Journal of Ecology 2009, 97, 385–392
doi: 10.1111/j.1365-2745.2009.01483.x
Release from foliar and floral fungal pathogen species
does not explain the geographic spread of naturalized
North American plants in Europe
Blackwell Publishing Ltd
Mark van Kleunen* and Markus Fischer
Institute of Plant Sciences, University of Bern, Altenbergrain 21, CH-3013 Bern, Switzerland
Summary
1. During the last centuries many alien species have established and spread in new regions, where
some of them cause large ecological and economic problems. As one of the main explanations of the
spread of alien species, the enemy-release hypothesis is widely accepted and frequently serves
as justification for biological control.
2. We used a global fungus–plant host distribution data set for 140 North American plant species
naturalized in Europe to test whether alien plants are generally released from foliar and floral
pathogens, whether they are mainly released from pathogens that are rare in the native range, and
whether geographic spread of the North American plant species in Europe is associated with release
from fungal pathogens.
3. We show that the 140 North American plant species naturalized in Europe were released from
58% of their foliar and floral fungal pathogen species. However, when we also consider fungal
pathogens of the native North American host range that in Europe so far have only been reported
on other plant species, the estimated release is reduced to 10.3%. Moreover, in Europe North American
plants have mainly escaped their rare, pathogens, of which the impact is restricted to few populations.
Most importantly and directly opposing the enemy-release hypothesis, geographic spread of the
alien plants in Europe was negatively associated with their release from fungal pathogens.
4. Synthesis. North American plants may have escaped particular fungal species that control them
in their native range, but based on total loads of fungal species, release from foliar and floral fungal
pathogens does not explain the geographic spread of North American plant species in Europe. To
test whether enemy release is the major driver of plant invasiveness, we urgently require more studies
comparing release of invasive and non-invasive alien species from enemies of different guilds, and
studies that assess the actual impact of the enemies.
Key-words: biological invasions, enemies, fungal pathogens, invasiveness, mildews, plant invasions, rust fungi, smut fungi
Introduction
During the last centuries many alien species have successfully
established and spread in new regions, where some of them
cause large ecological and economic problems (Nentwig
2007). An explanation for the success of these alien species
has been offered by the enemy-release hypothesis (Elton 1958;
Crawley 1987), which postulates that successful alien species
have a fitness advantage over species native to the new
region because alien species have been fully or partly released
from their natural enemies, including herbivores and
pathogens.
*Correspondence author. E-mail: [email protected]
The enemy-release hypothesis is now one of the most prominent hypotheses in invasion biology (Hierro et al. 2005;
Inderjit et al. 2005) and is frequently used as one of the main
justifications for classical biological control programs
(Mitchell & Power 2003; Hajek 2004). Although most of these
programs have failed (Babendreier 2007), the few that have
been successful have frequently been regarded as evidence
supporting the enemy-release hypothesis (Crawley 1987; but
see Keane & Crawley 2002). To date, the strongest support for
the enemy-release hypothesis comes from biogeographical
studies that compare infestation or damage by enemies
between native and invasive populations of the same species
(Colautti et al. 2004; Liu & Stiling 2006). Most of these studies,
however, included only widespread invasive alien plant species
© 2009 The Authors. Journal compilation © 2009 British Ecological Society
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M. van Kleunen & M. Fischer
and no non-successful alien species. The latter are, however,
also likely to be released from natural enemies, and therefore,
it remains largely unknown whether the establishment success
and spread of alien species is associated with release from
enemies.
There are two notable exceptions to the general lack of tests
of the actual association between enemy release and invasiveness or spread of alien plant species. Cappuccino and Carpenter
(2005) assessed damage by herbivores for nine invasive and
nine non-invasive alien plant species in Ontario and found the
invasive ones significantly less damaged than the non-invasive
species. These results are in line with the enemy-release
hypothesis. However, the limited number of species studied
and the lacking assessment of plant damage by herbivores in
the native range of the species precludes generalizations on
release from herbivores.
In another inspiring study, Mitchell and Power (2003)
tested the release from viral pathogens and from foliar and
floral fungal pathogens of 473 European plant species that
have established (i.e. have become naturalized) in North
America. By using a global fungus–host plant distribution
data base, these authors showed that, on average, 84% fewer
fungal species infect a plant species in its naturalized North
American range than in its native European range. Such a
large degree of release from pathogenic fungi is surprising
because spores of pathogenic fungi might easily be imported
accidentally with plant material (Hulme et al. 2008). Moreover,
spores of some fungal pathogens might cover huge – even
transatlantic – distances by wind currents (Bowden et al.
1971; Nagarajan & Singh 1990). Mitchell and Power (2003)
also showed that among the 45 declared noxious weeds (i.e.
primarily species with a negative impact on agriculture) and
among the 92 declared invasive plant species in their data set,
the proportion of United States in which a species was
declared noxious and the proportion of United States in which a
species was declared invasive were positively associated with
the release from fungal pathogens. As a consequence, this
study is the most widely cited empirical study in support of the
enemy-release hypothesis, and has considerably contributed
to general acceptance of enemy release as a key determinant
of the spread of alien plants. However, it is not known whether
these results can be generalized to target regions other than
North America.
The results apparently supporting the enemy-release
hypothesis deserve a careful closer look (Colautti et al. 2004).
The reported high rate of release of European plants from
fungal pathogens in North America might simply reflect an
overall higher sampling effort in Europe than in North America
due to a higher density of mycologists and a longer history of
mycology in Europe. Moreover, because alien plants are
relatively new to the invaded habitat, one cannot exclude the
possibility that mycologists have under-sampled alien compared to native species. This would imply that alien plant
species might have accumulated more pathogens than we are
currently aware of. Furthermore, the positive associations of
noxiousness and invasiveness with release from fungal pathogens (Mitchell & Power 2003) were only found when the
non-noxious and non-invasive alien species were excluded
from the data set. Noxious weeds were, however, not released
from more fungal pathogens than non-noxious species
(Mitchell & Power 2003), suggesting that fungal pathogen
release might not be the major determinant of noxiousness
and invasiveness of alien plants. Finally, even if alien plants
have escaped some of their fungal pathogens, it is likely that
they have mainly escaped the pathogens that are rare in their
native range. Although rare pathogens might be highly virulent
in local populations, it is unclear to what extent the loss of rare
enemies will result in an effective release from damage for
their host (Colautti et al. 2004). For these reasons the role of
release from fungal pathogens as a cause of plant invasiveness
might have been overestimated.
Here we analyse fungus–host plant distribution data for
140 North American plant species reported as established in
Europe. This allows us to test whether the results reported by
Mitchell and Power (2003) for European plants naturalized in
North America are of a more general nature, and to take
potential biases into account. In particular, we accounted for
potential bias due to differences in sampling effort between
Europe and North America by adding to the European fungal
pathogens of a host, the ones of its native North American
range that have been reported in Europe but so far only on
other plant species. Furthermore, we accounted for size of the
native distribution of the host species, which is likely to be
positively associated with the number of pathogens (Mitchell
& Power 2003), and for minimal residence time of the host
plant in Europe, which is likely to be positively associated
with geographic range size of the host plant (Pysek & Jarosik
2005). We addressed the following specific questions: (i) Are
North American plant species released from their floral and
foliar fungal pathogen species in Europe? (ii) Are North
American plant species mainly released from their rare
pathogen species? (iii) Is geographic spread of the North
American plant species in Europe associated with their
release from fungal pathogen species?
Methods
DATA COLLECTION
In our analysis, we included all 140 plant species that are naturalized
(i.e. have established wild populations) in Germany (i.e. Central
Europe) according to the BioFlor data base (www.ufz.de/biolflor/
index.jsp; Klotz et al. 2002) and are native to (i.e. originate from)
North America according to the USDA Plants data base (http://
plants.usda.gov). We restricted our study to the species of the
BiolFlor data base, because these species share broadly similar
climatic preferences, and because for most of the exotic species in this
data base the minimum residence time is known. Like Mitchell and
Power (2003), we used the USDA Fungus–Host Distribution data
base (http://nt.ars-grin.gov/fungaldatabases/fungushost/fungushost.cfm)
to assess the number of foliar and floral fungal pathogens reported
on each of the 140 plant species and the number of records of each
fungus–host plant combination in North America and in Europe.
The fungal pathogens included rust (Basidiomycota-rusts) and smut
(Basidiomycota-smuts) fungi and powdery (Erysiphales), downy
© 2009 The Authors. Journal compilation © 2009 British Ecological Society, Journal of Ecology, 97, 385–392
Release of alien plants from fungal pathogens 387
(Peronosporales) and black (Meliolales) mildews. Because the USDA
Fungus–Host Distribution data base does not include data from two
authoritative compilations of Central European (Gaumann 1959)
and British (Wilson & Henderson 1966) rusts, we also added data for
rust pathogens observed on the 140 host plants from these two
compilations (also see Mitchell & Power 2003).
For each of the plant species, as a measure of geographic spread,
we assessed the number of European geographic regions in which
the species is established from the recently completed DAISIE data
base (www.europe-aliens.org/; Lambdon et al. 2008). The number of
geographic regions is a crude estimate of the naturalized range
size of a species, because it does not account for the local abundance
of species. However, in our data set the number of European
geographic regions occupied by a species correlates positively
(Spearman’s ρ = 0.693, n = 140, P < 0.001) with the number of 10′
longitude × 6′ latitude grid cells the species occupies in Germany
(www.floraweb.de). This indicates that our measure of geographic
spread is robust.
As a measure of native range size, we included the number of
continental United States and Canadian provinces and territories in
which the species occurs from the USDA Plants data base. For 134
of the 140 plant species, we obtained data on minimum residence
time in Europe from the BioFlor data base (Klotz et al. 2002),
and supplemented data for species missing in BioFlor from the
Catalogue of alien plants of the Czech Republic (Py sek et al.
2002), the Nobanis data base (www.nobanis.org/) and the DAISIE
data base.
ANALYSES
Because data on the number of fungal pathogen species per plant
species in North America and Europe were not normally distributed,
we compared them with the nonparametric Wilcoxon’s-signed-rank
test for paired data. To test whether the degree of release differed
between the five groups of fungal pathogens, we used the nonparametric Friedman test for non-independent data. Both nonparametric
tests were done with the statistical software spss, version 15 (SPSS
Inc. 2006).
To test whether North American plant species are more likely to
be released from their rare fungal pathogen species than from their
common fungal pathogen species in Europe, we used logistic regression
as implemented in the statistical software Genstat, 9th edition
(Payne et al. 2005). In this analysis, the binomial response variable
was the European presence (yes, no) of each fungal pathogen that
had been recorded on the host in North America, and the independent
variable was the number of records of each of these fungus–host
plant combinations in North America. Because each host plant may
have more than one associated fungal pathogen, we corrected for
this non-independence by including ‘host species’ as a random
factor in the analysis.
To test whether the release from fungal pathogens is associated
with the geographic spread of the North American plants in Europe,
we also used logistic regression. In this analysis, the response variable
was the number of European regions in which the species has established naturalized populations. To analyse the number of regions as
a binomial variable in the logistic regression, we set the binomial
total to 52, which equals the number of geographic regions covered
by the DAISIE data base for terrestrial plants (i.e. effectively, for
each plant species we had presence-absence data for 52 regions, and
the results apply to the proportion of European regions in which a
plant species has established). The main independent variable of
interest was the difference in the number of fungal pathogens on a
plant species between North America and Europe (i.e. the absolute
release from fungal pathogens). Additionally, to correct at least partly
for a potential under-sampling of the alien species, we analysed our
estimate of minimum release from fungal pathogens in which we also
considered those fungal pathogens of the native North American
host range that in Europe so far have only been reported on other
plant species. To correct in both analyses for the number of fungal
pathogens recorded on a plant species in North America, we
included that number in the model before the absolute release from
fungal pathogens. To assess whether the association between geographical spread and pathogen release is robust, we performed
additional analyses in which we corrected for several variables that
might affect geographical spread of the North American host plants
in Europe. Because the number of fungal pathogens found on a species
in North America may depend on the species’ range size there (Clay
1995), and because plants with a large native range size might have
been more frequently introduced to Europe (i.e. have a higher propagule pressure; Pysek et al. 2004), we included the logarithm of the
number of continental United States and Canadian provinces and
territories in which the host plant occurs as a covariate in the model.
It has been suggested that only species that perform better in their
naturalized than in their native range should be considered invasive
(Hufbauer & Torchin 2007). Therefore, an additional benefit of
correcting spread in the naturalized range for spread in the native
range is that our analysis conforms to this definition of invasiveness.
Furthermore, because the size of the naturalized range may increase
with time since introduction and might depend on the taxonomic
affinity of species, we included the logarithm of minimum residence
time as a covariate and taxonomic subclass as a factor, respectively,
in the model.
To assess whether net effects of release were mainly due to the
escape from North American fungal pathogens or the gain of new
European fungal pathogens, we also ran logistic regressions analysing
escape from North American pathogens and gain of new European
pathogens separately.
Results
On average, 58.0% fewer fungal pathogen species were
recorded for the 140 North American plant species in their
naturalized European range than in their native North American range (Fig. 1a; Wilcoxon’s-signed-rank test: Z = –6.634,
n = 140, P < 0.001). The release of North American plants
was significantly different between the five groups of fungal
pathogen species (Friedman test: χ24 = 70.91, P < 0.001).
North American plants were significantly released from smut
fungi (–85.9%; Wilcoxon’s-signed-rank test: Z = –5.978,
n = 140, P < 0.001), rust fungi (–72.0%; Z = –4.131, n = 140,
P < 0.001) and downy mildews (–75.4%; Z = –4.548, n = 140,
P < 0.001), but there was no significant release from powdery
mildews (+3.1%; Z = –0.125, n = 140, P = 0.901; Fig. S1 in
Supporting Information). Black mildews were only recorded
in North America, but only on three of the 140 species, and as
a consequence the release from black mildews was not significant (Z = −1.342, n = 140, P = 0.180; Fig. S1).
When we considered the estimate of minimum pathogen
release rather than the reported release by adding to the
European fungal pathogens of a host, the ones of its native
North American range that have been reported in Europe, but
so far only on other plant species, the average release from
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388
M. van Kleunen & M. Fischer
Fig. 2. In Europe, North American plant species are mainly released
from their rare fungal pathogen species. Each dot indicates the
estimated likelihood of the presence of the fungus on its host in
Europe, presented as an adjusted proportion value. These values
deviate from the original binomial proportions 0 (not present) and 1
(present), because they have been adjusted for host identity. The line
is the fitted relationship from the logistic regression.
Fig. 1. Release of North American plant species from fungal
pathogens in Europe. (a) In Europe, North American plant species
appear to be strongly released from fungal pathogen species based on
actually recorded fungus–host plant combinations. (b) Release from
pathogens appears much smaller when in addition to the fungal
pathogens recorded on a North American host in Europe, we added
those of its native range that have been reported in the naturalized
range, but so far only on other plant species. The size of the bubbles
is proportional to the number of species with that combination of
numbers of fungal pathogen species in North America and Europe.
The bold lines are the fitted relationships from regression and are
shown as illustration of fungal pathogen release. Release from fungal
pathogens is apparent as the fitted lines are below the bisecting lines
indicating identical numbers of fungal pathogens in North America
and Europe.
fungal pathogens decreased to 10.3% (Fig. 1b; Z = –2.039,
n = 140, P = 0.041). The release of North American plants
was still significantly different between the five groups of
2
fungal pathogens (Friedman test: x 4 = 99.96 , P < 0.001).
These analyses yielded a smaller, but still significant, release
from smut fungi (−30.6%; Z = −4.565, n = 140, P < 0.001)
and rust fungi (–39.1%; Z = −2.004, n = 140, P = 0.045;
Fig. S1). The release from black mildews did not change,
but there was no significant release from downy mildews
anymore (–8.2%; Z = −1.387, n = 140, P = 0.166; Fig. S1).
Moreover, there was even a significant gain in powdery
mildews (+73.4%; Z = −5.417, n = 140, P < 0.001; Fig. S1).
This indicates that despite a significant, but small, release of
North American plant species from fungal pathogens in
Europe, enemy-release does not apply to all types of fungal
pathogens, and that there is potentially an enemy-gain of
some types of fungal pathogens.
North American plants naturalized in Europe were on
average much more released from their rare fungal pathogens,
that is, from pathogens with lower numbers of records on the
host in North America, than from their more common fungal
pathogens (Fig. 2; quasi-F1,474 = 4.35, P = 0.038). This might
imply that the release from fungal pathogens might have little
impact on the range dynamics of the host species.
Geographic spread of the North American plant species,
measured as the proportion of European regions in which
they have established naturalized populations, was significantly negatively associated with fungal pathogen release
(quasi-F1,131 = 8.40, P = 0.004), after correction for the
number of fungal pathogens recorded on a plant species in
North America (quasi-F1,131 = 3.74, P = 0.055). The negative
association between geographic spread and fungal pathogen
release remained significant (Fig. 3a; quasi-F1,120 = 6.89,
P = 0.010) after correction for the positive effects of size of
native range (quasi-F1,120 = 23.12, P < 0.001) and minimum
residence time (quasi-F1,120 = 20.07, P < 0.001) on size of
the naturalized range and for plant taxonomic subclass
(quasi-F9,120 = 1.88, P = 0.061).
© 2009 The Authors. Journal compilation © 2009 British Ecological Society, Journal of Ecology, 97, 385–392
Release of alien plants from fungal pathogens 389
Fig. 3. European geographic spread of North American plant species is negatively correlated with release from fungal pathogens. (a) Release
based on actually recorded number of fungal species on host species in North America and Europe. (b) Similar to (a), but with those pathogen
species added to the European fungal pathogens of a host, which have been recorded on the host in its native range and also have been recorded
in the naturalized range, but so far only on other plant species. Proportions of European regions in which the plant species have established have
been adjusted for taxonomic plant subclass, size of the native range, minimum residence time and number of fungal pathogen species recorded
on the host in North America. The lines are the fitted relationships from logistic regressions.
Net release from fungal pathogens is composed of the
escape from North American fungal pathogens and the
accumulation of new European fungal pathogens. Geographic
spread of the North American plant species in Europe was
not significantly associated with escape from North American
fungal pathogens (Fig. S2a; quasi-F1,120 = 1.84, P = 0.177),
whereas it was positively associated with the gain of new
European fungal pathogens (Fig. S2b; quasi-F1,120 = 7.22,
P = 0.008). This indicates that the negative association between spread and fungal pathogen release of North American
plant species in Europe was mainly driven by the gain of new
pathogens in Europe.
When we considered the estimate of minimum enemy
release rather than the reported release by adding to the
European fungal pathogens of a host, the ones of its native
range that have been reported in the naturalized range, but so
far only on other plant species, the negative association
remained (Fig. 3b; quasi-F1,120 = 10.59, P = 0.001). Moreover,
also when we restricted the analysis to the 69 North American
species that are categorized as natural-area invaders in
Europe (so-called agriophytes; Klotz et al. 2002), the negative
association between geographic spread and release from
fungal pathogens remained significant (quasi-F1,56 = 10.91,
P = 0.002). These results indicate that, based on total loads of
fungal species, release of North American plant species from
fungal pathogens in Europe does not explain geographic
spread of these plant species.
Discussion
RELEASE FROM FUNGAL PATHOGENS
On average, 58.0% fewer fungal pathogen species were recorded
on the 140 plant species in their naturalized, European, range
than in their native, North American, range. Although this
indicates a large release from fungal pathogens of North
American plants in Europe, it is considerably smaller than the
reported release of 84% fewer fungal pathogen species on
European plant species in North America (Mitchell & Power
2003). Possibly, this difference in the rate of release from fungal
pathogens reflects a higher sampling intensity in Europe
compared to North America rather than a true biological
pattern. In an additional analysis for 122 species that have
established in both Europe and North America but originate
from other continents, we found that, on average, 54.2% more
fungal pathogen species were reported on each of these
species in Europe than in North America. This suggests that
there is a sampling bias between North America and Europe.
When we correct the 84% release reported by Mitchell &
Power (2003) for this sampling bias, the actual release is
reduced to 75%.
Despite the apparently higher sampling intensity in
Europe, the observed release of North American plant species
from fungal pathogen species in Europe could also be due to
a general sampling bias against alien compared to native
plant species. In other words, some of a host’s fungal pathogen
species might be present in the naturalized range but might
simply not have been reported for the host species yet
(Colautti et al. 2004). Indeed, when we additionally considered
fungal pathogen species of the native, North American, host
range that in Europe so far have only been reported on other
plant species, the average release from fungal pathogens
decreased to 10.3%. Even if some of these fungal pathogen
species that occur in the hosts’ native ranges do truly not
occur on the hosts in Europe yet, it is likely that the hosts will
encounter them in the future, and thus that enemy release will
decay over time.
The primary assumption of the enemy-release hypothesis is
that alien organisms are released from their enemies. However,
the rate of release might depend on the nature of the enemies,
in particular on their degree of host specialization (MüllerSchärer et al. 2004). While there was a significant release from
smut and rust fungi, there was no significant release from
downy mildews, and even a potential gain in powdery mildews
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M. van Kleunen & M. Fischer
(Fig. S1). It is notoriously difficult to classify organisms as
specialists or generalists (Novotny et al. 2002), and particularly
so for pathogens that may be associated with several hosts
(implying that they are generalists), but have a high host
specificity for some of their life cycle stages (Callan & Carris
2004). Nevertheless, the potential gain in powdery mildews is
probably due to the more generalized nature of powdery
mildews compared to the other groups of pathogenic fungi in
our analyses (Callan & Carris 2004). Our results for enemy
release from different groups of fungal pathogens clearly show
that despite an overall release from enemies, enemy-release
does not apply to all types of enemies.
In addition to foliar and floral fungal pathogens, plants are
affected by many other guilds of enemies, such as soil pathogens,
nematodes, bacteria, viruses and herbivores that might control
plant range dynamics. Mitchell & Power (2003) showed that
European plant species have also been released from viruses
in North America but to a lesser extent than from fungal
pathogens. Unfortunately, there are no large enemy–host
plant distribution data sets available for most of the other
guilds of enemies. Empirical studies on single or small groups
of invasive plants frequently revealed plant release from these
other guilds of enemies (herbivores and fungal pathogens:
Wolfe 2002; DeWalt et al. 2004; soil pathogens: Reinhart
et al. 2003; also see overviews in Colautti et al. 2004 and Liu
& Stiling 2006). However, it would be premature to generalize
from such a limited number of species, and because these
studies only include invasive species, they do not provide
insight into whether the degree of invasiveness or spread is
related to enemy release.
Another approach to test the enemy-release hypothesis is to
compare richness of enemies or damage by enemies between
invasive and native plant species. Carpenter and Cappuccino
(2005) found that the average damage by herbivores was
larger on 30 native species than on 39 exotic species in
Ontario. Van Grunsven et al. (2007) found that there was a
smaller negative plant–soil feedback for three exotic species
compared to three native species in the Netherlands. However, a
comparative study between 30 taxonomically paired native
and exotic plants in Ontario showed that escape generally was
inconsistent among different guilds of enemies (Agrawal
et al. 2005). Therefore, it remains open whether, averaged
over all possible enemies, enemy-release is a major driver of
plant invasiveness. Another open question is whether effects
of release from different enemies might interact. Such interactions are likely because infection with pathogens might
make some plant species less (Rayamajhi et al. 2006) or more
(Ericson & Wennstrom 1997) attractive to herbivores and
vice versa.
Although many studies have reported release of alien
plants from enemies, we are aware of only one experimental
study that tested whether invasiveness is driven by enemy
release. Cappuccino and Carpenter (2005) found that damage
by herbivores was lower for nine invasive alien plant species
than for nine non-invasive ones in Ontario. This is a promising
approach and future studies should assess experimentally
how invasiveness is related to the degree of release from other
guilds of enemies such as soil pathogens, nematodes, bacteria,
viruses and foliar and floral fungal pathogens.
DEPENDENCE OF ESCAPE ON RARITY OF THE FUNGAL
PATHOGEN
Fungal pathogens that are rare in the native range of a host
plant might be as virulent as or even more virulent than
widespread pathogens, but the impact of rare pathogens on
population dynamics is more localized and therefore less
likely to drive the range dynamics of the host species in the
native range. In the naturalized range these rare pathogens
might, however, be as important as or even more important
than widespread pathogens in driving the range dynamics
when the naturalized range is still small, while this is less likely
the case when the naturalized range is already large. Therefore, it is unclear whether the release from rare pathogens will
drive range dynamics of the alien plant species (Colautti et al.
2004). We found that North American plant species naturalized
in Europe were on average much more released from their rare
pathogens, that is, from pathogens with lower numbers of
records in North America, than from their more common
pathogens (Fig. 2). Possibly, to some degree this association
might simply reflect that pathogens that are rare in the native
range of a host are also bound to be rare in the non-native
range, and as a consequence are less likely to be detected.
However, the main biological consequence of their rarity in
the native range is a lower chance to be introduced into the
non-native range. Therefore, the detected much higher
release from rare than from common pathogen species
might imply that, overall, the release from fungal pathogens
could have little impact on the range dynamics of the host
species.
GEOGRAPHIC SPREAD OF PLANTS AND RELEASE
FROM FUNGAL PATHOGENS
While we found that, overall, North American plant species
are released from fungal pathogen species in Europe, there
was large variation in the degree of release among the 140
plant species, and some species were associated with even
more fungal pathogen species in Europe than they were in
North America (Fig. 1). Therefore, a test of the enemy-release
hypothesis should not be restricted to only investigating
whether there is a release of alien plants from enemies but also
whether actual invasiveness or geographic spread of the host
species is associated with such enemy release (Mitchell &
Power 2003; Cappuccino & Carpenter 2005). Directly opposing
the predictions of the enemy-release hypothesis, the proportion
of European regions in which a North American plant species
has established naturalized populations – the only available
measure of geographic spread of these plant species in their
new range – was significantly negatively associated with fungal
pathogen release after correction for the number of fungal
pathogens recorded on a plant species in North America.
This is also the opposite result to the positive association
between invasiveness and proportional release from pathogens
© 2009 The Authors. Journal compilation © 2009 British Ecological Society, Journal of Ecology, 97, 385–392
Release of alien plants from fungal pathogens 391
reported for European plants naturalized in North America
(Mitchell & Power 2003). In contrast to Mitchell and Power
(2003), we corrected for taxonomic subclass, minimum residence time and native range size. However, even when we
did not correct for these variables, the negative association
between geographical spread of the North American plants in
Europe and their pathogen release was significant. Moreover,
when we, like Mitchell and Power (2003) did, included in the
analysis proportional pathogen release as the ratio between
number of pathogens in Europe and the number of pathogens
in North America, which biases the data set against plant
species without pathogens in North America, the association
between geographic spread and pathogen release remained
significantly negative (results not shown). Furthermore, when
we, like Mitchell and Power (2003) did, restricted our data set
to naturalized species categorized as natural-area invaders,
the negative association remained significant. Therefore, it is
very unlikely that the contrasting results for European plant
species in North America and North American plant species
in Europe are a consequence of differences in methodology.
The negative association between geographic spread of
North American plants in Europe and pathogen release could
reflect that North American plants with a restricted naturalized
range in Europe are less likely to have encountered their
potential pathogens yet. If this were the case, one would
expect a negative association between size of the naturalized
range and the number of pathogens from the native range that
have so far only been reported in Europe on other plant species.
We, however, did not find such a negative association
(Spearman’s ρ = 0.142, N = 140, P = 0.093; note that the
trend of the non-significant correlation is even positive).
Therefore, also the strength of the negative association
between geographic spread and pathogen release did not
decrease after adding to the European fungal pathogens of a
host, the ones of its native range that have been reported in
Europe but so far only on other plant species (Fig. 3). Thus,
based on total loads of fungal species, release from foliar
and floral fungal pathogens does not explain the geographic
spread of North American plant species in Europe.
One possible explanation for the negative association
between geographic spread of North American plants in
Europe and their release from fungal pathogens is that it
reflects a trade-off between the high expansion capacity of
some species and their ability to defend themselves against
enemies. If species with a high capacity for spread are more
vulnerable, they are likely to accumulate more enemies in the
non-native range. This idea corresponds well with our finding
that the negative association between geographic spread and
release mainly reflects a positive association between spread
and accumulation of new European fungal pathogens. At the
same time this finding indicates that the accumulated new
fungal pathogens hardly influence the geographic spread of
their new host species.
While the negative association between geographic spread
of alien plant species and their release from pathogen species
contradicts the predictions of the enemy-release hypothesis, it
supports some of the opposing hypotheses that have received
hardly any attention in studies on plant invasiveness (Colautti
et al. 2004). The enemy-inversion hypothesis postulates that
natural enemies could have a positive effect on their hosts in
the naturalized range because of interactions with abiotic factors
that differ from the native range or through a restructuring of
multi-species interactions (Pearson et al. 2000; Pearson &
Callaway 2003; Colautti et al. 2004; Parker & Gilbert 2007).
For example, Pearson et al. (2000) found that two flower-head
inhabiting gall flies introduced to North America as biologicalcontrol agents of the invasive Centaurea maculosa became the
main food resource for deer mice that thereby inadvertently
dispersed seeds of C. maculosa. Another hypothesis, the
enemy-of-my-enemy hypothesis, postulates that enemies
co-introduced with an invasive organism may have a larger
impact on competitors in the introduced range than on the
original host itself (Sabelis et al. 2001; Tompkins et al. 2003;
Colautti et al. 2004). For example, the parapox virus that was
introduced into Europe with the grey squirrel from North
America is reducing populations of the European red squirrel
to a larger extent than the populations of the grey squirrel
(Tompkins et al. 2003). Clearly, understanding and counteracting spread of alien plants very urgently requires tests of the
general importance of these currently neglected alternative
hypotheses.
Conclusions
Our results show that North American plants accumulate not
much fewer fungal pathogen species in Europe than in their
native range. Moreover, we show that the North American
plant species are mainly released from their rare pathogens.
Most importantly, we show that geographic spread of the
North American plant species in Europe is negatively instead
of positively associated with the release from fungal pathogens. One obvious limitation of our study is that we assessed
fungal pathogen richness while we could not assess pathogen
virulence. Although it is likely that a large number of fungal
pathogens will include some highly virulent ones, this is not
necessarily the case. Future studies should therefore assess the
impact of fungal pathogens in the native and naturalized
ranges of successful and unsuccessful alien plant species.
Furthermore, our fungus-focused study cannot preclude that
the predictions of the widely accepted enemy-release hypothesis
hold for other guilds of plant enemies. Our results show,
however, that, based on total loads of fungal species, release
from floral and foliar fungal pathogens does not explain
geographic spread of North American plant species in
Europe. To test whether enemy release is the major driver of
spread of alien plant species, we urgently require more studies
comparing release of successful and non-successful alien
species from other guilds of enemies.
Acknowledgements
The authors thank Beatrice Senn-Irlet and Volker Kummer for help with the
fungal pathogen categorization, Erin McCray for data files from the USDA
Fungus-Host-Distribution data base, and Wim van der Putten, Ragan Callaway and two anonymous referees for helpful comments on an earlier version of
© 2009 The Authors. Journal compilation © 2009 British Ecological Society, Journal of Ecology, 97, 385–392
392
M. van Kleunen & M. Fischer
this manuscript. The authors acknowledge funding by the Swiss Science Foundation (Project number 3100A0-117722/1) and the Swiss National Centre of
Competence in Research – Plant Survival.
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Handling Editor: Ray Callaway
Supporting Information
Additional Supporting Information may be found in the
online version of this article:
Fig. S1. Release of North American plants from different
groups of fungi.
Fig. S2. Spread of North American plant species in Europe
in relation to escape from native fungi and accumulation of
new fungi.
Please note: Wiley-Blackwell are not responsible for the
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© 2009 The Authors. Journal compilation © 2009 British Ecological Society, Journal of Ecology, 97, 385–392