Molecular recircumscription of Broussonetia (Moraceae) and the identity and taxonomic status of B. kaempferi var. australis
Botanical Studies volume 58, Article number: 11 (2017)
Despite being a relatively small genus, the taxonomy of the paper mulberry genus Broussonetia remains problematic. Much of the controversy is related to the identity and taxonomic status of Broussonetia kaempferi var. australis, a name treated as a synonym in the floras of Taiwan and yet accepted in the floras of China. At the generic level, the monophyly of Corner (Gard Bull Singap 19:187–252, 1962)’s concept of Broussonetia has not been tested. In recent studies of Broussonetia of Japan, lectotypes of the genus were designated and three species (B. kaempferi, Broussonetia monoica, and Broussonetia papyrifera) and a hybrid (B. ×kazinoki) were recognized. Based on the revision and molecular phylogenetic analyses, this article aims to clarify these issues.
Herbarium studies, field work, and molecular phylogenetic analyses indicate that all Taiwanese materials identifiable to B. kaempferi var. australis are conspecific with B. monoica of Japan and China. Molecular phylogenetic analyses showed that Broussonetia sensu Corner (Gard Bull Singap 19:187–252, 1962) contains two clades corresponding to sect. Broussonetia and sect. Allaeanthus, with Malaisia scandens sister to sect. Broussonetia.
Based on our analyses, B. kaempferi var. australis is treated as a synonym of B. monoica and that B. kaempferi is not distributed in Taiwan. To correct the non-monophyly of Broussonetia sensu Corner (Gard Bull Singap 19:187–252, 1962), Broussonetia is recircumscribed to contain only sect. Broussonetia and the generic status of Allaeanthus is reinstated.
Prior to Corner (1962)’s circumscription, Broussonetia L’Hér. ex Vent. was known as a genus of three species distributed in East Asia and continental Southeast Asia: the type species Broussonetia papyrifera (L.) L’Hér. ex Vent., Broussonetia kaempferi Siebold, and Broussonetia kazinoki Siebold (Ohwi 1965; Liu and Liao 1976), with a hybrid between B. kazinoki and B. papyrifera known from Japan (Kitamura and Murata 1980; Yamazaki 1989; Okamoto 2006) and Korea (Yun and Kim 2009). Corner (1962) expanded the generic concept by combining Allaeanthus Thwaites as Broussonetia sect. Allaeanthus (Thwaites) Corner, stating that “there are no major differences between these sections (i.e., sect. Broussonetia and sect. Allaeanthus), which are not generically distinct” (Corner 1962). Currently, Broussonetia sect. Allaeanthus comprises four species: B. greveana (Baill.) C.C. Berg of Madagascar, B. kurzii (Hook. f.) Corner of China (Yunnan), India (Assam), Myanmar, and Thailand, B. luzonica (Blanco) Bureau of the Philippines and Sulawesi, and B. zeylanica (Thwaites) Corner of Sri Lanka (Corner 1962; Berg 1977; Zhou and Gilbert 2003; Berg et al. 2006). Based on Corner (1962)’s circumscription, Broussonetia is characterized by membranous stipules, globose syncarps, drupes covered by thickly sets of slender stalked bracts of various shapes, crustaceous to ligneous endocarps, and conduplicate to plane cotyledons. Although Corner (1962)’s expanded concept has been followed by most authors (e.g., Berg 1977; Rohwer 1993; Chang et al. 1998; Zhou and Gilbert 2003; Berg et al. 2006) except for Capuron (1972) who sustained the generic status of Allaeanthus, the monophyly of Broussonetia sensu Corner (1962) has not yet been tested (Zerega et al. 2005; Clement and Weiblen 2009) and much about the taxonomy of the genus remains unsettled.
Commonly known as paper mulberry, Broussonetia papyrifera is renowned as a fibrous tree essential to the development of paper making technique in ancient China around 100 A.D. (Ling 1961; Barker 2002). Long before Linnaeus’ time, paper mulberry had been cultivated widely in European gardens (Barker 2002) and, as documented during Captain James Cook’s circum-Pacific voyages, clonally propagated across Remote Oceanic islands by Austronesian-speaking peoples for making bark cloth (tapa), a non-woven textile that is highly symbolic of Austronesian material culture (Matthews 1996; Whistler and Elevitch 2006; Seelenfreund et al. 2010). This fast-growing dioecious weedy tree species is most likely native to China, Taiwan, and continental Southeast Asia (Matthews 1996); however, because of its long history of utilization (Matthews 1996; Barker 2002; Chang et al. 2015), considerable discrepancies exist in the literature regarding distribution ranges of B. papyrifera (Table 1). Based on the phylogeographic analysis of chloroplast ndhF-rpl32 intergenic spacer, Chang et al. (2015) demonstrated that Pacific paper mulberry originated in southern Taiwan, providing the first ethnobotanical support for the “out of Taiwan” hypothesis of Austronesian expansion. Peñailillo et al. (2016) further showed that Pacific paper mulberries are predominately female, consolidating reports on the clonal nature and corroborating Chang et al. (2015)’s inference. In addition to its long-fiber, this fast growing weedy tree has also been introduced for erosion control worldwide (Matthews 1996). Consequently, the multipurpose paper mulberry has been naturalized in southern Europe and become invasive in Argentina, Ghana, Uganda, Pakistan, the Philippines, Solomon Islands, and USA. (Matthews 1996; Barker 2002; Morgan and Overholt 2004; Florece and Coladilla 2006; Whistler and Elevitch 2006; Marwat et al. 2010; Bosu et al. 2013).
Although paper mulberry has long been introduced to Europe (Barker 2002), it is Kaempfer (1712)’s plate (“Kampf. amoen. 471. t. 472”) depicting paper mulberry (as “Morus papyrifera”) in Japan cited by Linnaeus (1753) that was lectotypified (Florence 1997) for Morus papyrifera L., the basionym of Broussonetia papyrifera. In Japan where paper mulberry is known as “Kajino-ki” (Okamoto 2006), B. papyrifera has long been regarded as non-native (Schneider 1917), also introduced for paper making around ca. 610 A.D. (Matthews 1996; Barker 2002). Quite confusingly, the name Kajino-ki was taken by Siebold (1830) for B. kazinoki, a name long applied to a small ‘monoecious’ shrub with ‘globose’ staminate catkins ca. 1 cm across known as Hime-kôzo in Japan (Chûjô 1950; Kitamura and Murata 1980; Yamazaki 1989; Okamoto 2006). Elsewhere, B. kazinoki is also widely found in China (Chang et al. 1998; Zhou and Gilbert 2003), Taiwan (Liao 1989, 1991, 1996), and Korea (Yun and Kim 2009). The natural hybrid between Hime-kôzo and Kajino-ki known as Kôzo in Japan (as B. kazinoki × B. papyrifera; Kitamura and Murata 1980; Okamoto 2006) and Daknamu in Korea (Yun and Kim 2009) has also been long cultivated and favored by Japanese and Korean farmers for traditional paper making for centuries (Yamazaki 1989). In 2009, this natural hybrid was further named B. ×hanjiana M. Kim (Yun and Kim 2009). The third species, B. kaempferi, is a ‘dioecious’ lianascent climber with ‘spicate’ staminate catkins ca. 1.5–2.5 cm long distributed in Japan (known as Tsuru-kôzo), central to southern China, and Vietnam (Ohwi 1965; Yamazaki 1982; Zhou and Gilbert 2003; Okamoto 2006), with a controversial record in Taiwan (Suzuki 1934; Kanehira 1936; Liu and Liao 1976; Liao 1989, 1991, 1996).
In the article titled ‘A speciograhical revision on Broussonetia kazinoki’, Suzuki (1934) studied a set of highly variable specimens akin to “Hime-kôzo” collected from Taiwan first identified as B. kaempferi sensu Forbes and Hemsley (1894) by Hayata (1911). After comparing with specimens collected from Japan, Suzuki (1934) concluded that B. kazinoki and B. kaempferi are different species and that all the Taiwanese specimens should be collectively recognized as a distinct taxon, which he named B. kaempferi var. australis T. Suzuki. However, Suzuki (1934)’s treatment was not cited in Kanehira (1936), the most influential pre-World War II work on the woody flora of Taiwan (Li 1963). Instead, Kanehira (1936) followed Hayata (1911)’s treatment, identifying the entity as B. kaempferi and stating that the species is dioecious. Interestingly, although a majority of the treatments of Kanehira (1936)’s ‘Formosan Trees’ were followed in the first edition of the Flora of Taiwan (Liu and Liao 1976) and its predecessor (Liu 1962), both Liu (1962) and Liu and Liao (1976) treated the species as B. kazinoki, with B. kaempferi var. australis synonymized under B. kazinoki [though mistakenly typed as B. “kazinoki” Sieb. var. australis Suzuki in Liu and Liao (1976)]. Subsequently, Yamazaki (1982) revisited the issue. Yamazaki (1982) emphasized the differences in leaf shapes, adopting Suzuki (1934)’s treatment by circumscribing B. kaempferi var. kaempferi as a variety endemic to Japan and B. kaempferi var. australis a variety distributed in southern China, Taiwan, and Vietnam. Yamazaki (1982)’s treatment was adopted by most treatments of the Chinese floras (e.g., Chang et al. 1998; Zhou and Gilbert 2003; Liu and Cao 2016) with rare exceptions such as Cao (2000) in which B. kaempferi var. australis was treated as a synonym of B. kaempferi. The taxonomic status of B. kaempferi var. australis was further complicated when Liao (1989, 1991, 1996), in addition to B. kazinoki, reported B. kaempferi from Taiwan, with B. kaempferi var. australis again treated as a synonym of B. kazinoki. Liao (1989, 1991, 1996)’s treatment has been followed by all subsequent works of Taiwan (Liu et al. 1994; Yang et al. 1997; Lu et al. 2006) as well as local online blogs (e.g., Nature Campus http://nc.kl.edu.tw/bbs/index.php). In a recent assessment of the conservation status of the flora of Taiwan, B, kaempferi is listed as a ‘vulnerable’ species with its small and declining populations (Wang et al. 2015).
Given the complicated taxonomy of these names, it is rather surprising that none of the abovementioned authors had attempted to examine and clarify type materials of the two names described by Siebold (1830) as well as B. kaempferi var. australis. After lectotypifying Siebold’s Japanese plant names (Akiyama et al. 2013), Ohba and Akiyama (2014) revised the taxonomy of Broussonetia of Japan. Surprisingly, the specimen of Siebold’s collections of Japanese plants that matched best to the protologue of B. kazinoki and thus lectotypified (M-0120984) turned out to be Kôzo (Akiyama et al. 2013; Ohba and Akiyama 2014), the natural hybrid between Hime-kôzo and Kajino-ki cultivated for traditional paper making. Consequently, B. monoica Hance, the next valid name long synonymized under B. kazinoki (e.g., Zhou and Gilbert 2003) becomes the correct name for Hime-kôzo (Ohba and Akiyama 2014). For B. kaempferi, the plate of ‘Papyrus spuria’ in Kaempfer (1712) was lectotypified (Akiyama et al. 2013). Based Ohba and Akiyama (2014)’s treatment, the four species of Broussonetia in Japan are B. kaempferi (Tsuru-kôzo), B. ×kazinoki (Kôzo), B. monoica (Hime-kôzo), and B. papyrifera (Kajino-ki).
Because Ohba and Akiyama (2014) dealt only with Japanese materials, this study attempts to clarify the distribution range of B. papyrifera and resolve controversies surrounding the name B. kaempferi var. australis based on herbarium work, field observation, and molecular data. We also sampled species of Broussonetia sect. Allaeanthus which thus far has never been sampled (e.g., Zerega et al. 2005; Clement and Weiblen 2009) to test the monophyly of Broussonetia sensu Corner (1962).
Herbarium specimens of A, BM, E, GH, HAST, K, TAI, TAIF, and TNM (herbarium acronyms according to Index Herbariorum; Thiers 2016) were examined. Specimen images of Naturalis Biodiversity Center (http://bioportal.naturalis.nl/?language=en&back), the Chinese Virtual Herbaria (http://www.cvh.org.cn/), and Global Plants on JSTOR (http://plants.jstor.org/) were consulted. Fieldtrips were conducted in Taiwan, China (Zhejiang, Fujian, Guangdong, and Guangxi), and the Philippines. All voucher specimens were deposited in HAST. To expand geographic range of our taxon sampling, herbarium collections were also sampled with the permission from E, HAST, Harvard University Herbaria (A and GH), TAIF, and TNM. The HTTP URIs of the images of important (types and vouchers) specimens examined are listed in Table 2.
Molecular phylogenetic analyses
To test the monophyly of Broussonetia sensu Corner (1962), Clement and Weiblen (2009)’s aligned DNA matrix of chloroplast ndhF and nuclear 26S (TreeBASE Study ID S2229) assembled for phylogenetic analyses of Moraceae was adopted, with morphological characters of the matrix excluded. The analyses of Clement and Weiblen (2009) sampled 76 species representing 32 Moraceae genera and B. papyrifera was shown as a sister taxon of Malaisia scandens (Lour.) Planch. in the tribe Dorstenieae. All three species of sect. Broussonetia, plus B. ×kazinoki, and three of the four species of sect. Allaeanthus were sampled (Additional file 1) for phylogenetic analyses. Conditions for PCR amplification of ndhF and 26S detailed in Clement and Weiblen (2009) were followed. Phylogenetic analyses were performed using MrBayes v3.2.6 (Ronquist et al. 2012) for Bayesian inferences (BI) and GARLIC (Bazinet et al. 2014) for maximum likelihood (ML) analyses. Based on Akaike Information Criterion implemented in jModeltest 2 (Darriba et al. 2012), the models GTR + I+Γ and TVM + Γ, which were chosen in previous study (Zerega et al. 2005), were selected for 26S and ndhF, respectively. For both BI and ML analyses, the matrix was partitioned. For ML analysis, five independent searches and 500 replicates of bootstraps were performed and results were summarized by PAUP v. 4.0a150 (Swofford 2002). For Bayesian inferences, all parameters were unlinked and estimated independently for each data partition. Two analyses were performed in parallel, each with 4 chains of 20 million generations with temperature set to 0.1, and posterior distribution was sampled every 500 generations. Model parameters and tree statistics were summarized in MrBayes and posterior probabilities higher than 0.75 were mapped to the maximum likelihood best tree manually.
Results and discussion
Type specimens of Broussonetia kaempferi var. australis
In the protologue of Broussonetia kaempferi var. australis, Suzuki (1934) designated his own (“ST”) collection No. 8336 as the type (holotype), stating “[Typus] ST 8336—in silvis secundariis ad Heikôkô prope Sinten (S uzuki-Tokio Apr. 2, 1933) in Herb. Univ. Imper. Taihoku.” Currently in the Herbarium of National Taiwan University (TAI), successor of the Herbarium of the Taihoku Imperial University, no collection bearing T. Suzuki 8336 was located. However, a collection of T. Suzuki 8362 bearing the stamp of “Typus” is labeled as the holotype of B. kaempferi var. australis T. Suzuki (http://tai2.ntu.edu.tw/Specimen/specimen.php?taiid=118781). Except for the number, all information on the label of ST 8362, “In silvis secundariis ad Heikôkô prope Sinten, Taihoku-syû, Taiwan. Suzuki-Tokio; 1933.4.2.”, matches exactly to the protologue. Unfortunately, ST 8362 is a badly damaged collection, leaving only a branch and a small leaf without diagnosable characters. Following the description of the taxon, Suzuki (1934) wrote “[Materiae] Typus-flor. mas. et fem. ST (1) 8337 et ST 4629–fl. fem.; ST 6841 et ST 8952-fruc.; SS (2) 3484 et ST 10829-steril. Fol. non partitis; SS 6042, SS 5998, ST 10827-steril. fol. partitis.” All the materials cited in “Materiae” in Suzuki (1934) are thus paratypes and all but two specimens (ST 8337 and ST 10829) are still available in TAI (Table 2). However, after careful examination of these paratypes, all of them should be identified as B. monoica sensu Ohba and Akiyama (2014).
In the treatments of Broussonetia, Liao (1989, 1991, 1996) cited three collections of B. kaempferi (Tanaka & Shimada 13557, Yamamoto 37610, and Onizuka 22022) and two collections of B. kazinoki (Liao & Wang 12332 and Liao 211714). For B. kaempferi, two collections of Tanaka & Shimada 13557 deposited in PH (Chung et al. 2009) and Yamamoto 37610 at TAI are available online (Table 2). For B. kazinoki, Liao 211714 was located in TAI. However, despite their determination by Liao (1989, 1991, 1996), all the voucher specimens cited should be identified as B. monoica sensu Ohba and Akiyama (2014).
Identity of Broussonetia kaempferi var. australis
Over the past few years, we have observed several wild populations in Taiwan that matched to the protologue and paratypes of B. kaempferi var. australis described in Suzuki (1934). Figure 1 summaries their morphological variation and key characteristics. Together with observations of herbarium specimens at A, BM, E, GH, HAST, K, TAI, TAIF, and TNM, we conclude that all Taiwanese materials are monoecious with globose staminate catkins (Fig. 1c–e), the key characteristics of B. monoica sensu Ohba and Akiyama (2014). We did not find any living or herbarium collections of Taiwan bearing spicate staminate catkins (Fig. 1n) that are characteristic of B. kaempferi (Ohba and Akiyama 2014).
Molecular phylogenetic analyses
Topologies of BI and ML analyses were identical with differences in support values. Figure 2 depicts results of ML analysis marked with both BI and ML support values. With the additional samples of Broussonetia sensu Corner (1962), the overall phylogenetic relationships of current analyses are congruent with Clement and Weiblen (2009), with samples of Broussonetia sensu Corner (1962) placed in tribe Dorstenieae (Fig. 2). However, although the monophyly of Broussonetia sect. Allaeanthus and sect. Broussonetia were each strongly supported, Malaisia scandens was placed as the sister clade to sect. Broussonetia, rendering Broussonetia sensu Corner (1962) paraphyletic. To correct the paraphyly of Broussonetia sensu Corner (1962), we propose to reinstate the generic status of Allaeanthus Thwaites. Alternatively, an expanded Broussonetia by including M. scandens would not only necessitate further nomenclatural changes but also generate a genus with no obvious diagnostic character.
Within the clade sect. Broussonetia, all samples of Taiwan that would be identified as B. kaempferi var. australis sensu Suzuki (1934), plus the natural hybrid B. ×kazinoki, were placed in a strongly supported clade of B. monoica (Fig. 2), supporting our observations that all Taiwanese materials are part of the highly polymorphic B. monoica. All three samples of B. kaempferi formed a strongly supported clade sister to the strongly supported clade of B. monoica, with the clade of B. papyrifera further sister to the clade composed of B. kaempferi and B. monoica.
Within the clade sect. Allaeanthus, B. kurzii and B. greveana were successively sister to the clade of B. luzonica with strongest supports. Although our sampling did not include Broussonetia zeylanica (≡Allaeanthus zeylanicus), the type species of Allaeanthus, we are confident that our analysis will sustain as morphologically B. luzonica and B. zeylanica are quite similar (Corner 1962), differing from each other merely by the length of staminate catkins (10–26 cm in B. luzonica vs. ca. 6 cm in B. zeylanica) and margins of leaves (entire vs. serrate) and stipules (entire vs. denticulate).
Our phylogenetic analyses revealed that species of Broussonetia sensu Corner (1962) were placed in two clades corresponding to sect. Allaeanthus and sect. Broussonetia, with Malaisia scandens placed sister to the clade of sect. Broussonetia with strongest supports. To correct the paraphyly of Broussonetia sensu Corner (1962), we propose to reinstate the generic status of Allaeanthus Thwaites. Within Broussonetia sect. Broussonetia, B. kaempferi var. australis is synonymized under B. monoica. The species B. kaempferi is not distributed in Taiwan.
Allaeanthus Thwaites, Hooker’s J. Bot. Kew Gard. Misc. 6: 302. 1854.—TYPE: Allaeanthus zeylanica
Allaeanthus zeylanicus Thwaites, Hooker’s J. Bot. Kew Gard. Misc. 6: 303, pl. IX.-B. 1854.—Type: SRI LANKA. Central Province. July 1833, Thwaites—C.P. 2215 (holotype: PDA; isotypes: B [B 10 0294368 image!], FR [FR-0031966 image!], GH [GH00034340 image!], K [K001050115 image!], K [K001050116 image!], L [L. 1583394 image!], MPU [MPU017376 image!]).—Broussonetia zeylanica (Thwaites) Corner, Gard. Bull. Singapore 19: 235. 1962.
Distribution. Sri Lanka.
Allaeanthus luzonicus (Blanco) Fern.-Vill. in Fl. Filip. (ed. 3) 4(13A): 198. 1880; Merrill, Sp. Blancoan. 122. 1918.—Neotype (designated by Merrill 1918, p. 122): PHILIPPINES: Luzon, Laguna Province, Los Baños, 14 March 1914, F.C. Gates & F.Q. Otanes 6663 (Merrill: Species Blancoanae No. 468) (US [00688524 image!]).—Morus luzonica Blanco, Fl. Filip. 703. 1837.—Broussonetia luzonica (Blanco) Bureau in de Candolle, Prodr. 17: 224. 1873; Merrill, Rev. Blancos Fl. Filip. 78. 1905; Corner, Gard. Bull. Singapore 19: 235. 1962; Berg et al., Fl. Malesiana, Ser. I 17(Part 1): 30, fig. 3. 2006.
Allaeanthus glaber Warb. in Perkins, Frag. Fl. Philipp. 3: 166. 1904.—Type: PHILIPPINES. Luzon Isl., Prov. Cagayan, Enrile, O. Warburg 12133 (holotype: B [B 10 0294369 image!]; isotype: NY [00025190 image!]).—Allaeanthus luzonicus var. glaber (Warb.) Merr., Enum. Philipp. Fl. Pl. 2: 37. 1923.—Broussonetia luzonica var. glabra (Warb.) Corner, Gard. Bull. Singapore 19: 235. 1962.
Distribution. Philippines and Indonesia (Sulawesi).
Notes: Type materials of most Blanco’s names, including Morus luzonica Blanco, are not known (Merrill 1918; Nicolson and Arculus 2001). Following Nicolson and Arculus (2001), No 468 of the “illustrative specimen” cited in Merrill (1918)’s Species Blancoanae is here taken as the effective neotypification for Morus luzonica Blanco.
Allaeanthus kurzii Hook. f, Fl. Brit. India 5(15): 490–491. 1888.—Lectotype (designated by Upadhyay et al. 2010, p. 22): MYANMAR (“BURMA”): Herbarium of the late East India Company, Birma, s.d., Griffith (Kew Distrib. 4657) [female plant] (K [K000357622 image!]).—Broussonetia kurzii (Hook. f.) Corner, Gard. Bull. Singapore 19: 234. 1962; Zhou & Gilbert, Fl. China 5: 27. 2003; Berg et al., Fl. Malesiana, Ser. I 17(Part 1): 30. 2006.
Distribution. China (Yunnan), Vietnam, Laos, Thailand, Myanmar, Bhutan, and India (Assam and Sikkim).
Allaeanthus greveanus (Baill.) Capuron, Fiches Bot. Ess. Forest. Madagascar: Fiche 1. 1968; Adansonia, n.s. 12(3): 386. 1972.—Ampalis greveanus Baill. in Grandidier, Hist. Phys. Madagascar t. 293-A. 1891.—Lectotype (here designated): MADAGASCAR. Bekopaka, near Morodava, H. Grevé 254 (P [P00108324 image!]; isolectotypes: P [P00108325 image!], P [P00108326 image!]).—Chlorophora greveana (Baillon) Léandri, Mém. Inst. Sci. Madagascar, Sér. B, Biol. Vég. 1: 18. 1948.—Maclura greveana (Baillon) Corner, Gard. Bull. Singapore 19: 237. 1962.—Broussonetia greveana (Baillon) C.C.Berg, Bull. Jard. Bot. Belg. 47: 356, fig. 21. 1977.
Notes: Of the three collections of Grevé 254 at P, P00108324 is here designated as the lectotype because the label of this collection contains the most information.
Broussonetia L’Hér. ex Vent., Tabl. Régn. Vég. 3: 547. 1799, nom. cons.—TYPE: Broussonetia papyrifera L’Hér. ex Vent.
Papyrius Lam., Tabl. Encycl. 4(2): pl. 762. 1797, nom. illeg.
Smithiodendron H.H. Hu, Sunyatsenia 3(2–3): 106. 1936.
Broussonetia papyrifera (L.) L’Hér. ex Vent., Tabl. Régn. Vég. 3: 547. 1799.—Morus papyrifera L., Sp. Pl. 2: 986. 1753.—Lectotype (designated by Florence 1997, p. 146): [icon] ‘Morus papyrifera’ in Kaempfer, Amoen. Exot. Fasc., 471, t.472. 1712.
Smithiodendron artocarpioideum H.H. Hu, Sunyatsenia 3(2–3): 107–109, pl. 6. 1936.—Type. CHINA: Yunnan, Shih-pin Hsien, 29 May 1933, H.T. Tsai 53462 (holotype: PE [1640641 image!]; isotypes: P [P06885709 image!], PE [00025034 image!], PE [00023979 image!], PE [00934142 image!]).
Distribution. The reported distributions of Broussonetia papyrifera are highly inconsistent across literature (Table 1), confounded by ancient and recent translocations of the species for multiple purposes around the world (Matthews 1996; Barker 2002; Seelenfreund et al. 2010; Chang et al. 2015). The distribution map in Matthews (1996) includes Japan, Korea, China (northern, central, and southern China), Taiwan, Vietnam, Laos, Thailand, Cambodia, Myanmar, India (Sikkim), island Southeast Asia (excluding the Philippines and Borneo), Melanesia, and Polynesia islands. Chang et al. (2015) showed a high chloroplast haplotype diversity in China, Taiwan, and Indochina, suggesting that these regions are likely native range of the species. Zhou and Gilbert (2003) provided a provincial distribution in China (Anhui, Fujian, Gansu, Guangdong, Guangxi, Guizhou, Hainan, Hebei, Hubei, Hunan, Jiangsu, Jiangxi, Shaanxi, Shandgon, Shanxi, Sichuan, SE Xizang, Yunnan, Zhejiang). In Northeast Asia, the non-native status of B. papyrifera in Japan has been repeatedly reported (Ohwi 1965; Kitamura and Murata 1980; Okamoto 2006) while this species is regarded as native in Korea (Yun and Kim 2009). Historically, the fibrous B. papyrifera had been introduced to Remote Oceanic islands via SE Asian islands (Matthews 1996; Chang et al. 2015); however, its growth and populations in these regions had declined significantly since last century (Matthews 1996). On the other hand, B. papyrifera has been introduced and become naturalized and invasive around the world (Florece and Coladilla 2006; Bosu et al. 2013; Rashid et al. 2014; Chang et al. 2015).
Broussonetia kaempferi Siebold, Verh. Batav. Genootsch. Kunst. 12: 28. 1830; Akiyama et al., J. Jap. Bot. 88: 351. 2013; Ohba & Akiyama, J. Jap. Bot. 89: 127. 2014.—Lectotype (designated by Akiyama et al. 2013, p. 351): [icon] ‘Papyrus spuria’ in Kaempfer, Amoen. Exot. Fasc, t.472, 474. 1712.
Broussonetia kaempferi var. australis auct. non T. Suzuki: Yamazaki, J. Phytogeogr. Taxon. 30(2): 69. 1982; Chang et al., Fl. Reipubl. Popul. Sin. 23(1): 27, pl. 7(9–13). 1998; Zhou & Gilbert, Fl. China 5: 27. 2003.
Distribution. Japan (Shikoku and Kyushu), central to southern China (Anhui, Chongqing, Fujian, Guangdong, Guangxi, Guizhou, Hubei, Hunan, Jiangxi, Yunnan, and Zhejiang), northern Vietnam, and India (Arunachal Pradesh; Naithani 1981).
Notes. Broussonetia kaempferi is not distributed in Taiwan; B. kaempferi var. australis is a synonym of B. monoica. The images of Broussonetia ‘kazinoki’ in Utteridge and Bramley (2015, p. 77, figs. 2 & 6) are a pistillate individual of B. kaempferi.
Broussonetia × kazinoki Siebold (in Verh. Batav. Genootsch. Kunst. 12: 28. 1830, nom. nud.) in Siebold & Zuccarini, Abh. Math.-Phys. Cl. Königl. Bayer. Akad. Wiss. 4(3): 221. 1846; Akiyama et al., J. Jap. Bot. 88: 352, fig. 44. 2013; Ohba & Akiyama, J. Jap. Bot. 89: 127. 2014.—Lectotype (designated by Akiyama et al. 2013, p. 352): JAPAN. von Siebold s.n. 1842 (M [M-0120984 image!]).
Broussonetia ×hanjiana M. Kim in Yun and Kim, Korea J. Pl. Taxon. 39: 82. 2009: 82, syn. nov. Type: —KOREA. Province Jeonnam, Is. Gageo, 16 May 2008, M. Kim 9944 (holotype: JNU).
Distribution. Japan and Korea.
Notes. Long regarded as Broussonetia kazinoki × B. papyrifera (Okamoto 2006), the Japanese Kôzo Broussonetia × kazinoki is actually the natural hybrid between B. monoica and B. papyrifera cultivated for paper making since ancient time in Japan and Korea (Yun and Kim 2009; Ohba and Akiyama 2014). Broussonetia × kazinoki is highly variable and “various intermediate forms are known between the parent species (i.e., B. monoica and B. papyrifera) in such features as plant sex (dioecious or monoecious), hairness of young shoots, and leaf shape and texture” (Okamoto 2006). Yun and Kim (2009) reports that B. × hanjiana (≡ B. × kazinoki) is dioecious. Further study is needed to understand the origins of this natural hybrid.
Broussonetia monoica Hance, J. Bot. 20 (238): 294. 1882; Ohba & Akiyama, J. Jap. Bot. 89: 127. 2014.—Type: CHINA. Guangdong (“prov. Cantonensis”), “Lien chau”, 1881, B. C. Henry 21933 (holotype: BM [BM000895739 image!]).
Broussonetia kaempferi auct. non Siebold: Hayata, J. Coll. Sci. Imp. Univ. Tokyo. 30: 273. 1911; Kanehira, Formos. Trees rev. ed. 146. 1936; Li, Woody Flora of Taiwan 113, fig. 35. 1963; Liao, Quart. J. Exp. Forest. 3(1): 148. 1989; Liu et al., Trees of Taiwan 331. 1994, pro parte; Liao, Fl. Taiwan, 2nd. ed. 2: 140. 1996, pro parte; Lu et al., Trees of Taiwan 2: 95, photos. 2006, pro parte.
Broussonetia kaempferi var. australis T.Suzuki, Trans. Nat. Hist. Soc. Taiwan 24: 433–435. 1934.—Type: TAIWAN. “In silvs secundris ad Heikoko prope Sinten”, T. Suzuki 8362 (“ST 8336”), 2 Apr 1933 (holotype: TAI [118781 image!]).
Broussonetia rupicola F.T. Wang & Tang, Acta Phytotax. Sin. 1(1): 128. 1951.—Type: CHINA. “Szechuan” (Sichuan), Nanchuan, F. T. Wang 10884 (holotype: PE [00760682 image!]), syn. nov.
Broussonetia jiangxiensis X.W Yu, J. Jiangxi Agric. Univ. (1): 3, fig. 2. 1982—Type: CHINA. Jiangxi, Nanchang, X.W Yu 1435 (holotype: JXAU), syn. nov.
Broussonetia kazinoki var. ruyangensis P.H.Liang & X.W.Wei, Bull. Bot. Res., Harbin 2(1): 155–156, fig. 1. 1982.—Type: CHINA. Guangdong: Ruyang, Wu-Zhi-Shan, 600–800 m, 28 Mar 1979, X.-W. Wei 4471 (holotype: CANT).
Broussonetia kazinoki form. koreana M. Kim, Korean J. Pl. Taxon. 39(2): 84, fig. 1F, 1G. 2009.—Type: KOREA. Province Jeonnam, Is. Gageo, 16 May 2008, M. Kim 9946 (holotype: JNU), syn. nov.
Broussonetia kazinoki auct. non Siebold: Liu, Illustrations of Native and Introduced Ligneous Plants of Taiwan 2: 707, pl. 561. 1962; Liu & Liao, Fl. Taiwan 2: 120, 122, pl. 234. 1976; Liao, Quart. J. Exp. Forest. 3(1): 148–149. 1989; Liu et al., Trees of Taiwan 331. 1994, pro parte; Liao, Fl. Taiwan, 2nd. ed. 2: 140, pl. 68, photo 59. 1996, pro parte; Chang et al., Fl. Reipubl. Popul. Sin. 23(1): 26, pl. 7(6–8), 1998; Zhou & Gilbert, Fl. China 5: 26–27. 2003; Lu et al., Trees of Taiwan 2: 95, photos. 2006, pro parte; Yun & Kim, Korean J. Pl. Taxon. 39(2): 84, fig. 1C, 1F, 1G. 2009.
Distribution. Japan (Honshu, Kyushu, Shikoku), Korea, central to southern China (Anhui, Fujian, Guangdong, Guangxi, Guizhou, Hainan, Henan, Hubei, Hunan, Jiangsu, Jiangxi, Sichuan, Yunnan, Zhejiang), Taiwan, and northern Vietnam.
Notes. Until the lectotypification of Siebold’s Japanese collections (Akiyama et al. 2013) and subsequent taxonomic revision of Japanese Broussonetia (Ohba and Akiyama 2014), this monoecious Broussonetia had long been mis-treated as B. kazinoki, which should be applied to the natural hybrid between B. monoica and B. papyrifera.
Leaves of B. monoica are highly polymorphic, varying considerably even within an individual throughout the growing season (Fig. 1). Specimens of B. monoica bearing undivided obovate to lanceolate leaves (Fig. 1i, j) are extremely similar to and difficult to be distinguished from B. kaempferi; misidentification and confusion of the two species are common both in herbarium collections and the literature. The most important and unambiguous diagnostic character that separates the two species is the shape of staminate catkins, with the dioecious B. kaempferi bearing spicate catkins ca. 1.5–2.5 cm long (Fig. 1n) and the monoecious B. monoica bearing globose ones ca. 1 cm across (Fig. 1c, d). However, based on our field observation, the globose staminate catkins of B. monoica flowers are extremely fragile and caducous during its flowering season in early spring, falling off shortly after their appearance. Consequently, it is highly probable that individuals bearing only the pistillate capitula are misidentified as female plants of B. kaempferi. Under this circumstance, sterile individuals of the two species can be distinguished by their growth habit and leaf morphology. Broussonetia kaempferi is a climbing and often twining liana (Fig. 1l, m) whereas B. monoica is a shrub often with slender twigs (Fig. 1f–h). Leaves of B. kaempferi are thinly chartaceous, narrowly oblong to lanceolate with almost symmetric (sub-)cordate leaf base and undivided and crenate margin. In contrast, leaves of B. monoica are thinly herbaceous and highly variable, ranging from oblique ovate or broadly ovate (Fig. 1a, b, f, g) similar to Morus australis Poir. (e.g., Pl. 68 Liao 1996) to narrowly ovate (Fig. 1i, j) similar to B. kaempferi.
Akiyama S, Thijsse G, Esser H-J, Ohba H (2013) Siebold and Zuccarini’s type specimens and original materials from Japan, Part 2. Angiosperms, Dicotyledoneae 1. J Jap Bot 88:346–377
Barker C (2002) Plate 432. Broussonetia papyrifera. Curtis’s Bot Mag 19:8–18. doi:10.1111/1467-8748.00324
Bazinet AL, Zwickl DJ, Cummings MP (2014) A gateway for phylogenetic analysis powered by grid computing featuring GARLI 2.0. Syst Biol 63:812–818. doi:10.1093/sysbio/syu031
Berg CC (1977) Revisions of African Moraceae (excluding Dorstenia, Ficus, Musanga and Myrianthus). Bull Jard Bot Nat Belg 47:267–407
Berg CC, Corner EJH, Jarrett FM (2006) Moraceae-genera other than Ficus. In: Nooteboom HP (ed) Flora Malesiana, series I, vol 17. National Herbarium Nederland, Leiden, pp 1–152
Bosu PP, Apetorgbor MM, Nkrumah EE, Bandoh KP (2013) The impact of Broussonetia papyrifera (L.) vent. on community characteristics in the forest and forest-savannah transition ecosystems of Ghana. Afr J Ecol 51:528–535. doi:10.1111/aje.12063
Cao Z (2000) Moraceae. In: Fu L, Hong T (eds) Higher plants of China, vol 4. Qingdao Publishing House, Qingdao, pp 27–74
Capuron R (1972) Contribution à l’étude de lat flore forestière de Madagascar. Adansonia, séries 2(12):375–388
Chang S, Wu C, Cao Z (1998) Moraceae. In: Chang S, Wu C (eds) Flora Reipublicae Popularis Sinicae, Tomus 23(1). Science Press, Beijing, pp 1–219
Chang C-S, Liu H-L, Moncada X, Seelenfreund A, Seelenfreund D, Chung K-F (2015) A holistic picture of Austronesian migrations revealed by phylogeography of Pacific paper mulberry. Proc Natl Acad Sci USA 112:13537–13542. doi:10.1073/pnas.1503205112
Chûjô K (1950) Notes on Broussonetia papyrifera vent. (Kazinoki), B. kazinoki Sieb. (Kôzo) and B. kaempferi Sieb. (Turu-Kôzo). J Jap For Soc 32:329–334
Chung K-F, Torke BM, Wu K (2009) Unearthing a forgotten legacy of 20th century floristics: the collection of Taiwanese plant specimens in the herbarium of the Academy of Natural Sciences (PH). Taiwania 54:159–167
Clement WL, Weiblen GD (2009) Morphological evolution in the mulberry family (Moraceae). Syst Bot 34:530–552. doi:10.1600/036364409789271155
Corner EJH (1962) The classification of Moraceae. Gard Bull Singap 19:187–252
Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772. doi:10.1038/nmeth.2109
Florece LM, Coladilla JO (2006) Spatial distribution and dominance of paper mulberry (Broussonetia papyrifera) in the vicinites of Mt. Makiling, Philippines. J Environ Sci Manag 9:54–65
Florence J (1997) Flore de la Polynésie française, vol 1. Editions de l’Orstom, Paris
Forbes FB, Hemsley WB (1894) An enumeration of all the plants known from China Proper, Formosa, Hainan, Corea, the Luchu Archipelago, and the Island of Hongkong, together with their distribution and synonymy—part XI. J Linn Soc Bot 26:397–456. doi:10.1111/j.1095-8339.1894.tb01641.x
Hayata B (1911) Materials for a flora of Formosa. J Coll Sci Imp Univ Tokyo 30:1–471
Hyam R, Drinkwater RE, Harris DJ (2012) Stable citations for herbarium specimens on internet: an illustration from a taxonomic revision of Duboscia (Malvaceae). Phytotaxa 73:17–30
Kaempfer, E (1712) Amoenitatum exoticarum politico-physico-medicarum, fasciculi V. Typis & Impenis Henricis Wilhelmi Meyeri, Lemgoviae
Kanehira R (1936) Formosan trees indigenous to the Island (Revised). Department of Forestry, Government Research Institute, Formosa
Kitamura S, Murata G (1980) Coloured illustrations of woody plants of Japan, vol II. Hoikusha Publishing Co., Osaka
LaFrankie JV (2010) Trees of Tropical Asia: an illustrated guide to diversity. Black Tree Publication Inc, Manila
Li H-L (1963) Woody flora of Taiwan. Livinston Publishing Company, Narberth
Liao JC (1989) A taxonomic revision of the family Moraceae in Taiwan (1) Genera Artocarpus, Broussonetia and Fatoua. Quart J Exp For Natl Taiwan Univ 3(1):145–151
Liao JC (1991) The taxonomic revisions of the family Moraceae in Taiwan. Department of Forestry, College of Agriculture, National Taiwan University, Taipei
Liao JC (1996) Moraceae. In Editorial Committee of the flora of Taiwan, 3rd edn (ed), Flora of Taiwan, vol. 2, 2nd edn, vol. 2. Department of Botany, National Taiwan University, Taipei, Taiwan, pp 136–195
Ling S-S (1961) Bark cloth culture and the invention of paper-making. Bull Inst Ethnol Acad Sinica 11:1–49
Linnaeus C (1753) Species plantarum, exhibentes plantas rite cognitas, ad genera relatas, cum differentiis specificis, nominibus trivialibus, synonymis selectis, locis natalibus, secundum systema sexuale digestas, vol .1. Salvius, Stockholm
Liu TS (1962) Illustrations of native and introduced ligneous plants of Taiwan, vol. 2. College of Agriculture, National Taiwan University, Taipei
Liu B, Cao Z (2016) Moraceae. In: Wang W, Liu B (eds) Higher plants of China in colour, vol 3. Science Press, Beijing, pp 123–151
Liu TS, Liao JC (1976) Moraceae. In: Li HL, Liu TS, Huang TC, Koyama T, Devol CE (eds) Flora of Taiwan, vol 2. Epoch Publishing Co., Taipei, pp 117–161
Liu YC, Lu FY, Ou CH (1994) Trees of Taiwan, Revised edition. College of Agriculture, National Chung-Shing University, Taichung
Lu F-Y, Ou C-H, Chen Y-C, Tseng Y-H, Lu K-C, Chi Y-S (2006) Trees of Taiwan, vol 2. Chern-Hsiung Ou, Taichung
Marwat KB, Hashim S, Ali H (2010) Weed management: a case study from north-west Pakistan. Pak J Bot 42:341–353
Matthews PJ (1996) Ethnobotany, and the origins of Broussonetia papyrifera in Polynesia: an essay on tapa prehistory. In: Davidson JM, Irwin G, Leach BF, Pawley A, Brown D (eds) Oceanic culture history: essays in honour of Roger Green. New Zealand Journal of Archaeology Special Publication, Dunedin, pp 117–132
Merrill ED (1918) Species Blancoanae: a critical revision of the Philippines species of plants described by Blanco and by Llanos. Bureau Printing, Mania
Morgan, EC, Overholt, W (2004) Wildland weeds: paper mulberry, Broussonetia papyrifera. University of Florida, IFAS Extension ENY-702
Naithani HB (1981) Broussonetia kampferi Sieb. et Zucc. and Rhododendron obtusum (Lindl.) Planch. new to Indian flora. Indian For 107:585–588
Nicolson DH, Arculus D (2001) Candidates for neotypification of Blanco’s names of Phlippines plants: specimens in the US National Herbarium. Taxon 50:947–954
Ohba H, Akiyama S (2014) Broussonetia (Moraceae) in Japan. J Jap Bot 89:123–128
Ohwi J (1965) Flora of Japan. Smithsonian Institute, Washington, DC
Okamoto M (2006) Moraceae. In: Iwatsuki K, Boufford DE, Ohba H (eds) Flora of Japan, vol IIa. Kodansha Ltd., Tokyo, pp 67–77
Peñailillo J, Olivares G, Moncada X, Payacán C, Chang C-S, Chung K-F, Matthews PJ, Seelenfreund A, Seelenfreund D (2016) Sex distribution of paper mulberry (Broussonetia papyrifera) in the Pacific. PLoS ONE 11:e0161148. doi:10.1371/journal.pone.0161148
Rashid M, Abbas SH, Rehman A (2014) The status of highly alien invasive plants in Pakistan and their impact on the ecosystem: a review. Innov J Agric Sci 2:1–4
Rohwer JG (1993) Moraceae. In: Kubitzki K, Rohwer JG, Bittrich V (eds) The families and genera of vascular plants, vol 2. Springer, Heidelberg, pp 438–453
Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Hohna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542. doi:10.1093/sysbio/sys029
Schneider C (1917) Moraceae. In: Sargent CS (ed) Plantae Wilsonianae, vol 3. The University Press, Cambridge, pp 292–311
Seelenfreund D, Clarke AC, Oyanedel N, Piña R, Lobos S, Matisoo-Smith E, Seelenfreund A (2010) Paper mulberry (Broussonetia papyrifera) as a commensal model for human mobility in Oceania: anthropological, botanical and genetic considerations. N Z J Bot 48:231–247. doi:10.1080/0028825X.2010.520323
Shimabuku K (1997) Check list vascular flora of the Ryukyu Islands, revised edition. Kyushu University Press, Fukuoka
Siebold PF (1830) Synopsis plantarum oeconomicarum universi regni Japonici. Verh Batav Genootsch Kunst 12:1–75
Suzuki T (1934) A speciographical revision on Broussonetia kazinoki Sieb. and allied forms. Trans Nat Hist Soc Formosa 24:429–435
Swofford, DL (2002) PAUP* 4.0: Phylogenetic Analysis Using Parsimony (* and other Methods), v. 4.0 Beta 10. Sinauer Associates, Sunderland
Thiers, B (2016) Index Herbariorum: a global directory of public herbaria and associated staff. New York Botanical Garden’s Virtual Herbarium. http://sweetgum.nybg.org/science/ih/. Accessed 9 Jan 2017
Upadhyay GK, Srivastava SK, Ansari AA (2010) Typification of the name Allaeanthus kurzii Hook. f. (Moraceae). Candollea 65:21–22. doi:10.15553/c2010v651a3
Utteridge T, Bramley G (eds) (2015) The Kew tropical plant identification handbook, 2nd edn. Royal Botanic Garden, Kew
Wang JC, Chiou WL, Chang HM (2015) A preliminary red list of Taiwanese vascular plants 94. Endemic Species Research Center & Taiwan Society of Plant Systematics, Chichi, Nantou
Whistler WA, Elevitch CR (2006) Broussonetia papyrifera (paper mulberry). In: Elevitch CR (ed) Traditional trees of Pacific Islands: their culture, environment, and use. Permanent Agriculture Resources (PAR), Holualoa, pp 171–182
Yamazaki T (1982) Taxonomic review of the Moraceae from Japan, Korea, Taiwan and adjacent areas (1). J Phytogeogr Taxon 30:61–73
Yamazaki T (1989) Moraceae. In: Satake Y, Hara H, Watari S, Tominari T (eds) Wild flowers of Japan: woody plants. Heibonsha Ltd., Tokyo, pp 85–93
Yang YP, Liu HY, Lu SY (1997) Manual of Taiwan vascular plants, vol. 2. II. Spermatophyta. The Council of Agriculture, The Executive Yuan, Taipei
Yun K-W, Kim M (2009) Taxnomic study of Broussonetia (Moraceae) in Korea. Korean J Plant Taxon 39:80–85
Zerega NJC, Clement WL, Datwyler SL, Weiblen GD (2005) Biogeography and divergence times in the mulberry family (Moraceae). Mol Phylogenet Evol 37:402–416. doi:10.1016/j.ympev.2005.07.004
Zhou Z, Gilbert MG (2003) Moraceae. In: Wu ZY, Raven PH, Hong DY (eds) Flora of China, vol 5. Science Press and and Missouri Botanical Garden Press, Beijing, pp 21–73
KFC conceived the idea and designed the project, conducted herbarium work, collected plant materials in Taiwan and China, and wrote the article. WHK, YHH, and YHL collected plant materials and molecular data. RRR collected plant material in the Philippines. WBX collected plant materials in China. All authors read and approved the final manuscript.
The authors are grateful to the followings for their assistance: Jarearnsak Sae Wai for providing silica-gel leaves of Allaeanthus kurzii from Thailand; Noriyuki Fujii for providing materials from Japan; Yunpeng Chao and Pan Li for assisting collecting Broussonetia in Zhejiang, China; A, BM, E, GH, HAST, K, TAI, TAIF, and TNM for access to their collections; A, GH, E, TAIF, and TNM for permissions to sample herbarium specimens. KFC’s visit to Harvard University Herbaria was supported by the 2016 Sargent Award for Visiting Scholar, Arnold Arboretum, Harvard University. This study was supported by grants of Biodiversity Research Center, Academia Sinica to KFC.
The authors declare that they have no competing interests.
Additional file 1. Taxon, voucher information [collector No. (herbarium acronym), Country of origins (Locality)], and NCBI accession numbers (26S/ndhF) of newly collected DNA sequences.
About this article
Cite this article
Chung, KF., Kuo, WH., Hsu, YH. et al. Molecular recircumscription of Broussonetia (Moraceae) and the identity and taxonomic status of B. kaempferi var. australis . Bot Stud 58, 11 (2017). https://doi.org/10.1186/s40529-017-0165-y
- Broussonetia ×kazinoki
- Broussonetia monoica
- Paper mulberry genus