Do alien plants escape from natural enemies of congeneric residents? Yes but not from all Natalia Kirichenko, Christelle Péré, Yuri Baranchikov, Urs Schaffner & Marc Kenis Biological Invasions ISSN 1387-3547 Biol Invasions DOI 10.1007/s10530-013-0436-9
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Author's personal copy Biol Invasions DOI 10.1007/s10530-013-0436-9
ORIGINAL PAPER
Do alien plants escape from natural enemies of congeneric residents? Yes but not from all Natalia Kirichenko • Christelle Pe´re´ • Yuri Baranchikov • Urs Schaffner • Marc Kenis
Received: 30 October 2012 / Accepted: 5 March 2013 Ó Springer Science+Business Media Dordrecht 2013
Abstract As predicted by the enemy release hypothesis, plants are supposedly less attacked by herbivores in their introduced range than in their native range. However, the nature of the natural enemies, in particular their degree of specificity may also affect the level of enemy escape. It is therefore expected that ectophagous invertebrate species, being generally considered as more generalists than endophagous species, are more prompt to colonise alien plants. In Swiss, Siberian and Russian Far East arboreta, we tested whether alien woody plants are less attacked by native herbivorous insects than native congeneric woody plant species. We also tested the hypothesis that leaf miners and gall makers show stronger preference for native woody plants than external leaf chewers. In all investigated regions, leaf miners and gall makers were more abundant and showed higher species richness on native woody plants than on congeneric alien plants. In contrast, external leaf chewers did not cause more damage to native plants
Electronic supplementary material The online version of this article (doi:10.1007/s10530-013-0436-9) contains supplementary material, which is available to authorized users. N. Kirichenko Y. Baranchikov V.N. Sukachev Institute of Forest SB RAS, Akademgorodok 50/28, Krasnoyarsk 660036, Russia C. Pe´re´ U. Schaffner M. Kenis (&) CABI, Rue des Grillons 1, 2800 Dele´mont, Switzerland e-mail:
[email protected]
than to alien plants, possibly because leaf chewers are, in general, less species specific than leaf miners and gall makers. These results, obtained over a very large number of plant-enemy systems, generally support the hypothesis that alien plants partly escape from phytophagous invertebrates but also show that different feeding guilds may react differently to the introduction of alien plants. Keywords Biological invasions Alien plants Enemy escape Herbivory Feeding guilds
Introduction The enemy-release hypothesis (ERH) is commonly proposed to explain the invasion success of nonindigenous plants and other invasive species. It states that invasive species do better in their area of introduction because they are released from the natural enemies, i.e. herbivores and pathogens for plants, that control them in the area of origin (Keane and Crawley 2002; Wolfe 2002; Cappuccino and Carpenter 2005). However, the general validity of the ERH has been frequently questioned (e.g. Colautti et al. 2004; van Kleunen and Fischer 2009; Chun et al. 2010). The ERH predicts that (1) specialist enemies of the study species will be absent from the new region; (2) specialist enemies of native congeners will rarely attack a new, previously un-encountered host species; and (3) generalists will have a greater impact on the
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native competitors (Keane and Crawley 2002). Thus, a prerequisite of the ERH is that alien plants escape from enemies, in particular host-specific enemies. Most studies having investigated the escape of enemies in alien plants were restricted to comparisons of natural enemy complexes and damage of single species in their introduced and native ranges, or to comparisons of the natural enemy densities and complexes between selected native and non-native species in the same area. Results obtained were not consistent, with numerous studies showing an escape from natural enemies in non-native plants (e.g. Memmott et al. 2000; Wolfe 2002; De Walt et al. 2004; Cappuccino and Carpenter 2005; Joshi and Vrieling 2005; Vila` et al. 2005; Sugiura 2009) while several others showed the opposite (e.g. Agrawal and Kotanen 2003; Beckstead and Parker 2003; Morrison and Hay 2011; Stricker and Stiling 2012). A few studies assessed the enemy escape by performing meta-analyses (Liu and Stiling 2006; Chun et al. 2010) or by broadly analysing natural enemies—host plant distribution databases (Mitchell and Power 2003; van Kleunen and Fischer 2009). Here again, some analyses concluded in the escape of enemies and others not, depending on the analytical methods used and the particular systems examined. The use of natural enemy—host plant distribution databases is particularly questionable because of various error sources such as sample bias between two regions, as pointed out by Pysˇek et al. (2008), or taxonomic misidentifications. Ecological interactions may influence the degree to which an introduced plant escapes natural enemies and, thus, the results of studies assessing the enemy release on single species (Colautti et al. 2004; Liu and Stiling 2006). For example, the presence of closelyrelated native plant species, e.g. congeneric species, in the region of introduction will positively influence the rate of adoption of alien plants by native natural enemies (Connor et al. 1980; Dalin and Bjo¨rkman 2006; Roques et al. 2006). Increasing residence time of alien species decreases the extent to which introduced plants escape from natural enemies (Mitchell et al. 2012). The nature of the natural enemies, in particular their degree of specificity may also affect whether an introduced plant escapes natural enemies and for how long (Halbritter et al. 2012; Lombardero et al. 2012). Non-native plants tend to be mainly attacked by generalist natural enemies and released from specific ones (Memmott et al. 2000; Mu¨ller-
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Scha¨rer et al. 2004; van Kleunen and Fischer 2009; Morrison and Hay 2011). Finally, the geographic distance between the native and the introduced range may also influence escape from natural enemies since greater distance between native and introduced ranges decreases the likelihood that there is overlap between the natural enemies occurring in the native range and in the region of introduction. To properly assess whether alien plants indeed routinely escape from enemies and to identify variations in escape levels between categories of enemies, damage by enemies needs to be compared over a large number of plants and enemy groups under standard conditions. Botanical gardens and arboreta are excellent tools for such studies because they gather together large numbers of plant species from different botanical and floristic regions and the introduced plants often grow in the vicinity of congeneric native plants (Dawson et al. 2008; Kenis et al. 2009). In Swiss and Russian arboreta, we tested whether alien woody plants are less attacked by native phytophagous insects and other invertebrates than their congeneric native species. We also tested the hypothesis that endophagous insects show stronger preference for native woody plants than ectophagous species because the latter tend to be more generalists than endophagous species. Finally, we tested whether the geographic isolation between the region of origin and the region of introduction influences the level of herbivory.
Methods Data collection We carried out observations in eight botanical gardens and arboreta: two in Switzerland and six in Russia, i.e. five in Central Siberia and one in Russian Far East (Table 1). In Switzerland, the distance between the two arboreta was about 40 km. In Central Siberia, the distances between arboreta varied from 10 to 650 km. The distance between the Far Eastern and Central Siberian sites was ca. 3,000–3,500 km. In each arboretum, we selected pairs of congeneric broad-leaved woody plants consisting of a tree or shrub belonging to a native species and a tree or shrub belonging to a congeneric alien species found in the same habitat within a radius of 300 m. For each pair, we recorded the continent of origin of the alien plant
Author's personal copy Alien plants escape from natural enemies Table 1 Swiss and Russian arboreta included in the study: location and insect guild surveyed Arboreta
Location
Latitude
Longitude
Elevation (m)
Insect guild surveyed
Geneva
46°130 36N
6°080 48E
SWITZERLAND 385
LM, LC, G
Aubonne
46°13 36N
6°080 48E
568
LM, LC, G
Arboretum of V.N. Sukachev Institute of Forest, the Siberian Branch of the Russian Academy of Sciences (SIF SB RAS)
Krasnoyarsk
55°590 11N
92°450 54E
255
LM, LC
Experimental arboretum ‘‘Pogorelskiy bor’’ of SIF SB RAS Arboretum ‘‘Karaulnaya’’ of Siberian technological University
Krasnoyarsk Krasnoyarsk
56°220 06N 55°580 06N
92°570 10E 92°370 00E
273 161
LM, LC LM
Botanical garden of Geneva Arboretum of Aubonne
0
RUSSIA
Siberian botanical garden of Tomsk State University
Tomsk
56°270 14N
84°590 43E
118
LM
Central Siberian botanical garden (CSBG) SB RAS
Novosibirsk
54°490 10N
83°060 10E
157
LM
170
LM, LC
V.L. Komarov Mountain-taiga station (MTS), the Far Eastern Branch of the RAS
Gornotayejnoe
0
43°41 21N
0
132°09 22E
LM leaf miners, LC leaf chewers, G gall makers
(i.e. Europe, Asia, North and South America). When several combinations of native-alien species were possible, we associated plant species according to their similarity in leaf size and shape. When various combinations of plants with similar leaf size and shape were possible, we set up pairs haphazardly. When various individual plants of the same species were available, we paired plants that were of similar size and as close as possible to each other. Alien plant species were used only once per arboretum but native species were sometimes associated with several alien species, in which case different individuals of the same native species and, when available, of different sub-species, varieties or cultivars were used for the different pairs. We selected new pairs of individual plants each time a new survey was carried out, independently of the previous pairings. All pairs used in the analyses are listed in (See ESM Appendix 1). Three functional groups of invertebrates were considered: leaf miners, gall makers and external leaf chewers. To compare the abundance of leaf miners and gall makers between alien and native plants, we haphazardly selected 500 leaves per plant on a minimum of five branches per plant in the low part (\2 m) of a tree crown or on a whole shrub and counted directly on the plant the number of leaves attacked by leaf miners or gall makers. Leaves on which several mines or galls of the same species were found were counted only once, but leaves on which two or more
species of leaf miners or gall makers were located were counted two or more times. In cases of trees with large compound leaves (e.g. Fraxinus spp.), we examined 500 leaflets and in case of trees with very large simple leaves (e.g. some Acer spp.) or shrubs with few leaves, we surveyed less leaves (i.e. 200–400 leaves), but the same number of leaves was counted within a plant pair. For each plant, we reported the abundance of leaf miners and gall makers per hundred leaves. When examining damaged leaves, we photographed and collected samples and questionable specimens for later identification. When possible, the identity of each leaf miner and gall maker was determined, based on the appearance of the mine or the gall, and the species richness, i.e. the number of different species found on the examined leaves, was calculated. However, although many leaf miners and gall makers could be identified to the species level using various identification keys (Gerasimov 1952; Shtakelberg 1955; Hering 1957; Buhr 1964–1965; Spencer 1976; Gusev 1984; Ler 1997; Edmunds et al. 2012; Ellis 2012), this was not always possible for all miners and gallers. Therefore, we calculated species richness according to the number of morpho-species rather than species, based on the appearance of mines and galls. We measured the level of damage by external leaf chewers on the same number of leaves as for leaf miners and gall makers. For each leaf, we visually estimated the percentage of leaf area removed by leaf
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chewers using five classes of folivory rate: 0 (0–5 % of the leaf surface missing); 15 (5–25 %); 37.5 (25–50 %); 62.5 (50–75 %); 87.5 (75–100 %). Leaves with 0–5 % of the leaf surface missing were given a 0 % folivory rate because, in most cases, these leaves had no sign of folivory or showed only very minor damage that could not be surely assigned to a leaf chewer. Surface area damaged by leaf miners or skeletonizers (i.e. insects that leave one of the two leaf epidermal layers intact) was not counted in the folivory rate. The average rate of folivory per plant was calculated by averaging the data for each leaf. Since different leaf miners and, for many species, two separate generations of the same leaf miner occur in spring and late summer, we carried out observations on leaf miners twice in some years. For gall makers and leaf chewers, we made observations only once per year. We analyzed gall makers only in Switzerland since the number of species in Siberia and Russian Far East was too low. In Switzerland, we surveyed leaf miners in September 2008 (in 40 plant pairs), June 2009 (54) and September 2009 (64); gall makers in September 2009 (70), and leaf chewers in June 2009 (61). In Siberia, we surveyed leaf miners in June 2009 (48) and August 2009 (49), and leaf chewers in August 2009 (50). In the Russian Far East, leaf miners and leaf chewers were assessed in July 2010 (27). Statistical analyses By sampling pairs of plants from native and alien congeneric, morphologically similar species, we eliminated phylogenetic and morphological biases that often constrain such comparative studies between alien and native or invasive and non-invasive species (Pysˇek and Richardson 2007). However, because most arboreta harbored more alien than native species, several species pairs included data from the same native species (albeit from different plant individuals; see ESM Appendix 1). Therefore, in order to avoid pseudoreplications, we decided not to base the statistical analysis on the paired sampling design, but to use each woody plant species within an arboretum as the experimental unit. In those cases where multiple samplings were made from the same native plant species within an arboretum, the results were pooled to calculate an average value. Nevertheless, for a better visualization of the results, we plotted all pairs of plants on graphs showing the abundance or species
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richness of the different herbivore guilds on native versus alien plants. We tested the effect of plant origin (native vs. alien) on abundance and species richness of leaf miners and folivory rate using a hierarchical general linear mixed model with region and arboretum as fixed factors, genus as random factor, origin as fixed factor and species as random factor. The analyses were also conducted separately for each region. Since we sampled gall makers in Switzerland only, the effect of plant origin on gall maker abundance was tested using a hierarchical general linear mixed model with arboretum as fixed factors, genus as random factor, origin as fixed factor and species as random factor. To meet the assumptions of a general linear model, we log-transformed the data on leaf miner abundance and richness as well as gall maker abundance. The majority of woody plant species were colonized by either no or one gall maker species, and very few plants by two species. We therefore decided to change the data to presence/absence of gall maker species; this allowed us to analyze them with a generalized linear mixed model with logit link and binomial error distribution with arboretum as fixed factor, genus as random factor, origin as fixed factor and species as random factor. For leaf miners and leaf chewers in Switzerland and Siberia, we analyzed alien species of different continents (Eurasia vs. America for Swiss data; other parts of Asia vs. Europe/America for Siberian data) separately to test whether alien plants originating from overseas or more distant continents were even less attacked by insects that alien plants coming from the same continent or continental landmass. Because of the small sample sizes, these analyses were not made for gall makers and the Russian Far East samples. All analyses were performed with SPSS Statistics 20.
Results Leaf miners were significantly less abundant on alien woody plants than on native plants both across (F1,142 = 55.846, P \ 0.001) as well as within each of the three regions examined (Switzerland: F1,73 = 37.332, P \ 0.001; Siberia: F1,41 = 23.137, P \ 0.001; Russian Far East: F1,33 = 6.205, P = 0.018) (Fig. 1). Similarly, the leaf miners’ richness was lower on alien than on native plants across all
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regions (F1,158 = 67.393, P \ 0.001) as well as within each of the three regions examined (Switzerland: F1,76 = 48.112, P \ 0.001; Siberia: F1,46 = 19.989, P \ 0.001; Russian Far East: F1,34 = 4.732, P = 0.037) (Fig. 2). In Siberia, leaf miners’ abundance was significantly reduced in alien species from both America or Europe (F1,22 = 30.653, P \ 0.001) and from other parts of Asia (F1,25 = 10.049, P = 0.003). Leaf miners’ abundance in Switzerland was also significantly reduced in alien species from both America (F1,21 = 30.349, P \ 0.001) and Eurasia (F1,58 = 25.254, P \ 0.001). Gall makers in Switzerland were significantly more abundant (F1,23 = 5.277, P = 0.037) and more species-rich (Quasi F1,86 = 26.009, P \ 0.001) on native hosts than on alien hosts (Fig. 3). In contrast, the folivory rate by leaf chewers was not different between native and alien trees neither across nor within each of the three regions (all P [ 0.9) (Fig. 4). In Siberia, the continent of origin of the alien species (American or Eurasian) did not explain a significant amount of variation in folivory rate (both P [ 0.2). In Switzerland, folivory rate was significantly higher on alien species from Eurasia than on native species (F1,17 = 8.049, P = 0.011), while no difference in folivory rate was found between native species and alien species originating from America (P [ 0.3).
Discussion In the three investigated regions, we observed higher leaf miners’ abundance and richness on native woody plants than on congeneric alien plants, no matter the continent of origin of the alien plant. Similarly, gall makers were also more abundant and diverse on native than on alien plants. In contrast, external leaf chewers did not show difference in damage rate on native and alien woody plants. This clearly supports the hypothesis that alien plants escape from phytophagous invertebrates, but that, at least for alien plants with native congeners, the level of escape depends on the feeding niche. The difference that we observed between the two endophagous feeding niches and leaf chewers is probably related to degree in host specificity. Indeed, concealed herbivore guilds are more specialized than those that feed externally (Mattson et al. 1988). In particular, leaf miners and gall makers are commonly
Fig. 1 Relative number of leaves with mines (%) in the pairs of closely-related native and alien woody plant species in a Switzerland, b Siberia and c Russian Far East. Each point represents one pair of native and alien woody plants. Points below the bisector represent pairs in which the native plant was more attacked by leaf miners than the alien plant; points above the bisector represent the opposite situation. One pair in Fig. 1b (15, 42) is outside the graph
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Author's personal copy N. Kirichenko et al. b Fig. 2 Richness of morpho-species of leaf mining insects in the
pairs of congeneric native and alien woody plant species in a Switzerland, b Siberia and c Russian Far East. Each point represents one pair of native and alien woody plants. Although the number of morpho-species is always represented by an integer, pairs with the same coordinates have been slightly shifted in order to visualize overlapping data points. Points below the bisector represent pairs in which the native plant hosted more leaf miners’ morpho-species than the alien plant; points above the bisector represent the opposite situation
specific to one or a few species within a single genus (e.g. Hering 1951; Buhr 1964–1965). These contrasting results between different categories of enemies, obtained over a large number of plant-enemy systems, are in accordance with most studies involving single systems.
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Fig. 3 Relative number of leaves with a galls (%) and b richness of gall makers’ morpho-species, in the pairs of closely-related native and alien woody plant species in Switzerland. Each point represents one pair of native and alien woody plants. Although the number of morpho-species is always represented by an integer, pairs with the same coordinates have been slightly shifted in order to visualize overlapping data points. The single point at the origin of Fig. 3b (i.e. 0, 0) represents 43 plant pairs. Points below the bisector represent pairs in which the native plant was more attacked by gall makers than the alien plant (Fig. 3a) or hosted more gall makers’ morpho-species than the alien plant (Fig. 3b); points above the bisector represent the opposite situation
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Fig. 4 Defoliation (%) in the pairs of closely-related native and alien woody plant species in a Switzerland, b Siberia and c Russian Far East. Each point represents one pair of native and alien woody plants. Points below the bisector represent pairs in which the native plant was more damaged by external leaf chewers than the alien plant; points above the bisector represent the opposite situation
The vast majority of studies including the assessment of endophagous insects detected a high level of enemy escape in the region of introduction (e.g. Memmott et al. 2000; Wolfe 2002; De Walt et al. 2004; Sugiura 2009; Cripps et al. 2010; Lombardero et al. 2012). Meanwhile, studies that failed to detect enemy escape with invertebrate herbivores usually focused on external leaf chewers (e.g. Radho-Toly et al. 2001; Agrawal and Kotanen 2003; Morrison and Hay 2011; Halbritter et al. 2012). Some other studies detected less damage by external leaf chewers in alien plants compared to native plants (Carpenter and Cappuccino 2005; Norghauer et al. 2011) or in specific plants in an introduction region compared to a native region (Wolfe 2002; De Walt et al. 2004; Adams et al. 2009; Norghauer et al. 2011), which seems to contradict our results. However, in our comparative analyses we included only congeneric species and excluded alien species that had no congeneric native species in the region. It is a well-known fact that alien plants that have congeneric native species in the region of introduction recruit more native herbivores than alien plants without native congeners (Connor et al. 1980; Dalin and Bjo¨rkman 2006; Roques et al. 2006). Had we included in the analyses the level of herbivory in alien plants without native congeners, we would most likely have observed even larger differences to native plants, possibly also on damage by external leaf chewers. Furthermore, not all external leaf chewers are polyphagous (e.g. Norghauer et al. 2011). It should be kept in mind that escaping from natural enemies is only a prerequisite for the ERH (Keane and Crawley 2002). Several studies (e.g. Vila` et al. 2005; Liu et al. 2007; Cripps et al. 2010) showed that a partial release from natural enemies does not necessarily affect plant growth, density and, most importantly, invasiveness. Inversely, alien and native species showing a similar rate of general herbivory may be differently affected by enemies because of single enemy species affecting plant species differently (Zwo¨lfer 1988). To assess the ERH on invasiveness, one needs to compare the impact of the natural enemies on the fitness or population dynamics of the invasive plant in the native and the introduced range (e.g. De Walt et al. 2004). Moreover, in order to assess the role of enemy escape on invasiveness, rates of herbivory should not only be compared between aliens and natives, or between invasives and natives, but also between alien invasives and alien non-invasives (Liu
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and Stiling 2006; Vasquez and Meyer 2011). Few studies have used this approach, with contrasting results (Cappuccino and Carpenter 2005; Liu et al. 2007; van Kleunen and Fischer 2009). In our study, comparing herbivory in alien invasives versus alien non-invasives was not possible because of the low number of invasive woody plants in our samples. Furthermore, many alien woody plants grown in botanical gardens are rarely planted elsewhere and, thus, the lack of invasion records may be due to a low propagule pressure or to a recent introduction rather than to a lack of invasion capacity. Even though our study does not allow us to link enemy escape and alien plant invasiveness, based on the analysis of a large number of plant-enemy systems, it supports the hypothesis that alien plants partly escape from phytophagous arthropods and also clearly illustrates that the level of escape depends on the degree of natural enemies specificity. Acknowledgments We thank the managers and botanists of Swiss and Russian arboreta for their cooperation and help, Diethart Matthies for statistical advice, Melanie Bateman and two anonymous reviewers for their comments on the manuscript. This work was supported by the European Union project PRATIQUE (No. 212459), the Swiss National scientific foundation (NSF) (No. IZKOZ3-128854), the Grant of the President of the Russian Federation (MR-7049.2010.4), the Russian Foundation for Basic Research (Grant No. 12-0431250) and the Krasnoyarsk regional fund of supporting scientific and technological activities (Grant No. 05/12).
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