Download When two invasion hypotheses are better than one

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When two invasion hypotheses
are better than one
Dozens of hypotheses attempt to explain the success of invasive
species (Catford et al., 2009). Though no single hypothesis explains
invasions in general (Gurevitch et al., 2011), the temptation to
search for a universal mechanism shared by most invasive species
has motivated much of the invasion research to date. Instead of
studying mechanisms in isolation from one another, perhaps
investigating synergies between disparate invasion hypotheses, as
Zheng et al. have in this issue of New Phytologist (pp. 1350–1359),
will do more to explain the success of invasive species.
‘The strength of this approach is that it used crosscontinental studies to provide evidence for multiple
ecological and evolutionary invasion mechanisms in a
Multiple biotic factors and the ERH
Over seven previously described invasion mechanisms focus on
biotic factors (Catford et al., 2009), including enemies, competitors, and mutualists. Some of these hypotheses explicitly consider
interactions between multiple factors (e.g. competition and
herbivory in the Enemy of My Enemy Hypothesis (Colautti et al.,
2004)), yet relatively few empirical studies consider effects of
multiple types of biotic interactions simultaneously. We conducted
an extensive search of the ERH literature and found only 19 studies
that manipulated more than one biotic interaction on native and
introduced species simultaneously (E. H. Schultheis et al., unpublished). All but one study was conducted on plants, and most were
conducted in the introduced range, not comparing the effects of
biotic interactions in both ranges. We found evidence that studying
more than one biotic interaction revealed important effects that
studying one biotic interaction alone would have missed. For
example, herbivores had a stronger effect on invasive plant
performance when competition was intense (Suwa & Louda,
2012), although other studies found that the effects of multiple
biotic factors were additive, and studying them in isolation provided
accurate estimates of their effects (e.g. Cripps et al., 2011).
real invasion.’
Resources and the ERH
From a basic ecology perspective, it is not terribly surprising that
one mechanism does not underlie all invasions, given the wide
variety of factors limiting the population growth and distributions
of native taxa. At least two potential scenarios likely explain the
observed lack of generality in invasions (Gurevitch et al., 2011):
first, invaders likely succeed through many different mechanisms.
In essence, most of the proposed invasion hypotheses may be
relevant for some taxa, in some environments, at some point in time
but do not apply in the majority of cases. Second, proposed
invasion mechanisms may act synergistically to promote invasions.
Though this second point is not a new concept, in the invasion
literature (Inderjit et al., 2005; Gurevitch et al., 2011), it has rarely
been investigated empirically.
Multicausality and interactions between invasion
mechanisms
Multiple factors may contribute to invasions, and these may act
additively or interactively. Effects may be minimal when each
mechanism is studied in isolation, and their full effects may only be
understood when studied in concert with other mechanisms. Next,
we highlight three examples of potential synergies between the
Enemy Release Hypothesis (ERH), one of the most extensively
tested invasion hypotheses, and other invasion mechanisms.
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Invasion may be facilitated by disturbance, which frees up resources
making them available for introduced species, or anthropogenic
addition of nutrients to the environment (Davis et al., 2000). These
nutrient effects may interact with enemy release. Faster growing
species tend to invest more in growth and less in producing high
quality, well-defended tissues. Because these fast growing species
may be susceptible to enemies when they become abundant and
apparent, these same species may be more likely to benefit from
enemy release. As a result, invasiveness may be promoted most
when invaders receive the dual benefits of high resource availability
and enemy release (Resource Enemy Release Hypothesis,
Blumenthal, 2006).
Darwin’s naturalization hypothesis and the ERH
Darwin’s naturalization hypothesis predicts that species closely
related to native community members will be poor invaders
because close relatives are more likely to be functionally similar and
intense competitors (Darwin, 1859). While the naturalization
hypothesis was initially based on assumptions about competitive
interactions, novel defenses may also facilitate invasion success
through interactions with the ERH. Introduced species with very
different defenses may succeed because native herbivores or
predators may not have the capacity to recognize or tolerate unique
defense compounds or behaviors to which they have limited
Ó 2015 The Authors
New Phytologist Ó 2015 New Phytologist Trust
New
Phytologist
Commentary
evolutionary experience. For example, introduced plants more
distantly related to the community they invade often experience
reduced herbivore damage (e.g. Harvey et al., 2012). A necessary
future step for these types of studies, however, is determining
whether reduced herbivory received by more distantly related
invaders actually promotes invasiveness.
Synergy between ERH, EICA and the NWH
Synergies between some invasion mechanisms may be more likely
than between others. Given that many novel weapons and defenses
in plants involve the production of potentially costly chemicals,
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synergies between the Novel Weapons Hypothesis (NWH) and the
ERH and/or the Evolution of Increased Competitive Ability
(EICA) hypothesis may be especially likely (Fig. 1; see also Callaway
& Ridenour, 2004; Bossdorf, 2013). The NWH suggests that the
success of some invaders is due to the novelty of their competitive,
defensive, or predatory traits (Callaway & Ridenour, 2004). In
essence, native species may have no evolutionary experience with,
and therefore may be extremely susceptible to, allelopathic or
defensive compounds produced by invaders. The EICA hypothesis,
in turn, proposes that escape from herbivores causes evolutionary
reductions in defense and resource reallocation to growth and
competitive ability (Blossey & N€otzold, 1995). While EICA
Native range community
Generalist
herbivores
Specialist
herbivores
Competing
plants
1
Invaded range community
Generalist
herbivores
Specialist
herbivores
Naïve
competing
plants
2
6
Reduced attack from
specialist enemies
4
Reduced
defense
8
3
Increased allelochemical
effectiveness
5
7
Increased competitive ability,
growth, fitness
Fig. 1 Plant species encounter very different communities in their invaded range compared to their native range; they typically escape specialist enemies and
encounter different competing plant species (1). Because of the absence of many specialist enemies in the introduced range, they may experience reduced attack
from specialist herbivores (2). Because herbivory can reduce plant growth and competitive abilities, plants may experience increased fitness in the introduced
range (3). Reduced attack from specialist enemies may also relax selection on plant defenses (4). Because of growth–defense trade-offs, relaxed selection on
plant defenses may lead to the evolution of increased growth or competitive ability (5). Invading plants also face different competitive environments (6).
Competing plants in the introduced range may be na€ıve to and more affected by novel competitive traits of the invader such as allelochemicals, leading to higher
growth and relatively higher competitive abilities in the introduced range (7). These relationships represent three common invasion mechanisms: Enemy Release
Hypothesis (ERH: yellow symbols, 1–2–3), the Evolution of Increased Competitive Ability (EICA) hypothesis (gray symbols, 1–2–4–5) and the Novel Weapons
Hypothesis (NWH: green symbols, 1–6–7). The ERH/EICA and NWH may be linked if biochemical or resource-based trade-offs between defensive and
offensive chemical production exist (blue symbol, 8). In this case, escape from enemies may relax selection on defenses allowing for increased allocation to
offensive chemical compounds over evolutionary time. Solid and dashed arrows indicate ecological and evolutionary processes respectively.
Ó 2015 The Authors
New Phytologist Ó 2015 New Phytologist Trust
New Phytologist (2015) 205: 958–960
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explicitly assumes a growth–defense trade-off, EICA and NWH
may be tightly related if evolutionary increases in competitive ability
do not arise from a growth–defense trade-off but instead from an
offense–defense trade-off. For example, reduced allocation to
defensive chemicals may allow increased production of allelochemicals. If these trade-offs between defensive chemical production and
allelochemical production are common, then novel weapons may
be especially potent mechanisms of invasion when accompanied by
enemy release. Integrating these hypotheses provides a mechanism
explaining increased allelochemical production and competitive
ability following invasion.
Several recent studies have used very different approaches for
investigating connections between NWH and EICA/ERH. Zheng
et al. link findings from separate experiments to build their case
that novel weapons and EICA are related. Their approach focuses
on identifying differences between invasive and native range
genotypes in a variety of biotic contexts (presence/absence of
competitors and enemies in both the native and introduced
range). The strength of this approach is that it used crosscontinental studies to provide evidence for multiple ecological and
evolutionary invasion mechanisms in a real invasion. As a result,
synergistic effects of NWH and EICA seem plausible, but the
connections between the two invasion mechanisms remain
tenuous; for example, NWH and EICA are tested in separate
experiments and not linked together by testing for genetic
correlations between allelochemical and defense production.
Using a different approach, Uesugi & Kessler (2013) employ
experimental evolution to show the potential for enemy release to
select for increased competitive ability and allelochemical
production, but it is unclear whether increased allelochemical
production evolved in invaded range populations of their study
taxa or what trade-offs produced this evolutionary shift.
Both approaches illustrate that NWH and EICA are two
invasion mechanisms with obvious potential for synergistic effects,
but the details of this synergism remain speculative. For example,
we now understand the role of Odoratin in allelopathic interactions, but does it also play a role in deterring belowground
herbivores or altering belowground microbial communities, a
hypothesis consistent with Zheng et al. findings of increased
defenses against belowground enemies and increased Odoratin
production in invaded range genotypes? Similarly, do trade-offs
between the production of the allelochemical Odoratin and other
defense traits explain the observed reductions in resistance and
increases in allelopathy in introduced populations? Only more
detailed functional ecology studies of the chemical compounds
involved, and explicit quantitative genetic studies to identify the
potential for correlated evolution and genetic trade-offs, will fully
link these invasion mechanisms.
As these studies illustrate, simultaneously considering multiple
invasion mechanisms is difficult, requiring a number of separate
experiments, long-term experimental evolution approaches, or
ideally fully factorial experiments with the capacity for considering
both ecological and evolutionary responses. Yet, these types of
experiments may help unify the many disparate hypotheses of
invasions and identify when invasion mechanisms are most likely to
New Phytologist (2015) 205: 958–960
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act synergistically. In short, while no magic bullet fully explains
invasiveness, combining multiple invasion hypotheses may lead to
important insights on the drivers of biological invasions and the
constraints and opportunities faced by species embedded in
complex natural communities more generally.
Acknowledgements
This is Kellogg Biological Station publication no. 1843.
Jennifer A. Lau* and Elizabeth H. Schultheis
Kellogg Biological Station & Department of Plant Biology,
Michigan State University, Hickory Corners, MI 49060, USA
(*Author for correspondence: tel +1 269 671 2107;
email [email protected])
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Key words: allelopathy, biological invasion, defense, enemy release, invasive
species, novel weapons, trade-off.
Ó 2015 The Authors
New Phytologist Ó 2015 New Phytologist Trust