Expansion of an invasive species, Ailanthus altissima, at a regional scale in Japan
Expansion of an invasive species, Ailanthus altissima, at a regional scale in Japan
Journal of Ecology and Environment. 2015. Feb, 38(1): 47-56
Copyright © 2015, The Ecological Society of Korea
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial Licens ( which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
  • Received : October 12, 2014
  • Accepted : December 30, 2014
  • Published : February 28, 2015
Export by style
Cited by
About the Authors
Misaki Chuman
Graduate School of Agricultural and Life Sciences, University of Tokyo, Tokyo 113-8657, Japan
Hiroyuki Kurokochi
Asian Natural Environmental Science Center, University of Tokyo, Tokyo 188-0002, Japan
Yoko Saito
Graduate School of Agricultural and Life Sciences, University of Tokyo, Tokyo 113-8657, Japan
Yuji Ide
Graduate School of Agricultural and Life Sciences, University of Tokyo, Tokyo 113-8657, Japan

Ailanthus altissima , which is recognized as an invasive tree in the Western world, has been widely observed in Japan. To investigate how A. altissima expanded within-population and to new populations within a region, 446 A. altissima trees were sampled from three separate sites (A, B, and C) including 35 distantly positioned patches, with three chloroplast DNA markers and nine nuclear microsatellite markers. We detected 2, 2, and 3 chloroplast haplotypes in sites A, B, and C, respectively. In addition, 271, 40, and 41 nuclear genotypes were detected in sites A, B, and C, respectively. The clonal richness value was 0.85, 0.78, and 0.53 in sites A, B, and C, respectively. Most trees with the same genotypes were distributed in the same patch, indicating that range expansion by asexual reproduction was limited to a maximum of 45 meters. According to autocorrelation analysis, the extent of nonrandom spatial genetic structure was approximately 0-2 km in sites A and C. KINGROUP analyses showed that 812, 74, and 111 nuclear genotype pairs were detected to have kinship in sites A, B, and C, respectively. Most nuclear genotype pairs were detected within the same patches or sites. These results indicate that the number of A. altissima trees gradually increased from seeds, some of which were produced by trees within sites, meaning that this species could regenerate naturally. This shows the need for the future management of A. altissima as an invasive species in Japan.
Ailanthus altissima (Mill.) Swingle (Simaroubaceae) is a deciduous and dioecious tree native to East China and North Vietnam ( Kowarik and Säumel 2007 ). It rapidly grows ( Little 1974 ) and can reproduce both sexually, i.e., by seed dispersal, and asexually, i.e., by adventitious roots ( Little 1974 , Kowarik 1995 , Kowarik and Säumel 2007 ). A. altissima has invasively expanded in Europe and North America, where it was introduced in the 1700’s ( Kowarik and Säumel 2007 ). A. altissima was first introduced into Japan in the late 1800’s. Recently, this species has spread widely throughout Japan ( Shimizu 2003 , Kurokochi et al. 2013 ). The establishment of an invasive woody species might alter ecosystem functioning, consequently having a major impact on native ecosystems ( Vitousek 1990 , Parker et al. 1999 ). The invasion of native ecosystems by non-native species is accelerating as the world’s human population multiplies and the transport of goods ever more rapidly increases on a global scale ( Pimentel 2002 ). Invasive species and their effects on ecosystems are a cause of biodiversity loss worldwide ( Pimentel 2002 ). Because the invasive expansion of A. altissima is possible in Japan as well as in other countries in Europe and North America, it is necessary to understand the range expansion of this species in Japan.
Kolar and Lodge (2001) indicated that invasiveness of a plant species is related to characteristics such as taxon, the history of invasion, and asexual reproduction. While an accurate history of the expansion of an introduced species is difficult to obtain, the range expansion of some invasive plants has been demonstrated through population-genetic analysis ( Bossdorf et al. 2005 , Rosenthal et al. 2008 , Pairon et al. 2010 ). For A. altissima , through the genetic analysis of five nuclear microsatellite markers, Aldrich et al. (2010) suggested that the dispersal of A. altissima is caused by the movement of seed via traffic along road and railway systems connecting cities in the Eastern part of the U.S. In our previous study, we focused on the history of A. altissima in Japan by analyzing 64 Japanese populations of A. altissima with a total of ca. 2400 bp of chloroplast DNA sequencing ( Kurokochi et al. 2013 ), showing that most A. altissima trees in Japan harbor one of two genetically dissimilar chloroplast haplotypes that are distributed throughout Japan. On the other hand, Liao et al. (2014) reported 12 cp-haplotypes from 440 individuals of 44 populations throughout China after chloroplast DNA sequencing (a total of approximately 1600 bp sequencing). These results indicate that the A. altissima populations in Japan have been initially derived from only a few geographically distinct regions in China and have widely spread throughout Japan. Determining the geographic pattern of range expansion of A. altissima in each location of Japan from the limited number of introductions is an additional challenge. Considering that A. altissima has abilities of both sexual and asexual reproduction, A. altissima populations may expand through a combination of both kinds of reproduction. However, the actual condition of A. altissima ’s expansion within population and to new populations within a region remains unclear.
It is known that the use of microsatellite markers for polymorphism analysis is quite effective for reproductive analyses in a wide range of organisms, from fungi to higher plants and animals. Nuclear microsatellite (nSSR) markers with high polymorphism can contribute to the analysis of parenthood, kinship, and population differentiation ( Kurokochi and Hogetsu 2014 ). The capability of asexual reproduction of woody species via adventitious roots could form large genets with a lot of ramets ( Gyokusen et al. 1991 , Kowarik 1995 , Ogawa and Hukusima 1996 , Kurokochi et al. 2010 ), and genets can be readily detected with high polymorphism nuclear DNA markers ( Jung et al. 2009 , Kurokochi et al. 2010 ).
In this study, to gain a better understanding of the method of range expansion of A. altissima on a regional scale in Japan, we investigated the genetic relationships among A. altissima trees by simultaneously evaluating the polymorphism of chloroplast and nuclear DNA markers.
- Site, patch, and sample collection
We collected A. altissima at three sites (A, B and C) in Japan. These sites were located in the center of Yamanashi prefecture, the center of Kumamoto prefecture, and the southwest of Yamaguchi prefecture, respectively ( Fig. 1 and Table 1 ).
PPT Slide
Lager Image
Locations of sites A, B, and C.
Site information and genetic indices of each site
PPT Slide
Lager Image
Lat, latitude; Long, longitude; N, number of analyzed samples; MLG, number of multilocus genotypes; Hap1 to Hap3, chloroplast haplotypes 1 to 3; R, clonal richness; AR, allelic richness; HE, expected heterozygosity; FIS, inbreeding coefficient; *P < 0.01.
There were many A. altissima patches of various sizes in the sites. In this study, a patch was defined as one A. altissima tree or one continuous stretch of A. altissima trees. The long sides of patches were shorter than 100 m. The distances between patches were more than 1 km. In total, 21, 6, and 8 patches were selected in sites A, B, and C, respectively ( Fig. 2 and Table 2 ).
PPT Slide
Lager Image
Distributions of 21, 6, and 8 patches in sites A, B, and C, respectively. Black filled circles represent patches. The names of patches are the same as in Table 2.
Patch information and detected multi-locus genotypes including the distribution of chloroplast haplotypes
PPT Slide
Lager Image
Lat, Long, N, MLG, Hap1 to 3, and R: same as for Table 1.
After A. altissima patches were haphazardly chosen from sites, A. altissima trees were chosen from each patch by the following rules: (1) the diameter at breast height (DBH) of the chosen trees was more than 10 cm and (2) the distance between the chosen trees (with DBH > 10 cm) was more than 5 m. A few leaflets were sampled from the chosen trees, whose stand positions were recorded with a hand GPS (Garmin, Chicago, IL, US), and leaflets were dried separately with silica gel in plastic bags, and stored at room temperature for later use.
- DNA extraction and microsatellite analysis
DNA was extracted from each leaflet using a modified CTAB method ( Kurokochi et al. 2013 ). Three chloroplast DNA (cpDNA) markers (Aacp01, Aacp02, and Aacp03; Kurokochi et al. in press) and nine nuclear SSR (nSSR) markers (Aa22, Aa68, Aa69, Aa75, Aa76, Aa79, Aa80, Aa82, and Aa92; Dallas et al. 2005 ) were used. All loci from the cpDNA and nSSR markers were amplified by polymerase chain reaction (PCR) with the Type-IT kit (Qiagen, Hilden, Germany). PCR products were electrophoresed using an ABI 3130 automated DNA sequencer (Applied Biosystems, Foster City, CA, USA), and their fragment sizes were analyzed with a GeneMapper software (Applied Biosystems).
- Statistical analysis
- Marker resolution, genotyping, and clonality
Chloroplast haplotypes (cp-haplotypes) of each tree were determined using the three cpDNA markers. For the nine nSSR markers, the number of alleles ( N A ), expected heterozygosity ( H E ), observed heterozygosity ( H O ), and combined non-exclusion probabilities of identity and sib-identity were evaluated with CERVUS 3.0.3 ( Marshall et al. 1998 ). Deviation from the Hardy–Weinberg equilibrium ( HWE ) was calculated using 1,000 permutations in FSTAT ver. ( Goudet 2001 ). In the analysis, trees of the same cp-haplotype and n-genotype belonged to the same haplotype group and genet, respectively. Clonal richness ( R ), a measure of the proportion of unique genotypes in the population, was calculated as R = ( G − 1)/( N − 1), where G denotes the number of genotypes and N the total number of genotyped samples ( Dorken and Eckert 2001 ). In a monoclonal stand R is ‘0’ and if R is ‘1’ then every sample has a unique genotype.
For the following statistical analyses, in cases where one n-genotype was detected for multiple trees, we selected one tree as a representative of that n-genotype.
- Genetic diversity for each site and genetic differentiation among sites
To understand the genetic diversity of each site, allelic richness ( El Mousadik and Petit 1996 ), Nei’s unbiased expected H E (Nei’s H E ) ( Nei 1987 ), and inbreeding coefficients ( F IS ) of the A. altissima patches in sites A, B, and C were calculated with FSTAT ver., using the nSSR markers. The significance of F IS deviation from zero was tested by 1000 random permutations using FSTAT ver.
In order to detect genetic differentiation among sites, pairwise F ST values were calculated with the Arlequin 2.0 software ( Schneider et al. 2000 ) with 1,000 permutations, using the nSSR markers.
- Genetic similarity among trees
In order to detect genetic correlation with geographic distance among trees, autocorrelation analysis was performed with SPAGeDi ( Hardy and Vekemans 2002 ), using the nSSR data set. Genetic correlation was calculated by Pairwise FRATERNITY coefficients.
For the detection of genetic relationship among trees, the presence of potential kinship among sampled trees was tested using the nSSR markers at a significance level of 0.01 with KINGROUP ver. 2 ( Konovalov et al. 2004 ) using 10,000,000 permutations following the protocol of Kurokochi and Hogetsu (2014) . N-genotype pairs with detected full-sibling and half-sibling relationships were considered as having kinship.
- Marker resolution, genotyping, and clonality
In total, 318, 51, and 77 samples from sites A, B, and C, respectively, were analyzed. Two, 2, and 3, cp-haplotypes were detected in sites A, B, and C, respectively. In addition, 271, 40, and 41 n-genotypes were detected in sites A, B, and C, respectively. Trees with the same n-genotype always had the same cp-haplotype. Cp-haplotypes were shared between patches within sites whereas no n-genotype was found in more than one patch. The clonal richness statistics were 0.85, 0.78, and 0.53 at sites A, B, and C, respectively ( Table 1 ). Using 271, 40, and 41 n-genotypes detected in sites A, B, and C, respectively, the values of N A , H E , and H O of each nSSR marker were calculated ( Table 3 ). The mean of N A , H E , and H O were 22.1, 0.843, and 0.650, respectively. The combined non-exclusion probabilities of identity and sib-identity were both <0.001.
Summary of genetic diversity based on nine nuclear microsatellite markers ofAilanthus altissima
PPT Slide
Lager Image
NA, the number of alleles per locus; HE, expected heterozygosity; HO, observed heterozygosity; P-HWE, deviation from Hardy–Weinberg equilibrium; *P < 0.01; combined nonexclusion probabilities of identity and sib identity were both <0.001.
In our previous study on a countrywide scale, we observed that some A. altissima populations contained plural cp-haplotypes, whereas others were composed of only one cp-haplotype with no significant genetic differentiation of cp-haplotypes by distance (Kurokochi et al. in press). In the present study, 19 patches had only one cp-haplotype and the other patches had more than one ( Table 2 ). Given that the cp-haplotype is derived from the mother tree, these distributions indicate that more than one seed source was present around the sites and that the A. altissima trees in the present study sites were derived from those sources.
Kowarik and Säumel (2007) indicated that A. altissima can disperse themselves by clonal ramets, although usually less than 50 m from the parent tree. In this study, all trees with the same n-genotype were located in the same patch ( Table 2 ). Our results suggest that A. altissima expanded by active asexual reproduction but the range expansion by asexual reproduction was limited to a maximum of about 45 m.
- Genetic diversity for each site and differentiation among sites
A R and H E of site A were highest and F IS of site C was the largest. The values of F IS were significantly greater than zero at all sites ( Table 1 ). Because a positive value of F IS is associated with homozygote excess, mating between relatives within sites may affect these significant deviations, which is similar to that in Robinia psedudoacacia , an invasive tree species in Japan ( Kurokochi and Hogetsu 2014 ). Or, it is also possible that F IS values at the site level are generated by there being gene frequency differences among patches due to the Wahlund effect, which could give rise to F IS values of the magnitude observed. In addition, pairwise F ST values were 0.206, 0.046, and 0.214 between sites A-B, B-C, and C-A, respectively, and those values were significantly larger than zero ( P < 0.05). These results indicate that there are genetic differentiations among the sites.
- Genetic relationship among trees
A. altissima produces many seeds; for instance, a matured A. altissima tree can produce a maximum of 325,000 samaras per year ( Bory and Clair-Maczulajtys 1980 ). A. altissima is typical of wind-dispersed trees ( Kowarik and Säumel 2008 ), and its seeds can be dispersed and established to up to more than 100 m ( Landenberger et al. 2007 ). In addition, 75% of seedlings were established up to 65 m away from the parent tree ( Cho and Lee 2003 ). According to the autocorrelation analysis, nonrandom spatial genetic structures were strong within 1 km in sites A and C ( Fig. 3 ), indicating that A. altissima trees could have gradually been established through seeds within a region, some of which were produced from trees within the sites. In contrast, a nonrandom spatial genetic structure was not detected in site B, of which area was narrower than those of sites A and C ( Fig. 3 ). However, in this study, it was still unclear that the result of site B came from small sample size or local conditions.
PPT Slide
Lager Image
Result of autocorrelation analysis among 271, 40, and 41 genotypes of Ailanthus altissima detected from sites A, B, and C, respectively. Dotted lines denote 95 % significance level.
KINGROUP analyses showed that 812, 74, and 111 n-genotype pairs had kinship in sites A, B, and C, respectively. Most of those pairs (782 of 812, 45 of 74, and 78 of 111 n-genotype pairs) were detected within the same patches or sites ( Table 4 ). These results also supported the autocorrelation analysis, suggesting that the dispersed seeds were mostly established within several hundred meters from mother trees and contributed to the expansion of A. altissima trees on a fine scale and that some of them could become founders of new A. altissima populations distant from mother trees. On the other hand, some ngenotype pairs having kinship were detected among trees in different sites ( Table 4 ) and this result seemed to have some relation with the results of autocorrelation analysis in site A, i.e., nonrandom spatial genetic structures were detected approximately in 5 and 22 km ( Fig. 3 ). It might be possible that dispersed seeds had traveled more than several hundred kilometers with the movement of traffic along road and railway systems like in connecting cities in the Eastern U.S. ( Aldrich et al. 2010 ), but it was very unlikely with consideration of the previous report about natural seed dispersal ( Cho and Lee 2003 ). Or, the curious pairs might have occured incidentally. It is worth noting that the absence of geographic genetic structure has been previously reported on a broad (countrywide and/or landscape) scale for several invasive woody plants ( Dunphy and Hamrick 2005 , Aldrich et al. 2010 , Le Roux et al. 2011 ), and this tendency has also been previously reported for A. altissima in the U.S. ( Aldrich et al. 2010 ) and Japan ( Kurokochi et al. 2013 ). Moreover, A. altissima trees derived from only a few genetically confined populations appear to have been introduced into Japan ( Kurokochi et al. 2013 ). In view of these previous studies, some trees established in a geographically distant location may share similar alleles. Such sharing may also account for the anomalous n-genotype pairs.
When cp-haplotypes of each tree were subjected to KINGROUP analyses, most n-genotype pairs showing kinship were detected among trees belonging to the same cp-haplotypes and only a few of these pairs showed different cp-haplotypes ( Appendix 1 ). Given that some n-genotype kinship pairs showed different cp-haplotypes, it is possible that two trees derived from different intercrossed cp-haplotype groups. Therefore, one reason why most of these n-genotype pairs were detected among trees belonging to the same cp-haplotypes despite the presence of several cp-haplotypes in the same patches may be due to the low number of initial trees in a location and/or short history of A. altissima establishment in each patch.
Numbers of nuclear genotype pairs connected by kinship in pairs of patches
PPT Slide
Lager Image
Patch, same as Table 1; in parentheses, number of nuclear genotype pairs connected by kinship detected among different chloroplast (cp)-haplotypes; before parentheses, number of nuclear genotype pairs connected by kinship.
- Range expansion ofAilanthus altissimain Japan
The mechanism of the range expansion of A. altissima trees at various locations in Japan was inferred by considering the active planting history of A. altissima in the past in Japan ( Uehara 1959 , Shimizu 2003 ), and findings of our previous ( Kurokochi et al. 2013 , Kurokochi et al. in press), and present study
First, some A. altissima trees derived from genetically limited populations were introduced to Japan ( Kurokochi et al. 2013 , Kurokochi et al. in press). Second, seedlings and/or seeds derived from the part of the introduced populations were planted in various locations ( Uehara 1959 , Shimizu 2003 ). At the same time, the planted trees grew, matured, and dispersed seeds to the surrounding area mostly within several hundred meters and a few more than several kilometers ( Fig 3 ). Third, a few dispersed seeds succeeded in being established at some distance from the planted trees ( Table 4 ). Fourth, the initially established trees grew, expanded to a maximum several dozen meters through asexual reproduction ( Table 2 ), and dispersed their seeds in the local vicinity ( Table 4 and Fig. 3 ), leading to the establishment of seedlings. As a consequence, A. altissima populations developed at various locations in Japan.
Kinship pairs of nuclear genotypes
PPT Slide
Lager Image
O, number of nuclear genotype pairs connected by kinship within each patch; A, number of nuclear genotype pairs connected by kinship with patches in site A; B, number of nuclear genotype pairs connected by kinship with patches in site B; C, number of nuclear genotype pairs connected by kinship with patches in site C.
This study was supported in part by a Grant-in-Aid for Scientific Research (C) from the JSPS to YS (22580157).
Aldrich PR , Briguglio JS , Kapadia SN , Morker MU , Rawal A , Kalra P , Huebner CD , Greer GK 2010 Genetic structure of the invasive tree Ailanthus altissima in eastern United States cities J Bot.
Bory G , Clair-Maczulajtys D 1980 Production, dissemination et polyphormisme des semences d’Ailanthus altissima (Mill.) Swingle, Simaroubacees [Production, dissemination and polymorphism of seeds in Ailanthus altissima] Rev Gen Bot 88 297 - 311
Bossdorf O , Auge H , Lafuma L , Rogers WE , Siemann E , Prati D 2005 Phenotypic and genetic differentiation between native and introduced plant populations Oecologia 144 1 - 11    DOI : 10.1007/s00442-005-0070-z
Cho CW , Lee KJ 2003 Seed dispersion and seedling spatial distribution of the tree of heaven in urban environments Kor J Environ Ecol 16 87 - 93
Dallas JF , Leitch MJB , Hulme PE 2005 Microsatellites for tree of heaven (Ailanthus altissima) Mol Ecol Notes 5 340 - 342    DOI : 10.1111/j.1471-8286.2005.00920.x
Dorken ME , Eckert CG 2001 Severely reduced sexual reproduction in northern populations of a clonal plant, Decodonverticillatus (Lythraceae) J Ecol 89 339 - 350    DOI : 10.1046/j.1365-2745.2001.00558.x
Dunphy BK , Hamrick JL 2005 Gene flow among established Puerto Rican populations of the exotic tree species, Albizia lebbeck Heredity 94 418 - 425    DOI : 10.1038/sj.hdy.6800622
El Mousadik A , Petit RJ 1996 High level of genetic differentiation for allelic richness among populations of the argan tree [Argania spinosa (L.) Skeels] endemic to Morocco Theor Appl Genet 92 832 - 839    DOI : 10.1007/BF00221895
Goudet J. 2001 FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3)
Gyokusen K , Iijima Y , Yahata H. 1991 Spatial distribution and morphological features of root sprouts in niseakasia (Robinia pseudo-acacia L.) growing under a coastal black pine [Pinus thunbergii] forest Bull Kyusyu Univ For 54 13 - 28
Hardy OJ , Vekemans X 2002 SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels Mol Ecol Notes 2 618 - 620    DOI : 10.1046/j.1471-8286.2002.00305.x
Jung SC , Matsushita N , Wu BY , Kondo N , Shiraishi A , Hogetsu T 2009 Reproduction of a Robinia pseudoacacia population in a coastal Pinus thunbergii windbreak along the Kujukurihama Coast, Japan J For Res 14 101 - 110    DOI : 10.1007/s10310-008-0109-1
Kolar CS , Lodge DM 2001 Progress in invasion biology: predicting invaders Trends Ecol Evol 16 199 - 204    DOI : 10.1016/S0169-5347(01)02101-2
Konovalov DA , Manning C , Henshaw MT 2004 KINGROUP: a program for pedigree relationship reconstruction and kin group assignments using genetic markers Mol Ecol Notes 4 779 - 782    DOI : 10.1111/j.1471-8286.2004.00796.x
Kowarik I 1995 Clonal growth in Ailanthus altissima on a natural site in West Virginia J Veg Sci 6 853 - 856    DOI : 10.2307/3236399
Kowarik I , Säumel I. 2007 Biological flora of Central Europe: Ailanthus altissima (Mill.) Swingle Perspect Plant Ecol Evol Syst 8 207 - 237    DOI : 10.1016/j.ppees.2007.03.002
Kowarik I , Säumel I 2008 Water dispersal as an additional pathway to invasions by the primarily wind-dispersed tree Ailanthus altissima Plant Ecol 198 241 - 252    DOI : 10.1007/s11258-008-9398-x
Kurokochi H , Hogetsu T 2014 Fine-scale initiation of nonnative Robinia pseudoacacia riparian forests along the Chikumagawa River in central Japan J Ecol Environ 37 21 - 29    DOI : 10.5141/ecoenv.2014.003
Kurokochi H , Saito Y , Chuman M , Ide Y 2012 Genetic variation of planted or naturalized Ailanthus altissima populations in Japan Japanese For Soc Cong 123 A03 -
Kurokochi H , Saito Y , Chuman M , Ide Y 2013 Low chloroplast diversity despite of phylogenetically divergent haplotypes in Japanese populations of Ailanthus altissima (Simaroubaceae) Botany 91 148 - 154    DOI : 10.1139/cjb-2012-0159
Kurokochi H , Saito Y , Ide Y. Genetic structure of the introduced Heaven Tree (Ailanthus altissima) in Japan: Evidence for two distinct origins with limited admixture Botany    DOI : 10.1139/cjb-2014-0181
Kurokochi H , Toyama K , Hogetsu T 2010 Regeneration of Robinia pseudoacacia riparian forests after clear-cutting along the Chikumagawa River in Japan Plant Ecol 210 31 - 41    DOI : 10.1007/s11258-010-9735-8
Landenberger RE , Kota NL , McGraw JB 2007 Seed dispersal of the non-native invasive tree Ailanthus altissima into contrasting environments Plant Ecol 192 55 - 70    DOI : 10.1007/s11258-006-9226-0
Le Roux JJ , Brown GK , Byrne M , Ndlovu J , Richardson DM , Thompson GD , Wilson JRU 2011 Phylogeographic consequences of different introduction histories of invasive Australian Acacia species and Paraserianthes lophantha (Fabaceae) in South Africa Divers Distrib 17 861 - 871    DOI : 10.1111/j.1472-4642.2011.00784.x
Liao YY , Guo YH , Chen JM , Wang QF 2014 Phylogeography of the widespread plant Ailanthus altissima (Simaroubaceae) in China indicated by three chloroplast DNA regions J System Evol 52 175 - 185    DOI : 10.1111/jse.12065
Little S , Schopmeyer CS 1974 Seeds of Woody Plants in the United States US Department of Agriculture, Forest Service Washington, DC Ailanthus altissima (Mill.) Swingle--Ailanthus 201 - 202
Marshall TC , Slate J , Kruuk LEB , Pemberton JM 1998 Statistical confidence for likelihood-based paternity inference in natural populations Mol Ecol 7 639 - 655    DOI : 10.1046/j.1365-294x.1998.00374.x
Nei M 1987 Molecular Evolutionary Genetics Columbia University Press New York, NY
Ogawa M , Hukusima T 1996 Root sprout and seedling dynamics of Prunus ssiori in an Abies mariesii forest in Oku-Nikko, Kanto District J Jpn For Soc 78 195 - 200
Pairon M , Petitpierre B , Campbell M , Guisan A , Broennimann O , Baret PV , Jacquemart AL , Besnard G 2010 Multiple introductions boosted genetic diversity in the invasive range of black cherry (Prunus serotina; Rosaceae) Ann Bot 105 881 - 890    DOI : 10.1093/aob/mcq065
Parker IM , Simberloff D , Lonsdale WM , Goodell K , Wonham M , Kareiva PM , Williamson MH , Von Holle B , Moyle PB , Byers JE , Goldwasser L 1999 Impact: towards a framework for understanding the ecological effects of invaders Biol Invas 1 3 - 19    DOI : 10.1023/A:1010034312781
Pimentel D 2002 Biological Invasions: Economic and Environmental Costs of Alien Plant, Animal, and Microbe Species CRC Press Boca Ranton, FL
Rosenthal DM , Ramakrishnan AP , Cruzan MB 2008 Evidence for multiple sources of invasion and intraspecific hybridization in Brachypodium sylvaticum (Hudson) Beauv. in North America Mol Ecol 17 4657 - 4669    DOI : 10.1111/j.1365-294X.2008.03844.x
Schneider S , Roessli D , Excoffier L. 2000 Arlequin ver. 2.000: a software for population genetics data analysis [user’s manual] University of Geneva, Genetics and Biometry Laboratory Geneva, Switzerland
Shimizu T 2003 Naturalized plants in Japan Heibon-sha Tokyo (in Japanese)
Uehara K 1959 Illustrations of Trees Ariake Shobou Tokyo, Japan (in Japanese)
Vitousek PM 1990 Biological invasions and ecosystem processes: towards an integration of population biology and ecosystem studies Oikos 57 7 - 13    DOI : 10.2307/3565731