Species Richness of Herbivores on Exotic Host Plants Increases With

Diversity and Distributions, (Diversity Distrib.) (2008) 14, 905–912

Blackwell Publishing Ltd BIODIVERSITY Species richness of herbivores on exotic RESEARCH host plants increases with time since introduction of the host Martin Brändle1,3*, Ingolf Kühn2,3, Stefan Klotz2,3, Christina Belle1 and Roland Brandl1,3

1Department of Animal Ecology, Faculty of ABSTRACT Biology, Philipps-University Marburg, Aim Species richness of insect herbivores feeding on exotic plants increases with Karl-v.-Frisch Str. 8, 35032 Marburg, Germany, 2Department of Community Ecology, abundance as well as range size of the host in the area of introduction. The formation Helmholtz Centre for Environmental of these herbivore assemblages requires a certain amount of time, and the richness of Research – UFZ, Theodor-Lieser-Str. 4, 06120 insect faunas should also increase with the length of time an exotic plant has been Halle, 3Virtual Institute Macroecology, present in the introduced range. Theodor-Lieser-Str. 4, 06120 Halle, Germany Location Central Europe. Methods We analysed the variation in species richness of leaf-chewing Lepidoptera larvae and sap-sucking Auchenorrhyncha (Hemiptera) associated with 103 exotic woody plant species in Germany in relation to time since introduction, range size, growth form (trees versus shrubs), biogeographical origin (distance from Central Europe) and taxonomic isolation of the host plant (presence or absence of a native congener in the introduced area). Results Using simple correlation analyses we found for Lepidoptera and Auchenor- rhyncha that species richness increased with time since introduction of the host plant. For the Lepidoptera the increase of species richness with time since introduction remained signiﬁcant even after removing the effects of all other independent variables. Main conclusions Our results provide some evidence that assemblages of insects *Correspondence: Martin Brändle, Department of Animal Ecology, Faculty of Biology, Philipps- on exotic plants do not reach saturation within a time scale of few hundred years. University Marburg, Karl-von-Frisch-Str. 8, This contrasts with previous ﬁndings for crop plants. 35032 Marburg, Germany. Tel.: +49 6421 2826607; Fax: +49 6421 2823387; Keywords E-mail: [email protected] Biological invasions, exotic plants, phytophagous insects, species richness.

The equilibrium model of island biogeography provides a INTRODUCTION conceptual framework for understanding species richness of her- Species richness of herbivorous insects increases with the host bivores in relation to the range size of hosts (Strong et al., 1984). plants’ architectonic complexity, range size and abundance, but According to this model, hosts are ‘islands in seas of unsuitable decreases with the host plants’ taxonomic isolation (Strong, environments’. If the colonization rate of herbivores increases 1974; Strong et al., 1977, 1984; Kennedy & Southwood, 1984; and/or the extinction rate decreases with increasing range size of Brändle & Brandl, 2001; Lewinsohn et al., 2005; Schoonhoven the host plant, species richness of herbivores should increase, et al., 2005). Interestingly, species richness of insects recorded on provided that the assemblages have reached equilibrium (Strong crops planted outside their native range also increased with the et al., 1984). Other hypotheses invoke the effect of encounter area on which the crop is planted, although the insect assemblages frequencies between hosts and herbivores. Widespread and large on these crops are relatively recent and have no (co)evolutionary host species are exposed to more potential colonizers. A variant history (Strong, 1974; Strong et al., 1977). Similarly, the number of this encounter hypothesis is the habitat diversity hypothesis, of moth species on exotic conifers in England was positively which states that widespread plant species are likely to occur in correlated with the area covered by the plantations (Fraser, 1997). more habitat types and are therefore exposed to a larger species Obviously, irrespective of the age of the insect assemblages, the pool from which herbivores colonize the host (Strong et al., increase of species richness with greater range size of the host is a 1984). Nevertheless, time must pass before a species pool is general pattern. exhausted. Therefore, the ‘host–age hypothesis’ or ‘species–time

M. Brändle et al. hypothesis’ predicts that as long as the assemblages are not host genera) showed significant positive correlations (Macro- saturated, species richness of herbivores on plant species should lepidoptera: r = 0.62, P = 0.001; Auchenorrhyncha r = 0.68, increase with the length of time hosts and potential colonizers P < 0.001). Although our data set is the most comprehensive are in contact (Birks, 1980; Rosenzweig, 1995; White et al., 2006; currently available for central Europe, there are several limitations. see also Fischer, 1960; Sanders, 1968). The data of Strong for First, we used presence/absence data without considering the crop species suggest that herbivore groups are able to reach abundance of insect species. Consequently, rare species have the equilibrium or saturation within less than 300 years (Strong, same influence on our results as common species. Second, rare 1974; Strong et al., 1977). host plants may be sampled less frequently. This leads to an We analyse here whether time since introduction of the host estimate of species richness biased against rare hosts. However, plant and range size are positively related to species richness of by considering range size as a measure of rarity, we compensated Lepidoptera (butterflies and moths) and Auchenorrhyncha at least in part for this bias. (leafhoppers) recorded on exotic woody hosts. Note that these two insect groups represent two feeding guilds: leaf chewers and Host plant characteristics sap suckers. However, the colonization of exotic plant species by insects is not only a time-dependent process but also requires Host plants that were introduced by man since the time of the preadaptations to cope with chemical, physical and mechanical Roman Empire are considered as exotics (Kowarik, 1992; Klotz defences of host plants (Ehrlich & Raven, 1964; Schoonhoven et al., 2002). The growth form of woody exotics was included as et al., 2005). Analogous to the effects of island isolation, the a variable, because it reflects the size, architectural complexity colonization events by herbivores should decrease with and generation time of the host. Shrubs or climbers are smaller taxonomic or biochemical isolation of the host plant (e.g. and typically characterized by a shorter generation time than tree Connor et al., 1980; Jaenike, 1990). Therefore, exotic host plants species. Obviously, shorter generation times increase propagule with native congeners should have more herbivores than exotics pressure and therefore the likelihood of becoming widespread, with no other representative of that genus in the same area which in turn increases the likelihood of accumulating herbivores (e.g. Soldaat & Auge, 1998; Agrawal & Kotanen, 2003; Agrawal (Strong et al., 1984). Plant species were assigned to two classes: et al., 2005). either shrubs/climbers (coded as zero) or trees (coded as one; see Central Europe provides an excellent model region for Appendix S2). Positive regression or correlation coefficients studying insect faunas of exotic (and native) hosts: (1) Entomologists indicate that more insects were present on exotic trees than on have accumulated knowledge about phytophagous insects and exotic shrubs/climbers. their hosts for more than 300 years. (2) Recently published The biogeographical origin of an exotic host plant reflects its atlases provide detailed data on the range size of host plants. (3) evolutionary history. An exotic from a distant biogeographical Introductions of exotic species span more than 2500 years, and area has evolved in an ecosystem with little resemblance to (4) times of introduction are fairly well documented (Kowarik, Europe. Therefore, we expected that few insects occurring in central 1992). Here we will use a comprehensive list of host records on Europe have preadaptations to colonize hosts from remote the level of host species to examine whether the length of time biogeographical regions. Thus, species richness of herbivores since introduction of exotic woody host species is positively should decrease with distance between Europe and the area of related to species richness of the associated insect assemblages, origin. Using data listed in Kowarik (1992) and Klotz et al. after considering confounding effects of growth form (trees (2002), we assigned each included exotic host to one of four bio- versus shrubs), taxonomic isolation and range size. geographical regions (Appendix S2): Europe, Asia and Middle East, Far East or North America. No host was introduced from the Australian, African or South American regions. We used a METHODS rank scale from 1–4 to code the distance of the area of origin from central Europe (Europe = 1; Asia and Middle East = 2; Data collection Far East = 3; North America = 4). From published sources (Ebert, 1991–2003; Nickel, 2003), we Taxonomic isolation of an exotic host species in Central Europe compiled host records of larvae of native butterflies and moths was equated to presence/absence of native congeners (Schmeil (448 species, 1878 host records) and host records of immature as et al., 2000), coded, respectively, as zero and one (Appendix S2). well as adult leafhoppers (214 species, 601 host records) on 179 Again, positive regression or correlation coefficients indicate that native and 103 exotic woody plant species from Germany (see more insects were attached to exotics with, rather than without, Appendices S1 and S2 in Supporting Information). Following a a native congener. Range size of native and exotic hosts was extracted conservative approach, only host records that reported the host from grid maps (10 min longitude × 6 min latitude, ≈ 130 km2) species were considered; those that reported only the genus were provided by the distribution atlases for West (Haeupler & not. These records were used to produce a presence–absence Schönfelder, 1989) and East (Benkert et al., 1996) Germany matrix of herbivores across hosts. Comparing insect herbivores (FLORKART data base; see http://www.floraweb.de, Appendix recorded on tree genera native to Germany (for data source see S1 and S2). Time elapsed since introduction is expressed as the Brändle & Brandl, 2001) with data collected during the present number of years that an exotic species has been present in study for native woody plants (averaged across species within Germany (from Kowarik, 1992 and Klotz et al., 2002) and

Species richness of insects on exotic plants denotes the period from the first documented occurrence of an species; Auchenorrhyncha: Prunus domestica eight species, Malus exotic plant species in Germany to 2005 (Appendix S2). domestica seven species). Sixty-seven (65%) of the exotic hosts had no record of a moth or butterfly larva and 87 (85%) of the exotic hosts had no record of an adult leafhopper or a larva. Statistical analysis As expected, exotic host species were colonized by a smaller Comparative studies can suffer from ‘pseudoreplication’ (Sol number of insect species than native hosts. For Lepidoptera, the et al., 2007). Therefore, we evaluated whether phylogenetic number of species on native and exotic hosts was, respectively, correction was necessary (but see Ricklefs & Starck, 1996; 9.10 ± 18.8 (mean ± standard deviation (SD), untransformed Carvalho et al., 2006). The total variance in species richness of data) and 2.39 ± 6.8 (P < 0.001 using transformed data, n = 282); the two insect groups was partitioned with a nested analysis of for Auchenorrhyncha, it was 3.09 ± 5.9 vs. 0.47 ± 1.4 (P < 0.001, variance across four different taxonomic levels of exotic host n = 282). However, the geographical range of exotic woody species: species within genus, genus within family and family plants was much smaller than that of natives, with the number of within order (for taxonomic relationships see Schmeil et al., occupied grids being, respectively, 181.5 ± 316.0 and 778.9 ± 842.0 2000, Appendix S2). We used the APE package in ‘R’ (R Develop- (P < 0.001, n = 242). To correct for this, data were analysed with ment Core Team, 2004; function ‘varcomp’; Paradis et al., 2004) analysis of covariances (ANCOVAs). For both insect groups, with the method ‘restricted maximum likelihood’ to calculate the species on exotic hosts accumulated more slowly than on natives variance components. If the largest amount of variance is due to as range size increased (Fig. 1a,b; significant interactions native/ variation between species within genera and not between higher exotic × range size: Lepidoptera: factor native versus exotic taxa, no correction is necessary (Freckleton et al., 2002). The P = 0.020, range size P < 0.001, interaction P = 0.035; Auchenor- analysis revealed that most of the variance in species richness of rhyncha: factor native versus exotic P = 0.005, range size P < 0.001, insects is distributed among exotic host species within a genus interaction P < 0.001). (percentage of total variance: Lepidoptera, 60%; Auchenorrhyncha, The number of host plants is a measure of niche-breadth 95%). Therefore, we first analysed our data at the species level. for each species of butterfly/moth reported from native and However, in Lepidoptera, a substantial part of the variation was introduced hosts (Fig. 2). In general, frequency distributions of distributed among genera within families (40%). Therefore, we niche-breadth of insects on natives and exotics followed a positively also adopted a conservative approach and averaged data across skewed distribution. Furthermore, exotics were predominantly species within genera. colonized by generalists rather than specialists (Fig. 2; P < 0.001, The statistical analysis of species data as well as means GLM, quasi-Poisson error). proceeded along two lines. Prior to all analyses, species richness Simple correlation analysis using host plant species as well as of insects was log10(x + 1) transformed; range size and time since means across species within host genera revealed that species introduction were log10 transformed. First, the relationships richness of Lepidoptera was higher on trees than on shrubs and between the different plant characteristics and species richness of increased with range size as well as the time since introduction of butterflies/moths and leafhoppers on exotic woody plants were the host, without an indication of levelling-off (Table 1, Fig. 1c). analysed using univariate correlations. This approach allowed For leafhoppers taxonomic isolation, biogeography and time use of a maximum of information for each relationship. Second, since introduction were consistently significantly correlated to multivariate analyses were undertaken by applying standard species richness (Table 1, Fig. 1d). multiple regression models as well as Bayesian Model Averaging In the multivariate analyses the plant characteristics considered (BMA). BMA accounts for model uncertainty inherent in the explained, respectively, 54% and 41% of the variation in species variable selection problem, by averaging over the best models richness of Lepidoptera across host species and host genera according to approximate posterior model probability (function (Table 1). For Lepidoptera, the multivariate approaches supported ‘bicreg’ in the BMA package version 3.03 for ‘R’; Raftery, 1995). the significant effects of range size and time since introduction on species richness (Table 1). For leafhoppers, the plant characteristics explained only 23% and 24% of the variation in species RESULTS richness. In contrast to the Lepidoptera, we found no relationship Species richness of butterflies/moths and leafhoppers showed between range size of the host and species richness of the considerable variation across native woody host species leafhoppers (Table 1). Time since introduction was significant in (Appendix S1). One hundred and twenty-nine species of the univariate analyses, but the results of the multivariate analyses Lepidoptera were recorded on Prunus spinosa and 115 species on did not support these finding. In contrast to the Lepidoptera, the Salix caprea, whereas 87 native hosts were without phytophage multivariate analyses point to consistent effects of taxonomic records (Appendix S1). The greatest numbers of species of leaf- isolation on species richness. hoppers were recorded on Quercus robur and Betula pendula (32 and 28, respectively), while a considerable number of native trees DISCUSSION and shrubs had no records (total: 114 taxa). Species richness of butterflies/moths and leafhoppers on exotic hosts (Appendix S2) Our data set represents a fairly comprehensive list of host records was highest on two introduced trees grown for their fruits and gives our analyses considerable statistical power. Overall, we (Lepidoptera: Prunus domestica 43 species, Malus domestica 42 obtained the following general results. First, with increasing

M. Brändle et al.

Figure 1 The upper graphs show the relationship between species richness and range size of host plant species for (a) Lepidoptera and (b) Auchenorrhyncha on native (ﬁlled symbols, solid regression line) and exotic (open symbols, dashed regression line) woody host plants. The lower graphs depict the relationship between species richness of (c) Lepidoptera and (d) Auchenorrhyncha and time since introduction of the host plant species. Note

that in all panels the y-axis was log10(x + 1) and

the x-axis log10 transformed

Figure 2 Proportion of Lepidoptera (left) and Auchenorrhyncha (right) species with different dietary niche breadth ranked according to increasing number of host plants exploited per species. The left part of the graphs depicts the frequency distribution for insects that exploit exotic hosts and the right part depicts those for native hosts. Symbols and bars indicate means and 95% conﬁdence intervals of the dietary niche breadth. For statistical comparisons see text. range size, insect species accumulated at a lower rate on exotic species richness of butterﬂies and moths among exotic hosts was than on native hosts. Second, assemblages on exotic hosts accounted for mostly by the range size of the host and time since consisted of generalists. Third, the importance of independent introduction of the host, whereas taxonomic isolation of the host variables differed between the two taxa analysed. The variation of was more important in determining variation of species richness

Species richness of insects on exotic plants

Table 1 The ﬁrst two rows show the univariate relationships between (i) growth form (tree or shrub/climber), (ii) biogeographical origin

(Europe, Middle East and Asia, Far East, North America), (iii) taxonomic isolation as presence of an indigenous congener, (iv) log10-transformed time since introduction in Germany, and (v) log10-transformed range size of the exotic host plant species and genus on log10(x + 1)-transformed species richness (significant correlation coefficients P < 0.1 in bold). The third and the forth row present multivariate analyses using ordinary standard regression analyses and the results of Bayesian model averaging. beta = standardized regression coefficient (significant betas P < 0.1 in bold); mean = posterior mean of each coefficient; SD = posterior standard deviation of each coefficient (from model averaging); prob = a posterior probabilities of independent variables.

Species Genera Species Genera

Independent variables nr P nr P beta mean SD prob beta mean SD prob

Lepidoptera Growth form 103 0.41 < 0.001 63 0.36 0.004 0 0 0.03 10 0.09 0.03 0.08 45 Biogeography 94 –0.16 0.126 59 –0.24 0.062 –0.02 0 0.01 10 0 0 0.02 12 Taxonomic isolation 103 0.14 0.152 63 0.16 0.198 0.29 0.24 0.10 94 0.22 0.10 0.13 50 Range size 71 0.50 < 0.001 52 0.50 < 0.001 0.54 0.31 0.06 100 0.39 0.24 0.09 98 Time since introduction 74 0.48 < 0.001 52 0.49 < 0.001 0.39 0.44 0.11 100 0.32 0.30 0.20 81 R2 0.54 0.41 Auchenorrhyncha Growth form 103 0.18 0.075 63 0.18 0.155 –0.11 0 0.02 10 –0.04 0.00 0.02 12 Biogeography 94 –0.31 0.003 59 –0.30 0.019 –0.27 –0.03 0.04 58 –0.24 –0.02 0.03 53 Taxonomic isolation 103 0.19 0.058 63 0.24 0.057 0.30 0.06 0.08 49 0.35 0.13 0.09 71 Range size 71 0.16 0.197 52 0.13 0.372 0.13 0 0.02 12 0.07 0.00 0.02 12 Time since introduction 74 0.30 0.009 52 0.33 0.015 0.23 0.11 0.12 56 0.20 0.11 0.11 44 R2 0.23 0.24 in leafhoppers. However, the data set for leafhoppers has many subtle estimates of taxonomic relatedness, but these data are at flaws and our results are therefore at best tentative. We will present only available for a small subset of the host plants concentrate our discussion on the variation of species richness in considered. However, sequence data are accumulating at a steadily butterflies and moths. increasing rate and should, in the near future, permit a more Similarly to the results of our study, most previous analyses of convincing analysis of the effects of taxonomic isolation. Note species richness of insects on exotic hosts also showed that the also that for the leafhoppers taxonomic isolation was the only range size of the exotic host is an important influencing factor. variables with a more or less consistent influence on species rich- Contrastingly, few previously published analyses provided ness. Ignoring for the moment the drawbacks of this data set, the support for the idea that species richness increases with the time importance of taxonomic isolation describing the existence of a since introduction (time hypothesis; Southwood, 1961; preadapted species pool is consistent with the feeding strategy of reanalysed by Strong, 1974; Strong et al., 1977; Birks, 1980; the leafhoppers: sap-sucking species come into close contact with Kennedy & Southwood, 1984; Andow & Imura, 1994; Rosenzweig, secondary compounds of the host plants and thus require certain 1995; Frenzel et al., 2000; Carpenter & Cappuccino, 2005; Cripps adaptations to colonize a particular host. et al., 2006). A drawback of many previous studies on species We were somewhat surprised by the fact that time since richness of insects on exotic plants was that many of them introduction and range size were not correlated in our data set considered only a single or a very small number of hosts (Strong, (n = 57, r = 0.18, P = 0.19). Therefore, even in the univariate 1974; Strong et al., 1977; Banerjee, 1981; Fraser, 1997). Furthermore, analyses the effects of time since introduction and range size are studies included only a limited set of factors that may influence more or less independent. Furthermore, range size is also a surrogate species richness (Connor et al., 1980; Kennedy & Southwood, for sampling intensity, if one accepts that entomologists have 1984; Burki & Nentwig, 1997; Frenzel et al., 2000) and the concentrated their sampling on widespread species and in majority of studies failed to consider confounding factors such as particular host species of some economic importance. However, biogeographical origin, growth form and taxonomic isolation in in our analysis of butterflies and moths, time since introduction the area of introduction (Rosenzweig, 1995; Sol et al., 2007). remained a significant independent variable even after considering For instance, Frenzel et al. (2000) stressed the importance of range size and all other included independent variables. Rosenzweig phylogenetic effects. Using data from Britain and Germany these (1995) argued that ‘the host–age pattern operates only over rela- authors found a significant species–time relationship for exotic tively brief periods in rather unnatural circumstances. It depends trees in Germany but not in Britain. However, only in Britain on introduced species or recent immigrants’. Our results support were the considered exotic hosts with and without native congeners. this view. Strong et al. (1984) also report examples of impoverished In our study, taxonomic isolation had no consistent influence on assemblages of insects on exotic trees that have been present in species richness of butterflies and moths. However, our dummy the range of introduction for 100 to 300 years. While acknowledging variable for taxonomic isolation is only a rough approximation. that cases of rapid evolution of new host associations do occur Molecular data may, in the future, allow derivation of more (e.g. Feder et al., 1988; Carroll & Boyd, 1992), molecular studies

© 2008 The Authors Diversity and Distributions, 14, 905–912, Journal compilation © 2008 Blackwell Publishing Ltd 909 M. Brändle et al. provide evidence that many phytophagous species evolved 01LM0206). The data base FLORKART on plant distribution in during the Tertiary (e.g. Rokas et al., 2003; McLeish et al., 2007). Germany (for numbers of occupied grid cells) was provided by It is apparent that in many, if not most, insect lineages, species the Federal Agency for Nature Conservation (BfN) on behalf of usually need considerable time to evolve the necessary adaptations the ‘German Network for Phytodiversity (NetPhyD)’. We thank to colonize a new host. Generalists are more likely to already possess Andrew D. Liston for correcting the language. the necessary adaptations. Endophagy is often associated with specialization on a single host plant (Spencer, 1990; Skuhravá & REFERENCES Skuhravy, 1997) and therefore miners and gall-formers have a very close association with their hosts. 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Appendix S2 Species richness of Lepidoptera and Auchenor- SUPPORTING INFORMATION rhyncha on exotic trees and shrubs in Germany. In addition, Additional Supporting Information may be found in the online growth form, biogeography, taxonomic isolation, the time since version of this article: introduction and the range size of the hosts are listed.

Appendix S1 Species richness of Lepidoptera and Auchenor- Please note: Wiley-Blackwell are not responsible for the content rhyncha on native trees and shrubs in Germany and the range or functionality of any supporting materials supplied by the size of the host plants (number of occupied grids). Range size authors. Any queries (other than missing material) should be was extracted from grid maps (10 min longitude × 6 min directed to the corresponding author for the article. latitude, approx. 130 km2).