Release from foliar and floral fungal pathogen species does not explain the geographic spread of naturalized North American plants in Europe
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 plan t species in Europe is associated wi th 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 inva- sions, 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.
*Correspolldellce author. E-mail: vkleullell@ips.ullibe.ch
The enemy-release hypothesis is now one of the most pro- minent hypotheses in invasion biology (Hierro el al. 2005;
lnderjit el 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 (Colaulli el al. 2004; Liu & Stiling2006). Most of these studies, however, included only widespread invasive alien plant species DOI: 10.1111/j.1365-2745.2009.01483.x
Konstanzer Online-Publikations-System (KOPS) URN: http://nbn-resolving.de/urn:nbn:de:bsz:352-133482
and no non-successful alien species. The latter are, howevet;
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 invasive- ness 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 com- pared 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 path- ogens (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 sizeof 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 el at. 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/fungaldatabaseslfungushost/fungushos1.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 (BasidioI11ycota-rusts) and SI11ut (Basidiomycota-sI11uts) fungi and powdery (Erysiphales), downy
(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 DAISI E data base (www.europe-aliens.org/; Lambdon el 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 p = 0.693,11 = 140, P < 0.001) with the number of 10' longitude x 6' latitude grid cells the species occupies in Germany (www.florawebde).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 el al. 2002), and supplemented data for species missing in BioFlor from the Catalogue of alien plants of the Czech Republic (Pysek el 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 nonpara- metric 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 el 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 estab- lished 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 geo- graphical 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 prop- agule pressure; Pysek el 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 Amer- ican range (Fig. I a; Wilcoxon's-signed-rank test: Z = -6.634, 11
=
140, P < 0.001). The release of North American plants was significantly dilTerent between the five groups of fungal pathogen species (Friedman test: X24 = 70.91, P < 0.00 I).North American plants were significantly released from smut fungi (-85.9%; Wi1coxon'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, 11 = 140, P < 0.001), but there was no significant release from powdery mildews (+3.1%; Z=-O.125, 11= 140, P=0.901; Fig. SI 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 signi- ficant (Z = -1.342, n = 140, P = 0.180; Fig. S I).
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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Fig. I. 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. I b; Z = -2.039,
11= 140, P = 0.041). The release of North American plants was still significantly different between the five groups of fungal pathogens (Friedman test:
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= 99.96, P < 0.001).These analyses yielded a smaller, but still significant, release from smut fungi (-30.6°;(l; Z = -4.565, 11 = 140, P < 0.001) and rust fungi (-39.1%; Z
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Fig. S I). The release from black mildews did not change, but there was no significant release from downy mildews anymore (-8.2%; Z=-1.387, 11= 140, P=0.166; Fig. SI).
Moreover, there was even a significant gain in powdery mildews (+73.4%; Z = -5.417,11 = 140, P < 0.001; Fig. SI).
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-Fl.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 signi- ficantly negatively associated with fungal pathogen release (quasi-Fwi
=
8.40, P=
0.004), after correction for the number of fungal pathogens recorded on a plant species in North America (quasi-FI.IJI = 3.74, P = 0.055). The negative association between geographic spread and fungal pathogen release remained significant (Fig. 3a; quasi-Fl.I2o = 6.89, P=
0.0 I 0) after correction for the positive effects of size of native range (quasi-FI.I2o=
23.12, P < 0.00 I) and minimum residence time (quasi-Fl.I2o = 20.07, P < 0.001) on size of the naturalized range and for plant taxonomic subclass (quasi-F9,12o=
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Recorded release from fungal pathogens Minimum release from fungal pathogens
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 filted 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-Fl.I2o
=
1.84, P=
0.177),whereas it was positively associated with the gain of new European fungal pathogens (Fig. S2b; quasi-Fl.I2o
=
7.22, P = 0.008). This indicates that the negative association be- tween 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-Fl.I2o
=
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-FI.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 red uced 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 plan t 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 (Colauui 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 (Mliller- Scharer el 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
(Fig. S I). 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 ef 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 inter- actions 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. There- fore, it is unclear whether the release from rare pathogens will drive range dynamics of the alien plant species (Colautti e/ 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. I). 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
reported for European plants naturalized in North America (Mitchell & Power 2003). In contrast to Mitchell and Power (2003), we corrected for taxonomic subclass, minimum re- sidence 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 num ber of pathogens in Europe and the num ber 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 p
=
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 fimgal 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 (Colautli
el 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 el al. 2004; Parker & Gilbert 2007).
For example, Pearson el al. (2000) found that two flower-head inhabiting gall flies introduced to North America as biological- control 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 (Sabel is el al. 200 I; Tompkins et al. 2003; Colautti el 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 counter- acting 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 patho- gens. 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 ror help with the rungal pathogen categorization. Erin McCray ror data files rrom the USDA Fungus-I-Iost-Distribution data base. and Wim van der Putten, Ragan Calla- way and two anonymous referees for helpful comments on an earlier version of
Ihis manuscrip!. The aUlhors acknowledge funding by Ihe Swiss Science Foun- dalion (ProjecI number 3100AO-11772211) and Ihe Swiss Nalional Cenlre of Competence in Research -Plant Survival.
References
Agrawal. A.A .. Kolanen. P.M., Milchell. CE., Power, A.G .. Godsoe, W &
Klironomos. 1. (2005) Enemy release? An experimenl wilh congeneric planl pairs and diverse above- and belowground enemies. Ecology. 86. 2979- 2989.
Babendreier. D. (2007) Pros and cons of biological conlrol. Biologicallllvasiolls (ed. W Nenlwig), pp. 403-418. Springer Verlag, Berlin.
Bowden. 1., Gregory, P.H. & Johnson, CG. (1971) Possible wind lranspor! of cofTee leaf rusl across Ihe Allanlic Ocean. Natllre. 229. 500-50 I.
Callan. B.E. & Carris, L.M. (2004) Fungi on living planl subslrala, including fruils. Biodiversity 0/ Fllllgi (eds G.M. Mueller, G.F.. Bills & M.S. Fosler).
pp. 105-126. Elsevier Academic Press. Burlinglon.
Cappuccino. N. & Carpenler, D. (2005) Invasive exolic planls suffer less herbivory Ihan non-invasive exolic plan Is. Biology Lelfers. 1. 435- 438.
Carpenler. D. & Cappuccino. N. (2005) Herbivory, lime since inlroduclion and Ihe invasiveness of exolic planls. JOIIl"llal 0/ Ecology. 93, 315-321.
Clay. K. (1995) Correlales of palhogen species richness in Ihe grass family.
Calladiall JOIIl"llal 0/ BotallY, 73, S42-S49.
Colaulli, R.I., Ricciardi, A., Grigorovich. I.A. & Macisaac. H.1. (2004) Is inva- sion success explained by Ihe enemy release hypolhesis? Ecology Lelfers. 7.
721-733.
Crawley, M.J. (1987) Whal makes a communilY invasible') Colollizatioll.
SlIccessioll alld StabililY (cds A.J. Gray. M.1. Crawley & P.J. Edwards), pp. 429-453. Blackwell Science, Oxford.
DeWall, S.1., Denslow, 1.S. & Ickes, K. (2004) Nalural-enemy release facililales habilal expansion of Ihe invasive Iropical shrub Clidelllia hirta. Ecology. 85.
471-483.
Ellon, CS. (1958) The Ecology 0/ III\'asiolls by Allilllals alld Plallis. Melhuen.
London.
Ericson, L. & Wennslrom, A. (1997) The efTecI of herbivory on Ihe inleraclion between the clonal plant Trielltalis ellrojJaea and its smut fungus UI'OC'yslis trielltalis. Oikos, 80, 107-111.
Gaumann, E.A. (1959) Die Roslpilze Millelellropas lIIil Besollderer Beriichich- tigllllg del' Sch",eiz. Buchdruckerei Biichler. Bern.
Hajek, A. (2004) Natllral Ellelllies - All IlIlrodllctioll 10 Biological COlllrol.
Cambridge UniversilY Press, Cambridge.
H ierro:1. L., Maron, 1. L. & Callaway, R. M. (2005) A biogeographical approach to plant invasions: the importance of studying exotics in their introduced and nalive range. JOIIl"llal 0/ Ecology. 93. 5-15.
Hufbauer. R.A. & Torchin, M.E. (2007) Inlegraling ecological and evolulion- ary Iheory on biological invasions. Biologicallllvasiolls (cd. W Nenlwig), pp. 79-96. Springer-Verlag, Berlin.
Hulme. P.E., Bacher, S., Kenis, M., Klolz, S., Kiihn, I., Minchin. D. et al.
(2008) Grasping al Ihe roules of biological invasions: a framework for inlegraling palhways inlo policy. JOIIl"llal 0/ Applied Ecology. 45. 403- 414.
Inderjil, Cadolle, M. W & Colaull;, R.I. (2005) The ecology of biological inva- sions: past, present and future. Invasive Plants: Ecological and Agriculrural Aspects (cd. Inderjil), pp. 19-43. Birkhiiuser Verlag. Basel.
Keane, R.M. & Crawley, M.J. (2002) Exolic planl invasions and Ihe enemy release hypolhesis. Trellds ill Ecology & Evoilltioll, 17. 164-170.
K 10lZ, S .. Kiihn, I. & Durka. W. (2002) BIOI.FI.OR -eille Darellballk :11 Biologisch- Okologische Merkllllliell der Gejiis;pjlllllzell ill Delltsclillllld. Biindesaml fiir Naturschutz, Bonn.
Lambdon, P.W, Pysek, P, Basnou, C. Hejda, M. Aranoulsou. M., Essi. F.
el al. (2008) Alien flora of Europe: species diversilY, lemporal Irends.
geographical pallems and research needs. Preslia, 80, 101-149.
Liu, H. & Sliling, P. (2006) Tesling Ihe enemy release hypolhesis: a review and mela-analysis. Biologicaill/I'asiol/s. 8, 1535-1545.
Milchell, CE. & Power. A.G. (2003) Release of invasive planls from fungal and viral palhogens. Natllre, 421.625-627.
Miiller-Scharer, H .. Schafrner. U. & Sleinger. T. (2004) Evolulion in invasive plants: implications for biologic,d control. Ii'ends ill Ecology & Evolwion, 19, 417-422.
Nagarajan, S. & Singh, D. V. (1990) Long-dislance dispersion of rUSI palho- gens. AIII/llal Rel'iew ~r Phytopalhology, 28, 139-153.
Nenlwig, W (2007) Biologicalllll'asiol/s. Springer-Verlag. Berlin.
Novolny, V .. Bassel. Y.. Miller, S.E .. Weiblen, G.D., Bremer, B., Cizek, L. &
Drozd, P. (2002) Low hosl specificily of herbivorous insecls in a Iropical fores!. Nalllre, 416, 841-844.
Parker, I.M. & Gilber!. G.S. (2007) When Ihere is no escape: Ihe efTecls of natural enemies on native, invasive. and noninvasive plants. Ecology, 88.
1210-1224.
Payne, R.W, Harding, S.A .. Murray. D.A., Soular, D.M., Baird. D.B ..
Welham, SJ .. Kane. A.F., Gilmour, A.R., Thompson. R .. Websler. R. &
TunniclifTe Wilson, G. (2005) The Gllide to Gellslla Release 9: Sialistics Part 2. VSN Inlernalional, Oxford.
Pearson, D.E. & Callaway, R.M. (2003) IndireclefTeclsof hosl-specific biological conlrol agenls. Trel/ds ill Ecology & Evolllliol/. 18,456-461.
Pearson, D.E., McKelvey, K.S. & Ruggiero. L.F. (2000) Non-Iarget etrecls of an inlroduced biological conlrol agenl on deer mouse ecology. Oecologia.
122,121-128.
Pysek, P. & Jarosik, V. (2005) Residence lime delermines Ihe dislribulion of alien planls. II/vasil'e Plal/ts: Ecological alld Agriclllillral Aspecls (ed. S.
Inderjil), pp. 77-96. Birkhiiuscr Verlag. Basel.
Pysek, P., Sildlo, 1. & Manditk, B. (2002) Calalogue of alien planls of Ihe Czech RepUblic. Prestia. 74, 97-186.
Pysek, P, Richardson. D.M. & Williamson. M. (2004) Predicling and explain- ing plant invasions through analysis of source area floras: some critical considerations. Dil'ersily al/d Disiriblliiol/s, 10, 179-187.
Rayamajhi, M.B., Van, T.K., Prall, P.D. & Cenler. T.D. (2006) Inleracliveasso- ciation between Pliccinia psidii and Oxyops viljostl, two introduced natural enemies of MelalellCll qllillqllellerl'ia in Florida. Biological COlltrol, 37. 56- 67.
Reinharl, K.O., Packer, A., van der PUllen, WH. & Clay, K. (2003) Planl-soil biota interactions and spatial distribution of black cherry in its native and invasive ranges. Ecology Lellers. 6.1046-1050.
Sabelis, M.W, Janssen, A. & Kanl, M.R. (2001)The enemy of my enemy is my ally. Sciel/ce, 291, 2104-2105.
SPSS Inc. (2006) spss Base 15.0jar Wil/dows User's Gllide. SPSS Inc., Chicago.
Tompkins, D.M .. While, A.R. & Bools. M. (2003) Ecological replacemenl of nalive red squirrels by invasive greys driven by disease. Ecology Lellers, 6, 189-196.
van Grunsven, R.H.A., van der PUllen. WH .. Bezemer, T.M., Tamis, WL.M ..
Berendse, F. & Veenendaal, E.M. (2007) Reduced pia Ill-soil feedback of plant species expanding their range as compared to natives. Journal of Ecology, 95, 1050-1057.
Wilson, M. & Henderson. D. M. (1966) British Rllsi FIII/gi. Cambridge Univer- sity Press, Cambridge.
Wolfe, L.M. (2002) Why alien invaders succeed: support for Ihe escape- from-enemy hypolhesis. Americall Narllralist, 160,705-711.
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.
