highly vulnerable to co-evolved natural enemies. This could explain the phenomenon of the 21 XII International Symposium on Biological Control of Weeds ophialum (Morgan-Jones and Gams) Glenn, Bacon and Hanlin. Tall fescue is a European species of high agronomic importance in North America despite the presence of the endophyte that produces highly toxic ergot alkaloids (Cross, 2003). Endophyte-infected plants are more vigorous, drought-tolerant and resistant to herbivores than endophyte-free ones, and one cultivar in particular (Kentucky 31), with enhanced endophyte activity, has now become a major invader of natural communities where it impacts directly on the native flora and fauna with long-term effects on successional dynamics and food webs (Clay and Holah, 1999). It has been argued that this is evidence of ecosystem vulnerability to human-induced invasion by an inbred, highly competitive exotic species (Saikkonen, 2000; Saikkonen et al., 2006) rather than a natural model. Whatever the interpretation, indirectly it lends support to the E-ERH, demonstrating the ecological importance of coevolved, mutualistic endophytes and the invasive threat from such associations in the absence of co-evolved natural enemies. Should classical biological control ever be considered as a management strategy for this invasive grass, the result would be an arms race between the endophyte and any introduced (co-evolved) natural enemies. This example also begs the question: do similar endophyte associations also occur in the invasive African grasses currently threatening the longterm stability not only of the Amazon region but also of global weather patterns (Mack et al., 2000)? ‘silver bullet’ in classical biological control, whereby the introduction of a single biological control agent can successfully and often unexpectedly, bring about the complete control of a rampant, invasive alien weed. Other alien plants, especially grasses with vertically transmitted endophytes, may arrive with their mutualistic endophytes, which, in the absence of co-evolved natural enemies, would give them a double advantage over local competitors. Such endophyte-enriched, alien-invasive weeds and those forming mutualistic associations with indigenous endophytes that afford protection from pests and diseases could help to explain why some classical biological control introductions fail to live up to expectations or that have only limited impact on the target weed. The endophyte-enemy release hypothesis (E-ERH) could help to resolve the on-going debate on the validity of the ERH (Wolfe, 2002; Mitchell and Power, 2003; Colautti et al., 2004; Parker et al., 2006), as well as clarify inconsistencies in both the new encounter and the evolution of increased competitive ability hypotheses (Hokkanen and Pimentel, 1984; Blossey and Notzold, 1995). It also has resonance with the recently proposed resource-ERH (Blumenthal, 2006), with a possible parallel situation in animal invasions, if protective endophytes can be compared to or are analogous with animal immune defence systems (Lee and Klasing, 2004). Evidence for the hypothesis Monocot hosts Dicot hosts Evidence for specialized or co-evolved mutualistic associations is unequivocal in the grass–Neotyphodium systems (Schardl and Phillips, 1997; Schardl and Moon, 2003). There is no clearer demonstration of the ecological and practical importance of mutualistic endophytes than the Poa annua–Neotyphodium association in northern United States, where endophtyeenriched seed is now routinely supplied to the turf-grass industry (Bouton and Hopkins, 2003). The serendipitous discovery of the co-evolved endophyte in seed of P. annua L. imported from northern Europe (the centre of diversity), as part of a breeding programme, led to research that demonstrated that the fungus not only afforded protection against generalist herbivores and pathogens but also conferred drought tolerance (J.F. White, Rutgers University, personal communication, 2002). Tests showed, however, that this fungus is not infective to Poa pratensis L. (Kentucky blue grass, actually a European species from the Mediterranean region), which is in high demand as a turf grass in southern United States. Ecological and economic logic dictate that surveys in southern Europe would pay dividends. In another example, which at first sight, may appear to contradict the E-ERH, involves Lolium (Festuca) arundinaceum (Schreber) S.B. Darbyshire or tall fescue and its co-evolved endophyte, Neotyphodium coen- In sharp contrast, it is much less likely that co-evolved endophytes will be carried to new ecosystems with their dicot hosts, given that these are horizontally transmitted and that most introductions (accidental or deliberate) are from seed. In effect, it would be a similar situation to that of co-evolved natural enemies, where there are few examples of them arriving together with their weed hosts. Therefore, it would be expected that most invasive alien dicots lack specialist or co-evolved endophytes. The degree of specificity of dicot endophytes, however, is not as clear-cut as for the grass endophytes discussed earlier, and it is probable that these are facultative rather than obligate in that, unlike Neotyphodium, they can survive saprophytically (Wilson, 2000). Surveys for endophytes of cocoa (Theobroma cacao L.) and its relatives in their South American centres of origin revealed that the stems and pods of healthy wild trees have a rich and unique endophytic mycobiota that becomes depauperate in plantation trees in exotic situations (Evans et al., 2003; Crozier et al., 2006). In vitro studies to test their biological control potential further demonstrated that some of these novel endophytes, pertaining to the Clavicipitaceae and Hypocreaceae (Hypocreales), are highly antagonistic to the co-evolved fungal pathogens of cocoa and, in addition, 22 The endophyte-enemy release hypothesis produce secondary metabolites known to be involved in plant defence mechanisms (Holmes et al., 2004; Samuels et al., 2006). From this work, there is an indication that specialized, perhaps co-evolved, endophytes dominate in native habitats, but these are replaced by generalists when the host is moved to exotic ecosystems. Similar results have been reported for other woody plant hosts (Wilson, 2000), and further support is coming from ongoing surveys of the endophytes associated with Lantana camara L. in both natural and degraded habitats in Brazil, where this plant is indigenous, as well as in its exotic invasive range in Pakistan (author, unpublished results). The endophytes isolated from L. camara in degraded sites in Brazil showed similarities with those recorded from Pakistan in that these belonged predominantly to a few well-known generalist fungal genera (Glomerella/Colletotrichum, Phomopsis), whereas those from a forest site population comprised an extremely rich mycobiota with many unusual genera being represented. It is tempting to suggest that these are part of a specialized endophytic guild of fungi that form mutualistic associations with L. camara and that, like the co-evolved natural enemies, they have been left behind as the plant host has been moved around the world. Preliminary studies on Japanese knotweed, Fallopia japonica (Houtt.) Ronse Decr., are yielding similar results. This plant, in urban situations in the United Kingdom, is virtually free of endophytes, whereas in climax habitats in Japan, it has a rich and diverse endophytic mycobiota (H. Evans, unpublished results). So much so that contaminating endophytes have hampered the culture and study of the fungal component of the plant’s co-evolved natural enemies. One of these, belonging to a monotypic asexual genus, which, unusually, also produces its sexual stage (a new discomycete genus) in culture, can be reinoculated into and readily reisolated from healthy knotweed leaves. Whether this species and the other endophytes from Japan are specific or co-evolved mutualists remains to be proven. However, it is evident that sophisticated recognition mechanisms are involved, enabling the fungus to bypass the plant’s defences. Y. Ono (Tomley and Evans, 2004). Unexpectedly, host mortality has been exceptionally high (75%) because of a lethal combination of rust- and drought-induced stress, whereas pod set and seedling recruitment have been almost nonexistent. Such dramatic impacts and high mortality are atypical of obligate pathogens especially in natural ecosystems and was never observed in Madagascar, where the rust constitutes part of a guild of natural enemies keeping the rubber vine population in check but neither eliminating flowering and fruiting nor killing seedlings and mature plants. Discussion The E-ERH is just one amongst a plethora of hypotheses put forward to explain invasiveness by alien species, especially by plants. Impressively, Colautti et al. (2004) list no less than eight nonexclusive theories for invasion success. Others have been added since (MüllerSchärer et al., 2004; Blumenthal, 2006). This has led to confusion and controversy, not to say a heady mix of acronyms. Each hypothesis could in itself explain a part of invasion ecology, or more likely, each invasive weed needs to be dealt with on a case-by-case basis. Clearly, the successful ‘silver bullet’ classical biological control projects against invasive weeds must have been driven by the ERH. In these cases, the E-ERH may further explain why the release of a single natural enemy can have such a dramatic and profound impact. Conversely, the presence of co-evolved mutualists, in the absence of co-evolved natural enemies, offers an explanation as to why certain grasses have become major invasive species with the ability to alter plant communities and reduce biodiversity (Clay and Holah, 1999; Mack et al., 2000). The E-ERH has direct pragmatic implications perhaps more so in plant disease rather than weedinvasion ecology. In fact, the germ of the E-ERH was sown during a project to evaluate the biological control potential of co-evolved endophytes in the centres of ori gin of the two major diseases of T. cacao. The finding of unique endophytes in wild cocoa with demonstrable antagonism towards the cocoa pathogens, together with their absence in cultivated cocoa, points to a role for mutualistic endophytes in plant protection (Evans et al., 2003; Holmes et al., 2004; Samuels et al., 2006). In the future, there could be the intriguing possibility that crop plants, like turf grasses in the United States, will be marketed as ‘endophyte-enriched’, planting material being inoculated with co-evolved mutualists to protect not only against pests and diseases but also against abiotic stresses, notably drought. Such inoculations with mycorrhizal fungi are now standard practice in tree nurseries. Perhaps it is fitting to touch on the subject of mycorrhizae because they may also play a role in invasion biology. Indeed, mutualistic ectomycorrhizal (EM) fungi Classical biological control The ‘silver bullet’ examples in classical biological control could be explained, at least in part, on the basis of the invasive alien weed having lost its protective co-evolved endophytes and not acquiring indigenous generalist mutualists to fill this role. Thus, the fitness of any introduced co-evolved natural enemy would be increased accordingly. An analysis of the successful rubber vine project in Australia offers empirical supporting evidence. This Madagascan asclepiad, Cryptostegia grandiflora (Roxb. ex R. Br.) R. Br., which covered more than 40,000 km2 of northern Queensland, has now been stopped in its tracks after the release of a co-evolved rust, Maravalia cryptostegiae (Cummins) 23 XII International Symposium on Biological Control of Weeds offer an explanation as to why exotic pine species have increased fitness and why, in some ecosystems, they have become highly invasive (Richardson et al., 2000). In contrast, non-specific VAM fungi (Glomales) occur in all soils and, seemingly, would readily be acquired by indigenous and non-indigenous plants alike (Read, 1999). They have even been considered to be ‘arguably the most important group of all living organisms’ (Brundrett, 2002). Significantly, however, there are plant families that are predominantly non-mycorrhizal, including Amaranthaceae, Brassicaceae, Chenopodiaceae, Commelinaceae, Cyperaceae, Polygonaceae and Urticaceae. Many of these ‘are pioneer colonizers of marginal habitats or weedy, opportunistic invaders of disturbed soil’, that ‘have expanded into more marginal environments since mid-Mesozoic, a trend which appears to be accelerated by man’s escalating agricultural and industrial activities’ (Pirozynski, 1981). Could it be that they no longer needed VAM fungi and the tradeoffs this entailed, relying instead on mutualistic endophytes for competitive advantages? Indeed, the main feature of the roots of these plant families is the capacity to actively exclude VAM fungi through the release of anti-fungal metabolites (Brundrett, 2002). The exclusion of VAM fungi would conserve energy, increase fitness and, therefore, should be another factor to be included in the long list of why some plants become invasive. Tantalizingly, Richardson et al. (2000) briefly reflect on fungal endophytes as possible promoters of plant invasions, concluding that: ‘the specificity and the nature of such associations are poorly known as is their role in invasion’. 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