Predicting naturalization of southern African Iridaceae in other regions

MARK VAN KLEUNEN,* STEVEN D. JOHNSON* and MARKUS FISCHER t * Centre for In vasion Biology, School of Biological and Conservation ScienceJ; University of KwaZulu-Natal, P Bag X01, Scottsville, Pielermaritzburg 3209, South Aji'ica; and t InstilLlte of Planl Science.l; University of Bern, Aitenbergrail1 21, CI-/-3013 Bern, Switzerland

Summary

1. One of the major challenges in invasion biology is to predict the li ke lihood of nat­ uralization, and ultimately invasiveness, of species from properties that can be assessed in the native range prior to a species' introduction elsewhere. This is particularly relevant as intentional introduction for horticultural usage has been predicted to be the over-riding factor associated with naturalization. 2. We compiled a data set on 1036 species of Iridaceae native to southern Africa to test whether traits differ between horticulturally used and unused species, whether the likelihood of naturali zation elsewhere is higher for horticulturally used species, and whether it differs according to species' taxonomic affinities, geographical range size, altitudinal range, number of subtaxa and plant size. 3. Our results show that at least 306 southern African Iridaceae species are used in horticulture elsewhere. Of the 67 that have become naturalized elsewhere, no less than 62 are in horticulture, indicating horticultural trade as the main source of naturalized Iridaceae. 4. Global horticultural usage differs among the three subfamilies and among the genera. In addition, horticultural usage is more likely for species with a larger distributional range, a lower maximum altitude, more subtaxa and a taller height. This indicates that species introduced elsewhere for horticultural usage have a biased set of biogeographical and biological characteristics that should be corrected for in analyses of naturalization. 5. After correction for horticultural usage, naturalization differs between genera, and is more likely for species with lower maximum altitude, species with higher numbers of subtaxa and taller species. 6. Cross-validation of our predictive logistic regression model revealed a low kappa (0 '279 ± 0·069, mean ± SE) that was significantly different from zero. This indicates that the estimates from our logistic regression model can be used to predict naturalization of Iridaceae but that the accuracy is relatively low. 7. Synthesis and applications. Our study shows that screening protocols for potential invasiveness of species of Iridaceae should include international horticultural usage, and taxonomic, biogeographical and biological cha racteristics in the native range, as predictors. Moreover, for the development of more accurate predictive models, experi­ mental assessment of other plant characteristics associated with naturalization is still required.

Key-words: ali en species, altitude, biological invasions, climatic similarity, competitive ability, distributional range, genetic variation, horticulture, plant height

Correspondence: Ma rk van K leunen, Centre for Invasion Biology, School of Biological a nd Conservation Sciences, University of KwaZu lu-Natal, P Bag XO I, Scollsvill e, Pi eterma rit zburg 3209, South Africa (fax +27 33 2605 105; e-mail [email protected]). 595 Important potential determinants of naturalization Introduction that can be assessed easily in the native range i nc1 ude During the past few centuries a large number of species the following. Biogeographical characteristics, such as has been introduced into new regions. Some of these the size of the distributional range and maximum alti­ alien species have become naturalized and, in many tude, are likely to reflect the environmen tal tolerance of cases, also invasive (for terminology see Richardson species (Scott & Panetta 1993; Goodwin, McAllister & el al. 2000a). Biological invasions homogenize the Fahrig 1999; Prinzing el al. 2002) and the chance of a Earth's biota (Wilson 1975) and constitute a threat to species being introduced elsewhere (Pysek, Richardson agriculture, natural ecosystems and biodiversity (Drake & Williamson 2004). The number of intraspecific subtaxa el al. 1989; Vitousek el al. 1997). Moreover, biological is likely to reflect high intraspecific genetic variation, invasions cause tremendous economic costs (Pimentel which increases both the chance of pre-adapted geno­ el al. 2000). The control of invasive organisms is expen­ types of the species being present and the potential for sive, labour intensive and usually has limited success post-introduction evolution (Blossey & Notzold 1995; (Myers el al. 2000; Hulme 2006). Therefore it is important MUller-Scharer, Schaffner & Steinger 2004). Plant height to prevent new introductions of potentially invasive is likely to be positively associated with competitive species. Unfortunately, while highly relevant in this ability, which may increase naturalization (Crawley context, we know little about species' characteristics 1987; Blossey & Notzold 1995; Remanek el al. 2005). associated with their successful establishment out­ Comparative studies between naturalized and non­ side the native range (Kolar & Lodge 200 I). This naturalized species are potentially mos t powerful in information is required to develop screening procedures elucidating predictors of naturalization (Baker 1965). for potential invasiveness of species considered for Most of the few existing studies involve comparisons introduction. between natura li zed and non-naturalized introduced In the field of invasion ecology, there has been consider­ species in their introduced range (Richardson, van able confusion about correct terminology (Richardson Wilgen & Mitchell 1987; Rejmanek & Richardson el al. 2000a). Generally, we adhere to the definitions 1996; Reichard & Hamilton 1997; Mihulka, Pysek & used in the proposed framework of Richardson el al. Martinkova 2003; Burns 2004). However, to address (2000a). In this framework, a natura lized plant species the ultimate challenge of identifying determinants of is an alien species that manages to reproduce consist­ naturalization that can be assessed before introduction ently and sustains populations over many life cycles elsewhere, large-scale studies are required that com­ without direct intervention by humans. An invasive pare naturalized and non-naturalized species in their plant species, on the other hand, is a naturalized species common native range (Pysek, Richardson & Williamson that shows pronounced spread outside its native range. 2004). This has been done in very few studies (Scott & However, species that are considered invasive by some Panetta 1993; Goodwin, McAllister & Fahrig 1999; biologists are considered to be only naturalized by Prinzing el al. 2002). Indeed, we are not aware of any others. Because of these ambiguities, and because both previous study that has compared naturalized and non­ naturalized and invasive plants have successfully esta­ naturalized species in their common native range while blished outside their native range, we will not distinguish at the same time controlling for whether non-naturalized between both classes and refer to them jointly as species had actually been introduced elsewhere. naturalized plant species. We use the Iridaceae (iris family) from southern Previous work has shown that naturalization is affected Africa to test for determinants of naturalization. Of the by the frequency of and time since introduction (Scott c. 1800 species of this cosmopolitan family, more than & Pflowers, many have been intro­ Kleunen & Johnson 2005), hybridization with, and duced outside their native range for horticultural pur­ introgression of genes from, other species (Bleeker & poses (Manning, Goldblatt & Snijman 2002; Burbank Hurka 200 1; Hurka, Bleeker & Neuffer 2003), global 2004). Some species of Iridaceae are among the world's change (Dukes & Mooney 1999), a nthropogenic most invasive species (Weber 2003). Data on intraspe­ disturbances (Byers 2002) and interactions of species cific taxonomic diversity, and on biogeographica l and with their new environments (Richardson el al. 2000b; biological species characteristics, which may be import­ Heger & Trepl 2003). Most of these factors, however, ant potential predictors of naturalization, are readily cannot be used as predictors of naturalization before available for these species. Therefore; this study system introduction of a species because either the required is ideal for testing for characteristics associated with information is lacking or it can only be assessed after horticultural introduction and naturalization. the species has been introduced outside its native range. We compiled and analysed a data set comprising a ll Therefore one of the major challenges in invasion bio­ 1036 species of the Iridaceae native to southern Africa. logy remains identifying determinants of naturalization Our specific objectives were to test whether the likelihood that can be assessed in the native range of a species before of (i) in trod uction for horticultural purposes is associated its introduction elsewhere. with taxonomic affinity and simple biogeographical 596 and biological species characteristics, and (ii) natural­ Similarly, while maximum altitude in the native range ization is associated with global horticultural usage, was available for most species, minimum a ltitude was taxonomic affinity and simple biogeographical and available for only a few. As an estimate of the size of the biological species characteristics. distributional range within southern Africa, we counted the number of geographical regions in southern Africa in which the species occurred. These regions were the Methods countries Botswana, Lesotho, Namibia and Swaziland, and the nine provinces of South Africa. As a crude estimate COMPILATION OF THE DATA SET of genetic variation within each species, we counted the We used the checklist of the Plants of Southern Africa number of subspecies and varieties for each of the species. (POSA; available at http://www.nbi.ac.za/frames/ To test whether the proportion of naturalized species infofram.htm; accessed 12 February 2007) of the South differs between horticultural and non-horticultura l African National Biodiversity Institute to compile a species, we used a chi-squared test. We used logistic li st of all the species and their natural subtaxa (i.e. sub­ regression on all species with complete data to test species and varieties) of the Iridaceae native to southern whether horticultural usage and naturalization are Africa, which includes all African countries south of associated with the biogeographical and biological the Kunene and Limpopo Rivers. For each species, species characteristics. Additionally, we used logistic the POSA checklist reports, where available, data on regression on the subset of horticultural species to test the biological characteristics of life cycle, life form and whether their naturalization is associated with the minimum and maximum plant height, and the biogeo­ biogeographical and biological species characteristics. graphical characteristics of minimum and maximum In these analyses, we corrected for taxonomy by fitting altitude in its native range and whether it occurs in subfamily, tribe (nested within subfamily) and genus Botswana, Lesotho, N amibia, Swaziland and each of (nested within subfamily and tribe) before the biogeo­ the nine provinces of South Africa. graphical and biological characteristics. Moreover, in For each of the native species on the POSA checklist, the analysis of naturalization that used all species, we we assessed whether it was naturalized outside its native tested for the importance of introduction for horticul­ range by using the data in a global compendium of weeds tural purposes by fitting horticultural usage before (Randall 2002). The global compendium of weeds pre­ taxonomy and the species characteristics. Further, to sents the most comprehensive list of naturalized and correct for potential correlations among the biogeo­ weedy plants world-wide that is currently available. graphical and biological characteristics, we ran the The compendium also includes some species that are logistic regressions four times in such a way that each of only weedy in their native range or that are considered the four characteristics was fitted last. We calculated as potential alien weeds although they have not become ratios of mean deviance changes (quasi F-values), which naturalized yet. Therefore, we only considered species approximately follow the F-distribution (Payne et al. as naturalized when they were specifically labelled as 1993). such, i.e. were defined by Randall (2002) as alien species Because we had incomplete data, mainly on maximum that had self-sustaining and spreading popUlations wi th altitude, our analyses included 690 of the 1036 species. no human assistance. To assess whether a species had Species with incomplete data were less frequently been introduced for horticultural purposes outside its found among horticultural (Xf = 68'21, P < 0·00 I) and native range, we used three of the most comprehen­ naturalized species (Xf = 10'99, P =0·00 I), presumably sive databases on globally used horticultural plants because these species were more frequently studied. (Plant Finder of the Royal Horticultural Society, However, the frequency of these species did not differ http://www.rhs.org.uk/rhsplantfinder/plantfinder.asp; between naturalized and non-naturalized horticultural PlantFiles of Dave's Garden, http://davesgarden.com/ species (Xf = 0'20, P = 0'654), indicating that the pf/ ; HortiPlex Plant Database of GardenWeb, http:// potential bias as a result of exclusion of species with hortiplex.gardenweb.com/plants/; all accessed 12 Feb­ incomplete data from the analyses is likely to be small. ruary 2007). For each species, we included its subfamily and Moreover, when we excluded maximum altitude from tribe by using the database of the Germplasm Resources the analyses, there were no major changes in the results. Informa tion Network (http://www.ars-grin.gov2/ To assess the predictive value of the estimates from cgi-bin/npgs/htmllindex.pl; accessed 12 February 2007). our logistic regression model on naturalization, we used the cross-validation approach (Prinzing et al. 2002). We randomly excluded 100 species from the data set, ANALYSES calculated the estimates of the logistic regression model In the analyses, we did not include life cycle and life for the remaining 590 species, and used these estimates form beca use all of the species of Iridaceae are perennial to calculate the probability that each of the 100 excluded and the vast majority of species are geophytes (Gold­ species would become naturalized according to this blatt, Manning & Archer 2003). Further, because data model. This cross-validation procedure was repeated on minimum plant height of species were often lacking, 10 times. As a measure of overall agreement between we only included maximum plant height in the analyses. the predicted naturalization status and the true one, we 597 Table I. Horticultural usage and naturalization of the 1036 species of the Iridaceae native to southern Africa. The 1036 species are grouped according to the three subfamilies, six tribes (between parentheses) and 32 genera

Non-horticultural Horticultural

Genus Non-natura li zed Naturalized Non-natura li zed Naturalized Total

Iridiodeae (Iridia) Dietes 0 0 2 3 5 Fen'aria 9 0 3 I 13 Moraea 139 2 29 7 177 Iridiodeae (Sisyrinchieae) Bobartia 14 0 0 15 Ixioideae (Ixieae) Babiana 44 0 20 4 68 Chasmanthe 0 0 I 2 3 Crocosmia 0 0 5 2 7 Devia 0 0 0 I Dierama 13 0 22 2 37 Duthiastrum I 0 0 0 I Freesia 6 0 5 5 16 Geissorhiza 77 0 8 0 85 Gladiolus 97 0 58 II 166 Hesperantha 63 0 13 I 77 Ixia 39 I 6 6 52 Melasphaerula 0 0 I 0 I Radinosiphon 2 0 0 0 2 Romulea 51 I 2 1 3 76 Sparaxis 6 I 4 4 15 Syringodea 8 0 0 0 8 Tritonia 16 0 7 3 26 Tritoniopsis 23 0 0 24 Xenoscapa 2 0 0 0 2 Ixioideae (Pillansieae) Pillansia 0 0 0 Ixioideae (Watsonieae) Lapeirousia 34 0 3 0 37 Micranthus 2 0 I 0 3 Thereianthus 8 0 0 0 8 Watsonia 21 0 26 5 52 Nivenioideae Aristea 34 0 7 3 44 Klattia 3 0 0 0 3 Nivcnia 10 0 0 0 10 Witsenia 0 0 0 I Total 725 5 255 51 1036

calculated Cohen's coefficient of concordance (kappa; (Ixia campanulata, Moraea lelVisiae, Moraea miniata, Cohen 1960). Values of kappa can range from - I (com­ RomulaflavlI and Sparaxis pillansii) of the natura lized plete disagreement) via 0 (no agreement) to + I (perfect species were not found in the three databases on horti­ agreement). We used a t- test to assess whether kappa cultural plants (Table I), which exemplified that species was signifi cantly different from zero. of lridaceae that have been intentionally introduced elsewhere for horticultural purposes have a disproportion­ ally high probability of being naturalized compared Results with non-horticultural ones (Xf = 136'61, P < 0·001).

PROPORTIONS OF HORTICULTURAL AND NATURALI ZED SPEC IES POTENTIAL DETERM I NANTS OF HORTI C ULTURA L USAGE At least 306 of the 1036 species of lridaceae native to southern Africa were used in international horticulture, T he percentage of horticultural species was significantly and at least 67 were naturalized elsewhere (Table I; see higher in the subfamily l xioideae (33%) than in the Appendix S I in the supplementary material). Only five subfamilies lridiodeae (22 01<,) and Nivenioideae (17%; 598 Table 2. Summary of logistic regression of horticultural usage and naturali zation over all species, and of naturalization of horticultural species for the Iridaceae native to southern Africa. Because for some species data on o ne or more of the biogeographical and biological characteristics were missing, the logistic regression was based on 690 instead of 1036 species. Parentheses indicate nesting of the taxonomic levels. Horticultural usage and the taxonomic levels were fitted sequentially, and the biogeographica l and biological characteri stics were fitted aft er all the other effects. * P < 0'05, ** P < 0·01, *.* P < 0·001

Naturalization of Horticultural usage Naturalization horticultural species

Mean Mean Mean Effect d.r. deviance Quasi-F d.f. deviance Quasi-F d.r. deviance Quasi-F

Horticultural usage 9 1· 55 1 244' 15*** Subfamily 2 7· 123 6'49** 2 0·118 0·09 2 0·344 0·21 Tribe (subfamily) 3 1·749 1·59 3 1·333 0·92 2 1·632 0·90 Genus (tribe, subfamily) 26 5·381 4'90*** 26 1·450 3'87*** 17 1·8 17 1'97* Distribution in southern Africa 12·705 11 '57*** 0·039 0·10 I 0·053 0·06 Maximum altitude 13·1 6 1 11 ·99**· 4·624 12'33*** 4·837 5'23* Number of subtaxa I 8·070 7'35** 7·320 19'52*** 6·063 6'56* Maximum height %85 9'69*** I 4·537 12·10**· 4·550 4'92* Residual 654 1·098 653 0·375 235 0·924

1·50 (a) (b) Vi' Q) :::J 1·25 § 0 Q) - 0 00>0 Cll rn 1·00 ~ 0 0 0 0 00 l}l ~ o 9 0 0

00 0 .3 0 0·25 a~ 0 :e-g 0·00 0 I(f)o ~ -0·25 ::::J 0 '5' - 050 0 ~ -0·75 2 3 4 5 6 7 8 9 0 500 1000 1500 2000 2500 3000 3500 Number of native regions Maximum altitude [m)

1·50 (e) (d) 0 Vi' 0 Q) 1·25 ::::J 0 0 ~~ 1·00 0 s CIl c S () ~ .Q 0·75 I -t ~& 0·50 .3 0 0 0·25 · I 0 ~o. i 0·00 Cl 0 :e-g ~ 0 Io ~(f) -0·25 0 :::J 8 '5' - 0·50 ~ -0·75 ,- 2 3 4 5 6 0·0 0·5 1·0 1·5 2·0 25 Number of subtaxa Maximum height [m)

Fig. I. Adjusted values of horticultural usage and fitted lines of logistic regression fo r (a) size of distributional range (logistic regression coefficient ± SE =0·3077 ± 0'0928), (b) maximum altitude (- 0'000601 ± 0'000177), (c) number of subtaxa (0 ·466 ± 0' 177) and (d) maximum height ( 1'004 ± O' 344). All logisti c regression coeffi cients a re significant (see Table 2). Adjusted values of ho rticultural usage for each species characteristic are corrections of the original binomial values 0 (not used in ho rticulture) and I (used in horticulture) for the contribution of taxonomic status and the remaining biogeographical and biological characteristics.

Tables I and 2) . Moreover, horticultural species were taxonomy, the likelihood of horticultural usage was not randomly distributed among the genera (Table 2). significantly negatively associated with maximum The genera with the highest percentage of horticultural altitude, and significantly positively associated with species were Dietes, Crocosmia and Melasphaerula (a ll size of the distributional range in southern Africa, the 100%), while there were eight genera wi tho ut horticul­ numper of subtaxa and maximum height (Fig. I a nd tural species (Table I). This indicated that horticultural Table 2). T hi s indicated that horticultural usage was usage of species was not taxonomically independent. associated with biogeographical and biological chara­ After taking into account variation as a result of cteristics of species in thei r native range. 599 1.25 (a) (b) Ul Q) 1·00 ::l o o fJ 00 iii 0·75 00 c > o o 8 o c o .- 0 0·50 ~t .!::! 0 0·25 o o ~g- 0·00 _::l 0..~ "'"0 -0·25 Z Q) -0·50 ~ - 0·75 '0 o ~ - 1·00 L,-~~~-~~~~~~ 2 3 4 5 6 7 8 9 o 500 1000 1500 2000 2500 3000 3500 Number of native regions Maximum altitude 1m]

1.25 (c) (d) Ul Q) o 0 ::l 1·00 I o iii o o > 0·75 o c c @ .Q 0 0·50 8 o 1il'E I 8 N 0 0·25 o 0 I = 0.. ~ e .a 0.. "'"0 Z Q) iii ::l '0 - 0·75 o ~ - 1·00 L,--~-~-_~-~-.,.- 2 3 4 5 6 0·0 0·5 1·0 1·5 2·0 2·5 Number of subtaxa Maximum height 1m]

Fig. 2. Adjusted values of naturalization and fitted lines of logistic regression for (a) size of distributional range (logistic regression coefficient ± SE = 0·0317 ± 0·0985), (b) maximum altitude (-{)·000761 ± 0·000223), (c) number of subtaxa (0·652 ± 0·149) and (d) maximum height (1 ·094 ± 0·314). The three significant relationships are indicated with solid lines and the non-significant relationship with a dashed line (see Table 2). Adjusted values of naturalization for each species characteristic are corrections of the original binomial values 0 (not naturalized) and I (naturalized) for the contribution of horticultural usage, taxonomic status and the remaining biogeographical and biological characteristics.

POTENTIAL DETERMINANTS OF NATURALIZATION PREDICTIVE VALUE OF THE STATISTICAL MODEL After taking into account variation explained by horti­ cultural usage of species, the likelihood of naturalization The predicted probabilities of naturalization in the cross­ differed significantly between genera but not between validation of the estimates of the logistic regression model higher taxonomic levels (Table 2). The genera with the on naturalization were significantly higher for species highest percentage of naturalized horticultural species found to be naturalized than fo r the species found not were Chasmanlhe (67%) and Dieles (60%), while there to be naturalized (Fig. 3; Mann- Whitney U = 10715, were six horticultural genera without naturalized species Z = - 11 ·47, P < 0·00 I). When using a probability cut­ (Table I). This indicated that naturalization of species off of O· 5, we found that, of the 43 species predicted to was not taxonomically independent. be naturalized, 21 (49%) were naturalized, while of the After also taking into account variation explained 957 species predicted not to be naturalized, 889 (93%) by taxonomy, there was no significant association were not naturalized. The mean ± SE of kappa over the between the likelihood of naturalization and size of 10 runs of cross-validation was 0·279 ± 0·069 and was the distributional range in southern Africa (Fig. 2a and significantly different from zero (19 = 4·03, P = 0·003). Table 2) . However, the likelihood of naturalization was These results indicated that the estimates of our logistic significantly negatively associated with maximum regression model on naturalization could be used to predict altitude, and significantly positively associated with naturalization but that their accuracy was rel atively low. the number of subtaxa and maximum height (Fig. 2b-d and Table 2). In a separate analysis including only horti­ Discussion cultural species, these results did not change (Table 2). In other words, the likelihood of naturalization of horti­ HORTI C ULTURAL USAGE AND cultural species was significantly negatively associated NATURALIZATION with maximum altitude, and significantly positively associated with the number of subtaxa and maximum Horticultural usage of plants is frequently mentioned height (Table 2). These results indicated that natural­ as one of the main reasons why species have been intro­ ization was associated with both biogeographical and duced outside their native range (Reichard & Hamilton biological characteristics of species in their native range. 1997) but, to our knowledge, the association between 600 1·0 that the phytogeographical status of species should be carefully considered because this might be associated 0·8 • with the likelihood of being introduced elsewhere. We £;' accounted specifically for the latter by including horticul­ ~E .0", 0·6 tural usage in the analysis. Additionally, we accounted [~ ~ for phytogeographical status by using a restricted, geo­ "0.,il T .~ c 0-4 graphically well-defined source region, and byaccount­ "0_- '" ~ 0 ing for the distributional range within this source region. 0.. • 0·2 Although we account for the issues raised by Pysek, Richardson & Williamson (2004), it should be kept in ...L 0·0 mind that there are still potentially important factors Non-naturalised Naturalised that we, and most other studies, could not account for, Observation such as the intensity and time of horticultural usage. Fig. 3. Predicted probability of naturalization from the logisti c Three earlier studies reported differences in proper­ regression model on naturalization for non-naturalized ties of naturalized and non-natura lized species. Scott & (/I =911) and naturalized (11 = 89) species of Iridaceae. The Panetta (1993) found that plants from southern Africa figure summari zes data from 10 runs of cross-validation for that are naturalized in Australia are described as weeds 100 randomly selected species. The boundaries of the box around the median indicate the 75 th and 25th percentiles. The and are geographically and climatically more wide­ whiskers indicate the 90th and 10th percentile, and the dots spread than non-natura li zed plants in their native above and below each box indicate the 95th and 5th range. Goodwin, McAllister & Fahrig (1999) found percentiles, respectively. that plants from Europe that are naturalized in New Brunswick, Canada, are taller, flower longer and are geographically more widespread than non-naturalized horticultural usage and naturalization has rarely been congeners in their native range. Prinzing et al. (2002) tested explicitly. However, a study by Mack & Erneberg found that plants from Europe that are naturalized in (2002) on the naturalized flora of the USA also indi­ two Argentine provinces generally have a ruderal life cates that it is largely the product of deliberate intro­ strategy, a greater preference for warm and nitrogen­ duction. Our study shows that 92% of the naturalized rich conditions, and are more frequent in Germany and species of Iridaceae native to southern Africa are li sted cover more flori stic regions than non-naturalized plants in international horticultural databases. The remaining in their native range. Although Prinzing et al. (2002) 8% of the naturalized species (five species) may have also found a positive association between naturaliza­ been introduced elsewhere by other mea ns, such as tion in the two Argentine provinces and utilization by agricultural contaminants. It could also be that the humans, the latter was not specifically assessed for three international horticultural databases that we these provinces. This means that, while similar studies used do not cover a ll horticultural species of Iridaceae. on naturalization of animals often correct for whether Indeed, the weed compendium of Randall (2002), the non-naturalized species have actually been introduced which was used to assess naturalization status of the (Kolar & Lodge 2002; Jeschke & Strayer 2006), none of species, mentions that these five species are cultivated. the earlier studies on naturalized plants contro lled Our study strongly indicates that horticulture is the specifically for this. As a consequence, the reported main source of introduction for naturalized species of differences in biogeographical and biological chara­ Iridaceae. Nevertheless, it also shows that only a small cteristics between naturalized and non-naturalized plants proportion (20%) of the horticultural species of Iridaceae could indicate biased introduction of species with have become naturalized outside southern Africa to specific biogeographical and biological characteri stics date. Many species of Iridaceae and other geophytes in rather than characteri stics associated with naturali za­ South Africa still await discovery by horticulturists tion itself. (Manning, Goldblatt & Snijman 2002) and it is import­ Our study showed that horticultural speciesofIridaceae ant that such species are carefully screened for their are taxonomically biased and have a larger distributional naturalizati on potential. range, lower maximum altitude, more subtaxa and are taller than non-horticultural species (Fig. I and Table 2) . In other words, species of I ridaceae that have been intro­ CO MPARATIV E STUDIES BETWEEN duced elsewhere for horticultural purposes are not a NATURALIZED AND NON-NATURALIZED random sample from the source pool. The positive SPECIES association between horticultural usage and distribu­ Comparative studies of naturalized and non-naturalized tional range (Fig. I a) might refl ect the fact that such species in their native range are promising for assess­ species are more likely to be encountered by horticul ­ ing predictors of naturalization. Pysek, Richardson & turists searching for interesting plants in the native Williamson (2004) pointed out that such compa ri sons region or that species are selected with a hi gh environ­ should be restricted to those species that are nati ve to mental tolerance. The negative association between the same source region, as was the case in our study, and horticultural usage and maximum altitude (Fig. I b) 601 could also reflect the fact that such species are more suggest that naturalized species of the Iridaceae have a likely to be encoun tered by horticulturists searching for lower tolerance to climatic conditions at higher altitudes interesting plants in the native region. Moreover, it than non-naturalized ones. Most probably, however, it could be that lowland plants are preferentially used in reflects that the climate at lower altitudes in southern horticulture because gardens tend to be in lowland Africa is more similar to the climate in the naturalized regions. The positive association between horticultural regions, which mainly include regions with a Mediter­ usage and number of subtaxa (Fig. Ic) could simply ranean or subtropical climate in Australia and North reflect the fact that species with many subtaxa have a America (see Appendix S I in the supplementary mater­ higher chance that at least one of their subtaxa is well­ ial). Moreover, because most settlements with gardens suited for horticulture. Finally, the positive association are in lowland areas, it is more likely that species are between horticultural usage and plant height (Fig. Id) introduced and become naturalized in lowland areas could be because tall plants are more conspicuous and where species from low altitude in the native range may thus more attractive garden plants. Whatever the exact have an advantage. The database information underly­ reasons are for these horticultural preferences, it shows ing our study did not allow us to test these possibilities that it is important to account for horticultural usage in and we suggest addressing it in biogeographical stud­ comparisons between naturalized and non-naturalized ies of environmental similarities between native and species. introduced ranges. The positive association between naturalization and number of subtaxa (Fig. 2c) could simply reflect the DIFFERENCES I N BIOGEOGRAPHICAL fact that at least one subtaxa of a species with many AND BIOLOGICAL CHARACTERISTICS subtaxa has a higher chance of having properties that BETWEEN NATURALIZED AND makes it likely to become invasive. Moreover, when NON-NATURALIZED SPECIES several subtaxa of a species are introduced in the same The likelihood of naturalization differed among genera, region, the high amount of genetic variation provides indicating that some genera possess characteristics that potential for evolution of characteristics that increases make them more likely to become naturalized than the likelihood of naturalization (Blossey & Niitzold other genera. After accounting for variation in natural­ 1995; MUlier-Scharer, Schaffner & Steinger 2004). ization as a result of taxonomy, naturalized species came, Competitiveness of plants is likely to increase with size on average, from lower maximum altitudes, have more (Pianka 1970) and therefore it has often been suggested subtaxa and are taller (Fig. 2 and Table 2) . Although that plant size may promote naturalization of a species these species characteristics were also associated with (Crawley 1987; Blossey & Niitzold 1995). Indeed, several horticultural usage, they did not simply reflect horti­ plant communities, mesic ones in particular, are more cultural usage because this was accounted for in the likely to be invaded by tall plant species (reviewed by analysis. However, it could be that, among the horti­ Rejmfll1ek el al. 2005). This is consistent with our find­ cultural species, the ones with these characteristics ing that naturalization was positively associated with have been used more frequen tly or for longer. Similarly, plant height (Fig. 2d). Crawley, Harvey & Purvis (1996) suggested that the high prevalence of geophytes and woody plants among PREDICTING NATURALIZATION alien plants of the British Isles may reflect horticultural taste rather than ecological performance. Nevertheless, For the development of screening protocols for potential it does appear that the characteristics included in our invasiveness of species considered for introduction study increase the likel ihood of naturalization when elsewhere, it is not only important to know which factors intensity and time of horticultural usage do not differ and species characteristics are associated with natural­ among species. ization but also how well they predict naturalization. It has often been suggested that environmental toler­ Cross-validation of the estimates of our logistic regres­ ance is likely to increase the chance of species becoming sion model revealed that, of the species predicted to naturalized (Baker 1965, 1974). Although environmental become naturalized, 49% were found to be so, while of tolerance is likely to be positively associated with the those species predicted not to become naturalized, 93% size of the distributional range (Scott & Panetta 1993; were found to be so. These classification percentages Goodwin, McAllister & Fahrig 1999; Prinzing el al. are in the range of percentages found in similar studies. 2002), the latter was not significantly associated with A study by Prinzing el al. (2002) on naturalization of naturalization (Fig. 2a). Nevertheless, it might be that European species in two Argentine provinces revealed this res ult would change if more precise estimates of correct classification percentages of 21% and 97%, range sizes were available, such as distribution within respectively (Pysek, Richardson & Williamson 2004). the geographical regions of southern Africa and the A study by Reichard & Hamilton (1997) on invasive few cases where the range of native species extends woody plants introduced into North America revealed beyond southern Africa. correct classification percentages of 97% and 71 %, respe­ The negative association between naturalization and ctively. It should be noted, however, that comparisons maximum altitude in the native range (Fig. 2b) could of percen tages of correctly classified species between 602 studies is hampered by the fact that they depend on Burbank, L. (2004) Making tlte Giadioills SlIfpass lIself: the actual number of species found in each category Teaclting tlte Plant Nell' Habits. Atbena University Press, Barcelona, Spain. (Pysek, Richardson & Williamson 2004). Therefore, Burns, J.I-I. (2004) A comparison of invasive and non-invasive coemcients of concordance, such as kappa and delta dayflowers (Commelinaceae) across experimental nutrient and (Prinzing et af. 2005), might be preferable. The kappa water gradients. Dillersity and Distributions, 10, 387 - 397. value in our study was 0,278, which indicates that the Byers, J.E. (2002) Impact of non-indigenous species on estimates of our logistic regression model have some natives enhanced by anthropogenic alteration of selection regimes. Gikos, 97, 449 - 458. predictive power but that their accuracy is relatively Cohen, J. (1960) A coefficient of agreement for nominal scales. low. This is not surprising because database information Edllcational and Psycltological Measllrement, 10, 37 - 46. is missing on several species' traits that could contribute Crawley, M.1. (1987) What makes a community invasible? to more accurate predictions. Colonization, Sliccession and Stability (eds A.J. Gray, M.1. Crawley & P.1. Edwards), pp. 429 - 453. Blackwell Scientific Publications, Oxford, UK. CONCLUSIONS Crawley, M.1.l-larvey, 1'.1-1. & Purvis, A. (1996) Comparative ecology of the native and alien floras of tbe British Isles. To our knowledge, this is the first comparative study of Pltilosopilical Transactions 0/ tlte Royal Society 0/ London naturalized and non-naturalized plant species in their Series B, 351,1251 - 1259. common native range that has also controlled for the Drake, J.A., Mooney, I-I.A., di Castri, E , Groves, R.I-I., introd uction of non-naturalized species to other regions Kruger, F.1., Rejmanek, M. & Williamson, M . (1989) Bio­ logical Inllasions: A Global Perspectil'e. Wiley and Sons, through horticulture. This is important because species New York, NY. of Iridaceae introduced for horticultural purposes are Dukes, J.S. & Mooney, I-I.A. (1999) Does global change not a random sample from the species pool but actually increase the success of biological invaders? Trends in possess characteristics that are also associated with a Ecology alld Evolution, 14, 135 - 139. tendency to become naturalized. Although our results Goldblatt, P., Manning, J.e. & Archer, e. (2003) Iridacea. Plallts 0/ SOlltltem Africa: An Annotated Checklist (eds do not necessarily extrapolate to other families, it is likely G. Gennishuizen & N.L. Meyer), pp. 1074- 1117. National that they also apply to other families of geophytes. To Botanical Institute, Pretoria, South Africa. develop predictive models further and to elucidate the Goodwin, B.1., McAllister, A.J. & Fahrig, L. (1999) Predicting role of potentially important species' characteristics, invasiveness of plant species based on biological information. COllservation Biology, 13, 422- 426. such as breeding system and phenotypic plasticity I-Ieger, T. & Trepl, L. (2003) Predicting biological invasions. (Baker 1974), we advocate that similar comparative Biological Invasions, 5, 313 - 321. methods be based on additional experimentally assessed I-Iulme, PE. (2006) Beyond control: wider implications for tbe species' characteristics. management of biological invasions. JOllrnal 0/ Applied Ecology, 43,835- 847. I-Iurka, 1-1., Bleeker, W. & Neuffer, B. (2003) Evolutionary Acknowledgements processes associated with biological invasions in the Brassi­ caceae. Biologicallnllasiolls, 5, 28 1- 292. We are grateful to the South African National Biodiver­ Jeschke, J.M . & Strayer, D.L. (2006) Determinants of verte­ sity Institute, Rod Randall, the Royal Horticultural brate invasion success in Europe and North America. Global Society, Dave's Garden and Garden Web for making Cltange Biology, 12, 1608 - 1619. data on the plant species of southern Africa, world­ van Kleunen, M. & Johnson, S.D. (2005) Testing for ecolo­ gical and genetic Allee effects in the invasive shrub Selllla wide invasive weeds and horticultural plants publicly didymobotrya (Fabaceae). Americall JOll/'llal of BotallY, 92 , accessibl e. We thank Phil Lambdon, Phil Hulme and 11 24- 11 30. four anonymous referees for helpful comments on an Kolar, e.S. & Lodge, D.M. (2001) Progress in invasion biology: earlier version of the manuscript. This research was predicting invaders. Trellds in Ecology alld Evolutioll , 16, supported by a postdoctoral fellowship of the Swiss 199 - 204. Kolar, e.S. & Lodge, D.M. (2002) Ecological predictions and Science Foundation to M. van Kleunen and funding by risk assessment for alien fishes in North America. SCiell ce, the DST-NRF Centre for Invasion Biology to S. Johnson. 298,1233- 1236. Kowarik, I. (1995) Time lags in biological invasions with regard to the success and failure of a lien species. Plallt References Invasions: General Aspects alld Special Problems (eds P. Pysek, K. Prach, M. Rej lmlnek & M. Wade), pp. 15 - 38. SPB Aca­ ilaker, I-I.G. (1965) Characteristi cs and modes of origin of demic Publishing, Amsterdam, the Netherlands. weeds. Tlte Genetics 0/ Colon izing Species (eds I-I.G. Baker Liebhold, A. & Bascompte, J. (2003) The Allee effect, stochastic & G.L. Stebbins), pp. 147- 172. 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Pysek, P., Richardson, D.M. & Williamson, M. (2004) Pre­ dicting and explaining plant invasions through analysis of Supplementary material source area floras: some critical considerations. Diversity and Distributions, 10,179- 187. The following supplementary material is available for Randall, R.P. (2002) A Glob{d Compendium of Weeds. R. G. & this article. F. 1. Richardson, Melbourne, Australia. Reichard, S.H. & Hamilton, C. W. (1997) Predicting invasions Appendix S 1. List of horticultural and non-horticultural of woody plants introduced into North America. Conservation Biology, II, 192 - 203. species of Iridaceae that are native to southern Africa Rejmilllek, M. & Richardson, D.M. (1996) What attributes and have become naturalized in other continents. make some plant species more invasive? Ecology, 77, 1655 - 1661. Rejmanek, M., Richardson, D.M., Higgins, S.I., Pitcairn, MJ. & Grotkopp, E. (2005) Ecology of invasive plants: state of the art. Illvasive Alien Species: A New Synthesis (eds H.A. Mooney, R.N. Mack, J.A. McNeely, L.E. Neville, PJ. Schei & J.K. Waage), pp. 104- 161. Island Press, Washington, DC. Richardson, D.M., Allsopp, N., D 'Antonio, C.M., Milton, SJ. & Rejmanek, M. (2000b) Plant invasions: the role of mutualisms. Biological Reviews, 75, 65 - 93. Richardson, D.M., Pysek, P., Rejmanek, M., Barbour, M.G., Panetta, F.D. & West, CJ. (2000a) Naturalization and Appendix S1. List of horticultural and non-horticultural species of Iridaceae that are native to

southern Africa and have become naturalised in other continents.

Species Horticultural Continent of naturalisation

Aristea ecklonii Yes Australia, Europe Aristea ensifolia Yes Australia Aristea gerrardii Yes North America Babiana angustifolia Yes Australia Babiana nana Yes Australia Babiana stricta Yes Australia Babiana tubulosa Yes Australia Chasmanthe bicolor Yes Australia, Europe Chasmanthe floribunda Yes Australia, North America Crocosmia masoniorum Yes Europe Crocosmia paniculata Yes Australia Dierama pendulum Yes Australia Dierama pulcherrimum Yes Australia Dietes bicolor Yes Australia Dietes grandiflora Yes Australia Dietes iridioides Yes Australia Ferraria crispa Yes Australia Freesia alba Yes Australia Freesia corymbosa Yes North America Freesia laxa Yes North America Freesia leichtlinii Yes Australia Freesia reJracta Yes Australia, North America Gladiolus alatus Yes Australia Gladiolus angustus Yes Australia Gladiolus cardinalis Yes Australia Gladiolus carneus Yes Australia Gladiolus caryophyllaceus Yes Australia Gladiolus floribundus Yes Australia Gladiolus gueinzii Yes Australia Gladiolus papilio Yes North America Gladiolus tristis Yes Australia, North America Gladiolus undulatus Yes Australia Gladiolus watsonius Yes Australia Hesperantha Jalcata Yes Australia Ixia campanulata No Europe, North America Ixia flexuosa Yes Australia Ixia longituba Yes Australia lxia maculata Yes Australia, North America lxia paniculata Yes Australia, Europe lxia polystachya Yes Australia lxia viridiflora Yes Australia Moraea aristata Yes Australia Moraea bellendenii Yes Australia Moraea collina Yes Australia, Europe Moraeaflaccida Yes Australia Moraeafugax Yes Australia Moraea lewisiae No Australia Moraea miniata No Australia Moraea ochroleuca Yes Australia Moraea vegeta Yes Australia Romulea flava No Australia Romulea minutiflora Yes Australia Romulea obscura Yes Australia Romulea rosea Yes Australia, North America Sparaxis bulbifera Yes Australia Sparaxis fragrans Yes North America Sparaxisgrandiflora Yes Australia, Europe Sparaxis pillansii No Australia Sparaxis tricolor Yes Australia, North America Tritonia crocata Yes Australia Tritonia lineata Yes Australia Tritonia squalida Yes Australia Watsonia aletroides Yes Australia Watsonia borbonica Yes Australia, North America Watsonia marginata Yes Australia, North America Watsonia meriana Yes Australia, North America Watsonia versJeldii Yes Australia