Selection for commercial forestry determines global patterns of alien

A Journal of Conservation Biogeography

Diversity and Distributions, (Diversity Distrib.) (2010) 16, 911–921

BIODIVERSITY RESEARCH

Selection for commercial forestry determines global patterns of alien conifer invasions Franz Essl1,2*, Dietmar Moser2, Stefan Dullinger3,4, Thomas Mang3,4 and Philip E. Hulme1

1

The Bio-Protection Research Centre, Lincoln University, PO Box 84, Canterbury, New Zealand, 2Environment Agency Austria, Spittelauer La¨nde 5, 1090 Vienna, Austria, 3 Department of Conservation Biology, Vegetation and Landscape Ecology, Faculty Centre of Biodiversity, University of Vienna, Rennweg 14, 1030 Vienna, Austria, 4Vienna Institute for Nature Conservation & Analyses, Giessergasse 6/7, 1090 Vienna, Austria

ABSTRACT Question Are the patterns of alien conifer (Pinaceae, Cupressaceae) invasions different between continents, and how is invasion success influenced by commercial forestry practices? Location Temperate and subtropical countries and regions (n = 60) from five continents spanning both hemispheres. Methods We used generalized linear mixed models to test how continent identity, region area and use in commercial forestry affect probabilities of Pinaceae and Cupressaceae species to escape following introduction and cumulative logit regression models to assess how these predictors affect the likelihood that a species becomes naturalized or invasive.

Diversity and Distributions

Results Sixty Pinaceae of a global total of 232 and 26 Cupressaceae of a total of

142 species have escaped from cultivation across the study regions examined. Average numbers of both alien Pinaceae and Cupressaceae species per region were highest in Oceania, followed by Africa. Moreover, the probability of alien Cupressaceae and Pinaceae becoming naturalized or invasive was particularly high in these two continents. For both families, species used in commercial forestry have a significantly higher probability of escape than those which are only introduced for ornamental or other purposes. In the case of Pinaceae, forestry species also become naturalized or invasive more frequently than non-forestry species, while no such effect was detectable for Cupressaceae. Conclusions We found that non-native conifers are more likely to escape from cultivation, naturalize and turn into invasive weeds on the continents of the Southern Hemisphere. In addition to this biogeographic signal, introduction effort strongly determines the behaviour of introduced Pinaceae, and less so, Cupressaceae. A clear conflict exists between the economic benefits of conifer forestry and the risks to the environment from invasions. Future expansion of commercial forestry should address spatial planning to ecosystems vulnerable to invasion and adopt comprehensive risk assessment procedures. *Correspondence: Franz Essl, Environment Agency Austria, Spittelauer La¨nde 5, 1090 Vienna, Austria. E-mail: [email protected]

Keywords Biological invasions, Cupressaceae, forestry, global patterns, Pinaceae, propagule pressure.

Many conifer species have been planted outside their native range around the world, mainly for forestry and ornamental purposes. An increasing number of these have escaped, often

naturalized and consequently led to significant conservation problems (Richardson, 1998b; Haysom & Murphy, 2003; Richardson & Rejmańek, 2004; Carillo-Gavilan & Vila`, 2010; Simberloff et al., 2010). Most introduced conifers are members of the two most species rich families, the Pinaceae (232 species)

ª 2010 Blackwell Publishing Ltd

DOI: 10.1111/j.1472-4642.2010.00705.x www.blackwellpublishing.com/ddi

INTRODUCTION

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F. Essl et al. and the Cupressaceae (142 species) (The Gymnosperm Database, 2009). Both families are phylogenetically modern conifers. Their natural distributions are predominantly restricted to the Northern Hemisphere where they are often among the dominant species either in cool and wet, or hot and dry, nutrient-poor environments of boreal, temperate and Mediterranean biomes (Richardson, 1998a). In the Southern Hemisphere, Pinaceae and – to a lesser extent – Cupressaceae have largely been absent prior to European colonization. During the past 200 years, a variety of both Pinaceae and Cupressaceae species have been introduced into the Southern Hemisphere, with several commercially valuable species cultivated across large areas. The subsequent spread of several of these introduced conifer species is a significant problem in the Southern Hemisphere where these species encroach and overgrow native communities (e.g. fynbos in South Africa, tussock grasslands in New Zealand, Patagonian steppe in Argentina), and thereby change species composition, nutrient cycling, hydrology and fire regimes (e.g. Richardson & Rejmańek, 2004; Richardson & van Wilgen, 2004; Simberloff et al., 2010). Alien conifers have been a prime subject of study in invasion biology because of the detailed knowledge on functional and demographic traits of many species (Richardson, 1998a, 2006), and introduction histories are often well documented (Evans, 2009). Hence, potential relationships between invasion success and particular traits of conifers have been screened frequently (e.g. Rejmańek & Richardson, 1996; Grotkopp et al., 2002, 2004; Boulant et al., 2009; Laungani & Knops, 2009), and regional invasion patterns have been reported in several case studies (see overview in Richardson et al., 1994; Richardson, 2006 and an update for Europe in Carillo-Gavilan & Vila`, 2010). Hence, available data on conifer invasions allow for sampling of a wide range of geographical regions, which is crucial to identify regional differences in invasion patterns and to derive robust generalizations (Pysˇek et al., 2008). However, a quantitative comparative assessment of conifer invasions at the global scale has yet to be undertaken (but see Richardson et al., 1994 for an analysis of invasion success of Pinus on the Southern Hemisphere). In this study, we aim for such a global assessment using data of alien Pinaceae and Cupressaceae from 60 temperate and subtropical regions across both hemispheres. We analyse these data with respect to the following questions: (1) What are the geographic and taxonomic patterns of conifer species invasions? (2) Does invasion success differ between hemispheres and continents? (3) Does the mode of introduction, in particular the use of a species in commercial forestry, modify invasion success? METHODS Study regions The selection of study areas was performed in a two-step approach: first, we compiled a list of potential regions covering

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a wide range of climatic and other environmental factors, human land use intensity and invasion history. From this list, only those regions were retained for which comprehensive and up to date data sets on the distribution of alien conifers were available. In total, we selected 60 temperate and subtropical regions (Fig. 1, Appendix S1). Thirty-nine of these regions were located in the Northern Hemisphere (European countries and islands, US federal states) and 21 in the Southern Hemisphere (provinces, federal states or islands of South Africa, southern South America and Oceania including New Zealand & Australia). We used subnational regions to hold area sizes roughly within one order of magnitude (c. 25,000– 500,000 km2), although some islands were significantly smaller (Appendix S1). We were not able to include regions from Asia in our study. Although there has been an increasing interest in plant invasions in temperate and subtropical East Asia recently and hence the knowledge of its alien flora is growing fast, significant gaps of the alien flora of East Asia still remain (Weber et al., 2008; Wu et al., 2010). Data Species list and distribution data The taxonomic concept was taken from the treatment in the most authoritative continental floras: nomenclature and taxonomy follow Flora of North America (FNA Editorial Committee, 1993) for North American taxa, Flora Europaea (Tutin et al., 1964) for European taxa and The Gymnosperm Database (2009) for the taxa of all other regions. We included only approved species into the analysis because of inconsistent taxonomic treatment and poor data coverage at the infraspecific level (e.g. subspecies in Pinus nigra). We extracted distribution data of alien conifers (see Appendix S2) from several sources: first, we searched key literature on conifer invasions (e.g. all references listed in the Appendix of Richardson & Rejmańek, 2004), large authoritative databases (e.g. DAISIE, 2009; USDA, 2009) and standard floras as listed in Frodin (2001). These data sets were supplemented by an exhaustive literature search (see Appendix S3) both on the ISI Web of Science and, as far as possible, in non-indexed journals, as many floristic records are published in the latter. Finally, we contacted c. 20 regional experts (see acknowledgements) who checked the data set and provided additional data. Based on the terminology proposed by Pysˇek et al. (2004), alien conifers that had escaped following introduction were classified for each region according to their invasion status as casuals (only small, non-self-sustaining populations), naturalized (at least one persisting population of considerable size) and invasive (naturalized species reproducing offspring in large numbers and at considerable distances from parent plants). This assessment was undertaken by the first author based on information provided in the data sources. In fact, the assignment to invasion status categories (see Appendix S2)

Diversity and Distributions, 16, 911–921, ª 2010 Blackwell Publishing Ltd

Global patterns of alien conifer invasions (a)

(b)

Figure 1 Locations of the 60 study regions (shaded), together with the number of alien Pinaceae (a) and Cupressaceae (b) species recorded in each of them.

proved to be difficult on occasions. In doubtful cases, we followed a conservative approach and chose the lowest invasion category. The importance of each conifer species for commercial forestry was assessed based on information provided by USDA Forest Service (1965), Richardson (1998a), Richardson & Higgins (1998), CABI (2002), and Simberloff et al. (2010). Species being listed as commercially important outside their native range were classified as forestry species and the remainder as non-forestry species. Of course, we acknowledge

that forestry species will have been introduced to particular regions for ornamental or other purposes too. Statistical analyses The compiled database included all species of both the Pinaceae and Cupressaceae that had escaped from cultivation in at least one of the 60 regions considered. We analysed these data by considering invasion status as both a binary (escaped/ not escaped) and an ordered multinomial response variable


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F. Essl et al. (with levels casual < naturalized < invasive). The binary probabilities of escape were assessed using generalized linear mixed models (GLMMs) with a binomial response distribution and the canonical logistic inverse link function (Faraway, 2006). Fixed-effect predictors consisted of the continent to which a region belongs, the use of a species (forestry or nonforestry), and the region’s area to account for species-area relationships (area log-transformed and studentized to facilitate linearity and symmetry); to account for correlations among species and spatial structuring, the mixed models included orthogonal random effect intercepts with species and regions as grouping factors. The full multinomial response variable (casual, naturalized or invasive) was assessed using cumulative logit (proportional odds) models (Guisan & Harrel, 2000; Agresti, 2002), again with continent, forestry use and log-area as predictors. Proportional odds models simultaneously fit all transition probabilities among an ordered response (in our case casual fi naturalized, naturalized fi invasive) and assume that predictors impact all these transitions quantitatively identically. Each predictor is hence associated with a single coefficient and test statistics, independent of the number of response categories. GLMMs and cumulative logit models were fitted independently for Pinaceae and Cupressaceae families, respectively. Because of the overall lower number of alien records for Cupressaceae in Africa and North America, the cumulative logit model for this family was fitted omitting these continents. This choice improved the numerical stability of the overall model, but inferences were robust towards inclusion or exclusion of these two continents. To test for within-continent spatial autocorrelations, the residuals of the response variable were evaluated by Moran’s I correlograms (Dormann et al., 2007), using distances between regions calculated from geographic coordinates (geographic mid points of each region). We found low levels of residual autocorrelation (I < 0.25) in most cases and no spatial trend of autocorrelation. We hence conclude that residual spatial autocorrelation will not change results qualitatively. Statistical analyses were carried out in R (R Development Core Team, 2009). GLMMs were fitted using function glmer of the lme4 package and cumulative logit models using function lrm of the Design package, respectively.

RESULTS Geographic patterns of invasion At least one alien Pinaceae species was recorded as having escaped in 56 of the 60 regions (Fig. 1a). The regions with highest numbers of alien Pinaceae (Appendix S4) were the South Island of New Zealand (24 species), followed by the United Kingdom (22 species) and the North Island of New Zealand (18 species). Of all 358 alien Pinaceae records in our data set, 15% were invasive, 62% had only naturalized, and 23% were casuals. Highest numbers of alien Cupressaceae (Appendix S4) were found for Italy (11 species), followed by the United Kingdom, Austria and Spain (eight species each), whereas no alien Cupressaceae species have been recorded in 23 regions (Fig. 1b). Of all 118 alien Cupressaceae records, 3% were invasive, 44% were only naturalized and 53% were casuals. Numbers of alien Pinaceae and Cupressaceae per region were significantly correlated both with respect to the total numbers of species having escaped from cultivation (Spearman’s rank-correlation coefficient: q = 0.54, P < 0.001) and to subsets of species with a particular invasion status (casual: q = 0.68, P < 0.001; naturalized: q = 0.31, P = 0.01; invasive: not calculated because of too few records for Cupressaceae). For both Pinaceae and Cupressaceae, the probability of escape from cultivation, and hence also total alien species numbers per region, was significantly different among continents (GLMMs; P = 0.004 and P < 0.001, respectively). The same continent-effect was also detectable in the proportional odds models, i.e. with respect to the probability of alien species becoming casual, naturalized or invasive within a region (P < 0.001 and P = 0.02, respectively). For this model, Southern Hemisphere continents had consistently higher transition probabilities (= greatest estimated regression coefficients) into higher invasion status categories than their Northern Hemisphere counterparts (Tables 1–3). Highest average numbers of alien Pinaceae were recorded in Oceania, followed by Africa, whereas Europe and Oceania ranked first and second with respect to alien Cupressaceae (Fig. 2). North America consistently showed the lowest probabilities of conifer escape from cultivation, and hence also lowest total alien

Table 1 Means and standard deviations (in brackets) of alien Pinaceae and Cupressaceae species numbers across regions of different continents (numbers of regions per continent in parentheses). Values are provided for total numbers of alien Pinaceae and Cupressaceae, as well as separately for subsets pertaining to different invasion status categories. Pinaceae

Europe (n = 25) N America (n = 14) Oceania (n = 8) S America (n = 11) Africa (n = 2)

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Cupressaceae

Casual

Naturalized

Invasive

Total

Casual

Naturalized

Invasive

Total

2.2 0.6 1.2 0.5 0.5

3.8 3.1 5.5 2.7 3.5

0.6 0.0 2.6 0.8 4.5

6.7 3.8 9.4 4.1 8.5

2.0 0.1 0.8 0.3 0.0

1.1 0.1 1.9 0.5 1.5

0.1 0.0 0.2 0.0 0.0

3.2 0.3 2.9 0.7 1.5

[2.7] [1.0] [2.3] [0.5] [0.7]

[3.3] [2.5] [5.2] [2.0] [0.7]

[1.1] [0.0] [2.0] [1.0] [0.7]

[4.9] [3.1] [8.5] [2.0] [0.7]

[2.3] [0.4] [1.4] [0.6] [0.0]

[1.2] [0.5] [2.1] [0.7] [0.7]

[0.3] [0.0] [0.5] [0.0] [0.0]

[3.1] [0.6] [2.4] [0.9] [0.7]


Global patterns of alien conifer invasions Table 2 Coefficients, their standard errors (SE) and associated P-values for predictor variables in the generalized linear mixed models (GLMMs) of the probability of Pinaceae and Cupressaceae species to escape in a particular region.

Pinaceae

Cupressaceae

Predictor variable

Coef.

SE

Europe N America Oceania S America Africa forestry species region area

)3.42 )4.53 )3.32 )4.16 )3.46 1.58 0.71

0.28 0.34 0.38 0.36 0.62 0.30 0.14

P-value

Coef.

9 > =

)2.77 )5.52 )2.90 )4.50 )3.67 1.53 0.20

0.004

> ;

< 0.001 < 0.001

SE

P-value

0.30 0.68 0.47 0.54 0.96 0.46 0.18

9 > = > ;

< 0.001

< 0.001 0.26

The mixed model assessed the effect of continent, species use in forestry and regions’ (log) area as fixed effect, and included species and region as orthogonal random effect intercepts to account for taxonomic and spatial correlations among the data. For all predictors, greater coefficient values correspond to higher escape probabilities and are hence greatest for forestry species and the continents Europe, Oceania and Africa, and lowest for North America. For continents, the factor as a whole (all levels jointly) was subjected to a likelihood-ratio test to asses whether escape probabilities are equal for all continents (null-hypothesis) or different between at least two of them (alternative-hypothesis); as such jointly for all continents (= factor levels), only a single P-value exists and quantifies the null-hypothesis support. Standard deviations of random effects: Taxon: Pinaceae = 0.99, Cupressaceae = 0.72; Region: Pinaceae = 0.70, Cupressaceae = 0.97.

Table 3 Coefficients, their standard errors (SE) and associated P-values for predictor variables in cumulative logit (proportional odds) models of the probability of alien Pinaceae and Cupressaceae species to become casual, naturalized or invasive in a particular region.

Pinaceae Coef.

Predictor variable Cutpoint status ‡ naturalized Cutpoint status ‡ invasive North America Oceania South America Africa Forestry species Region area

)0.33 )3.77 0.23 1.19 0.81 2.51 1.51 0.29

Cupressaceae SE 0.25 0.34 0.32 0.31 0.37 0.54 0.28 0.17

P-value 0.001

< 0.001 0.08

Coef. )0.54 )3.90 – 1.63 0.85 – )0.02 )0.10

SE 0.28 0.59 – 0.51 0.75 – 0.42 0.19

P-value 0.02

0.96 0.59

Greater estimated coefficient values correspond to greater probabilities of reaching higher invasion status categories. The cutpoints represent the two baseline intercepts for (non-forestry) species in Europe to reach at least naturalized and invasive status, respectively. Significance was assessed using likelihood-ratio tests, with a joint test on all factor levels in case of continents to asses if invasion probabilities are equal for all continents (null-hypothesis) or different between at least two of them (alternative-hypothesis); as such jointly for all continents (= factor levels), only a single P-value exists and quantifies the null-hypothesis support. Because of the low number of alien records for Cupressaceae in Africa and North America, these continents were omitted from the models.

species numbers (Fig. 2, Table 2). With respect to status classes, most casual Pinaceae and Cupressaceae were recorded in Europe, but transition probabilities to higher invasion categories were lowest there among all continents (Table 1, Appendix S1). Highest numbers of naturalized species of both families were once more recorded in Oceania. Region area was positively correlated to overall escape probabilities (GLMMs) of Pinaceae (P < 0.001), but not of Cupressaceae species (P = 0.26) (Table 2). By contrast, we could not detect any area effect on the probabilities of either Pinaceae or Cupressaceae species becoming naturalized or invasive in a region (proportional odd models; P = 0.08 and P = 0.59, respectively).

Taxonomic patterns of invasion In total, 60 Pinaceae (26% of all species in the family) and 26 of 142 Cupressaceae (18% all species in the family) were recorded as alien in at least one the 60 regions considered here. The most wide-spread alien Pinaceae (Fig. 3a) was Pseudotsuga menziesii (escaped from cultivation in 28 regions), followed by Pinus radiata (27 regions), P. nigra and P. pinaster (both 18 regions). The most wide-spread alien Cupressaceae (Fig. 3b) were Chamaecyparis lawsoniana (14 regions), Cupressus macrocarpa, C. sempervirens (both 13 regions) and Thuja orientalis (10 regions). Most species escaped from cultivation in only a few regions, with 26


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Figure 2 Boxplots of non-forestry (open) and forestry (shaded) Pinaceae (a; nnon-forestry = 29, nforestry = 31) and Cupressaceae species (b; nnon-forestry = 22, nforestry = 4) per region in different continents, and total proportion of regions per continent with at least alien respective naturalized occurrence for Pinaceae (c; nPinaceae = 60) and Cupressaceae (d; nCupressaceae = 26) species. For both families, probabilities of alien occurrence are significantly higher for forestry species (P < 0.001 and P < 0.001, respectively) and differ between continents (Pinaceae: P = 0.004; Cupressaceae: P < 0.001). Europe: n = 25 regions, North America: n = 14, Oceania: n = 8, South America: n = 11, Africa: n = 2. For assignment of conifers as forestry / non-forestry species, see Appendix S2.

Pinaceae and 13 Cupressaceae species recorded as alien in only two or fewer regions. The role of forestry A total of 31 Pinaceae species have been planted for forestry outside their native range on a significant scale (see Appendix S2), with a few species (Pinus contorta, P. radiata, Pseudotsuga menziesii) being especially widely used. Non-native conifer plantations were dominated by Pinaceae species in nearly all of the regions considered here. By contrast, only four Cupressaceae species play a significant role in commercial forestry on a global scale (Chamaecyparis lawsoniana, Cryptomeria japonica, Cupressus macrocarpa, Thuja plicata), and none of them is as widely cultivated as the predominant Pinaceae species. For both Pinaceae and Cupressaceae, species used in commercial forestry had a significantly higher probability of escape from cultivation (GLMMs; P < 0.001 and P = 0.001, respectively) (Table 2). For Pinaceae, the ratio of forestry (n = 31) to non-forestry species (n = 29) recorded as alien (casual, naturalized or invasive) in at least one of the 60 regions is close to unity. Nevertheless, on each continent, the average number of alien forestry species per region was higher than the average number of non-forestry species (Fig. 2a). In addition, forestry species occur as aliens more frequently [mean number

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of regions = 9.1, standard deviation (SD) = 7.2] than non-forestry species (mean = 2.7, SD = 2.3) (Fig. 3a). Only a minor fraction of those Cupressaceae species which occurred as alien in at least one of the 60 regions are used in commercial forestry (four out of 26). However, because of their much higher probability of escape, the average numbers of forestry and non-forestry species per region were approximately balanced across all continents (Fig. 2). As in the case of Pinaceae, Cupressaceae species used in forestry occur as aliens in a wider variety of regions outside their native range (mean = 10.2, SD = 3.8) than non-forestry species (mean = 3.5, SD = 3.2, Fig. 3b). Apart from a generally higher probability of escape from cultivation, forestry Pinaceae also tend to become naturalized or invasive more frequently (proportional odds model; P < 0.001, Table 3, Fig. 4a). No comparable difference was detectable among Cupressaceae used or not used in commercial forestry (P = 0.96, Fig. 4b), but the low sample size of forestry Cupressaceae limits the generality of this result. DISCUSSION Is the Southern Hemisphere more invaded? Several authors (e.g. Richardson, 1998b; Richardson & Higgins, 1998; Mortensen & Mack, 2006; Simberloff et al., 2010) have


Global patterns of alien conifer invasions (a)

30

No. of regions

25 20 15 10 5

Pin rig

*Pin mur

Abi pin

Tsu can

Pin thu

Pin wal

Pic gla

Pic pun

*Pin tae

*Tsu het

*Pin ell

*Pin pat

Pin cana

Seq sem

*Pic sit

*Pin ban

Jun comm

Ced atl

Ced deo

*Abi gra

Pin mug

*Abi alb

*Abi nor

*Pin hal

*Pin pon

*Pin str

*Pin syl

*Lar kae

*Lar dec

*Pin pinea

*Pic abi

*Pin con

*Pin nig

*Pin pinas

*Pin rad

*Pse men

0

Species

(b)

14

No. of regions

12 10 8 6 4 2 Thu dol

Jun conf

Jun chi

Cup macna

Cup gov

Cup gla

Tet art

Cha obt

Seq gig

Cal rho

Cal obl

Tax dis

Cup lus

Cha pis

Cup ari

Jun vir

Cal dec

*Cry jap

*Thu pli

Thu occ

Thu ori

Cup sem

*Cup macro

*Cha law

0

Species

Figure 3 Pinaceae (a; only species with occurrences in > 2 study regions are shown) and Cupressaceae (b) ordered by decreasing numbers of regions where they have been recorded as escaped from cultivation. Regions where the respective species are considered to be invasive are given in black, where they are classified as naturalized in dark grey, and where they only casually escape from cultivation in bright grey. Forestry species are labelled by an asterisk (*). Note that scales of the y-axes are not equal. For species abbreviations, see Appendix S2.

argued that the continents on the Southern Hemisphere are more invaded by alien conifers than their counterparts in the Northern Hemisphere. Indeed, our global comparison demonstrates that average alien Pinaceae species numbers are highest in Oceania and South Africa and that, additionally, alien species in this family more easily become naturalized or become invasive on the continents of the Southern Hemisphere. For Cupressaceae, biogeographic trends are less clear. However, as for Pinaceae, alien Cupressaceae seem to naturalize, or become invasive, more frequently in the Southern Hemisphere, which often translates into invasions causing substantial impact on native biota. Hence, these results generally corroborate the suggestion that the Southern Hemisphere has a higher level of conifer invasions than the regions north of the equator. Most conifers alien to North America or Europe have native congeners, whereas exotic Pinaceae and Cupressaceae in the Southern Hemisphere lack such closely related species. This fact likely plays a role in explaining the biogeographical differences in conifer invasion success north and south of the equator. In particular, phylogenetic proximity between alien and native species may increase colonization rates of natural enemies on alien trees (Gossner et al., 2009), i.e. non-natives might recruit

pathogens and phytophages from their native congeners, thereby decreasing their capacity to spread in the new range (Carillo-Gavilan & Vila`, 2010). Moreover, phylogenetic nicheconservatism or at least phylogenetic signals in ecological requirements (Losos, 2008) implies that empty niches for nonnative species are more likely to exist where closely related native species are lacking (Thuiller et al., 2010; but see Diez et al., 2008). As an example, South African mountain fynbos has very few native tree species and relatively low above-ground biomass, which facilitate the encroachment of non-native conifers into this ecosystem as resources are not fully used by the resident vegetation (Richardson et al., 1990; Richardson & Cowling, 1992). In general, alien conifer escape, naturalization and invasion should be less hampered by competition in the Southern than in the Northern Hemisphere because of the widespread lack of congeners or even confamiliars south of the equator (Simberloff et al., 2010). Vice versa, with respect to positive interactions, recent studies have shown that invasions of conifer species have additionally gained momentum after important mutualistic ectomycorrhizal fungi have been introduced into their new range in the Southern Hemisphere (Schwartz et al., 2006; Dickie et al., 2010).


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Figure 4 Probabilities of alien forestry Pinaceae (a) and Cupressaceae (b) (dark-grey symbols) and non-forestry species (open symbols) to become naturalized (circles) or invasive (squares) in different continents as estimated by the cumulative logit models (Tab. 3). The baseline figure (100%) is the total number of alien Pinaceae and Cupressaceae respectively known to have escaped cultivation. For Cupressaceae, as too few naturalized and invasive species were recorded for North America and Africa, these continents were omitted from the model fitting, and hence no data are shown. Legend: Europe (n = 25 regions), N America (n = 14), Oceania (n = 8), South America (n = 11), Africa (n = 2). Abbreviations: f. = forestry species; non-f. = non-forestry species.

Forestry and propagule pressure Surrogates of propagule pressure and human disturbance of natural systems (Cassey et al., 2004; Taylor & Irwin, 2004; Chiron et al., 2009; Hulme, 2009; Pysˇek et al., 2010a) have repeatedly been shown to correlate with regional differences of plant and animal invasions. Here, we found that Pinaceae used in forestry have higher probabilities of alien occurrence and are more likely to become naturalized or invasive, and forestry species of both families colonize on average more regions (Figs 2c & 4). We argue that the higher level of invasion success associated with the use of a species in commercial forestry most probably results from a combination of high introduction effort with deliberate matching of species environmental requirements with conditions in the region of introduction (Lambdon et al., 2008; Pysˇek et al., 2009; Richardson, 2011). Forestry deliberately introduces species suitable for particular climatic and edaphic conditions (to maximize yields) and implements large-scale planting, which creates massive propagule pressure over comparatively long periods of time facilitating the rise of continuously re-establishing populations (Krˇivańek et al., 2006). Taken together, these factors make forestry a very effective pathway for invasions (Richardson, 1998b; Rouget et al., 2002; Pysˇek et al., 2009; Wilson et al., 2009). As a consequence, the higher incidence of casual, naturalized and invasive conifers in the continents of the Southern Hemisphere might, besides the scarcity of competitors and natural enemies, be additionally driven by higher introduction effort, e.g. because of larger size of plantation areas (Richardson & Higgins, 1998). The relative effect of propagule pressure on invasion success is, however, not easy to disentangle from the role that particular functional traits play in facilitating invasions. For

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example, compared to Cupressaceae, Pinaceae species are planted on a much larger scale, and a greater proportion is used in commercial forestry (Evans, 2009). This seems to explain the higher number of Pinaceae species becoming invasive across all continents. However, the more widespread use of Pinaceae for silvicultural purposes is related to the specific traits of individual species. In particular, many species in the genus Pinus are fast-growing and easy to cultivate (Richardson, 2006, 2011), which, of course, also promotes invasive spread (Grotkopp et al., 2002). A more detailed analysis of the processes behind conifer invasion patterns would have hence to include information on relevant functional traits as well as on plantation areas per species and region and, ideally, also on region-specific plantation histories (e.g. Krˇivańek et al., 2006; Bucharova & van Kleunen, 2009; Dawson et al., 2009; Pysˇek et al., 2009). Conclusions In this study, we focused on the biogeographic context of the recipient regions and on aspects of the introduction mode of alien Pinaceae and Cupressaceae. We found that geographic setting and a proxy for introduction effort, i.e. the use as forestry species, significantly impact the risk that introduced conifers escape from cultivation and become invasive. Besides possible genuine differences in invasion potential, the higher introduction effort for Pinaceae when compared to Cupressaceae is suggested as a prime driver for observed differences in invasion patterns among these two families. During the recent decades, conifer plantations have strongly increased in many parts of the world (Richardson, 1998b; Richardson & Higgins, 1998; FAO, 2000; Simberloff et al.,


Global patterns of alien conifer invasions 2010). Pinus spp. (20% of global plantation area) are the dominant tree species planted world-wide, while other coniferous species contribute for another 11%. As alien conifers are considered to have high silvicultural potential under future climate change scenarios, this trend will probably continue, or even increase, in the future (Broncano et al., 2005; Essl, 2005; Krˇivańek et al., 2006). Taking into account the substantial time lag associated with tree invasions (Kowarik, 1995; Krˇivańek et al., 2006; Pysˇek et al., 2009; Jackson & Sax, 2010; Simberloff et al., 2010), future levels of alien conifer invasions will hence probably rise sharply. To effectively reduce impacts of alien conifers, future management strategies must address spatial planning (e.g. establishing buffer zones to protected areas and susceptible habitats), include comprehensive risk assessment procedures and provide adequate resources for monitoring and eradicating eventually escaping populations as early as possible (Hulme, 2006). ACKNOWLEDGEMENTS Many colleagues have contributed their knowledge to the underlying data set (in brackets: region for which data have been provided): E. Branquart (Belgium), G. Brundu (Sardinia), L. Celesti-Grapow (Italy, Sicily), G. Domina (Sicily), N. Fuentes (Argentina & Chile), M. Finckh (Chile), H. Gatehouse (New Zealand), F. Hrusa (California), M. Josefsson (Sweden), J. Greimler (Juan Fernandez Islands), B. Hoagland (Oklahoma), C. Ludwig (Virginia & North Carolina), R. Mack (USA), A. Pauchard & B. Langdon (Chile), D. Richardson (Western and Eastern Cape Province, South Africa), M. Vila` (Spain, Baleares), and P. A. Williams (New Zealand). For discussions and comments on previous versions of the manuscript, we are obliged to T. Dirnbo¨ck, I. Ku¨hn and W. Rabitsch. The comments of two anonymous reviewers of the handling editor John Wilson and of Dave Richardson greatly improved the manuscript. This work was supported by a Visiting Research Fellowship to the Bio-Protection Research Centre awarded to the lead author. REFERENCES Agresti, A. (2002) Categorical data analysis, 2nd edn. Wiley, New York. Boulant, N., Garnier, A., Curt, T. & Lepart, J. (2009) Disentangling the effects of land use, shrub cover and climate on the invasion speed of native and introduced pines in grasslands. Diversity and Distributions, 15, 1047–1059. Broncano, M.J., Vila`, M. & Boada, M. (2005) Evidence of Pseudotsuga menziesii naturalization in montane Mediterranean forests. Forest Ecology and Management, 211, 247– 263. Bucharova, A. & van Kleunen, M. (2009) Introduction history and species characteristics partly explain naturalization success of North American woody species in Europe. Journal of Ecology, 97, 230–238.

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SUPPORTING INFORMATION Additional Supporting Information may be found in the online version of this article: Appendix S1 Regions (n = 60) included in this study with geographical variables and their alien Pinaceae respective Cupressaceae species numbers. Appendix S2 Alien Pinaceae and Cupressaceae species in the 60 regions included in this study. Appendix S3 Data sources for records of alien Pinaceae and Cupressaceae species in the 60 regions included in this study. Appendix S4 Regions ordered by decreasing numbers of alien Pinaceae (A) and Cupressaceae (B). As a service to our authors and readers, this journal provides supporting information supplied by the authors. Such materials are peer-reviewed and may be re-organized for online delivery, but are not copy-edited or typeset. Technical support issues arising from supporting information (other than missing files) should be addressed to the authors. BIOSKETCH Franz Essl is a vegetation ecologist at the Biodiversity and Nature Conservation Department of the Austrian Environment Agency. He is interested in causes and patterns of biological invasions, in diversity patterns of species and habitats and in the impact of climate change on distribution of biota and the resulting consequences for nature conservation.

Editor: John Wilson


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