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Biological Sciences Faculty Publications Biological Sciences
10-2004
Novel Weapons: Invasive Success and the Evolution of Increased Novel Weapons: Invasive Success and the Evolution of Increased
Competitive Ability Competitive Ability
Ragan M. Callaway
University of Montana - Missoula
, Ray.Callaway@mso.umt.edu
Wendy M. Ridenour
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Callaway, Ragan M. and Ridenour, Wendy M., "Novel Weapons: Invasive Success and the Evolution of
Increased Competitive Ability" (2004).
Biological Sciences Faculty Publications
. 223.
https://scholarworks.umt.edu/biosci_pubs/223
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436
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I
n the 13th century, eastern and central Europe experi-
enced one of the most surprising invasions in human
history. The Mongols, once restricted to a small portion of
central Asia, swept into Russia, Hungary, Poland, and
Germany and consistently defeated much larger European
armies. It was only the death of the Mongol leader, Ogedai
Khan, in 1242, and the ensuing internal politics, that pre-
vented Europe from becoming a collection of vassal states.
The reasons for the success of the Mongol invasion were
complex. Although it was in large part due to brilliant
strategy and discipline, these strengths were derived from
the possession of a novel weapon, the recurve bow carried
by most Mongolian soldiers (Figure 1). The recurve bow
fired arrows faster, farther, and with greater force than
anything the Europeans had ever experienced. Such novel
weapons have played a role in many human invasions, but
novel biological weapons have only recently been consid-
ered as possible drivers of invasions by non-human exotic
species. Here, we explore the possibility that novel
weapons, biochemical in nature, play a part in the exotic
plant invasions that are currently sweeping the world.
One of the mysteries in ecology is how exotic plants
occurring at low densities in their native ranges attain
extremely high densities in their introduced ranges
(Figure 2). Although only a small fraction of introduced
species have enjoyed such dramatic changes in fortune,
these have had extensive economic impacts and suggest
the existence of very powerful, yet poorly understood,
ecological processes. A number of explanations for this
invasion success have been proposed (Mack et al. 2000),
but consumer-based hypotheses predominate – the “nat-
ural enemies hypothesis” (Williams 1954; Elton 1958;
Crawley 1987, 1997; Mack et al. 2000; Maron and Vilà
2001; Levine et al. 2002) and a recent expansion of the
natural enemies hypothesis, “the evolution of increased
competitive ability” (EICA; Blossey and Nötzold 1995;
Müller-Schärer et al. 2004).
The natural enemies hypothesis attributes exotic plant
success to the fact that upon introduction many exotics
are liberated from their specialist herbivores and
pathogens. Exotics are thought to gain a substantial
advantage because their populations are no longer
directly suppressed by specialist consumers and
pathogens, and because they obtain a competitive advan-
CONCEPTS AND QUESTIONS
Novel weapons: invasive success and the
evolution of increased competitive ability
Ragan M Callaway and Wendy M Ridenour
When introduced to new habitats by humans, some plant species become much more dominant. This is
primarily attributed to escape from specialist consumers. Release from these specialist enemies is also
thought by some to lead to the evolution of increased competitive ability, driven by a decrease in the
plant’s resource allocation to consumer defense and an increase in allocation to size or fecundity. Here, we
discuss a new theory for invasive success – the “novel weapons hypothesis”. We propose that some invaders
transform because they possess novel biochemical weapons that function as unusually powerful allelo-
pathic agents, or as mediators of new plant–soil microbial interactions. Root exudates that are relatively
ineffective against their natural neighbors because of adaptation, may be highly inhibitory to newly
encountered plants in invaded communities. In other words, the novel weapons of some plant invaders
provide them with an advantage that may arise from differences in the regional coevolutionary trajecto-
ries of plant communities. Furthermore, the selective advantage of possessing a novel weapon may result
in rapid evolution of that weapon – for example, the production of greater quantities of allelopathic or
antimicrobial root exudates. Direct selection of competitive traits provides an alternative to the “grow ver-
sus defend” trade-offs that underpin the theory of the evolution of increased competitive ability.
Front Ecol Environ 2004; 2(8): 436–443
Division of Biological Sciences, The University of Montana, Missoula,
MT 59812 (ray.callaway@mso.umt.edu)
In a nutshell:
• The success of some exotic invasive plant species may be due to
the possession of “novel weapons”, biochemicals that native
species have never encountered
• The novel weapons hypothesis raises the possibility of coevolu-
tion among plants in different regions of the Earth, and that
mixing species from different regions increases the chances of
disrupting the ecological processes that lead to species coexis-
tence and greater community diversity
• Novel weapons suggest an alternative mechanism for the evo-
lution of increased competitive ability in invasive plants. If
invaders possess allelochemical weapons that provide greater
competitive advantages in their new habitats than in their
original ranges, then selection may act directly on those traits.
We call this the “allelopathic advantage against resident
species” hypothesis or “AARS”
RM Callaway and WM Ridenour Novel weapons
437
© The Ecological Society of America www.frontiersinecology.org
tage over natives that may suffer disproportion-
ately from attacks by these native enemies.
The EICA hypothesis argues that exotics long
liberated from their native specialist enemies
should lose costly traits that helped them resist
those enemies. By evolving to allocate less
resources to traits that conferred resistance to
their specialist enemies, which are absent in the
introduced range, exotics can use more
resources for traits that provide greater compet-
itive advantage, such as size or fecundity.
Although the EICA hypothesis refers only to
competitive ability, it was explicitly developed
in the context of the “grow or defend” paradigm
of allocation trade-offs (Herms and Matson
1992) and therefore reference to EICA implic-
itly attributes increased competitive ability to
such trade-offs. The novel weapons hypothesis,
described in detail below, addresses both inva-
sive success and the evolution of increased com-
petitive ability.
Convincing evidence exists for the natural
enemies hypothesis as an explanation of some
successful exotic invasions (Wolfe 2002;
Mitchell and Power 2003; Reinhart et al. 2003;
Siemann and Rogers 2003; Callaway et al. 2004;
DeWalt et al. 2004; Jakobs et al. 2004), but there are
reasons to be hesitant about accepting enemy release as
the only reason for invasive success. First, there is evi-
dence that the effects of natural enemies are weak on
some invaders (Callaway et al. 1999; Ridenour and
Callaway 2003; Lesica and Hanna 2004; Maron and
Vilá 2001). Also, consumer effects can be similar in
native and introduced ranges, (Beckstead and Parker
2003; Maron and Vilá 2001; Reinhart and Callaway in
press), and in some habitats natives and exotics appear
to receive similar amounts of damage (Agrawal and
Kotanen 2003). Second, the literature on
consumer–plant interactions in natural systems suggests
that the relative impact of consumers is often minimal
(Crawley 1989). Finally, little is known about the com-
parative effects of herbivores or pathogens on invasive
plants in their native ranges versus their invaded ranges
(see DeWalt et al. 2004 for an exception), and virtually
nothing is known about the relative effects of con-
sumers on the population ecology of invaders in native
versus invaded ranges.
There is evidence for EICA (Daehler and Strong
1997; Willis and Blossey 1999; Siemann and Rogers
2001; 2003a,b; Leger and Rice 2003) and against it
(Willis et al. 2000; Vilá et al. 2003; van Kleunen and
Schmid 2003; Bossdorf et al. 2004; Maron et al. 2004).
Although some invaders have been shown to be either
larger or more fecund than similar species back in their
native ranges, these studies have not shown that size
confers greater competitive ability. Furthermore, no
studies have explicitly linked greater size to the reallo-
cation of resources or energy from defense against spe-
cialist herbivores to competitive ability.
Biochemical novel weapons
The role of consumer interactions in plant invasions must
be crucial, but interactions between plants as determi-
nants of invasive success have been overlooked. The
novel weapons hypothesis that we propose holds that
some exotics transform from native weaklings to invasive
bullies by exuding biochemicals that are highly inhibitory
(allelopathic) to plants or soil microbes in invaded com-
munities, but relatively ineffective against natural neigh-
bors that had adapted over time (Rabotnov 1982; Mallik
and Pellisier 2000). Like the “guns, germs, and steel” used
by human European invaders against indigenous peoples
(Diamond 1997), the possession of novel weapons by
some plant invaders provides them with an advantage that
arises from regional differences in coevolutionary trajecto-
ries (Thompson 1999). To be precise, the definition of
novel weapons here is limited to biochemicals released
from invasive plants that affect native plants or the native
soil biota, and with which native plants interact. For
example, invasive plants may release biochemicals that
alter the soil biota in ways that disadvantage native plants.
One manifestation of different regional evolutionary
trajectories may be the huge number of different bio-
chemicals produced by plants. So far, a compositionally
diverse array of over 100 000 different low-molecular-
mass natural products has been identified, many of which
appear to be species-specific (Bais et al. 2002, 2003; Flores
1999). Far more are likely to be discovered. This rich
diversity is probably due to selection pressures for many
Figure 1. A Mongol warrior wielding the recurve bow.
Illustration by WM Ridenour
Novel weapons RM Callaway and WM Ridenour
different jobs, including soil nutrient acquisition, defense
against herbivory, root communication, and antimicro-
bial protection. Alternatively, many biochemicals may be
metabolic byproducts without particular functions. As
described below for the examples of Centaurea maculosa,
Centaurea diffusa, and Picea-Vaccinum communities, there
is no reason to think that novel weapons must have orig-
inally evolved for the purpose of poisoning other plants.
There may be good reason, however, to think that bio-
chemicals, once evolved, can affect other plants, that
other plants or microbes may evolve to tolerate the
chemicals exuded by their neighbors, and that possession
of novel weapons may lead to their proliferation.
The novel weapons hypothesis does have some strikes
against it. First, little unambiguous evidence for it exists –
what is known is presented below. Second, the allelo-
pathic mechanisms on which the hypothesis partially
rests have a murky history (Callaway 2002), and allelopa-
thy has been dismissed, perhaps unfairly, by many in plant
community theory in favor of resource-driven interac-
tions. On the other hand, biogeographic studies of allelo-
pathic effects of invasive plants in natural and invaded
communities may provide a new line of evidence for the
role of allelopathy in community theory (Baldwin 2003;
Fitter 2003). Finally, the notion that plant communities
consist, even to a small extent, of species adapted to each
other’s rhizosphere biochemistry is unsettling to people
raised on Whittaker’s (1951) ideas about individualistic
plant communities. Nevertheless, recent evidence sug-
gests that geographic coevolutionary trajectories
(Thompson 1999) based on unique biochemistry may
affect plant coexistence and the development of commu-
nities; disruption of these trajectories by invaders may
therefore have profound consequences (see also Callaway
and Hierro in press; Callaway et al. in press).
438
www.frontiersinecology.org © The Ecological Society of America
Diffuse knapweed (Centaurea diffusa), a
relatively minor member of a diverse genus,
occurs naturally across Europe and Asia.
Although capable of high densities immedi-
ately after agricultural disturbance in native
systems, it is rarely as abundant, widespread,
and dominant in its natural geographic
range as it is in the western North American
communities it has invaded (RM Callaway
pers obs). While working in the foothills of
the Caucasus Mountains, Callaway and
Aschehoug (2000) observed that many of
the genera outcompeted by C diffusa in
North America appeared to coexist in rela-
tive peace with C diffusa in their native
range (Figure 3). It did not seem likely that
C diffusa would possess some profound com-
petitive advantage for resources over North
American species, yet not have similar
advantages over species that were similar in
size and phylogeny in the Caucasus. To test
this, Callaway and Aschehoug collected
seeds of C diffusa and several coexisting grass species in the
Caucasus. They then grew the Caucasian species and
related North American species in competition with the
Caucasian C diffusa. Most importantly, they included
treatments in which these competing species were grown
in sand mixed with a small amount of activated carbon, a
compound that absorbs organic molecules and has been
used in previous experiments to ameliorate the allelo-
pathic effects of root exudates of Centaurea maculosa and
other species (Mahall and Callaway 1992; Ridenour and
Callaway 2001).
They found that C diffusa suppressed the growth of
North American species by about 70% more than it sup-
pressed the growth of Caucasian species. Furthermore,
activated carbon sharply reduced the inhibitory effect of
C diffusa on the North American plants, but not its effect
on the Caucasian plants. The story is more complicated,
however, as C diffusa strongly suppressed the ability of
North American species to acquire phosphorus-32 (
32
P; a
radioactive isotope of phosphorus), but had no influence
on the Caucasian species in this regard. The effect on the
North American plants was not altered by the presence of
activated carbon. The reason for this difference is not
known; it is possible, however, that activated carbon
interfered with the phosphorus-chelating properties of C
diffusa’s root exudates (see below) as well as their toxic
properties, and allelo-tolerant Eurasian grasses suffered
from the adsorption of their neighbor’s P-chelating root
exudates.
Providing more mechanistic detail, Vivanco et al.
(2004) identified a chemical in the root exudates of C dif-
fusa, 8-hydroxyquinoline, which had not previously been
reported as a natural product and which has strong metal-
chelating properties. Although they have similar effects,
8-hydroxyquinoline is not related to (±)-catechin. They
Figure 2. An invasive monoculture of kudzu (Pueraria montana) in the
southeastern US. As with many exotic invasive plants, kudzu causes much more
damage in its invasive range than in its native range.
Courtesy of J Anthony
RM Callaway and WM Ridenour Novel weapons
439
© The Ecological Society of America www.frontiersinecology.org
also found that experimental commu-
nities built from North American
grass species were far more susceptible
to invasion by C diffusa than commu-
nities built from Eurasian species,
regardless of the biogeographical ori-
gin of the soil biota. These results cor-
respond well with those of Callaway
and Aschehoug (2000). In addition,
8-hydroxyquinoline applied to plants
growing in field soils in pots sup-
pressed the growth of North
American species about 30% more
than it did the growth of Caucasian
species. Considered as a package, the
results of Callaway and Aschehoug
(2000) and Vivanco et al. (2004) raise
the possibility that Eurasian plants
have evolved tolerance to the root
exudates of C diffusa and a particular
chemical constituent of C diffusa’s
root exudates, while North American
plants have not. This suggests the pos-
sibility of evolved compatibility
among plants within natural commu-
nities, and that the disruption of this
compatibility can destroy these com-
munities.
Mallik and Pellissier (2000) con-
ducted experiments comparing the
effects of leaves, leaf extracts, and
humus from Vaccinium myrtillis, a wide-
spread understory shrub in coniferous
forests of Eurasia that has strong allelo-
pathic effects, on an exotic North
American neighbor, Picea mariana, and
on a long-term native neighbor, Picea
abies. They found that V myrtillus gen-
erally had stronger biochemical effects
on the exotic plant than on the native
one. Their results also support the idea of a coevolutionary
aspect to allelopathy (Rabotnov 1982).
Similar evidence exists for a plant in the same genus as
C diffusa, the even nastier invader C maculosa. Probably
introduced with alfalfa seed from Europe, it now occupies
over 7 million acres of the US (http://www.fs.fed.us/data
base/feis/plants/forb/cenmac/all.html; Figure 4). Like C
diffusa, C maculosa is not a dominant, or even common,
species in Europe. In the US, C maculosa has been the
target of an aggressive biological control effort, with 13
species of insects introduced to control the weed. So far,
biocontrol has not been successful (Müller-Schärer and
Schroeder 1993; Pearson and Callaway 2003), suggesting
that the lack of specialist insect herbivores is a minor
component of its invasive success. In fact, specialist bio-
control root herbivory may stimulate the growth and
competitive ability of C maculosa (Callaway et al. 1999;
Ridenour and Callaway 2003), an odd phenomenon that
may be due to the effects of herbivory on the exudation of
allelochemicals into the rhizosphere (GC Thelen and
RM Callaway unpublished).
By integrating ecological, physiological, biochemical
signal transduction, and genomic approaches to the root
exudates of C maculosa, Bais et al. (2003) were able to iso-
late (
-)-catechin, a chemical that has phytotoxic proper-
ties and is produced by C maculosa roots. Although unre-
lated chemically to 8-hydroxyquinoline, and not as rare
in natural systems, (
-)-catechin has been found in only a
few plant species. Further supporting the novel weapons
hypothesis, the germination and growth of European
grasses were more resistant to (
-)-catechin than were the
germination and growth of naïve North American plants
of the same genus.
Using a biogeographic approach similar to that of
Figure 3. (a) Palouse prairie in eastern Oregon; (b) prairie south of the Caucasus in
the eastern part of the Republic of Georgia. The regions share many genera which are
similar in size and morphology. Centaurea diffusa is native to the Caucasus region and
invasive in the Palouse and intermountain prairies of North America.
(a)
(b)
