Regional- and Local-scale Drivers of
Establishment and Invasion Success of Alien Plants
Dissertation submitted for the degree of Doctor of Natural Sciences
Presented by Yanhao Feng
at the
Faculty of Sciences Department of Biology
Day of the oral examination: 28 October 2015 Referee 1: Prof. Dr. Mark van Kleunen
Referee 2: Prof. Dr. Eric Allan
Konstanzer Online-Publikations-System (KOPS) URL: http://nbn-resolving.de/urn:nbn:de:bsz:352-0-306836
人法地，地法天，天法道，道法自然
---《老子道德经》
Man follows Earth Earth follows heaven Heaven follows the Tao Tao follows nature --- <Daodejing>
(Adapted from the translation by Gia-Fu Feng)
ii
Table of Contents
Summary... iv
Zusammenfassung ... vi
General Introduction ... 1
CHAPTER 1 ... 9
Introduction history, climatic suitability, species characteristics and their interactions explain establishment success and spread of Chinese woody species in Europe ... 10
Abstract ... 11
Introduction ... 13
Methods ... 16
Results ... 22
Discussion ... 24
Acknowledgements ... 31
CHAPTER 2 ...
71Responses to shading of naturalized and non-naturalized exotic woody species ... 72
Abstract ... 73
Introduction ... 75
Materials and Methods ... 78
Results ... 83
Discussion ... 85
Acknowledgements ... 89
CHAPTER 3 ... 105
Do phylogenetic relatedness and functional traits drive direct and indirect interactions among alien and native plants? ... 106
Summary ... 107
Introduction ... 109
Materials and Methods ... 113
Results ... 122
Discussion ... 124
Acknowledgements ... 130
General discussion ... 149
Declaration of authors’ contributions ... 159
General Acknowledgements ... 160
References ... 162
iv
Summary
Due to intensive human activities across the globe, a vast number of alien plants are introduced to new biogeographical areas. A major theme in ecology is to
understand why only some of them manage to become established and further invasive in new ranges, where they threaten biodiversity and ecosystem functioning.
This is a challenging theme because plant invasion is a complex process occurring across ecological scales at different invasion stages. In this thesis, I explored both regional- and local-scale drivers of alien plants establishment and invasion success using dataset analysis, and common-garden and greenhouse experiments.
First, I explored how regional-scale establishment success and spread of 449 Chinese woody species in Europe were interactively associated with a broad range of factors. I found that the establishment success and spread significantly increased with residence time (only in spread), planting frequency and climatic suitability.
Although none of species traits had significant main effects on the establishment, having a longer flowering period and compound leaves favored the spread of
established species. The role of some traits (fruiting duration, leaf retention and leaf type) in the establishment and/or spread was dependent on other factors (residence time, planting frequency, climatic suitability and other species traits). These findings explicitly show how the role of some factors in the invasion process is context- dependent.
Second, I explored whether the ability of alien woody plants to cope with shading explained their regional-scale establishment success. Overall, the established and non-established species did not differ greatly in biomass production, morphological characteristics and CO2 assimilation, across five light intensities (from 100% to 7% of
ambient light). However, the established species grew taller and reduced total leaf area more than the non-established ones in response to shading. Furthermore, the established species maintained a greater low-light CO2-assimilation capacity under shading. Overall, these differences were small, and therefore I conclude that the response to shading is not important for the successful establishment of alien woody plants.
Last, I explored local-scale direct and indirect interactions among alien and native plant species. In particular, I tested whether a native species that is
phylogenetically closely related rather than distantly related to an alien species can directly suppress the alien, and as a consequence can indirectly reduce competitive effects of the alien on other co-occurring native species. Overall, competition was more severe between more closely-related alien species and native species,
although this pattern was partly dependent on the regional-scale commonness of the alien. However, the presence of distantly-related rather than closely-related native species indirectly offset strong competitive effects of alien species on target native species. These interactions were explained by functional traits (e.g. plant height, SLA, leaf area ratio, root length ratio and shoot weight ratio) rather than by phylogenetic/functional distances of the interacting species. This implies that functional traits could help to disentangle complex interactions among plants.
To sum up, my thesis explored different mechanisms across ecological scales in the process of plant invasions. My findings may shed lights on the future studies to systematically integrate regional-scale processes (by considering complex
interactions among various factors) with local-scale processes, such as adaptation to local environments and species interactions to ultimately explain and predict success of alien plants outside their native ranges.
vi
Zusammenfassung
Aufgrund intensiver weltweiter anthropogener Aktivitäten wurde eine Vielzahl nichtheimischer Arten in neuen biogeografischen Regionen eingeführt. Eine der grundlegende Fragen der Ökologie ist, warum nur einige dieser Arten es schaffen sich in ihren neuen Verbreitungsgebieten zu etablieren und sogar invasiv zu werden, wodurch sie dort die Biodiversität und Ökosystemprozesse bedrohen. Das ist eine anspruchsvolle Fragestellung, da solche Invasionen nichtheimischer Pflanzenarten ein komplexer Prozess ist, welcher über verschiedene ökologische Skalen in
unterschiedlichen Invasionsstadien auftritt. Im Rahmen dieser Arbeit werden beide, regional- und lokal-skalige ökologischen Faktoren des Etablierungs- und
Invasionserfolgs nichtheimischer Pflanzen mit Hilfe von Datensetanalysen, sowie
„common garden“- und Gewächshausexperimenten untersucht.
Zuerst wurde untersucht wie der regionalskalige Etablierungserfolg und die Ausbreitung von 449 chinesischen holzigen Pflanzenarten interaktiv mit einer Reihe an Faktoren zusammenhängt. Dabei zeigte sich, dass die Etablierung und
Ausbreitung signifikant mit dem Einführungszeitraum, der Häufigkeit an Pflanzungen und der klimatischen Eignung zunimmt. Keine der Artmerkmale hatte direkten
signifikanten Einfluss auf den Etablierungserfolg, allerdings zeigte sich, dass eine länger Blühperiode und zussammengesetzte Blätter eine Etablierung begünstigen.
Die Rolle einiger Merkmale (Frutifikationszeitraum, Blattart und Lebensdauer der Blätter) bezüglich Etablierung und Ausbreitung war von anderen Faktoren abhängig (Einführungszeitraum, Häufigkeit an Pflanzungen, klimatische Eignung sowie weitere Artmerkmale). Diese Ergebnisse zeigen explizit, das die Rollen einiger Faktoren in einem Invasionsprozess kontextabhängig sind.
Zum Zweiten wurde untersucht, ob Unterschiede in der Fähigkeit nichtheimischer Pflanzen Beschattung zu tolerieren einen Einfluss auf den regionalskaligen Etablierungserfolg hat. Etablierte und nicht etablierte Pflanzen unterschieden sich jedoch nicht wesentlich in ihrer Biomasse, den morphologischen Charakteristika oder der CO2 Assimilation unter fünf verschiedenen Lichtintensitäten (zwischen 100% und 7% des natürlichen Tageslichts). Allerdings zeigten die
etablierten Arten einen höheren Wuchs und wiesen eine stärkere Reduktion der Blattfläche als Reaktion auf die Beschattung auf, als die nicht etablierten Arten.
Darüber hinaus hielten etablierte Arten eine höhere CO2 Assimilatioskapazität unter Beschattung aufrecht. Insgesamt waren die Unterschiede jedoch klein und es lässt sich daher Schlussfolgern, dass die Reaktion auf Beschattung weniger bedeutend für den Etablierungserfolg nichtheimischer holziger Arten ist.
Zuletzt wurde untersucht wie heimische und nichtheimische Pflanzen auf lokaler Skala direkt und indirekt interagieren. Insbesondere wurde getestet, ob eine heimische Art, die phylogenetisch eng mit einer fremden Spezies verwandt ist, diese nichtheimische Art direkt unterdrücken kann, und als Folge indirekt den
Konkurrenzdruck der nichtheimischen Art auf eine gemeinsam auftretende heimische Art verringern kann. Insgesamt zeigte sich, dass die Konkurrenz zwischen eng
verwandten heimeischen und nichtheimischen Arten stärker ausgeprägt war.
Allerdings war dieses Ergebnis auch von der regionalen Häufigkeit der
nichtheimischen Art abhängig. Nicht eng verwandte Arten allerdings vermindern indirekt die starken Konkurrenzeffekte nichtheimischer Arten auf heimische Zielarten.
Diese Wechselwirkungen ließen sich durch funktionale Merkmale (z.B.
Pflanzengröße, spezifische Blattfläche (SLA), Blattflächen Verhältnis, Wurzellänge Verhältnis undSpross Gewicht Verhältnis) und nicht durch phylogenetische Distanz
viii der interagierenden Arten erklären. Das impliziert, dass die funktionalen Merkmale
helfen könnten, komplexe Interaktionen zwischen Pflanzen zu erklären.
Zusammenfassend werden in dieser Arbeit die Zusammenhänge
unterschiedlicher Mechanismen über verschiedenen ökologische Skalen bezüglich Invasionen nichtheimischer Pflanzenarten untersucht. Die Ergebnisse können dazu beitragen systematisch regionalskalige Prozesse (durch berücksichtigung der komplexen Wechselwirkungen verschiedener Faktoren) und lokale Prozesse zu integrieren, wie zum Beispiel lokale Anpassung an Umwelteinflüsse und
Interaktionen zwischen Arten, um letzlich den Erfolg gebietsfremder Arten außerhalb ihrer heimischen Verbreitungsgebietes zu erklären und vorherzusagen.
General Introduction
Plant invasion
Due to intensive human activities across the globe, a vast number of plant species are introduced to new biogeographical areas (Elton 1958; Mack & Lonsdale 2001), where some of them have established self-sustaining populations (van Kleunen et al. 2015). This has largely reshaped the ecological and evolutionary composition of global biota (Qian & Ricklefs 2006; Winter et al. 2009). Especially, a small subset of these established species further become invasive (i.e. widely spread) in new ranges (Williamson 1996; Richardson & Pyšek 2006; Blackburn et al. 2011), where they threaten biodiversity and ecosystem functioning (Kolar & Lodge 2001;
Pimentel 2002). For example, Ailanthus altissima (tree of heaven) was originally introduced from China to Europe as an ornamental tree in the 1740s, but now it becomes an invasive species that causes serious ecological and economic damage, according to the DAISIE report (http://www.europe-aliens.org/). Therefore, a major theme in ecology is to understand why some alien plants become successful in new ranges while others fail. This is a challenging theme, because plant invasion is a multistage ecological process along the introduction-establishment-invasion continuum (sensu Richardson et al. 2000), in which numerous casual factors are likely to play their roles in complex ways (Richardson & Pyšek 2012). For instance, different factors may play important roles at different stages in the process of plant invasions (Theoharides & Dukes 2007; Richardson & Pyšek 2012).
Ecological scales
Moreover, in natural ecosystems, ecological phenomena (e.g. plant invasions in a new region, maintenance of biodiversity and ecosystem functioning, consequence
2 of climate change) often involve the complex organization of many mechanistic
component parts over ecological scales (see Fig. A) (Schmitz 2010). For instance, the mechanisms and processes of plant invasions in a new region are relevant to all the ecological scales in terms of region, landscape, ecosystem, community,
population, and individual (Elton 1958; Catford, Jansson & Nilsson 2009; Gurevitch et al. 2011).
Studies over last several decades have almost explored the causes and impacts of plant invasions at all of those ecological scales (Elton 1958; Sax, Stachowicz &
Gaines 2005; Gurevitch et al. 2011; Richardson 2011; Lockwood, Hoopes &
Marchetti 2013). For example, studies have explored whether an alien plant species is more successful in a region if it was introduced earlier and in multiple instances to that region (i.e. with respect introduction history) (Lockwood, Cassey & Blackburn 2005; Bucharova & van Kleunen 2009; Pyšek, Křivánek & Jarošík 2009). Moreover, environmental suitability (e.g. with respect to climate, soil type, resource availability) might be fundamental or even prerequisite for the establishment of alien plants in a region (Theoharides & Dukes 2007; Petitpierre et al. 2012). Within a region, the landscape with greater environmental heterogeneity is thought to maintain higher degrees of alien species diversity (Davis, Grime & Thompson 2000; Davies et al.
2005; Melbourne et al. 2007). Studies have also suggested that ecosystem types (e.g.
forest, grassland) and processes (e.g. nutrient cycling rates) are relevant to the
resistance to invasion by alien plants (Martin, Canham & Marks 2008; Gurevitch et al.
2011; Richardson & Rejmánek 2011). Within an ecosystem, diversity of a recipient community has been empirically and theoretically shown to influence invasibility (MacArthur 1972; Case 1990; Levine & D'Antonio 1999; Herben et al. 2004; Fridley et al. 2007). Moreover, biotic species interactions (e.g. competition, facilitation,
herbivory, predation) in a recipient community should be also important for the
success of alien plants (Keane & Crawley 2002; Levine, Adler & Yelenik 2004;
Mitchell et al. 2006). Range expansion of alien plants can be better understood through the research on population dynamics (with demographic models) and the evolution of life histories (Sakai et al. 2001; Burton, Phillips & Travis 2010). Finally, large-scale (e.g. regional-scale) invasion patterns are also apparently relevant to the performance of alien plant individuals (e.g. phenotypic plasticity) (Richards et al.
2006; Hulme 2008; Davidson, Jennions & Nicotra 2011).
For some factors (especially species traits), it is not always apparent whether and how they ultimately affect invasion patterns of alien plants through what
mechanisms and processes at which ecological scales. For instance, species traits are likely to affect environmental filtering in the process of community assembly with alien and native plants (Fargione, Brown & Tilman 2003; McGill et al. 2006; Funk et al. 2008). Life history traits such as growth, survival, dormancy and clonality
determine range expansion of alien plants as populations (Sakai et al. 2001). Of course, species traits may also influence plant invasions because traits can reflect the ability of alien plants to cope with abiotic environments and biotic interactions with other organisms in a system (van Kleunen, Weber & Fischer 2010; Pérez-
Harguindeguy et al. 2013). Partly because of this potentially multi-scale involvement of species traits in the invasion process, it has been a challenge to understand the relationship between species traits and large-scale invasion patterns (Baker 1974;
Pyšek & Richardson 2007; Thompson & Davis 2011; van Kleunen, Dawson & Dostal 2011; Leffler et al. 2014; Dawson, Maurel & van Kleunen 2015; van Kleunen,
Dawson & Maurel 2015).
Furthermore, it has also been a challenge to understand how multiple causal factors and mechanistic processes at different ecological scales jointly shape large-
4 scale invasion patterns (Blackburn et al. 2011; Foxcroft, Pickett & Cadenasso 2011;
Gurevitch et al. 2011). This is because the success of alien plants in a region is a complex process which involves a systematic and hierarchical ecological
organization by multiple causal factors, interactions between these factors, and direct and indirect effects and feedbacks, across ecological scales (Callaway et al. 2004;
White, Wilson & Clarke 2006; Melbourne et al. 2007; Gurevitch et al. 2011).
Therefore, to thoroughly understand how numerous causal factors across ecological scales systematically shape large-scale invasion patterns, it is essential to resolve the complexity of the interactions between them. However, with few exceptions (Thuiller et al. 2006; Küster et al. 2008; Bucharova & van Kleunen 2009; Dawson, Burslem & Hulme 2009), many previous studies ignored the importance of the interactions in the invasion process (Gurevitch et al. 2011; van Kleunen, Dawson &
Maurel 2015). Especially, very few studies have explicitly explored whether and how multiple causal factors interact, i.e. the effect of a factor is dependent on other factors (Kueffer, Pyšek & Richardson 2013; van Kleunen, Dawson & Maurel 2015). This context-dependency has the potential to explain why those correlative studies assessing the association between invasion patterns and causal factors (especially species traits) do not always find consistent results (reviews by Theoharides & Dukes 2007; Richardson & Pyšek 2012; van Kleunen, Dawson & Maurel 2015). For instance, the effect of phenological traits is frequently shown to be dependent on climatic
factors (Cleland et al. 2007; Sedlacek et al. 2015). Therefore, it is likely to end up with opposite results in testing the importance of phenological traits when the suitable climate is available or not in the first place.
To gain a mechanistic (than correlative) understanding of causes of plant invasions, empirical studies are also needed to disentangle how mechanistic processes eventually influence large-scale invasion patterns. The ability of alien
plants to cope with abiotic and biotic environments has the potential to affect fundamental mechanistic processes in plant invasions, e.g. local adaptation,
community assembly, range expansion (Mitchell et al. 2006; Going, Hillerislambers &
Levine 2009; Gurevitch et al. 2011). Therefore, it is essential to understand whether and how regional-scale invasion patterns are associated with local-scale abiotic and biotic mechanistic processes (e.g. in local communities). One of the major abiotic environments that alien plants need to cope with during their lifetime is ubiquitous abiotic stress in nature, such as shading, drought and low nutrients (Alpert, Bone &
Holzapfel 2000; Martin, Canham & Marks 2008; Valladares & Niinemets 2008; Funk 2013). However, the importance of the adaptation to abiotic stress in the invasion process has been largely overlooked (Funk & Vitousek 2007).
The ability of alien plants to cope with biotic interactions (e.g. competition, facilitation, herbivory, predation) should be also fundamental (Keane & Crawley 2002;
Levine, Adler & Yelenik 2004; Mitchell et al. 2006). Several hypotheses or theories in invasion ecology, e.g. Darwin’s naturalization hypothesis (Darwin 1859), limiting similarity theory (Macarthur & Levins 1967; Emery 2007), enemy release hypothesis (Keane & Crawley 2002), invasional meltdown (Simberloff & Von Holle 1999) and novel weapons (Callaway & Ridenour 2004), are associated with biotic species interactions. For instance, according to Darwin’s naturalization hypothesis and the limiting similarity theory (Darwin 1859; Macarthur & Levins 1967), alien species should be less successful in a region where their closely-related natives sharing ecological niches are present. However, the interactions in nature are much more complex because plants are usually involved in multispecies interactions composed of not only direct but also indirect interactions (Strauss & Irwin 2004; Callaway &
Howard 2007; Allesina & Levine 2011). Moreover, the outcomes of multispecies
6 theories (e.g. Darwin’s naturalization hypothesis) have focused on (Strauss 1991;
Wootton 1994; Strauss & Irwin 2004). Therefore, to understand how regional-scale invasion patterns are influenced by local-scale biotic mechanistic processes such as species interactions, it is essential to disentangle the complexity of multispecies interactions among alien and native plants and the niche-based mechanisms thereof.
Contribution of this thesis
In short, my thesis explored how mechanisms and processes at different ecological scales shape invasion patterns of alien plants, by addressing three research topics using a combination of large dataset analysis, and common-garden and greenhouse experiments. First, I explored how multiple casual factors
interactively drive regional-scale invasion patterns of 449 Chinese woody species in Europe. Second, I addressed whether the response to shading plays an important role in the establishment of these woody species. Third, I disentangled how regional- scale plant invasions are mechanistically linked to the complexity of local-scale direct and indirect biotic interactions among alien and native plants.
In the 1st chapter, I explored how various casual factors and their interactions explained the establishment success and spread of 449 Chinese woody species in Europe. Specifically, I tested whether and how the establishment success of these species in Europe was associated with residence time (time since earliest planting), planting frequency, climatic suitability, various species traits and native range size, and with interactions between these variables. For the 38 out of the 449 species that have established, I also tested how these variables and their interactions explained spread of these species in Europe. In these two analyses, I explicitly explored whether and how the effect of a factor was dependent on other factors.
In the 2nd chapter, I tested whether the response of plant individuals to shading is associated with the continental establishment success of 38 Chinese woody species (shrubs and trees) in Europe. Shading is a common abiotic stress if these alien shrubs and trees supposedly spread into habitats such as forest and shrub land.
These 38 species (half of them have become established in Europe) from the 449 species in the first study. I grew each of these species under five shading levels from 100 to 7% of ambient sunlight, to specifically test whether, compared to non-
established woody species, established ones (1) maintain better growth performance under shading, and (2) express greater adaptive plasticity in terms of morphological and physiological responses to shading.
In the 3rd chapter, I explored whether and how regional-scale invasiveness of alien plants is mechanistically linked to the complexity of local-scale direct and indirect biotic interactions. Specifically, I used nine groups of alien and native herbaceous species to explore how direct and indirect interactions operate among them. Each group has an alien species that is common (invasive) or rare (less
invasive), two natives that are phylogenetically closely-related and distantly-related to the alien respectively, and a “target” native species on which I assessed the
competitive effects. I grew the four species of each group alone, and in two-species and three-species combinations in greenhouse. Specifically, I tested whether how the presence of the closely rather than distantly related native species directly
suppressed the alien, which as a consequence indirectly alleviated competitive effects of the alien on other co-occurring native (“target”) species. Moreover, I tested whether and how these interactions explained the commonness (i.e. invasiveness) of alien plants. In addition, I tested whether and how these interactions were driven by niche differences of the interacting species that are associated with phylogenetic
8 In the final part of the thesis, I provide a General Discussion that summarizes and discusses the most important findings, and that draws a final conclusion and an outlook.
Fig. A Ecological scales in the invasion process of alien plants.
CHAPTER 1
10 Introduction history, climatic suitability, species characteristics and their
interactions explain establishment success and spread of Chinese woody species in Europe
Yanhao Feng*1, Noëlie Maurel1, Zhiheng Wang2, Lei Ning1,3, Fei-Hai Yu3 & Mark van Kleunen1
1Ecology, Department of Biology, University of Konstanz, Universitätsstrasse 10, Konstanz, D-78464, Germany
2Department of Ecology and Key Laboratory for Earth Surface Processes of the Ministry of Education, College of Urban and Environmental Sciences,
Peking University, Beijing 100871, China
3School of Nature Conservation, Beijing Forestry University, Beijing 100083, China
*Corresponding author:
Yanhao Feng Tel: +49-7531-88-4305
Email: yanhao.feng@uni-konstanz.de Global Ecology and Biogeography (In review)
Abstract Aim
To understand what explains success of non-native plants, it is essential to assess whether success is linearly or non-linearly related to potential explanatory factors, and how these interact. We tested how introduction history, climatic suitability,
species characteristics and interactions thereof explained establishment and spread of Chinese woody species in Europe.
Location
Europe (non-native range) and China (native range) Methods
We tested how establishment success of 449 Chinese woody species in Europe was linearly or non-linearly associated with residence time (time since earliest planting), planting frequency, climatic suitability, various traits and native range size in China, and with interactions between these variables. For the 38 out of the 449 species that have established, we also tested how these variables and their interactions explained spread of these species in Europe.
Results
Establishment of the 449 species was positively associated with residence time, planting frequency and climatic suitability. However, residence time was not important for spread of the 38 established species. None of the traits had significant main effects on establishment, but having a longer flowering period and compound leaves favored spread of established species. However, the positive association between establishment success and residence time was stronger for evergreen than for deciduous species, and evergreen species, in contrast to deciduous ones, showed a positive association between establishment success and fruiting duration. Moreover, spread of the established species was positively associated with planting frequency
12 for compound-leaved but not for simple-leaved species, and its association with
fruiting duration went from negative to positive with increasing climatic suitability.
Main conclusions
We show explicitly that the role of some traits in the invasion process depends on the values of other factors. This could explain inconsistent results of previous studies, and implies that future studies should explicitly address how various factors interactively co-determine success of non-native plants.
Keywords
Alien plants, naturalization, invasion, year of introduction, propagule pressure, biomod2, climatic niche, flowering and fruiting phenology, maximum height
Introduction
More than 13,000 plant species have established permanent populations outside their native ranges (van Kleunen et al. 2015). The spread and dominance of some of these non-native plants can constitute a major threat to natural ecosystems (Pimentel 2002). Given that not all of the many introduced non-native plants have established self-sustaining populations in the wild, and only few of these spread to large degrees in the new range (Blackburn et al. 2011), a major challenge in ecology is to
disentangle the mechanisms underlying success of non-native plants at different invasion stages (Theoharides & Dukes 2007; van Kleunen, Dawson & Maurel 2015).
In particular, it is essential to explicitly unravel how historical factors, environmental factors and species characteristics codetermine establishment and spread (sensu Blackburn et al. 2011) in the new range (Richardson & Pyšek 2012; Kempel et al.
2013; van Kleunen, Dawson & Maurel 2015).
Historical factors, such as when and how frequently a non-native species has been introduced, are likely to affect the chances of establishment and subsequent spread of the species in the wild (Lockwood, Cassey & Blackburn 2005; Bucharova &
van Kleunen 2009; Pyšek, Křivánek & Jarošík 2009). However, due to a dearth of quantitative data on the actual year of introduction, especially for large numbers of non-native species, studies have often used the time since first record in the wild (Richardson & Pyšek 2006). This has the disadvantage that it excludes those species that failed to establish after introduction (Kowarik 1995). Furthermore, most studies used indirect proxies of introduction frequency (propagule pressure), such as the intensity of global commercial trade and tourism (Seebens et al. 2015), instead of more direct proxies, such as planting frequency (Bucharova & van Kleunen 2009;
Pyšek, Křivánek & Jarošík 2009). Therefore, we need studies that account for and assess the role of introduction history on establishment success and subsequent
14 spread of non-native plants by using data on the year of actual introduction and
planting frequency.
Environmental variables related to, for example, climate, soil type and resource availability are another set of factors that may influence establishment and spread of non-native plants in new ranges (Theoharides & Dukes 2007). Climate in particular is likely to be a major environmental filter determining whether non-native plants can survive, grow and reproduce, and thereby establish populations and spread in new ranges (Richardson & Pyšek 2012). Niche-based species distribution models
(SDMs), parameterized with data from the native range, have been frequently used to assess occurrence probability of non-native species in new ranges (Thuiller et al.
2005). However, to the best of our knowledge, the role of climatic suitability in
establishment success has not been tested explicitly yet by correlating the predicted occurrence probability from SDMs with the actual establishment success and spread of non-native plants.
The traits of a species reflect its ecological strategies (associated with survival, growth, reproduction and dispersal), and mediate its responses to abiotic and biotic environmental factors (Pérez-Harguindeguy et al. 2013). Therefore, species traits have the potential to determine large-scale establishment and spread patterns of non-native plants (Baker 1974; Pyšek & Richardson 2007; van Kleunen, Weber &
Fischer 2010; van Kleunen, Dawson & Maurel 2015). For instance, some studies have shown that success of non-native plants is positively associated with the length of the flowering period (e.g. Chrobock et al. 2013; Gallagher, Randall & Leishman 2015), most likely because a long flowering period may lead to a greater reproductive output. Moreover, as a biogeographic characteristic, the native range size of plants may explain their distribution in a new region, by reflecting their environmental tolerance and/or dispersibility (Gaston 2003; Hui et al. 2011). Although there has
been intensive research on the roles of species characteristics of introduced non- native plants, it is still not clear how important these characteristics are.
Despite evidence for the role of various factors in establishment success and spread of non-native plants, studies do not always find consistent results (Pyšek &
Richardson 2007; van Kleunen, Dawson & Maurel 2015). A likely explanation for the inconsistent results among studies is that the role of certain factors in establishment success and spread of non-native plants is context-dependent (Kueffer, Pyšek &
Richardson 2013; van Kleunen, Dawson & Maurel 2015). However, surprisingly few studies have explicitly addressed the nature of this context-dependency within a single study by testing for interactions among the various factors (but see Küster et al. 2008). Furthermore, while most studies implicitly assume linear relationships between establishment success or spread and potential explanatory variables, some relationships might be non-linear (van Kleunen, Dawson & Maurel 2015). Therefore, to better understand how and in which context certain factors relate to establishment and spread of non-native plants, we need studies that consider non-linear
relationships and interactions between the various factors.
In this study, we tested how establishment success of 449 woody species (that have been introduced from China to Europe) in Europe is associated with linear and non-linear effects of residence time, planting frequency, climatic suitability and
species characteristics, and with interactions between these variables. In addition, for 38 out of the 449 species that have established in Europe, we also tested how their further spread in Europe is associated with these variables and their interactions.
16 Methods
Compilation of data set
We compiled a data set of 449 woody species (276 shrubs, 142 trees and 31 lianas) that have all been deliberately introduced to Europe (i.e. planted in European gardens) from their native range in China (or Japan), since the 16th century (Goeze 1916). For each species, we checked in the DAISIE database (http://www.europe- aliens.org/, last accessed on July, 2014) whether it has become established or not in each of the 15 European countries for which we had data on planting frequency (see below). We calculated residence time of each of the 449 species in Europe by
subtracting the year of its earliest planting in European gardens, as reported in Goeze (1916) and Bärtels (2001), from 2014. To quantify planting frequency for each species, we counted the number of gardens (i.e. botanic gardens, arboreta and parks) listed in Bartels et al. (1982) that the species has been planted in (for locations of the gardens, see Appendix S1 in Supporting Information). This planting-frequency data was available for the following 15 European countries: Austria (16 gardens listed), Belgium (3), Czech Republic (28), Denmark (3), Finland (5), France (4), Germany (103), Hungary (4), the Netherlands (10), Norway (2), Poland (5), Romania (1), Slovakia (2), Sweden (4) and Switzerland (8). As a proxy of planting frequency of each species in Europe as a whole, we divided the total number of gardens where a species has been planted by 145 (i.e. the total number of gardens for which planting data were available). To estimate planting frequency of each species in each of the 15 countries separately, we divided the number of gardens in a country where a species has been planted by the total number of gardens listed for that country. The proportion of gardens is not an absolute measure of planting frequency but a proxy.
So, if a species was not planted in any of the gardens in a country for which we had data, its true planting frequency in that country is not necessarily zero, but likely to be
low.
To test whether species characteristics play a role in establishment and spread of the 449 Chinese woody species in Europe, we collected data on traits for each species from the Flora of China (Wu, Raven & Hong 1994–2010). The following traits were included: maximum height, growth form (tree, shrub or liana), earliest flowering month, flowering duration, earliest fruiting month, fruiting duration, sexual system (hermaphrodite, dioecious or monoecious), leaf retention (deciduous or evergreen), leaf type (simple or compound), leaf size (i.e. maximum length of a simple leaf or of a leaflet for compound-leaved species) (Table 1). Maximum height of a plant is likely to be associated with its competitive ability and dispersibility (Pyšek, Křivánek & Jarošík 2009; Thomson et al. 2011). The traits on flowering and fruiting phenology and on sexual system are relevant to plant reproduction, and therefore these traits might influence establishment and spread of non-native plants in new ranges (Baker 1974;
van Kleunen, Weber & Fischer 2010). Leaf traits of a species reflect its strategies to adapt to seasonality and its ability to utilize light (Pérez-Harguindeguy et al. 2013), and therefore might also be important in the invasion process of non-native plants. In addition, as a measure of the native range size, we calculated the proportion of grid cells in which the species occurs in China (4017 grid cells in total) (Fang, Wang &
Tang 2011).
Bioclimatic niche-based modeling
We assessed climatic suitability of each of the 449 Chinese woody species in the 15 European countries (for which we had planting-frequency data) based on the native distribution of each species in China, using BIOMOD, a niche-based ensemble platform for species distribution modeling (Thuiller et al. 2009). Details on the
distribution modeling are provided in Appendix S2. In short, we obtained the
distribution of each species in its native range from an atlas of woody plants in China,
18 with a resolution of 0.5 degree (c. 50 × 50 km) (Fang, Wang & Tang 2011). A set of 19 bioclimatic variables, known to be relevant determinants of species distributions, was obtained from WorldClim (http://www.worldclim.org/) for both China and Europe (Hijmans et al. 2005) (Table S1, see Appendix S2). We first used BIOMOD to
calibrate models by correlating the occurrence of each species with the 19 bioclimatic variables in the native range. After this, we projected the calibrated model onto
Europe to assess climatic suitability of each species in each 0.5 degree grid cell (c.
50 × 50 km) of the 15 European countries (1847 grid cells). Since we expected a species to be able to establish in Europe as soon as the climate in some of its parts is suitable, even if the rest of Europe is climatically not very suitable, we used the maximum instead of the median or mean climatic suitability of the 15 European countries considered. Similarly, we also assigned each country a value of climatic suitability by taking the maximum suitability over all grid cells in that country.
BIOMOD was implemented in R package ‘biomod2’ (Thuiller, Georges & Engler 2014).
Data analysis
To assess how introduction historical factors, environmental factors and various species characteristics, as well as their interactions are related to the establishment success and spread of the Chinese woody species in Europe, we did two major sets of analyses. First, we analyzed the complete data set of all 449 Chinese woody species to test how their establishment success in Europe as a whole (i.e.
established in Europe yes or no) was explained by different variables and their
interactions. Second, we analyzed the subset of 38 Chinese woody species that have established in at least one of the 15 European countries with planting frequency data, to test how different variables as well as their interactions determined their
establishment success in each of the 15 European countries (i.e. their spread in
Europe).
1. Establishment success of the 449 species in Europe
We used generalized linear mixed-effects models with a binomial error distribution to test whether the establishment success of the 449 Chinese woody species in Europe (i.e. whether they have established in at least one of the 15
countries for which we had planting data) could be explained by linear and non-linear (i.e. quadratic) components of residence time, planting frequency, climatic suitability, various species characteristics and interactions between these variables. As we had many explanatory variables (Table 1), relative to the number of observations (n=449), we could not include all of them both as linear and quadratic terms, as well as all pairwise interactions between the variables in a single model. Therefore, to avoid overfitting, we stepwise built a minimum adequate model by largely following the procedure recommended by Hosmer Jr and Lemeshow (2004). First, we ran
separate models for each explanatory variable to test for the significance of its linear effect and, in the case of a continuous variable, also its non-linear effect. Each continuous variable was centered on a mean of zero and scaled to a standard deviation of one. Second, to test for the significance of interactions between variables, we ran separate models for each possible pairwise combination of the explanatory variables. However, as some of the categories of the variable ‘sexual system’ (dioecious, monoecious, hermaphrodite) did not contain all levels of the other variables, we could not fit interactions associated with sexual system. In both steps, the significance of each term was assessed with log-likelihood-ratio tests comparing models with and without the term of interest. Finally, we ran a multivariate model including all linear, quadratic and interaction terms that were significant or marginally significant (α=0.1) in one of the preceding two steps. To find a minimum adequate model, we then removed the non-significant terms (α=0.05) one by one from the
20 multivariate model, starting with the least significant interaction term. We repeated
this until only significant interactions remained. Then, to test the significance of the quadratic term of each variable, we first made a reference model from which all interactions were removed. After this, we removed the non-significant terms (α=0.05) one by one from the multivariate model, starting with the least significant quadratic term, followed by the corresponding linear term. This process was repeated until we had a minimum adequate model in which all variables had significant (α=0.05) linear, quadratic and/or interaction terms. Model fit was assessed by calculating the
marginal R2 (pseudo-R2), indicating the variance explained by fixed factors, following Nakagawa and Schielzeth (2013). In all these models, we accounted for phylogenetic non-independence of the species by including family as a random factor. All analyses were done in R version 2.15.3 (R Core Team 2013), and the generalized linear
mixed-effects models were run with the R package ‘lme4’ (Bates et al. 2013).
2. Spread of the 38 species that have established in Europe
For the subset of 38 species that have established in at least one of the 15 European countries, we tested how their establishment success across these 15 countries (i.e. their spread) was explained by the same variables and interactions used in the first set of analyses. We followed the same approach as in the first set of analyses to find a minimum adequate model. The response variable was the
establishment success (established, non-established) of each species in each of the 15 European countries. In other words, we had 15 observations for each species, one for each of the 15 countries. Accordingly, we used country-level estimates of planting frequency and climatic suitability instead of Europe-wide estimates. As
random factors, we included species and country to account for non-independence of observations for the same species in different countries and for the same country among different species. We also tried to include random slopes with species or
country in the models, but as these models did not converge, we did not further consider them.
Three of the 38 species showed significant spatial autocorrelation in their spread in Europe, based on Moran’s I index, calculated using coordinates of geographic center of each country with R package ape (Paradis, Claude & Strimmer 2004).
Therefore, to account for spatial autocorrelation, we also redid the analysis with generalized linear mixed-effects models including the geographic coordinates of the countries using the function corrHLfit in the R package spaMM (Rousset & Ferdy 2014). However, as the results (Appendix S4) were very similar to the ones from the model without correcting for spatial autocorrelation, we only present the latter in the paper.
22 Results
Establishment success of the 449 non-native woody species
Of all variables with significant (α=0.05) or marginally significant (α=0.1) terms in the univariate and bivariate models that were part of the model reduction steps (Table 1; also Table S3 in Appendix S3), residence time, planting frequency, climatic suitability, fruiting duration and leaf retention were retained in the minimum adequate multivariate model (marginal R2=0.735). In this model, the probability of
establishment of the 449 woody species in Europe significantly increased with residence time, planting frequency and climatic suitability (Table 2; Fig. 1). None of the main terms of the species traits (see Table 1 for an overview) was significantly associated with establishment success (Table 2). However, interactions between leaf retention and residence time, and between leaf retention and fruiting duration were significant (Table 2). The increase in establishment probability with residence time was stronger for evergreen than for deciduous species (Fig. 2(a)). Moreover,
establishment probability increased with fruiting duration for evergreen species, while it decreased with fruiting duration for deciduous ones (Fig. 2(b)).
Spread of the 38 established woody species
Of all variables with significant (α=0.05) or marginally significant (α=0.1) terms in the univariate and bivariate models that were part of the model reduction steps (Table 3; also Table S4, see Appendix S3), planting frequency, climatic suitability, flowering duration, fruiting duration and leaf type were retained in the multivariate minimum adequate model (marginal R2=0.333). In this model, the spread of the 38 established woody species significantly increased with planting frequency, climatic suitability and flowering duration, but not with residence time (Table 4; Fig. 3(a)-(c)).
Spread of the woody species was non-linearly related to climatic suitability (Table 4;
Fig. 3(b)): it increased with climatic suitability from intermediate to high climatic
suitability (values higher than ca. 0.6), but little change or even a slight decrease in spread with climatic suitability was observed when climatic suitability is low.
Moreover, woody species with compound leaves had a significantly higher
establishment success per country than the ones with simple leaves (Fig. 3(d), Table 4).
Although most of the species traits had no significant main effects, the interaction between planting frequency and leaf type, and the interaction between climatic suitability and fruiting duration were significant (Table 4). For species with compound leaves, the probability of establishment per country strongly increased with planting frequency, while there was no such increase for the ones with simple leaves (Fig. 4(a)). Furthermore, the probability of establishment per country
increased with fruiting duration when climatic suitability was very high, while the opposite was true when climatic suitability was intermediate or low (Fig. 4(b)).
24 Discussion
In our study, only 38 of the 449 introduced Chinese woody species have become established in the wild in Europe. This low rate of successful establishment is in line with the idea that only few of the introduced non-native plants can manage to
reproduce and establish in new ranges (Williamson & Fitter 1996). The establishment success of the 449 species in Europe was positively associated with residence time, planting frequency and climatic suitability. These factors, except for residence time, were also positively associated with the further spread of the 38 established woody species in Europe, which indicates stage-dependence of the role of residence time (Richardson & Pyšek 2012). In addition, although spread was explained by flowering duration and leaf type (compound, simple), establishment success was only
associated with some of the traits (e.g. leaf retention, fruiting duration) through their interactions with other factors (e.g. residence time). Moreover, leaf type and fruiting duration played roles in spread through interactions with planting frequency and climatic suitability, respectively. This study is therefore among the first to empirically show that the importance of species traits during the invasion process is context dependent.
Residence time and planting frequency
The establishment success of the 449 species in Europe was higher if the species had been introduced earlier and planted more frequently. This is in line with expectations (Richardson & Pyšek 2006), and implies that in the future, when residence time has increased, some of the currently non-established species might manage to establish, particularly if their planting frequencies also increase. However, after a woody species had become established, and thus had managed to overcome the reproductive barrier (Richardson & Pyšek 2006), residence time no longer played a significant role in its further spread in Europe. This indicates that the effect of
residence time is invasion-stage dependent (Richardson & Pyšek 2012; van Kleunen, Dawson & Maurel 2015), and that other factors, such as propagule pressure and dispersal ability, might be more important than residence time for spread after establishment (Theoharides & Dukes 2007).
Most of our woody species have been introduced for horticultural purposes, and a higher planting frequency of them may have fostered their establishment and spread in Europe. Indeed, planting frequency, which was available for each of the European countries considered in the analysis, was positively related to both the establishment success of the 449 introduced woody species and the subsequent spread of the 38 established ones. Most previous studies on non-native woody species have also shown that increasing planting frequency fosters local and regional establishment (Křivánek, Pyšek & Jarošík 2006; Bucharova & van Kleunen 2009; Pyšek, Křivánek &
Jarošík 2009). Therefore, we conclude that planting frequency is a consistent driver of establishment and spread of non-native woody species.
The individual contributions of residence time and planting frequency are difficult to separate as a long residence time may also have resulted in a more widespread planting of the species. In our data set, planting frequency and residence time were only weakly positively correlated (r=0.198, n=449, p<0.001; also see Fig. S7(a) in Appendix S3), and establishment success was positively associated with each variable after accounting for the other in the analysis. This indicates that residence time and planting frequency are not completely confounded, and have partly independent contributions to establishment success and subsequent spread.
Climatic suitability
The availability of suitable ecological (e.g. climatic) niches is likely to be a major determinant of the potential geographic distribution of non-native plants (Thuiller et al.
2005; Petitpierre et al. 2012). In support of this, we found that species with a highly
26 suitable climate in Europe (based on their climatic niches in China) were more likely to establish and spread than species for which this is not the case. Interestingly, the probability of establishment per country (i.e. spread) rapidly increased above an intermediate climatic suitability (Fig. 3(b)). This indicates that climatic suitability only increased spread of the established species above a certain threshold. Furthermore, this shows that studies on drivers of the establishment and spread of non-native species should also consider non-linear relationships.
The fact that some species with low or intermediate climatic suitability have nevertheless managed to establish (Figs 1(c) and 3(b)) indicates that not all species have filled their fundamental climatic niche space in their native range or that it was not captured by their distribution in China. Alternatively, it may suggest climatic niche shifts of the non-native populations after introduction of the species from their native range, as shown for several invasive species in recent studies (e.g. Broennimann et al. 2007). Nevertheless, the overall positive association between climatic suitability and establishment success and spread indicates that climate niches of species tend to be conserved between ranges (Petitpierre et al. 2012). This shows that climate is an important environmental driver in the invasion process, at least so for the 449 Chinese woody plants in Europe, although other environmental factors such as soil type and resource availability, which may correlate with climate, could also play a role.
Species characteristics and their interactions with other variables
Few, if any, traits have been reported to be universally associated with establishment or spread of non-native plants (Pyšek & Richardson 2007; van Kleunen, Weber & Fischer 2010). Therefore, it has frequently been suggested that the importance of species traits in establishment success or spread is context- dependent (Richardson & Pyšek 2012; Funk 2013; van Kleunen, Dawson & Maurel
2015). Surprisingly, this has rarely been tested explicitly. In our study, none of the species traits (maximum height, flowering and fruiting phenology, growth form, sexual system, and leaf retention, type and size) had significant main effects on the
establishment success of the 449 Chinese woody species in Europe. However, in line with the idea of context dependency, some species traits were important through their interactions with other factors (Fig. 2). Evergreen and deciduous Chinese woody species were introduced to Europe at similar times (t=0.201, df=245, p=0.841), and did not differ in their overall establishment success in Europe. However, the positive effect of residence time on establishment was stronger for evergreen species than for deciduous ones (Fig. 2(a)). Moreover, although evergreen and deciduous species did not differ, on average, in fruiting duration (F1,447=0.01, p=0.925), the evergreen ones were more likely to establish when they had a longer fruiting period, while the
opposite was true for the deciduous ones (Fig. 2(b)). For instance, most of the
evergreen species (e.g. Ligustrum lucidum and Pittosporum tobirahas) with a fruiting duration more than six months have successfully established in Europe, whereas most of the deciduous ones (e.g. Rhododendron yunnanense, Vitis flexuosa) with a similarly long fruiting duration have not established in Europe. This is possibly because a longer fruiting period, which is correlated with a longer flowering period (r=0.460, n=449, p<0.001), could promote reproductive success of the evergreen species that can photosynthesize and grow over most time of a year, while a long fruiting period might be very risky for many deciduous ones, which have a restricted growing season.
Among the 38 species that have established in Europe, the ones with a more extended flowering period spread to a larger extent across the European countries.
This finding is in line with the results of many previous studies (e.g. Küster et al.
2008; Chrobock et al. 2013; Gallagher, Randall & Leishman 2015), although some
28 other studies failed to detect such a relationship (Thompson, Hodgson & Rich 1995).
A longer flowering period may allow plants to allocate more resources to reproduction over the entire year. Moreover, for species that rely on pollinators for reproduction, a longer flowering period can also increase the likelihood that the activity period of suitable pollinators overlaps with the flowering period. Therefore, a longer flowering period may lead to a greater annual reproductive output, and hence a greater potential for spread of established species (Baker 1974).
Phenological traits of species are frequently dependent on climatic factors (Cleland et al. 2007; Sedlacek et al. 2015), and having the wrong phenology in the wrong climate may prevent reproduction and thus hinder spread of non-native plants.
This appeared to be the case in our study, because the further spread of the 38 established species in Europe was only positively associated with fruiting duration when climatic suitability was high, while the association was even negative when climatic suitability was low (Fig. 4(b)). Other studies on woody plants have shown that those that have become invasive often have a longer fruiting period (Reichard &
Hamilton 1997; Harris 2008). These other studies, however, did not test for
interactions and the pool of non-native species they considered might all have been climatically suitable for the study region. This might have prevented many studies from detecting the climate-context dependence of phenological traits.
Among the 38 woody Chinese species that have established in Europe, those with compound leaves had overall a higher probability of spread in Europe than the ones with simple leaves (Fig. 3(d)). The architecture of compound leaves is thought to promote light capture, and may be an adaptation that allows rapid growth
(Malhado et al. 2010). Therefore, our results may indicate that the compound-leaved woody plants are better able to maintain growth and thereby establish self-sustaining populations and spread than simple-leaved ones. However, the difference in spread
between species with compound leaves and the ones with simple leaves was only apparent for species that had a high planting frequency per country; at low planting frequencies both groups of species had low spread (i.e. establishment success per country) (Fig. 4(a)). This suggests that the advantage of having compound leaves may not be realized with insufficient planting frequency. Again, this emphasizes that the role of species traits in the success of non-native plants is dependent on other factors.
Some species characteristics, such as maximum plant height and native range size that have frequently been reported to be associated with success of non-native plants (e.g. Bucharova & van Kleunen 2009; Hui et al. 2011; Gallagher, Randall &
Leishman 2015), did not appear to be important for establishment and spread of species in our study. For maximum plant height, we found that in the bivariate model its effect on establishment depended on growth form; there was a relatively strong positive effect of height among lianas, an intermediate effect among shrubs and no or a very weak effect among trees (Table S3 and Fig. S4(b) in Appendix S3). However, this interaction was not retained as significant after inclusion of other variables in the minimum adequate multivariate model. Similarly, although native range size in China had a significant positive effect on establishment success in the univariate model (Table 1, Fig. S3(d) in Appendix S3), it was also not retained as significant in the minimum adequate multivariate model. Native range size is usually thought to be associated with success of non-native plants in new ranges because it may reflect environmental tolerance and dispersibility (Gaston 2003; Hui et al. 2011), and also because it may affect the chance that a species is picked up and introduced elsewhere. In line with the idea that species with a large native range size have a high environmental tolerance, climatic suitability was positively correlated with native range size (for establishment: r=0.596, n=449, p<0.001; for spread: r=0.540, n=570,
30 p<0.001; Fig. S7(d) and Fig. S8 in Appendix S3). The fact that we explicitly
accounted for climatic suitability as well as for introduction history in the multivariate model could explain why native range size was then not significant anymore. So, it is likely that native range size is frequently associated with establishment and spread of non-native species because it is a proxy for other factors (e.g. climatic suitability) that are not explicitly included in the analyses but contribute to establishment and spread.
Overall, our results, in particular the empirical evidence for context-
dependencies, could help to explain the frequently mixed findings of previous studies testing for the role of various factors in the success of non-native plants. Therefore, our results imply that future studies should explicitly assess the roles of potentially relevant factors in the invasion process by considering them and their interactions together. This is an essential step before we can fully understand the causes of establishment and spread of non-native plants outside their native ranges.
Acknowledgements
YHF and LN are grateful to the support by the China Scholarship Council (CSC).
NM and MvK acknowledge support by the DFG (grant KL 1866/5-1). We thank David J. Currie, Erica Fleishman and two anonymous referees for valuable comments on a previous version of the manuscript. We thank Wayne Dawson for English corrections.
32 Biosketch of Yanhao Feng
I am currently in the final year of my PhD in the Ecology group headed by Prof.
Mark van Kleunen at the University of Konstanz. My research interests lie in understanding the processes that shape and maintain species diversity in natural ecosystems, as well as assessing the impact of anthropogenic environmental changes, such as plant invasion and climate change, on species diversity and ecosystem functioning.
Supporting information
Appendix S1 Location of the gardens in Europe Appendix S2 Bioclimatic niche-based modeling
Appendix S3 Results of the univariate and bivariate models
Appendix S4 Results of analysis accounting for spatial autocorrelation
34 Table 1 Results of generalized linear mixed-effects models testing the linear and non-linear (i.e. quadratic) effects of each single explanatory variable (univariate models), and the effect of interactions between all pairwise combinations of the explanatory variables (bivariate models), on the establishment success of 449 Chinese woody species in Europe.
Variable* Explanation Linear effect Non-linear effect Interaction‡
df χ2 p* df χ2 p*
Introduction history
Residence time Years since introduction to Europe 1 34.61 <0.001 1 0.04 0.848 yes Planting frequency Proportion of gardens in which the
species was planted in Europe
1 48.85 <0.001 1 1.02 0.313 no Climatic suitability Maximum of weighted mean occurrence
probability in Europe (between 0 and 1)
1 11.63 0.001 1 1.11 0.292 no Species traits
Maximum height Maximum height (m) 1 2.30 0.129 1 0.46 0.499 yes
Earliest flowering month From 1 (January) to 12 (December) 1 2.50 0.114 1 2.62 0.105 no Flowering duration Number of flowering months 1 0.15 0.698 1 0.33 0.565 yes Earliest fruiting month From 1 (January) to 12 (December) 1 0.21 0.644 1 2.21 0.137 yes Fruiting duration Number of fruiting months 1 0.03 0.866 1 2.43 0.119 yes
Growth form Tree, shrub, liana 2 3.54 0.171 --- --- --- yes
Sexual system Dioecious, hermaphrodite, monoecious 2 0.46 0.796 --- --- --- ---
Leaf retention Deciduous, evergreen 1 0.25 0.615 --- --- --- yes
Leaf type Simple, compound 1 0.03 0.854 --- --- --- no
Leaf size Maximum leaf, or leaflet, length (cm) 1 0.11 0.746 1 0.05 0.827 yes Native range size Number of grid cells in China where a
species occurs
1 17.11 <0.001 1 0.25 0.620 no
* Variables with significant (α=0.05) or marginally significant (α=0.1) effects are printed in bold or bold italic, respectively.
‡ The “Interaction” column indicates whether an explanatory variable was significant (α=0.05, “yes” in bold) or marginally significant (α=0.1, “yes” in bold italic) in at least one of the interaction terms involving the explanatory variable in any of the bivariate models (for more details, see Table S3 in Appendix S3).
36 Table 2 Results of the minimum adequate model testing the linear and non-linear
(i.e. quadratic) effects of each single explanatory variable, and the effect of interactions between the explanatory variables, on the establishment success of 449 Chinese woody species in Europe. The marginal R2 indicating the variance explained by fixed factors in the model is 0.735.
Fixed
Variable or interaction* df χ2 p*
Introduction history
Residence time in Europe 1 20.92 <0.001 Planting frequency in Europe 1 36.82 <0.001 Climatic suitability in Europe 1 4.40 0.036 Species traits
Fruiting duration 1 0.01 0.917
Leaf retention 1 0.08 0.778
Interactions
Leaf retention: Residence time 1 4.25 0.039 Leaf retention: Fruiting duration 1 3.96 0.047
Random Variance SD
Family 0.133 0.364
* Variables and interactions with significant (α=0.05) effects are printed in bold.
Table 3 Results of generalized linear mixed-effects models testing the linear and non-linear (i.e. quadratic) effects of each single explanatory variable (univariate models), and the effect of interactions between all pairwise combinations of the explanatory variables (bivariate models), on the spread of 38 established Chinese woody species in 15 European countries.
Variables* Explanation Linear effect Non-linear effect Interaction‡
df χ2 p* df χ2 p*
Introduction history
Residence time Years since introduction to Europe 1 0.70 0.401 1 1.26 0.262 yes Planting frequency Proportion of gardens in which the
species was planted per country
1 6.63 0.010 1 0.29 0.590 yes Climatic suitability Maximum of weighted mean occurrence
probability per country
1 5.73 0.017 1 4.59 0.032 yes Species traits
Maximum height Maximum height (m) 1 1.18 0.278 1 0.26 0.609 no
Earliest flowering
month From 1 (January) to 12 (December) 1 0.35 0.552 1 0.38 0.538 yes Flowering duration Number of flowering months 1 3.22 0.073 1 0.01 0.943 no Earliest fruiting month From 1 (January) to 12 (December) 1 0.35 0.552 1 0.35 0.553 yes Fruiting duration Number of fruiting months 1 0.44 0.506 1 0.23 0.631 yes
Growth form Tree, shrub, liana 2 1.21 0.545 --- --- --- no
Sexual system Dioecious, hermaphrodite, monoecious 2 4.85 0.088 --- --- --- ---
Leaf retention Deciduous, evergreen 1 1.68 0.195 --- --- --- yes
Leaf type Simple, compound 1 4.36 0.037 --- --- --- yes
Leaf size Maximum leaf, or leaflet, length (cm) 1 0.41 0.522 1 0.03 0.872 no Native range size Number of grid cells in China where a
species occurs 1 0.61 0.436 1 1.99 0.158 yes
38
* Variables with significant (α=0.05) or marginally significant (α=0.1) effects are printed in bold or bold italic, respectively.
‡ The “Interaction” column indicates whether an explanatory variable was significant (α=0.05, “yes” in bold) or marginally significant (α=0.1, “yes” in bold italic) in at least one of the interaction terms involving the explanatory variable in any of the bivariate models (for more details, see Table S4 in Appendix S3).
Table 4 Results of the minimum adequate model testing the linear and non-linear (i.e.
quadratic) effects of each single explanatory variable, and the effect of interactions between the explanatory variables, on the spread of 38 established Chinese woody species in 15 European countries. The marginal R2 indicating the variance explained by fixed factors in the model is 0.333.
Fixed
Variable or interaction* df χ2 p*
Introduction history
Planting frequency in European country 1 7.42 0.006 Climatic suitability in European country 1 5.10 0.024 (Climatic suitability in European country)2 1 4.15 0.042 Species traits
Flowering duration 1 5.28 0.022
Fruiting duration 1 1.64 0.201
Leaf type 1 8.90 0.003
Interactions
Planting frequency: Leaf type 1 7.64 0.006 Climatic suitability: Fruiting duration 1 6.38 0.012 Random
Variance SD
Species 0.104 0.322
Country 1.565 1.251
* Variables and interactions with significant (α=0.05) effects are printed in bold.
