Seven contexts can alter the influence of each ERH factor
Ecological context modulates the occurrence and strength of the
component factors contributing to the ERH (Table 1c; Figs. 1c, 3). These
seven contexts contribute to inconsistencies between studies when not
accounted for (Box 2; Fig. 4). Once accounted for, apparent
‘inconsistencies’ can become explicable by ecological context (Catfordet al. 2022), enabling predictions on how future invaders
experiencing similar contexts may or may not benefit from enemy release.
For brevity, we discuss only three of the seven contexts in detail: time
since introduction; relative resource availability in species’ home and
invaded ranges; phylogenetic relatedness of native and exotic plants. In
each case, we describe how the context influences enemy impact, enemy
diversity and host adaptation, before discussing appropriate ways to
measure the context. We then briefly introduce the four other contexts
(temporal and spatial asynchronicity; number of introduction events;
type of enemy; strength of growth-defence trade-offs), highlighting the
factors they especially influence. These seven contexts are key
moderators of the ERH based on our review of the literature, but this
list is not necessarily exhaustive.
Time since introduction
Effect on enemy impact: Immediately after arrival in a new range,
exotic species may experience a lower enemy impact relative to natives
(Fig. 3a). This lower impact is because generalist enemies in the
invaded range can be less effective at exploiting exotic species (e.g.
Beaulieu et al. 2019). Lower impact on exotics will enhance
performance relative to co-occurring native species over short time
scales, even if enemy richness is the same for native and exotic
populations. Through time, this benefit to exotics can erode as
generalists in the new range evolve to target the exotic more
efficiently (Carroll et al. 2005) and thus increase their impact
on the exotic (Fig. 3a). Alternatively, enemy impact on exotics could
also further reduce with time, as exotics develop new defences against
generalists (Müller-Schärer et al. 2004).
Effect on enemy diversity: Invaders lose and (re)gain enemies
through time (Fig. 3b). There should be an immediate reduction in
specialist enemies upon introduction, as specialists that only target
the invasive plant are absent from the invaded range (Keane & Crawley
2002). The diversity of local generalist enemies could also be initially
low on the exotic, as they may be poorly adapted or unused to targeting
it (Bezemer et al. 2014). Over time there is typically a steady
accumulation of generalists as they, for example, become familiar with
the chemical signature of the plant (Novotony et al. 2003; Iqbalet al. 2021).
Effect on host adaptation: Host adaption caused by enemy release
is a phenotypic- or genetic-based response to reduced enemy impact or
diversity (Inderjit et al. 2005; Medina-Villar et al.2022). How quickly host adaptation occurs will depend on the generation
time of the host plant in question, the strength of selection (the
degree to which enemy pressure is reduced, Fig. 2) and other contexts
that affect investment into growth and defence, such as resource
availability (see Context ii below; Fig. 3f).
Measurement: Time since introduction should be measured in the
number of generations of the exotic species, rather than in an absolute
measure such as years since introduction. 150 years means something very
different to an annual daisy than it does to an oak tree. Further,
‘generations since introduction’ should be considered at a population
level (Table 1c). An exotic species may have multiple distinct
populations in the invaded range, that have been established for
different lengths of time. These populations could show different
support for the ERH, especially if they are isolated (Fig. 4).
Relative resource availability in home and invaded range
Effect on enemy impact : Relative resource availability refers to
difference in resource levels between the home and invaded range of an
exotic population. The impact of enemies is strongly correlated with the
availability of resources. Plants in high-resource environments tend to
be more resource-acquisitive, a characteristic of invasive species (van
Kleunen et al. 2010a, b). High resource availability encourages
investment in growth rather than defence, so herbivores perform better
on resource-acquisitive plants (Morrow et al. 2022). Therefore,
if exotics come from a high-resource environment relative to the invaded
environment, enemy impact is likely to be higher on the exotic than
co-occurring native species, as exotics are more palatable than natives
(Fig. 3d, red line). Contrastingly, species from low-resource
environments show higher investment in defence, as tissue is less easily
replaced and more valuable (Endara & Coley 2011). Therefore, enemy
impact relative to natives is likely to be lower on exotics from
resource-poor home ranges (Fig. 3d, blue line). In the absence of host
evolution or phenotypic adaptation where a plant upregulates growth and
downregulates defence (but see Fig. 3f), these differences should
persist through time.
Effect on enemy diversity: High resource availability encourages
poorly defended, nutrient-rich plants, promoting a high diversity of
natural enemies (Blumenthal 2006; Allen et al. 2017). Exotics
coming from resource-rich environments have more enemies to lose (Fig.
3e, red line) and are particularly likely to benefit from enemy release
(the resource-ERH: Blumenthal 2006; Blumenthal et al . 2009).
However, exotics from resource-rich environments also accumulate enemies
at a faster rate than exotics from resource-poor environments because
their poorly defended and nutrient-rich tissues are more attractive to
generalist enemies (Ebeling et al. 2021; Morrow et al.2022) (Fig. 3e).
Effect on host adaptation : Resource availability can alter
trade-offs between growth and reproduction (Agrawal 2020). Exotics
coming from low-resource environments likely have a lower growth-defence
ratio than co-occurring natives (Endara & Coley 2011) (Fig. 3f, blue
line). If they are released from enemies and have more resources
available, exotic plants will evolve to invest more in growth than
defence (Coverdale & Agrawal 2022). This adaptation can happen in as
little as 150 growing seasons (Wolfe et al. 2004) and underpins
the well-known evolution of increased competitive ability (EICA)
hypothesis (Blossey & Notzold 1995). Alternatively, if exotics
experience reduced resource availability in their invaded range and can
no longer use growth to compensate for high enemy damage, exotics from
high-resource environments may evolve to invest more in defence and less
in growth (Fig. 3f, red line).
Measurement. We define relative resource availability as the
difference in resource availability between the home and invaded range
of an exotic population (Table 1c). While absolute resource availability
is important, there is evidence for fine-scale responses to resources
even within low-resource populations (Hahn et al. 2021),
suggesting the potential for exotic adaptation even if they are moving
between two sites with low levels of absolute resource availability.
Therefore, we present the difference in resources between the home and
invaded range as the key metric of this context.
Phylogenetic relatedness of exotic and native species
Effect on enemy impact: Phylogenetic relatedness represents the
evolutionary distance between exotic and co-occurring native plants.
Exotics that are phylogenetically close to the native community usually
show lower reductions in enemy impact (Fig. 3g, blue line). This is
because specialist enemies in the invaded range can more effectively
exploit closely related exotics (Castells et al. 2013; Harveyet al. 2013; Aldorfová et al. 2020). Distantly related
exotics have novel defences to which enemies in the invaded range are
naïve (Cappuccino & Carpenter 2005). Enemy impact will then increase
through time, as generalists in the invaded range evolve to target
exotics (Carroll et al. 2005), as noted above. However, enemy
impact can saturate at a lower level for distantly related exotics even
over prolonged time scales (Beaulieu et al. 2019; Liu et
al. 2023) (Fig. 3g, blue and black lines). While Fig. 3g represents our
general prediction, we note the opposite can also be true.
Phylogenetically close exotics may possess defences that are well
adapted to the herbivores in an invaded range (Ricciardi & Ward 2006;
Morrison & Hay 2011).
Effect on enemy diversity: Distantly related exotics typically
experience greater reductions in enemy diversity (Fig. 3h, blue line),
as the ability for enemies to switch from co-occurring natives is lower
(Ebeling et al. 2008). In contrast, exotics with congeners in the
invaded range tend to accumulate enemies quickly (Mitchell et al.2006; Fig. 3h, black line), or are targeted by enemies to such an extent
they show no evidence for release at all (Ivison et al. 2023; Fig. 3h,
red line). Enemy diversity will generally saturate until exotic and
native plants have similar enemy numbers (Fig. 3h), though the rate at
which this occurs is contested (Hawkes 2007; Mitchell et al.2010).
Effect on host adaptation: Distantly related exotics experience
greater reductions in enemy pressure (because of lower enemy impact and
diversity) than exotics that are closely related to co-occurring
natives. Distantly related exotics may therefore adapt to invest less in
defence and more in growth, evolving more competitive phenotypes that
increase invasiveness (Fig. 3i).
Measurement: Phylogenetic relatedness can be measured in various
ways (Pinto-Ledezma et al. 2020), but we suggest that evolutionary
distance to the most closely related co-occurring native species
(“nearest neighbour”) is the most relevant metric (Table 1c). An
exotic that is distantly related on average to the community but with
one very close native relative is more likely to be immediately affected
by that native’s specialists than an exotic with intermediate average
relatedness and no close relative. However, mean relatedness might also
be important when considering overall native-exotic competition and how
this interacts with release, and it would also be important to consider
weighting the abundance or frequency of potential “nearest
neighbour/s” as has been done with functional traits (Gallien et
al. 2014; Catford et al. 2019). We do not explore these nuances
further here but suggest that aspect of the ERH warrants further
development. We also note that phylogenetic relatedness may not always
map on to phenotypic similarity or result in closely related specialist
enemies. Considering shared traits (which are not necessarily
phylogenetically conserved) may also be valuable (Cadotte et al .
2017).
Temporal and spatial asynchronicity between plant and enemy
populations
Temporal or spatial asynchronicity between exotic plants and their
potential enemies affects the diversity of enemies that accumulate
(Gsell et al. 2023). Temporally, exotic species can benefit from
‘invasion windows’ if generalist enemies are less abundant in a given
season (Agrawal et al. 2005; Geppert et al. 2021). Within
a single season, exotics can flower at different times to natives and so
avoid periods of intensive native herbivore activity (Fan et al.2016), leading to higher reproductive success than natives the following
season (García & Ehrlén 2002). Spatially, there may be microhabitats or
microclimates in the invaded range where disease or herbivore pressure
is lower (Parker & Gilbert 2007; Halliday et al. 2021). This is
because the niche breadth of exotic plants can exceed that of generalist
enemies, facilitating increased exotic survival in enemy-free areas (Luet al. 2013; Kambo & Kotanen 2014). We predict that enemy
diversity will generally decline as exotic plants and generalist enemies
become more asynchronous.
Number of introduction events
The number of introduction events affects enemy diversity (over
ecological time scales), and host adaptation (over evolutionary time
scales). Ecologically, an increasing number of introduction events
increases the likelihood of co-introducing specialist enemies from the
home range, eroding the initial benefit of lowered enemy diversity
(Mitchell & Power 2003; Mitchell et al. 2010; Schultheiset al. 2015; Warren & Bradford 2021). This effect is not
captured by simply accounting for time since first introduction.
Evolutionarily, the number of introduction events alters the genetic
potential for host adaptation. Founder effects could limit adaptive
potential (Felker-Quinn et al. 2013; Harvey et al. 2013;
Smith et al. 2020) or promote rapid divergence from the home
range (Bossdorf et al. 2005), both of which are ameliorated by
greater numbers of introduction events. Therefore, considering the
number of introduction events is crucial when testing the ERH,
independently of the time since (first) introduction.
Type of enemy
The likelihood and impact of losing or gaining an enemy will vary
depending on enemy type. The distinction between specialists and
generalists is fundamental when considering changes in enemy diversity.
Specialists should be lost to a much greater degree that generalists on
movement to a new range (Joshi & Vrieling 2005; Zhang et al .
2018) (Fig. 3b). The likelihood of losing specialists partly depends on
functional attributes of the specialist; for example, plants are more
likely to lose insect herbivores than fungal pathogens or viruses that
can co-invade with exotic seeds (Hawkes 2007; Parker & Gilbert 2007).
The type and generation times of enemies also affects their impacts. For
example, generalist mammalian herbivores provide the strongest biotic
resistance to exotic plant spread compared to other types of enemy
through their consumption of whole plants (Levine et al. 2004).
Enemies with fast generation times (e.g. viruses) can adapt faster to an
exotic, and thus exert a larger impact more quickly. Because different
types of enemy may be lost and gained at different rates, and have
different impacts through time, reporting trends for a limited number of
enemies may not fully capture the degree of enemy release (Fig. 2).
Presence and strength of trade-offs
The presence and strength of growth-defence trade-offs affect the
likelihood and strength of host adaptation mediated by enemy release.
Although there is evidence for trade-offs between species (i.e.
one species has high defence and low growth, while another species has
the opposite; Lind et al. 2013; Rotter & Holeski 2018; Heckmanet al. 2019) (but see Chauvin et al. 2018; Hinman et
al. 2019), evidence for within-species trade-offs is weaker (Heckmanet al. 2019; Hahn et al. 2021) yet this is more pertinent
as host adaptation requires within-species variation. However, specific
plant organs can show trade-offs related to defence and growth (Agrawalet al. 2012; Medina-Villar et al. 2022), and there is
evidence that some species can adaptively lower defence and increase
growth in response to lower enemy pressure (Wolfe et al. 2004;
Coverdale & Agrawal 2022). Evolutionary changes in growth and defence
because of enemy release should only benefit exotics that show strong
growth-defence trade-offs. These clear trade-offs may be relatively
uncommon, as plant resource management strategies are complex so a
single trade-off axis is unlikely (Lau & Schultheis 2015; Agrawal
2020).