Download The endophyte-enemy release hypothesis

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’. Here, it is proposed that their role, in the case
of specialized or co-evolved mutualistic endophytes, is
twofold: their presence increasing plant fitness in the
absence of co-evolved natural enemies, especially in
grass hosts with vertically transmitted endophytes;
their absence coupled with release from co-evolved
natural enemies, contributing to increased plant fitness,
especially in dicot hosts with horizontally transmitted
endophytes, but leaving them highly vulnerable to classical biological control agents.
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Acknowledgements
This paper contains data, both published and unpub­
lished, from studies funded by the Environment Agency
(United Kingdom), Conselho Nacional de Desenvolvimento Cientifico e Tecnologico (Brazil) and USDA–
ARS (Beltsville, MD).
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