Reproductive characteristics as drivers of alien plant naturalization and invasion

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Reproductive characteristics as drivers of alien plant naturalization and invasion

Dissertation submitted for the degree of Doctor of Natural Sciences

presented by

Mialy Harindra Razanajatovo

at the

Faculty of Sciences Department of Biology

Date of the oral examination: 12 February 2016 First referee: Prof. Dr. Mark van Kleunen

Second referee: Prof. Dr. Markus Fischer

Konstanzer Online-Publikations-System (KOPS) URL: http://nbn-resolving.de/urn:nbn:de:bsz:352-0-324483

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Summary

Due to human activity and global movements, many plant species have been introduced to non-native regions where they experience novel abiotic and biotic conditions. Some of these alien species manage to establish reproducing naturalized populations, and some naturalized alien species subsequently become invasive. Invasion by alien plant species can negatively affect native communities and ecosystems, but what gives the alien species an advantage under novel conditions is still not clear. Therefore, identifying the drivers of invasions has become a major goal in invasion ecology.

Reproduction is crucial in plant invasions, because propagule supply is required for founding new populations, population maintenance and spread in non-native regions. Baker’s Law, referring to the superior advantage of species capable of uniparental reproduction in establishing after long distance dispersal, has received major interest in explaining plant invasions. However, previous findings regarding Baker’s Law are contradicting. Moreover, there has been an increasing interest in understanding the integration of alien plant species into native plant-pollinator networks but few studies have looked at the pollination ecology of successful (naturalized and invasive) and unsuccessful (non-naturalized and non-invasive) alien plant species. Previous findings are also biased towards specific taxonomic groups and

geographical areas. More generalized approaches are required to advance our knowledge of the role of reproductive characteristics in alien plant naturalization and invasion.

Our quantitative breeding-system database of 1752 species from 116 regions around the globe, combined with data on species’ native range size and global naturalization success, is a powerful tool for testing Baker’s Law in alien plant naturalization. Consistent with Baker’s Law, our results show that selfing ability (self-compatibility and autofertility) is positively related to naturalization success. The effects are both direct and indirect, as selfing ability has a positive effect on native range size, which in turn has a positive effect on naturalization. We demonstrate that selfing ability contributes to naturalization, which strongly suggests that a lack of mates and pollinators is an important barrier to the establishment of alien plant species.

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To test whether alien plant naturalization is related to the ability to attract resident pollinators in non-native regions, we did a comparative study on flower visitation of 185 native, 37 naturalized alien and 224 non-naturalized alien plant species in the Botanical Garden of Bern, Switzerland. Botanical gardens offer unique opportunities for hosting comparative studies because species from a broad taxonomic range and from a wide geographic area are growing under comparable conditions. Our phylogenetically-informed analysis showed that non- naturalized alien species received fewer flower visits than both naturalized alien and native species. Native, naturalized alien and non-naturalized alien species were visited by similar flower visitor communities. Furthermore, among the naturalized alien species, those with a broader distribution in Switzerland received a more diverse set of flower visitors. We provide the first evidence that the capacity to attract flower visitors in non-native regions is different for

naturalized and non-naturalized alien plants, which strongly suggests that naturalization is related to flower visitation.

To test whether pollen limitation and low autofertility are important constraints to invasion, we performed a common garden breeding-system experiment. Using pollination treatments (pollen supplementation, open pollination, and pollinator exclusion), we assessed the degrees of pollen limitation and autofertility of 24 native and alien (both invasive and non- invasive, but naturalized) plant species (eight confamilial or congeneric triplets). The three plant groups had low degrees of pollen limitation and were almost all autofertile to some degree. The groups did not differ in their degrees of pollen limitation or autofertility. Because invasive alien species did not suffer lower pollen limitation and did not have higher autofertility than non- invasive aliens, our results suggest that pollen limitation and low autofertility may not play a major role in the spread of alien plants, once they have become naturalized.

Taken together, our findings strongly suggest that reproductive characteristics contribute to alien plant naturalization. Thus, a lack of mates and pollinators may be an important barrier to establishment in new non-native regions. A breeding system that favors uniparental reproduction and the ability to attract suitable pollinators may help alien plants successfully found and

maintain reproducing populations in non-native ranges. However, once the alien plant species becomes naturalized, reproductive characteristics may no longer play an important role. Other factors may be more important during invasion, when the alien plant species spread in the non- native ranges.

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Zusammenfassung

Wegen menschlichen Aktivitäten und globalen Bewegungen, sind viele Pflanzenarten in nicht-einheimische Regionen eingeführt worden, in denen sie neuen abiotischen und biotischen Bedingungen ausgesetzt werden. Einige dieser gebietsfremden Arten schaffen es, eingebürgerte sich fortpflanzende Populationen zu etablieren, und einige eingebürgerte gebietsfremde Arten werden anschließend invasiv. Invasion durch fremden Pflanzenarten kann einheimische Gemeinschaften und Ökosystemen negativ beeinflussen, aber es ist noch nicht klar was den gebietsfremden Arten einen Vorteil unter neuartigen Bedingungen gibt. Daher ist ein wichtiges Ziel der Invasionsökologie, die Treiber von Invasionen zu Identifizieren.

Reproduktion ist entscheidend bei Pflanzeninvasionen, weil Fortpflanzung für die Gründung, Instandhaltung und Ausbreitung neuer Populationen in nicht-einheimische Regionen erforderlich ist. Bakers Gesetz, welches sich auf die überlegenen Vorteile der Arten, die

uniparentaler Reproduktion fähig sind, bei der Einrichtung nach Langstreckenausbreitung bezieht, hat großes Interesse bei der Erklärung von Pflanzeninvasionen erhalten. Jedoch sind frühere Befunde über Bakers Gesetz widersprüchlich. Darüber hinaus gibt es ein wachsendes Interesse für das Verständnis der Integration von fremden Pflanzenarten in die einheimischen Pflanze-Bestäuber-Netzwerke, aber nur wenige Studien haben sich mit der Bestäubungsökologie von erfolgreichen (eingebürgerten und invasiven) und erfolglose (nicht eingebürgerte und nicht- invasiven) gebietsfremden Pflanzenarten befasst. Vorherige Ergebnisse sind auch auf bestimmte taxonomische Gruppen und Regionen eingeschränkt. Allgemeinere Ansätze sind erforderlich, um die Kenntnisse über die Rolle der reproduktiven Eigenschaften gebietsfremder Pflanzen in der Einbürgerung und Invasion zu verstehen.

Unsere quantitative Fortpflanzungssystem-datenbank mit 1752 Arten aus 116 Regionen der Welt, kombiniert mit Daten über die Ausbreitung der einheimischen Arten, ist ein

leistungsfähiges Mittel um Bakers Gesetz zu testen. In Übereinstimmung mit Bakers Gesetz, zeigen unsere Ergebnisse, dass die Fähigkeit zur Selbstbefruchtung (Selbst-Kompatibilität und Autofertilität) positiv auf den Einbürgerungserfolg wirken. Die Effekte waren sowohl direkt als auch indirekt, da die Gebietsgröße proportional zur Selbstbefruchtungsfähigkeit ist, welche sich wiederum positiv auf die Einbürgerung auswirkt. Wir zeigen, dass die

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Selbstbefruchtungsfähigkeit positiv zur Einbürgerung beiträgt, was stark darauf hinweist, dass ein Mangel an Partnern und Bestäubern ein wichtiges Hindernis für die Einbürgerung von gebietsfremden Pflanzenarten ist.

Um zu testen, ob die Einbürgerung gebietsfremder Pflanzen mit der Fähigkeit,

einheimische Bestäuber in gebietsfremden Regionen anzuziehen verbunden ist, haben wir eine Vergleichsstudie über Blumenbesuche von 185 einheimische, 37 eingebürgerten und 224 nicht eingebürgerte Neophyten im Botanischen Garten in Bern , Schweiz, durchgeführt. Botanische Gärten bieten einzigartige Möglichkeiten um Vergleichsstudien durchzuführen, weil Arten aus vielen taxonomischen Bereichen und aus vielen geografischen Gebieten unter vergleichbaren Bedingungen gezüchtet werden können. Unsere phylogenetisch informierte Analyse zeigte, dass nicht eingebürgerte fremden Arten weniger Blütenbesucher als eingebürgerte fremden und einheimischen Arten erhielten. Einheimische, eingebürgerte fremde und nicht eingebürgerte fremde Arten wurden durch ähnliche Bestäuber Gemeinden besucht. Außerdem erhielten unter den eingebürgerten gebietsfremden Arten, die mit einer breiteren Verbreitung in der Schweiz, eine vielfältigere Gruppe von Blütenbesucher. Wir stellen den ersten Beweis dafür, dass die Fähigkeit, Blütenbesucher in nicht-native Regionen zu gewinnen, verschieden für eingebürgerten und nicht eingebürgerten fremde Pflanzen ist, was stark darauf hinweist, dass die Einbürgerung mit Blumenbesucher zusammenhängt.

Um zu testen, ob Pollen Begrenzung und niedrige Autofertilität eine wichtige

Einschränkungen für Invasionen sind, führten wir einen Fortpflanzungssystem Experiment aus.

Mit Hilfe von Bestäubungs-Behandlungen (Pollen Ergänzung, offene Bestäubung und Pollenspender Ausgrenzung), untersuchten wir die Grade der Pollenbegrenzung und Autofertilität von 24 einheimischen und fremden (beide invasive und nicht-invasive, aber eingebürgert) Pflanzenarten (acht confamiliäre oder artverwandte Drillinge). Die drei Pflanzengruppen hatten niedrige Grade der Pollenbegrenzung und waren fast alle zu einem gewissen Grad autofertil. Die Gruppen unterschieden sich nicht in ihrem Grad von Pollen Beschränkung oder Autofertilität. Da invasive gebietsfremde Arten nicht unteren Pollen

Begrenzung leiden und keine höhere Autofertilität als nicht-invasive fremde Arten hatten, legen unsere Ergebnisse nahe, dass Pollen Begrenzung und niedrige Autofertilität möglicherweise

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nicht eine wichtige Rolle bei der Verbreitung von gebietsfremden Pflanzen spielen, sobald sie sich eingebürgert haben.

Insgesamt deuten unsere Ergebnisse stark darauf hin, dass reproduktive Eigenschaften zur Einbürgerung fremder Pflanzenarten beitragen. So kann ein Mangel an Partnern und Bestäuber eine wichtige Barriere für die Einbürgerung in neuen nicht-native Regionen sein.

Fortpflanzungssysteme, welche die uniparentale Reproduktion und die Fähigkeit, geeignete Bestäuber anzulocken bevorzugen, können fremden Pflanzen helfen, erfolgreich sich fortpflanzende Populationen zu etablieren und zu erhalten. Sobald jedoch die fremden

Pflanzenarten eingebürgert sind, spielen Reproduktionseigenschaften möglicherweise nicht mehr eine wichtige Rolle. Andere Faktoren können während der Invasion wichtiger sein, wenn die fremden Pflanzenarten sich in den nicht-native Bereiche verbreiten.

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List of figures

Fig. I.1 Frequency distributions of self-compatibility and autofertility indices based on fruit set and seeds per flower compiled in a global database on breeding systems of angiosperms. ... 22 Fig. I.2 Results of six path analyses testing the direct and indirect effects of a species’ degree of self-compatibility and autofertility on its global naturalization success. Indices were calculated using fruit set. ... 24 Fig. I.S1 Procedure used for selection of studies for the compilation of a global database on breeding systems using Web of Science and other sources. ... 33 Fig. I.S2 A phylogenetic tree of the 1752 angiosperm species included in the global database on breeding systems. ... 34 Fig. I. S3 Results of six path analyses testing the direct and indirect effects of a species’ degree of self-compatibility and autofertility on its global naturalization success. Indices were calculated using seed production per flower. ... 35 Fig. II.1 (a) Total number of insect visits, (b) average duration of individual visits, (c) number of flower-visitor groups, and (d) Shannon-diversity indices of flower-visitor groups to native, naturalized alien and non-naturalized alien plant species in 15 minutes. ... 60 Fig. II.2 Probability of visits by different flower-visitor groups to native, to naturalized alien and to non-naturalized alien plant species. ... 62 Fig. III.1 Estimated means (±1 SE) of a binomial GLMM testing how the number of flowers that produced fruits (a) and estimated means (±1 SE) of a Poisson GLMM testing how the number of seeds per fruit (b) depended on pollination treatment (pollen-supplementation, open pollination, and pollinator-exclusion), plant group (native, invasive alien and non-invasive alien) and their interaction, with plant individual nested within species and species nested within family as random factors.. ... 107 Fig. III.2 Estimated means (±1 SE) of four phylogenetically controlled linear models testing how the pollen limitation index and the adjusted pollen limitation index (negative values set to zero) of 24 species (a) and how the autofertility index and the adjusted autofertility index (values

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larger than one set to one) of 23 species (b) depended on plant group (native, invasive alien and non-invasive alien) ... 109

Fig. III.S1 Fruit set and seed production in the three treatments (pollen supplementation, open pollination, pollinator exclusion) on eight confamilial triplets of native, invasive alien and non- invasive alien plant species. ... 117 Fig. III.S2 Phylogenetic tree of the 24 species used to test for differences in pollen limitation and autofertility among native, invasive alien, and non-invasive alien plant species in Germany. .. 121 Fig. III.S3 Correlation between autofertility and pollen limitation indices ... 122

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List of tables

Table I.1 Results of a phylogenetic logistic regression and two phylogenetic linear models testing how global naturalization success depend on native range size, monocarpy, self- compatibility index (based on fruit set), and the interaction between monocarpy and self-

compatibility index. ... 23 Table I.2 Results of a phylogenetic logistic regression and two phylogenetic linear models testing how global naturalization success depend on native range size, monocarpy, autofertility index (based on fruit set), and the interaction between monocarpy and autofertility index. ... 26

Table I.S1 Number of plant taxa of which breeding system data were documented. ... 36 Table I.S2 References used to add the remaining 486 species to a tree with 1266 tips in order to construct a phylogenetic tree of the 1752 species in the breeding system database. ... 37 Table I.S3 Results of a phylogenetic logistic regression and two phylogenetic linear models testing how global naturalization success depend on native range size, monocarpy, self- compatibility index (based on seed production per flower), and the interaction between

monocarpy and self-compatibility index. ... 46 Table I.S4 Results of a phylogenetic logistic regression and two phylogenetic linear models testing how global naturalization success depend on native range size, monocarpy, autofertility index (based on seed production per flower), and the interaction between monocarpy and

autofertility index. ... 47

Table II.1 Results of three phylogenetically corrected linear mixed-effects models testing how the number of insect visits, the average duration of individual visits, and the number of flower- visitor groups depend on traits related to conspicuousness of the plants and flowers and on

species status ... 59 Table II.2 Results of a linear mixed model testing how the Shannon-diversity index of flower- visitor groups depends on traits related to conspicuousness of the plants and flowers, and on status ... 61

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Table II.S1 List of the native, naturalized and non-naturalized alien plant species for which flower visitation was assessed, and the census data ... 69 Table II.S2 Number of plant species and average number of flower visitors observed during each observation census. ... 83 Table II.S3 List of references used to resolve polytomies within families for the phylogeny of native, naturalized and non-naturalized alien plant species for which flower visitation was

assessed. ... 84 Table II.S4 Plant and flower characteristics of native, naturalized and non-naturalized alien plant species ... 87 Table II.S5 Results of two linear mixed-effects models testing how the number of insect visits and the average duration of individual visits depend on the number of observed flower units and plant species status ... 88 Table II.S6 Results of two linear mixed-effects models testing how the number of insect visits and the average duration of individual visits depend on the number of observed flower units and plant species status and origin (European, non-European) of alien plant species. ... 89 Table II.S7 Results of three phylogenetically corrected linear mixed-effects models testing how the number of insect visits, the average duration of individual visits, and the number of flower- visitor groups depend on traits related to conspicuousness of the plants and flowers, and on status (naturalized, non-naturalized) and origin (European, non-European) of alien plant species ... 90 Table II.S8 Results of two linear mixed-effects models testing how the number of insect visits and the average duration of individual visits depend on traits related to conspicuousness of the plants and flowers, and on distribution of the naturalized alien plant species in Switzerland. .... 91 Table II.S9 Results of two linear mixed-effects models testing how the number of flower-visitor groups and the Shannon indices of flower-visitor groups depend on the number of observed flower units and plant species status ... 92 Table II.S10 Results of two linear mixed-effects models testing how the number of flower- visitor groups and the Shannon indices of flower-visitor groups depend on the number of observed flower units and plant species status (naturalized and non-naturalized ) and origin (European, non-European) of alien plant species. ... 93

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Table II.S11 Results of a linear mixed model testing how the Shannon-diversity index of flower- visitor groups depends on traits related to conspicuousness of the plants and flowers, and on status (naturalized, non-naturalized) and origin (European, non-European) of alien species. ... 94 Table II.S12 Results of four linear mixed-effects models testing how the number of flower- visitor groups and the Shannon-diversity indices of flower-visitor groups depend on traits related to conspicuousness of the plants and flowers, and on distribution of the naturalized alien plant species in Switzerland ... 95 Table II.S13 Results of six linear mixed-effects models testing how the average duration of individual visit of each flower-visitor groups depend on traits related to conspicuousness of the plants and flowers and on species status ... 96

Table III.1 Results of two generalized linear mixed-effects models testing for the main and interactive effects of pollination treatment (pollen supplementation, open pollination, and pollinator exclusion) and plant group (native, invasive alien, and non-invasive alien) and the main effect of year of treatment on mean fruit set and seed production per fruit. ... 108 Table III.2 Results of four phylogenetically informed linear models testing for the effects of plant group (native, invasive alien and non-invasive alien) on pollen limitation and autofertility.

The analyses were conducted using raw and adjusted values for the indices of pollen limitation and autofertility ... 110

Table III.S1 A list of the 24 species used to test for differences in pollen limitation and

autofertility among native, invasive alien and non-invasive alien plant species in Germany. ... 123 Table III.S2 Plant materials used to test for differences in pollen limitation and autofertility among native, invasive alien, and non-invasive alien plant species in Germany ... 129 Table III.S3 Results of two generalized linear mixed-effects models (in which Impatiens noli- tangere was dropped) testing for the main and interactive effects of pollination treatment and plant group and the main effect of year of treatment on mean fruit set and seed production per fruit. ... 131

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Table III.S4 Results of four phylogenetically informed linear models (in which Impatiens noli- tangere was dropped) testing for the effects of plant group on pollen limitation and autofertility ... 132 Table III.S5 A list of references used to resolve polytomies within families for the phylogeny of native, invasive, and non-invasive alien plant species for which the degrees of pollen limitation and autofertility were assessed... 133 Table III.S6 Indices of pollen limitation and autofertility of 24 native, invasive alien and non- invasive alien plant species in Germany. ... 134 Table III.S7 Results of two phylogenetically informed linear models from which the Apiaceae, Balsaminaceae and Papaveraceae triplets were dropped testing for the effects of plant group on pollen limitation and autofertility ... 136

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General introduction

Invasion ecology

Alien plant invasions as drivers and passengers of environmental change

All around the globe, humans have, intentionally or accidentally, introduced plants into new regions; such plants are called “aliens” (Hulme 2011). As a result, an estimated 3.9% of the global flora, at least, has established self-sustaining populations in regions where they did not naturally occur (van Kleunen et al. 2015). Such alien plants that managed to establish

reproducing populations in the wild, without further human intervention are called “naturalized”

(Richardson et al. 2000a). A fraction of naturalized alien plants manages to spread in the landscape and extend their range in the new regions; these are called “invasive” (Richardson et al. 2000a). Not all alien plants have become naturalized, and not all naturalized aliens have become invasive (Richardson & Pyšek 2012). Despite intensive research, why some alien plants are more successful than others remains largely unclear. Moreover, because invasive plants can cause considerable environmental and economic damage (Pimentel et al. 2000; Vilà et al. 2011), what drives alien plant invasions has become a major question in ecology. This not only

contributes to basic research but also informs applied science.

Colonization of new regions and range expansion are natural processes that have occurred throughout the evolution of life on earth, but human activity has rapidly increased establishment and spread of alien organisms, including plants (Vermeij 1991). Alien plants have rapidly changed entire systems in many parts of the world. For example, monocultures of the Canadian goldenrod Solidago canadensis dominate habitat patches within central European landscapes (Weber 1998), and dense patches of the Himalayan balsam Impatiens glandulifera cover moist valley areas (Pyšek & Prach 1995). The purple loosestrife, Lythrum salicaria, native to Northern Africa, temperate Asia and Europe, is similarly dominating wetland habitats in North America (Randall & Marinelli 1996). The fast growing Neotropical tree Cecropia peltata has displaced native gap pioneers in African, Asian and Pacific tropical forests (McKey 1988;

Binggeli, Hall & Healey 1998). The South American water hyacinth, Eichhornia crassipes has become widely naturalized in the tropics and subtropics, forming dense mats on rivers and lakes

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(Randall & Marinelli 1996). Such invasions by alien plants have not only transformed landscapes but have altered major environmental processes (e.g. hydrology, geomorphological processes, and fire regimes).

Alien plants have various impacts on native ecosystems. The magnitude of the impacts depends on different factors and can be negative, neutral or positive (reviewed in Vilà et al.

2009; Blackburn et al. 2014), but the overall effects are considered to be negative (Gaertner et al.

2009). Of major concerns are threats to rare and endemic species. In Germany, 37 threatened native plant species are known to hybridize with alien plants, which is a potential cause for extinction due, for example, to outbreeding depression (Bleeker, Schmitz & Ristow 2007). Alien plants have altered the diet of many endemic animals. On Madagascar, endemic mammals, such as lemurs, and birds have included the Neotropical shrubs and trees Cecropia peltata, Clidemia hirta, and Psidium cattleyanum in their diet, and have contributed to the dispersal of these global invaders (Razafindratsima 2015 and references therein). On the Galapagos, the breeding sites of the endemic petrel are threatened by the Neotropical shrub Lantana camara, which has invaded many parts of the world (Cronk & Fuller 2014). Furthermore, alien plants can attract resident pollinators to the disadvantage of the natives, as is the case for Impatiens glandulifera (Chittka &

Schurkens 2001) and Solidago canadensis (Moroń et al. 2009; Fenesi et al. 2015) in Europe (but see Moragues & Traveset 2005; reviewed in Morales & Traveset 2009). Due to the prevalence of negative impacts, causing economic damage and management costs (Pimentel et al. 2000), understanding the drivers of establishment and spread of alien plants has become the major goal of invasion ecology.

Identifying the drivers of alien plant invasions

Darwin (1859) already wondered why some species become naturalized while others do not, but the discipline of invasion ecology was actively started by Elton (1958). To identify the drivers of invasiveness, a stage-based approach initiated by Williamson and Fitter (1996) with the “tens rule” has been widely adopted. This approach recognizes biological invasions as complex processes including a progression through a series of stages, from the transport of alien organisms to a new non-native region, to their spread in the new region, with a sequence of abiotic and biotic barriers to be overcome (Richardson et al. 2000a; Dietz & Edwards 2006;

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Blackburn et al. 2011; Richardson & Pyšek 2012). Upon introduction into a new region, alien plants must overcome the “survival” and “reproduction” barriers in order to establish naturalized populations, and naturalized plants must overcome the “dispersal” and “environmental” barriers to become invasive (Richardson et al. 2000a; Blackburn et al. 2011). So, factors determining naturalization and invasion success of alien plants may differ (Dietz & Edwards 2006;

Richardson & Pyšek 2012), and may be context dependent (van Kleunen, Dawson & Maurel 2015). Thus, it is important to consider the actual stage when identifying the drivers of plant invasions.

To predict which species are likely to become invasive, many hypotheses have been formulated, and tests have yielded different conclusions (Cadotte & Colautti 2005; Catford, Jansson & Nilsson 2009). The Enemy Release Hypothesis (Keane & Crawley 2002), whereby successful invaders are given a competitive advantage because they have left their natural enemies behind, has often been assumed to be a main driver of invasiveness, but test outcomes have been inconsistent (e.g. Mitchell & Power 2003; Torchin et al. 2003; Dostal et al. 2013;

Dawson et al. 2014; Schultheis, Berardi & Lau 2015). The number of propagules introduced and the frequency of introduction events in non-native regions have also been suggested to play a key role in determining whether an alien species will become invasive or not (propagule pressure;

Lockwood, Cassey & Blackburn 2005). Intentional introductions such as for imported crops increase propagule pressure. In a database study including 466 species, Pyšek et al. (2015) showed that central European plant species that were cultivated in North America also became invasive in a larger number of regions. On the other hand, von der Lippe and Kowarik (2012) suggest that human-mediated seed dispersal of non-native species in Berlin, Germany, did not depend on propagule pressure, but rather depended on seed traits. In line with this, a multispecies introduction experiment by Kempel et al. (2013), using 45 native and 48 alien plant species in multiple Swiss grassland sites, showed that the importance of propagule pressure declines over time, while the importance of traits increased.

Most research in invasion ecology has focused on biological traits associated with invasiveness, at the latest stage of the invasion process (Lowry et al. 2013). A meta-analysis by van Kleunen, Weber and Fischer (2010) showed that successful invaders frequently have

superior values of many performance traits. In 146 pairs of non-invasive and invasive naturalized

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plant species in Australia, Gallagher, Randall and Leishman (2015) showed that invasive plants have larger specific leaf area, longer flowering time, and were taller than their non-invasive naturalized counterparts. Comparing 12 pairs of European plant species that have become invasive or not in the US, Keser et al. (2015) showed that invasive plants have superior root- foraging responses. In a similar way, comparing five pairs of invasive and non-invasive plant species in their native range, Jelbert et al. (2015) showed that invasive plants were taller and more fecund. So, previous studies suggest that performance traits might help predict which species will become invasive. Nevertheless, characteristics attributed to invasions might also reflect species’ introduction history, and therefore obscure such conclusions.

Introduced species have not been randomly sampled from the native range. Many accidental introductions have resulted from contaminants of agricultural products. For example, seeds of the common ragweed Ambrosia artemisiifolia, which is a major public health problem due to its highly allergenic pollen, were introduced to Europe as contaminants of cereals from North-America (Chauvel et al. 2006). Most alien plants have been introduced to non-native regions for horticultural use (Reichard & White 2001; van Kleunen, Johnson & Fischer 2007;

Hulme 2011). Of the major global invasive plants, 99% are cultivated in botanic gardens (Hulme 2015). So, as invaders are mostly escapees from cultivation, studying the potential drivers of naturalization and invasion in garden habitats is highly relevant. Furthermore, because humans may have selected species that have high yield for cultivation, rapid germination (Chrobock et al.

2011), or attractive ornamental features (e.g. showy flowers), many plant characteristics commonly associated with invasiveness might actually reflect introduction bias (Maurel et al.

unpublished manuscript). Consequently, it is important to account for these traits leading to introduction bias when identifying the drivers of invasion.

Research gaps

Applicability of Baker’s Law during naturalization and invasion of alien plants

Reproduction is crucial in understanding plant invasions, because propagule supply is required for founding new populations and population maintenance in non-native regions

(Barrett 2011; Burns et al. 2013). Indeed, reproduction has been suggested to be a key barrier for establishment of alien plants (Richardson et al. 2000a; Blackburn et al. 2011). As posed by

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Baker’s Law, organisms capable of uniparental reproduction are more likely to establish after long-distance dispersal, compared to ones that require mates and external vectors (pollinators) for reproduction (Baker 1955; Baker 1967; Pannell et al. 2015). This may apply to plant invasions, as a consequence of human-mediated long-distance dispersal (Pannell et al. 2015).

Because self-compatible and autofertile plants have at least an additional source of pollen which is themselves, and autofertile plants can set selfed seeds without pollinator visits, they may not require the presence of suitable mates and pollinators in the non-native regions to reproduce.

Baker’s Law may particularly apply at the naturalization stage where founder populations are usually small. Few studies have explicitly tested the applicability of Baker’s Law to the

naturalization process of alien plants (Pannell et al. 2015). A notable exception is a study by van Kleunen et al. (2008), showing that among South African Iridaceae that have been introduced elsewhere as garden plants, the ones that have become naturalized in the new range are more autofertile than the ones that have not. As this study was limited to representatives of the South African Iridaceae, a more powerful test of Baker’s Law requires a wider taxonomic group at a broader spatial scale.

Many invasive plants have shown consistency with Baker’s Law in different regions of the globe. Most invasive plants in South Africa, including many woody species, are autofertile (Rambuda & Johnson 2004). Self-compatible and autofertile invasive plants from Europe were reported in the largest number of states in the US (van Kleunen & Johnson 2007a). Hao et al.

(2011) showed similar patterns for invasive Asteraceae in China, as self-compatible plants were reported in the largest number of provinces. Self-pollinated (including self-compatible and autofertile) invasive neophytes were found to be more widely distributed than exclusively insect- pollinated ones in Europe (Pyšek et al. 2011). Invasive milkweeds that are usually self-

incompatible, were found to be self-compatible in Australia (Ward, Johnson & Zalucki 2012).

Petanidou et al. (2012) found that two global invaders, Echium plantagineum and Centaurea solstitialis, have higher degrees of self-compatibility in their invaded range compared to in the native range. These findings strongly suggest that Baker’s Law may apply, not only during the establishment phase but also at an advanced stage of the invasion process, where naturalized populations expand their range in the non-native regions. Nevertheless, many self-compatible naturalized and invasive alien plants depend on pollinators for maximum seed production (van Kleunen & Johnson 2005; van Kleunen et al. 2008; Rodger, van Kleunen & Johnson 2010;

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Petanidou et al. 2012; Ward, Johnson & Zalucki 2012). So, whether a lack of pollinators hampers naturalization and invasion is not clear yet.

Pollinator and pollen limitation of alien plants

In the same manner as leaving natural enemies behind (Enemy Release Hypothesis; see above), alien plants may also have lost their usual mutualists such as pollinators. Some alien plants suffer from pollinator limitation in the introduced range, and this has resulted in reduced reproductive success. In a review using 115 native and 26 alien plant species, Burns et al. (2011) demonstrated that alien plants were more pollen limited than native ones. Larson, Fowler and Walker (2002) showed that the Asian vine Lonicera japonica suffered from pollinator limitation in its naturalized range in central Arkansas, as fruit set was reduced 4.5-fold compared to

maximum reproduction. Parker (1997) found that all studied invasive populations of the Scotch broom Cytisus scoparius in prairies and urban habitats in western Washington, were also

pollinator limited. Bartomeus and Vilà (2009) suggest that pollen limitation of some populations of the invasive Carpobrotus aff. acinaformis are attributed to low efficiency of flower visitors.

However, few studies have explicitly tested the roles pollinator and pollen limitation may play in the establishment and spread of alien plants (Richardson et al. 2000b; Knight et al. 2005). In other words, few studies have compared pollinator and pollen limitation of successful and unsuccessful alien plants (but see Burns et al. 2011). Such comparisons are required to

understand whether a lack of pollinators in the non-native range is a barrier to naturalization and invasion of alien plants decoupled from their usual pollinators.

Integration of alien plants into native plant-pollinator networks

Alien plants can use resident pollinators to reproduce. Using a plant-pollinator network with 456 plant species and 1430 flower visitors, Memmott and Waser (2002) showed that in a community in central USA, alien plants were visited by generalist flower visitors. In line with this, using a removal experiment in the field, Lopezaraiza-Mikel et al. (2007) showed that Impatiens glandulifera in the city of Bristol, Great Britain, used native generalist pollinators and its pollen grains dominated pollen transport networks. Comparing 10 pairs of related native and introduced plant species in a site near St Louis, Missouri, Harmon-Threatt et al. (2009) showed that native and introduced plants had similar flower visitation rates. Moodley et al. (2015)

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showed that Australian Banksia species that were introduced in South Africa were pollinated by native insects and birds. Rodger, van Kleunen and Johnson (2010) found that Lilium

formosanum, native to Taiwan, is pollinated by its usual pollinator, as the latter also naturally occurs in the lily’s invaded range in South Africa. Some invasive alien plants have encountered suitable pollinators in non-native ranges, as their usual pollinators were also introduced (e.g.

Stout, Kells & Goulson 2002; Kaiser-Bunbury et al. 2011). However, few studies have explicitly tested whether successful alien plants (naturalized or invasive) are better than unsuccessful ones (non-naturalized or non-invasive) in attracting pollinators (but see Chrobock et al. 2013a). Such comparisons are required to unravel whether the ability to attract resident pollinators is different for successful and unsuccessful alien plants, and whether this might drive naturalization or invasion success (van Kleunen et al. 2010).

Contribution of this thesis

To investigate the role of reproductive characteristics in explaining naturalization and invasion of plants, this thesis comprises three studies using various multi-species approaches at global and local spatial scales.

Approaches used

Our current knowledge of the potential role of reproductive characteristics in explaining naturalization and invasion processes is largely based on studies using either a single or few species, or limited to specific geographic areas. To provide powerful insight, a multi-species approach is required (van Kleunen et al. 2014), and ideally one with a global geographic

coverage. First, despite the large number of studies that have quantitatively assessed the breeding systems of flowering plants all around the globe, few efforts have been made to compile such data into a global database. Such a database is a powerful tool that can be used to test Baker’s Law at the global scale for an extensive number of species. Second, as botanic gardens harbor multiple species from a wide range of geographic origins, and include alien plants with different degrees of naturalization or invasion success, they represent a unique tool for multi-species comparative studies (Primack & Miller‐Rushing 2009). Third, to avoid potentially confounding effects due to variation in environmental conditions and resources, a common garden experiment is required when comparing the reproductive characteristics of multiple species. Finally, because

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differently related species share different degrees of evolutionary history, phylogenetically informed design and analysis are required in multi-species comparative studies (Felsenstein 1985). Finding key general patterns in the drivers of naturalization and invasion will advance our basic knowledge of alien plants in a robust manner, due to increased replication within, and power of each study (van Kleunen et al. 2014). As such findings will contribute to providing a general prediction and prevention of invasions, they will better inform conservation practitioners and managers.

Outline of the thesis

In Chapter I, I present a database study testing the role breeding system has on global naturalization success of alien plants. To test the effect of selfing ability (self-compatibility and autofertility) on global naturalization success, I compiled a quantitative breeding-system database on the breeding systems of flowering plants into a global database. I combined it with data on life cycle, native range size and various measures of global naturalization success, using the Global Naturalized Alien Flora database (van Kleunen et al. 2015). My specific questions were: 1) How are self-compatibility and autofertility distributed among angiosperms globally?

2) As suggested by Baker’s Law, is global naturalization success of alien plant species associated with self-compatibility and autofertility? 3) What is the strength of direct and indirect effects of self-compatibility and autofertility on global naturalization success of alien plant species when accounting for life cycle and native geographic range size?

In Chapter II, I present a multi-species comparative study on flower visitation of 185 native, 37 naturalized alien and 224 non-naturalized alien plant species in the Botanical Garden of Bern, Switzerland. To test the importance of flower visitation for naturalization of alien plant species, my specific questions were: 1) Is flower visitation (number of visits, duration of visits, flower-visitor diversity) lower for non-naturalized species than for naturalized alien and native species? 2) Are native, naturalized alien and non-naturalized alien plant species visited by different insect communities? 3) Do alien species from other parts of Europe attract more flower- visitors than alien species from other continents? 4) Is flower visitation higher for more

widespread than for less widespread naturalized aliens in Switzerland?

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In Chapter III, I present a common garden experiment on a total of 24 native and alien (both invasive and non-invasive, but naturalized) plant species, comprising eight confamilial or congeneric triplets, testing whether pollen limitation in a new environment, is an important constraint to plant invasion, and whether autofertility is related to invasion success. My specific questions were: 1) Are non-invasive alien plants more pollen limited than co-occurring related invasive alien and native plants? 2) Are non-invasive alien plants less autofertile than co- occurring related invasive alien and native plants?

To conclude this thesis, I provide a General discussion. In this concluding part, I synthesize the findings presented in the three chapters, and explain in a broad context our new understanding of the importance of plant reproductive characteristics in alien plant naturalization and invasion.

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Chapter I

Direct and indirect effects of self-compatibility and autofertility on the global naturalization of alien plants

Mialy Razanajatovo, Noëlie Maurel, Wayne Dawson, Franz Essl, Holger Kreft, Jan Pergl, Petr Pyšek, Patrick Weigelt, Marten Winter and Mark van Kleunen

Abstract

Due to human activity, at least 3.9% of the global flora has established self-sustaining populations in regions where it did not naturally occur. However, it is still not clear whether naturalized plants can be characterized by certain traits. As suggested by Baker’s Law, self- compatible and autofertile plants should be more likely to establish in non-native regions, because they can reproduce from a single individual, when mates and pollinators are limiting.

We compiled quantitative data on the breeding system of 1752 angiosperm species into a global database, and combined these data with data on the species’ life cycle, native range size and global naturalization. To test whether naturalization success is related to selfing ability (self- compatibility and autofertility), we used phylogenetic generalized linear models. Then, to unravel the direct and indirect effects of selfing ability on naturalization success, and to quantify the causal relationships among a species’ selfing ability, native range size and naturalization success, we used path analysis. We found a continuous pattern in the species’ degrees of self- compatibility and autofertility, following a bimodal distribution. We showed a significant positive relationship between selfing ability and the number and area of regions where the species has naturalized. Additionally, we disentangled a significant direct positive effect of selfing ability on naturalization success, and a significant indirect positive effect via native range size. Thus, we provide robust evidence of the applicability of Baker’s Law on the global

naturalization of alien plants, and conclude that a lack of mates and pollinators may be a key barrier to establishment in the non-native range.

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Introduction

Due to human activity, an estimated 3.9% of the global flora, at least, has established self-sustaining populations in regions where it did not naturally occur (van Kleunen et al. 2015).

Most such naturalized plants have been introduced to non-native regions for horticultural use (Reichard & White 2001), and have subsequently escaped from gardens, nurseries, and arboreta (Hulme 2011). Other naturalized plants have resulted from accidental introductions, for example, as seed contaminant of imported crops (Hulme et al. 2008; Lambdon et al. 2008). Many of these naturalized plants have become invasive worldwide, and impacted native biodiversity to various extents (Blackburn et al. 2014). Thus, what drives naturalization has become a question of global interest.

Reproduction is of major interest in understanding naturalization success, because propagule supply is required for founding new populations and population maintenance (Barrett 2011; Burns et al. 2013). Baker’s Law poses that self-compatible and autofertile plant species are more likely to establish after long-distance dispersal, because they can reproduce from a single individual, when mates and pollinators are limiting (Baker 1955). This could apply to plants introduced into new regions by humans, because suitable mates and pollinators may be scarce there (Pannell et al. 2015). In such conditions, a breeding system that favors uniparental

reproduction, such as self-compatibility and autofertility, might give a superior advantage over a self-incompatible breeding system, which requires the presence of suitable mates and pollinators.

The role breeding system might play could be most relevant during the establishment phase of alien plants, termed “naturalization” (Richardson et al. 2000a), where species have to found and maintain populations locally (Pannell et al. 2015). Few generalized studies have explicitly tested whether a plant’s breeding system plays a significant role in alien plant naturalization ((Pannell et al. 2015) and references therein).

Previous studies on the applicability of Baker’s Law to introduced alien plants had divergent findings. On the one hand, many naturalized and invasive plants have shown high capacity for uniparental reproduction in the non-native range, as measured by their degree of self-compatibility and autofertility (Rambuda & Johnson 2004; van Kleunen & Johnson 2007a;

van Kleunen et al. 2008; Harmon-Threatt et al. 2009; Burns et al. 2011; Hao et al. 2011; Rodger, van Kleunen & Johnson 2013). On the other hand, some globally problematic invasive plants are

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not capable of uniparental reproduction and are self-incompatible (Sutherland 2004; Brennan, Harris & Hiscock 2005; Jesse, Moloney & Obrycki 2006; Hong et al. 2007; Lafuma & Maurice 2007; Moodley et al. 2015). A few studies even suggest that breeding systems only play a minor role in the process of invasions (Rejmánek 1996; Sutherland 2004; Moodley et al. 2015).

However, previous works were limited to specific taxonomic or functional groups, or to a

continental or lower level spatial scale. No efforts have been made yet to test the role of breeding system on the global naturalization of alien plant species. Such a generalized approach is

required to provide a robust support or rebuttal to the applicability of Baker’s Law during the establishment of alien plant species in non-native ranges.

An extensive number of studies have reported the breeding system of many flowering plants from experimental pollinations around the globe, but few efforts have been made to compile such findings into a quantitative global database. Almost 60 years ago, Fryxell (1957) classified c. 1500 plant species into eight categories of reproductive systems, but his

classification was only qualitative. More than 20 years ago, Lloyd and Schoen (1992) compiled a quantitative database on self-compatibility and autofertility of 66 species. A recent database by Raduski, Haney and Igić (2012) includes indices of self-incompatibility for c. 1200 species, but they did not compile data for autofertility. A complete quantitative database on breeding systems requires additional data from pollinator exclusion, pollinator exclusion combined with

emasculation, natural pollination and pollen supplementation. Such a global database is necessary to address general scientific questions related to plant reproductive strategies.

Several plant characteristics are associated both with naturalization success, and with self-compatibility and autofertility. First, an annual life cycle has been associated with weediness (Baker 1965), and often, annuals are selfers (Baker 1974; Pannell & Barrett 1998; Pannell et al.

2015). Second, native geographic range size is frequently related to naturalization success (Pyšek et al. 2014) and selfing ability (Randle, Slyder & Kalisz 2009; Grossenbacher et al. 2015).

Furthermore, species with different degrees of evolutionary relatedness might have different degrees of similarity of the plant traits associated with naturalization success, and self- compatibility and autofertility. Thus, it is important to account for other traits and phylogeny (Felsenstein 1985) when testing the relationship between naturalization success and breeding system, and it is important to unravel the complex associations among the different factors.

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To test the effect of self-compatibility and autofertility on global naturalization success, we assembled as much quantitative data as possible on the breeding system of flowering plants in a global database. We combined these data with data on life cycle, native range size and various measures of global naturalization success. We first used a phylogenetically informed generalized linear model approach. Further, to unravel direct and indirect effects of self- compatibility and autofertility on naturalization success, we used path analysis. Our specific questions were: 1) How are self-compatibility and autofertility distributed among angiosperms globally? 2) As suggested by Baker’s Law, is global naturalization success of alien plant species associated with self-compatibility and autofertility? 3) What is the strength of direct and indirect effects of self-compatibility and autofertility on global naturalization success of alien plant species when accounting for life cycle and native geographic range size?

Methods

Compilation of a global database on breeding systems

To assemble as much as possible of the published quantitative data on the breeding system of angiosperm species into a global database, we did a literature search in Web of Science (http://apps.webofknowledge.com; Fig. I.S1). We input the search keyword string

“TS=(("breeding system" OR "mating system" OR "self-compatib*" OR "self-fertil*" OR autogam* OR "auto-fertil*" OR outcross* OR apomixis) AND plant)”, and searched for all indexed documents from the year 1900 onwards. This search was done in April 2013, and the search result was weekly updated until February 2015. We scanned all 6678 resulting titles, and excluded the ones that obviously did not present breeding-system data for angiosperms (e.g.

studies on animals, cryptogams and gymnosperms, or studies involving only molecular techniques). Subsequently, we screened the abstracts of the remaining 1675 articles. All the studies that explicitly included all or a subset of the following treatments were selected: bagging of flowers to exclude pollinators (testing for autofertility), bagging of flowers in combination with self-pollination (testing for self-compatibility), bagging of flowers in combination with cross-pollination (testing for maximal seed production when bagged), bagging of flowers in combination with emasculation (testing for apomixis), supplemental hand-pollination (testing for pollen limitation) and unmanipulated control flowers (testing for seed set under natural

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conditions). Out of the 705 studies that fulfilled our criteria, we finally examined 696 full text documents, as nine studies were not accessible. We included in our database all studies that provided measures of fruit set (fruit/flower ratio) and/or seed set (number of seeds per plant or per flower or per fruit, or seed/ovule ratio) for all or a subset of the above-mentioned treatments.

Our literature search yielded 516 articles with suitable data. We additionally included in our database 244 documents that we encountered independently of the literature search, including 113 references used by Raduski, Haney and Igić (2012). We also included data from three of our own studies (including unpublished data).

For each species reported in each study, we documented all available fruit and seed production data in each of the different pollination treatments. For heterostylous species, we only included data from “legitimate” crosses between individuals of different morphs for the

outcrossing treatment. If data were provided in the text or in tables, we extracted them directly. If the data were provided in graphs only, we extracted the data using ImageJ (Abràmoff, Magalhães

& Ram 2004). According to the availability of the data, we obtained for each species and

treatment, the percentage of treated flowers that produced fruit (fruit set) and the number of seed produced per flower (Table I.S1). When the number of seeds per flower was not provided, we calculated it by multiplying fruit set by number of seeds per fruit (percentages of values that were calculated this way are given in Table I.S1). We also documented sample sizes and

standard errors if provided (number of plants, inflorescences and flowers used in the treatments).

When standard deviation and sample size were provided, we calculated standard errors.

However, as few studies provided standard errors or deviations, we did not use them in the analyses.

We found breeding system data for 1829 plant taxa. Because some of these taxa may be synonyms, and to facilitate alignment of the species list with other databases (see below), we standardized the scientific names of the species in our database following The Plant List

(http://www.theplantlist.org), using the package Taxonstand (Cayuela et al. 2012) in R (R Core Team 2012). For 14 taxa that did not occur in The Plant List, we kept the names given in the original study from which breeding system data were extracted.

Because a species’ breeding system is often related to its life history, we included, for each species, information on its life cycle (annual, biennial, perennial). When this was not

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provided in the publication from which the breeding-system data was extracted, we consulted other sources: Encyclopedia of Life (http://eol.org), Royal Botanic Gardens, Kew

(http://epic.kew.org), United States Department of Agriculture database

(http://plants.usda.gov/java/), Tropicos (http://www.tropicos.org), Instituto de Botanica Darwinion (http://www.darwin.edu.ar/Proyectos/FloraArgentina/fa.htm); and did extensive internet searches. We then classified each species as monocarpic (mostly annuals and biennials) or polycarpic.

As a broad native distribution may influence the naturalization success of an alien species, we compiled information on the native range size of each species in the database using the number and area of TDWG level-2 regions (52 regions in total; adapted from the scheme of the Biodiversity Information Standards or Taxonomic Databases Working Group; (Brummitt et al. 2001)) the species is native to. We extracted data from the World Checklist of Selected Plant Families (WCSP; http://apps.kew.org/wcsp/), the Germplasm Resources Information Network (http://www.ars-grin.gov/cgi-bin/npgs/html/index.pl), the Global Biodiversity Information Facility (http://www.gbif.org/), Tropicos (http://www.tropicos.org), the United States Department of Agriculture database (http://plants.usda.gov/java/), Encyclopedia of Life (http://eol.org), Australian National Botanic Gardens (https://www.anbg.gov.au/index.html), CIRAD (http://arbres-reunion.cirad.fr/accueil), IUCN (http://www.iucnredlist.org/), and African Violet Society of America (http://www.avsa.org/). For 21 species, we obtained information on the native range from the original study from which breeding system data were extracted.

To test whether global naturalization success of species is related to their breeding systems, we included data on global naturalization in our database. We used the Global Naturalized Alien Flora (GloNAF) version 1.1, which is the most comprehensive database of naturalized plants, as it includes 13,168 alien plant species that have become naturalized in 843 regions (481 mainland regions and 362 island regions) on the globe (~83 % of the Earth’s land area, (van Kleunen et al. 2015)). For each species in our database, we added data on

presence/absence in the GloNAF database (i.e. whether or not a species is listed in GloNAF), number and cumulative area of the ‘GloNAF regions’ where the species has become naturalized outside its native range.

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We removed 30 taxa that were not identified to the species level from the database, because we could not find information on native and naturalized range for these taxa. In total, using 763 references, we compiled quantitative breeding-system data for 1752 angiosperm species from 161 families, collected in 116 regions (covering tropics, subtropics and temperate zones). Our database covers experiments performed between 1868 and 2015 in natural

populations (1380 species), plantings (61 species), common gardens (143 species) and greenhouses (269 species). For 127 species, the breeding system was assessed outside their native range.

Phylogeny

To account for potential biases due to different degrees of relatedness among species in the analyses (Felsenstein 1985), we constructed a phylogenetic tree of the 1752 species in the database. We first pruned an existing megatree of 31,749 plant species (Zanne et al. 2014) using the ape package (Paradis, Claude & Strimmer 2004) in R. The pruned tree returned 821 species in our database which matched with the tips of the megatree. We then added all species

belonging to identical genera on the pruned tree and obtained a new tree with 1266 species. We added the 486 remaining species with the tree topology editor in MEGA6 (Tamura et al. 2013) using information from online and published phylogenies (Table I.S2). We estimated the branch length of the resulting phylogenetic tree using phylocom (Webb, Ackerly & Kembel 2008), which considers the node ages (Wikström, Savolainen & Chase 2001).

Data analysis

 Global patterns in self-compatibility and autofertility

For each species in each study, when multiple populations were studied, and when the experiments were done over multiple years, we averaged fruit and seed production in each treatment. To estimate the degree of self-compatibility and autofertility of each species in each study, we calculated an index of self-compatibility (SC; Lloyd & Schoen 1992) and an index of autofertility (AF; Lloyd & Schoen 1992; Eckert et al. 2010), respectively:

‐ ‐

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‐

Each index was calculated for fruit set and for seed production per flower.

A value of zero of these indices indicates that a species is not self-compatible or

autofertile, respectively; and a value of one indicates that the species is fully self-compatible or autofertile, respectively (Lloyd & Schoen 1992; Eckert et al. 2010). Values larger than one occurred when the outcome from self-pollination or pollinator exclusion was larger than that from cross-pollination (Lloyd & Schoen 1992). We set such values larger than one to one (15.94

%, 15.82 %, 6.55 %, and 7.39 % of observations for SC and AF based on fruit set and seeds per flower, respectively; see Raduski, Haney and Igić 2012).

 Self-compatibility and autofertility as drivers of global naturalization success of alien plants

To test the effect of self-compatibility and autofertility on global naturalization success, we used two approaches. First, we used a generalized linear model (GLM) approach that allowed us to correct for phylogenetic non-independence of species. Such a model controls for

phylogenetic non-independence of the species by including a variance-covariance matrix that contains the phylogenetic information combined with a model of evolution. Second, we used path analysis to unravel direct and indirect effects of self-compatibility and autofertility on naturalization success.

To test whether the presence of a species in the Global Naturalized Alien Flora (GloNAF) is associated with its degree of self-compatibility and autofertility, respectively, we fitted a phylogenetic logistic regression (Ives & Garland 2010) using the package phylolm (Ho & Ané 2014) in R. As a response variable, we used the presence/absence of a species in GloNAF. As covariates, we included native range size (natural log-transformed number and natural log-

transformed cumulative area of TDWG level-2 regions, respectively), monocarpy (yes/no), index of self-compatibility and autofertility, respectively, and its interaction with monocarpy. Since the results were qualitatively similar whether we used the number or the cumulative area of TDWG level-2 regions as a measure of native range size, we only present results using number of

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regions. To reduce collinearity and to allow comparisons among estimates, we standardized the covariates to a mean of zero and a standard deviation of one (Schielzeth 2010).

To test whether the extent of a species’ naturalization once naturalized in at least one region is positively related to its degree of self-compatibility and autofertility, respectively, we analyzed the subset of only the species listed in GloNAF. We fitted phylogenetic linear

regressions (Freckleton, Harvey & Pagel 2002) using the package phylolm in R. As a response variable, we used natural log-transformed number and natural log-transformed cumulative area of GloNAF regions, respectively. We used the same covariates as in the phylogenetic logistic regression described above.

We additionally analyzed the complex association of self-compatibility and autofertility of a plant species, respectively, with its life cycle (monocarpic or not; therefore termed

“monocarpy”), its native range size, and its naturalization success outside the native range, using path analysis (Grace 2006). To specify the path structure, we assumed the following

relationships: 1) naturalization success of a plant species outside its native range is driven by its degree of self-compatibility and autofertility, respectively, its native range size, and monocarpy;

2) native range size of a plant species is driven by its degree of self-compatibility and

autofertility, respectively, and monocarpy; 3) the degree of self-compatibility and autofertility of a plant species, respectively, is correlated with monocarpy. It is important to include this

correlation to avoid spurious relationships. We also run two alternative path models with directed paths between degree of self-compatibility and autofertility of a plant species and monocarpy:

first, assuming that self-compatibility and autofertility are driven by monocarpy and second, the other way around, but the results were the same as for the analysis including the correlation. This path analytical approach allows us to quantify the direct and indirect effects of self-compatibility and autofertility, respectively, of a plant species on its naturalization success outside the native range.

As in the previous models, we separately analyzed the presence/absence of a species in GloNAF, and for the subset of only the naturalized species, the number and cumulative area of GloNAF regions. For the analysis of the binary variable presence/absence in GloNAF, we used a diagonally weighted least square (DWLS) estimation method with robust standard errors. For the analysis of the number and cumulative area of GloNAF regions, we used a maximum likelihood

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estimation method with robust standard errors (MLR). We standardized all continuous variables to a mean of zero and standard deviation of one. We assessed model fit using a relative measure, the Comparative Fit Index (CFI), and an absolute measure, the Root Mean Square Error of Approximation (RMSEA). A CFI>0.95 and a RMSEA<0.06 are considered good (Hu & Bentler 1999). We did the path analysis using data on both fruit set and seed production per flower, but only focus on the results of fruit set in the main text, and present the results on seed production per flower in the supporting information. We did the path analysis using the lavaan package (Rosseel 2012) in R.

Results

 Global patterns in self-compatibility and autofertility

Our global dataset, comprising a total of 1752 species from all major clades of

angiosperms (Fig. I.S2), showed a continuous pattern from zero to one in their indices of self- compatibility and autofertility, following a bimodal distribution (Fig. I.1). We found that c. 25%

and 50% of the species had values close to zero for self-compatibility and autofertility indices, respectively; c. 30% and 12% had values close to one; and c. 50% had intermediate values in both cases (Fig. I.1). This indicates that self-compatibility and autofertility are not qualitative traits that can be defined by systematized cut-off values, but are quantitative traits. Furthermore, we found that monocarpic species are frequently fully self-compatible and autofertile (Fig. I.1).

 Self-compatibility as a driver of global naturalization success of alien plants

Our phylogenetically informed analysis showed that the presence of a species in GloNAF was not significantly associated with its degree of self-compatibility measured in terms of fruit set (Table I.1). However, number of GloNAF regions (but not cumulative area of GloNAF regions) where a species has been documented, was significantly positively related to its self- compatibility index (Table I.1). This indicates that, once a species has become naturalized outside its native range, its extent of naturalization may be positively related to its degree of self- compatibility.

The phylogenetically informed analysis also showed that the presence of a species in GloNAF was significantly related to native range size but number and cumulative area of

Reproductive characteristics as drivers of alien plant naturalization and invasion