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Asarum pubitessellatum, sp. nov. (sect. Heterotropa, Aristolochiaceae) from Taiwan based on morphological and palynological evidence

Botanical StudiesAn International Journal201354:28

DOI: 10.1186/1999-3110-54-28

Received: 3 August 2012

Accepted: 24 December 2012

Published: 30 August 2013

Abstract

Background

Recently, we discovered an unknown Asarum from Taiwan which is closely related to A. crassisepalum S.F. Huang, T.H. Hsieh and T.C. Huang and A. taipingshanianum S.F. Huang, T.H. Hsieh and T.C. Huang by sharing a thick leaf blade, spreading perianth-lobes and a conical to cylindrical perianth-tube. We compared it with other related species and identified this plant as a new species.

Results

This new species differs distinctly from the above two related species by having larger plant body, shortened rhizomes and an inner surface of the perianth-tube that is covered with numerous simple trichomes (vs. glandular trichomes). The pollen tectum in this new species is perforate, which differs from the incomplete reticulate with small supratectate granules in A. crassisepalum and the compact rugulate with small supratectate granules in A. taipingshanianum. Furthermore, these three species are geographically separated from one another.

Conclusions

Asarum pubitessellatum C.T. Lu & J.C. Wang, a new species is described and illustrated. The trichomes on the inner surface of the perianth-tube and pollen micromorphology were the valuable characters in the low-level classification of Heterotropa species in Taiwan.

Keywords

Asarum Asarum crassisepalum Asarum pubitessellatum Asarum taipingshanianum Heterotropa Pollen Taiwan

Background

Asarum L. (Aristolochiaceae) consists of more than 100 species mainly distributed in the north temperate zone (Cheng and Yang 1983; Kelly 19982001; Huang et al.2003). Most species are distributed in eastern Asia, some species in North America, and one species is endemic to Europe. On the basis of the infrageneric classification proposed by Kelly (1998), this genus was separated into two distinct subgenera, each with two sections. The subgenus Asarum, composed of the sections Asarum and Geotaenium, is characterized by connate styles with terminal stigmas, inferior ovaries, and the inner surface of perianth-tubes puberulent to strigose; while the subgenus Heterotropa, comprising sections Asiasarum and Heterotropa (including Hexastylis), is characterized by six free styles with lateral stigmas, superior or half-inferior ovaries, and the inner surface of perianth-tubes longitudinal or with a strong network of ridges (Cheng and Yang 1983; Sugawara 1987; Kelly 1997).

Section Heterotropa is morphologically diversified and composed of ca. 70 species mainly distributed in eastern Asia, particularly in the Sino-Japanese region. However, because the perianth-tube is fleshy and brittle, distortion of the flower in pressed specimens makes its structure difficult to recognize. Consequently, herbarium specimens of Heterotropa are difficult to identify reliably leading to underestimates of the species diversity of the section. In Taiwan, the Flora of Taiwan 2nd ed. recorded only four species in this section; however, our field expeditions in recent years have led to the discovery of 3 new species and 2 new records (Lu and Wang 2009; Lu et al. 2009; Lu et al. 2010).

Recently, Ms. Pi-Fong Lu discovered an unknown Asarum in Miaoli, Taiwan. We compared it with other related species and identified this plant as a new species based on the morphological and palynological evidence discussed here.

Methods

The plants examined in this study were collected from native habitats and then transplanted into the greenhouse of National Taiwan Normal University, Taipei, Taiwan. The morphological and palynological data for A. pubitessellatum were based on the voucher specimens: TAIWAN. Miaoli Hsien: Mt. Chialishan, C. T. Lu 812 (TNU) and same loc., P. F. Lu 19112 (TNU). The palynological data of A. crassisepalum were based on the voucher specimens: TAIWAN. Hsinchu Hsien: Yuanyang Lake, C. T. Lu 624 (TNU). The palynological data of A. taipingshanianum were based on the voucher specimens: TAIWAN. Ilan Hsien: Tsuifeng Lake, C. T. Lu 743 (TNU).

Morphological Study—The measurement of floral characters was conducted using a Mitutoyo CD-6″CS digimatic caliper.

Pollen morphology—Pollen grains for scanning electron microscopic (SEM) study were collected from fresh anthers and prepared using the method proposed by Erdtman (1952). The acetolyzed grains were dehydrated through an ethanol series, critical point dried, coated with gold, and examined with a Hitachi SM 2400 scanning electron microscope. Descriptive terminology for pollen morphology follows that of Huang et al. (1995).

Results

Taxonomic treatment

Asarum pubitessellatum C.T. Lu & J.C. Wang, sp. nov.—TYPE: TAIWAN. Miaoli Hsien: Nanchuang Township, Mt. Chialishan, alt. 1,400 m, 12 Dec. 2005, C. T. Lu 812 (holotype: TNU; isotype: TAIF). https://static-content.springer.com/image/art%3A10.1186%2F1999-3110-54-28/MediaObjects/40529_2012_Article_23_IEq1_HTML.gif (Figure 1).
https://static-content.springer.com/image/art%3A10.1186%2F1999-3110-54-28/MediaObjects/40529_2012_Article_23_Fig1_HTML.jpg
Figure 1

Asarum pubitessellatum . A. Habit; B. Front view of flower; C. Perianth-tube; D. Dissected perianth tube, showing stamens and pistil; E. Part of perianth tube, showing tessellated inner surface; F. Stamens; G. Style and stigma; H. Trichomes on the inner surface of perianth tube. (from the holotype, C. T. Lu, 812 (TNU)).

Diagnosis: Asarum pubitessellatum C.T. Lu & J.C. Wang is similar to A. crassisepalum S.F. Huang, T.H. Hsieh & T.C. Huang and A. taipingshanianum S.F. Huang, T.H. Hsieh & T.C. Huang but differs from the latter two by having larger plant body (20–30 cm vs. less than 10 cm tall); shortened rhizome; larger perianth-tube (ca. 1.5 cm vs. 1–1.2 cm in diam.); multicellular simple trichomes (vs. glandular trichomes) on the inner surface of perianth-tube.

Perennial herb. Rhizome short. Leaves 2 on each annual branchlet, with petiole 10–23 cm long. Leaf lamina triangular-ovate to sagittate, thick, 8.5–13 × 6–7.5 cm, acute to acuminate at apex, auriculate at base, base of the sinus 3–4.7 cm wide, glabrous adaxially, with white blotches along mid-vein, glabrous and pale green abaxially. Flowering branch with 2–3 cataphylls at its base, ovate, 16–18 mm long, margin ciliate, shed when leaves fully grown. Flowers solitary, facing downward, yellow-greenish to purple-greenish, perianth-tube conical, ca. 13–15 mm long, lower portion 12–13 mm in diam., upper portion 8–10 mm in diam., peduncle 10–18 mm long; outer surface glabrous, pale yellow-greenish and with numerous brownish red spots; internal surface purplish red, tessellated and with ca.12 longitudinal ribs, covered with numerous pubescences along longitudinal and transverse ribs. Tube throat slightly constricted, annual ca. 1–1.5 mm wide, orifice ca. 3–5 mm. Perianth-lobes 3, broadly triangular-ovate, yellow-greenish to purple-greenish, ca. 10–11 × 12–14 mm, spread, without forming semicircular pulvinate areas between the lobes and orifice. Stamens 12 in two whorls, filaments very short, anthers 2.5 mm long, with connective obtuse; ovary superior, 6-locular, styles 6, free, with slightly bifid apices; stigma oblong-ovoid, lateral, inserted in apex notch, extrorse; ovules 8 in each locule.

Pollen morphology

Pollen grains in A. pubitessellatum are oblate spheroidal to suboblate, penta-colporate in equatorial view (Figure 2C), ca. 25.5 × 27 μm–27 × 28.6 μm (P × E). Pollen tectum is perforate without supratectum granules (Figure 2F).
https://static-content.springer.com/image/art%3A10.1186%2F1999-3110-54-28/MediaObjects/40529_2012_Article_23_Fig2_HTML.jpg
Figure 2

Comparison of pollen morphology between A. crassisepalum (A, D), A. taipingshanianum (B, E) and A. pubitessellatum (C, F). A-C. whole pollen. D-F. closed view of pollen tectum.

Habitat and geographical distribution

To date, this new species is only known from the type locality in Mt. Chialishan, Miaoli Hsien, Taiwan. It was found under a shaded and moist plantation of the coniferous species Cryptomeria japonica (L.f.) D. Don. The habitat is similar to those of its allies, A. crassisepalum and A. taipingshanianum, which grow in mixed coniferous-broadleaf forests, often among mosses. These three species all occur in cloudy forest zones at middle elevation but in geographically different areas. Asarum crassisepalum inhabits the mountainous area around Yuanyang Lake in Hsuehshan Mountain Range, A. taipingshanianum inhabits the mountainous area of Taipingshan in the Central Mountain Range, and A. pubitessellatum can only be found on Mt. Chialishan on the western side of the Hsuehshan Mountain Range (Figure 3).
https://static-content.springer.com/image/art%3A10.1186%2F1999-3110-54-28/MediaObjects/40529_2012_Article_23_Fig3_HTML.jpg
Figure 3

Geographical distribution of A. crassisepalum (), A. taipingshanianum (□), and A. pubitessellatum ().

Conservation assessment

Only two localities with less than 50 plant individuals of A. pubitessellatum have been found. The area of occurrence is estimated to be 10 km2. According to the IUCN red list categories (IUCN 2001) criteria, this species is categorized as critically endangered CR (B2abiii, C2a).

Etymology

We name this species A. pubitessellatum based on the inner surface of its perianth-tube being covered with numerous simple trichomes along ridges. This character is different from other Taiwanese, Chinese, and Japanese Heterotropa species, which have perianth-tubes that are covered with glandular trichomes.

Discussion

Morphologically, Asarum pubitessellatum appears to resemble A. crassisepalum and A. taipingshanianum. These three species share the following common characters: lustrous, thick leaves, perianth-lobes spreading horizontally, perianth-tube only slightly constricted at the throat, inner surface with tessellated ridges, base of perianth-lobes smooth (lacking tubercles) or scarred by only a few lines (Figure 4). Despite these similarities, A. pubitessellatum is clearly distinguished from A. crassisepalum and A. taipingshanianum by the following characteristics: (1) larger plant body (20–30 cm high vs. usually less than 10 cm) with shorter rhizomes; (2) larger perianth-tube (ca. 1.5 cm vs. 1–1.2 cm) (Figure 4); and (3) multicellular simple trichomes on the inner surface of perianth-tube (vs. sessile unicellular glandular trichomes in A. crassisepalum and unicellular-stalked glandular trichomes in A. taipingshanianum) (Figure 5). A more detailed comparison between A. pubitessellatum and its allies, A. crassisepalum and A. taipingshanianum is given in Table 1 in aid of their identification. Species in sect. Heterotropa usually bear short-stalked, unicellular glandular trichomes on the inner surface of the perianth-tube (Sugawara 1987; Kelly 1997). However, it is normally not possible to preserve trichomes in herbarium specimens; therefore, this character has often been ignored by taxonomists. According to this study, we consider that the trichome type on the inner surface of perianth-tube can be a valuable character in the low-level classification of sect. Heterotropa.
https://static-content.springer.com/image/art%3A10.1186%2F1999-3110-54-28/MediaObjects/40529_2012_Article_23_Fig4_HTML.jpg
Figure 4

Comparison of floral morphologies of A. crassisepalum (A, D, G, J), A. taipingshanianum (B, E, H, K) and A. pubitessellatum (C, F, I, L). A-C. Front view; D-F. Perianth-tube; G-I. Dissected perianth-tube, showing anthers and pistils; J-L. Dissected perianth-tube, showing inner tessellated ridges.

https://static-content.springer.com/image/art%3A10.1186%2F1999-3110-54-28/MediaObjects/40529_2012_Article_23_Fig5_HTML.jpg
Figure 5

Trichome types on the inner surface of perianth-tube. A. A. crassisepalum; B. A. taipingshanianum; C. A. pubitessellatum.

Table 1

Comparison of Asarum pubitessellatum and its allies, A. crassisepalum and A. taipingshanianum

 

A. crassisepalum

A. taipingshanianum

A. pubitessellatum

Rhizomes

Elongated

Elongated

Short

Leaves

   

Shape

Triangular-oblong to sagittate

Triangular-oblong

Triangular-ovate to sagittate

Size

4–9 × 3.5–6 cm

3–6 × 3.4–4.1 cm

8.5–13 × 6–7.5 cm

Apex

acute to acuminate

obtuse to acute

acute to acuminate

Flower

   

Size (in diameter)

1–2 cm

1–2 cm

ca. 3 cm

Perianth-tube shape

Conical

Conical to cylindrical

Conical

Tubercle on the base of perianth-lobe

Scar-like

Absent or scar-like

Absent

Trichome type on the inner surface of perianth-tube

Sessile unicellular glandular trichome

Stalked unicellular-- glandular trichome

Multicellular single trichome

Pollen micromorphology

Incomplete reticulate with small supratectate granules

Compactly rugulate with small supratectate granules

Perforate

Checking the chromosome number of members of sect. Heterotropa, the species from Taiwan and Japan share the same basic chromosome number x = 12 (2n = 24, rare 36 or 48) rather than x = 13 (2n = 26 or 39, mainly distributed in southwestern China) (Huang et al. 1995; Kelly 1997; Lu and Wang 2009; Maekawa and Ono 1965; Ono 1960; Shi et al. 2008; Sugawara 19811985a1985b199219982003; Sugawara and Ogisu 1992; Yinger 1983; Yuasa and Maekawa 1976), suggesting that the Taiwanese taxa are more closely related to the Japanese species than the Chinese species.

Pollen micromorphology is another valuable character in the low-level classification of the genus Asarum (Mi and Yang 1981; Huang et al. 1995; Lu and Wang 2009). Pollen exine ornamentation in sect. Heterotropa has been described as cerebelloid under verrucae for the Chinese species (Mi and Yang 1981), with rugulate-perforate, perforated subunits, incomplete reticulate or compact rugulate with large warts to small granules or none on supratectum for the Taiwanese species (Huang et al. 1995; Lu and Wang 2009; Lu et al. 2009; Lu et al. 2010) and microreticulate or microporate with gammae or verrucae or none for the North American species (as Hexastylis) (Niedenberger 2010).

The perforate pollen tectum without gammae or verrucae on the supertectum in A. pubitessellatum is quite different from its related allies: incomplete reticulate with small supratectate granules in A. crassisepalum (Figure 2A,D) and compact rugulate with small supratectate granules in A. taipingshanianum (Figure 2B,E). This type of pollen is similar to that of A. hypogynum and A. chatienshanianum from Taiwan (Huang et al. 1995; Lu and Wang 2009) and A. naniflora from North America (Niedenberger 2010). However, due to a lack of palynological information from the most diversified area, Japan, we cannot validate the significance of pollen morphology in the infra-section classification of sect. Heterotropa.

Geographically, A. pubitessellatum, A. crassisepalum, and A. taipingshanianum are currently distributed allopatrically, though they all occur in a similar habitat, under cypress forest [mainly composed of Chamaecyparis formosensis Matsum. or C. obtusa Sieb. & Zucc. var. formosana (Hayata) Rehder or both]. Their similar gross morphologies, pollen features, and habitat suggest that they are closely related. The contemporary geographic isolation of these three species may result from a decreased forest range or forest fragmentation. Further phylogeographical study is in progress to test this hypothesis.

The two editions of Flora of Taiwan (1975–1979; 1994–2003) and the Supplement to the Flora of Taiwan, 2nd ed. (Wang and Lu 2012) completely described Taiwan’s flora up to 2009. However, most recent findings, including new generic records, e.g., Ypsilandra (Hsu et al. 2011) and Phacellanthus (Chung et al. 2010), new species, e.g., Cotoneaster rosiflorus and C. chingshuiensis (Chang et al. 2011a, b), Pouzolzia taiwaniana (Peng et al. 2012), Thismia huangii (Chiang and Hsieh 2011), and Tripterospermum hualiense (Hsu and Chung 2012), and numerous newly recorded species, indicate that the documentation of the island’s vast and unique biodiversity is incomplete. This study echoes the suggestion of Hsu et al. (2011) and Peng et al. (2012) that the continuation of the botanical inventories is needed, especially those areas rarely botanized.

The following key is provided to distinguish the species of sect. Heterotropa in Taiwan.

Key to Taiwanese Species of Asarum sect. Heterotropa (modified from Lu and Wang 2009)
  1. 1.

    Leaves coriaceous, blades ovate, triangular-cordate to lanceolate-ovate; adaxial surface glabrous or sparsely hairy, dark green with white spots or maculate, abaxial surface glabrous or hairy along veins, light-green or purple; veinlet on abaxial surface indistinct. 2

     
  2. 1.

    Leaves subcoriaceous or chartaceous, blades triangular-ovate to broad ovate; adaxial surface sparsely hairy, dark green with white maculate, abaxial surface hairy along veins, green or purple; veinlets on abaxial surface distinct. 7

     
  3. 2.

    Plant erect; rhizome short; leaves longer than 7 cm; flowers 2–5 cm in diam. 3

     
  4. 2.

    Plant creeping; rhizome elongated; leaves less than 5 cm; flowers 1–2 cm in diam. 6

     
  5. 3.

    Leaves up to 30 cm; flowers ca. 3–5 cm in diam.; perianth-lobes longer than perianth-tube, throat constricted, neck-like; orifice rim developed, usually decurved, forming a funnel shape. A. hypogynum

     
  6. 3.

    Leaves less than 20 cm; flowers ca. 2–3 cm in diam.; perianth-lobes shorter than perianth-tube, throat constricted or slightly constricted, not neck-like; orifice rim present, not decurved. 4

     
  7. 4.

    Leaves lanceolate-ovate, margin undulate; throat constricted; perianth-tube length less than width. A. tawushanianum

     
  8. 4.

    Leaves triangular-ovate, margin entire; throat slightly constricted, perianth-tube length longer than width. 5

     
  9. 5.

    Leaf apex acute; outer surface of perianth-tube hairy, tubercles on base of perianth-lobes present, bar-like; filament attached to the base of perianth-tube. A. yaeyamense

     
  10. 5.

    Leaf apex acuminate; outer surface of perianth-tube glabrous, without tubercles on base of perianth-lobes; filament attached to the ovary. A. pubitessellatum

     
  11. 6.

    Perianth-tube conical or tubiform, length longer than width, lobes less than tube length; orifice less than 3 mm in diam. A. crassisepalum

     
  12. 6.

    Perianth-tube tubiform, length equal to width, lobes nearly equal to tube length; orifice more than 5 mm in diam. A. taipingshanianum

     
  13. 7.

    Perianth-tube pyriform; style laterally compressed, stigma unciform, terminal or subterminal; longitudinal ridges on inner surface 24 or more. 8

     
  14. 7.

    Perianth-tube tubiform or obconical; style not laterally compressed, stigma elliptic or lachrymiform, lateral; longitudinal ridges on inner surface 12–24. 9

     
  15. 8.

    Perianth-lobes longer than perianth-tube, with well developed tubercles on the base; orifice less than 3.5 mm in diam.; orifice rim well developed; inner surface of perianth-tube irregularly tessellated thoroughly, longitudinal ridges 24. A. macranthum

     
  16. 8.

    Perianth-lobes shorter than perianth-tube, with few tubercles on the base; orifice larger than 10 mm in diam.; orifice rim narrow; inner surface of perianth-tube irregularly tessellated on the upper half, but only longitudinal ribs on the lower half, longitudinal ridges more than 24. A. satsumense

     
  17. 9.

    Perianth-tube tubiform, length equal to width, inner surface of perianth-tube regularly tessellated, longitudinal ridges 12. A. albomaculatum

     
  18. 9.

    Perianth-tube obconical or tubiform, length longer than width, inner surface of perianth-tube irregularly tessellated, longitudinal ridges 12–24. 10

     
  19. 10.

    Perianth-tube tubiform, upper part slightly inflated; lobes yellow-greenish or purple-greenish, adaxial surface pubescent; outer surface yellow-greenish, inner surface purple. A. chatienshanianum

     
  20. 10.

    Perianth-tube obconical; lobes maroon, adaxial surface densely villous; flowers all maroon. A. villisepalum

     

Conclusions

Asarum pubitessellatum C.T. Lu & J.C. Wang, a new species is described and illustrated based on the morphological and palynological evidence. The present study showed the trichomes on the inner surface of the perianth-tube and pollen micromorphology were the valuable characters to distinguish the closely related Heterotropa species in Taiwan.

Declarations

Acknowledgments

We would like to extend our thanks to Dr. David E. Boufford and an anonymous reviewer for providing comments and advices on the manuscript. We would especially thank Ms. Pi-Fong Lu who told us about her discovery of this new species and aided in the field collection. This study was supported in part by Taiwan Forestry Research Institute, ROC. (No. 9521013500110502G345).

Authors’ Affiliations

(1)
Department of Life Science, National Taiwan Normal University
(2)
Botanical Garden Division, Taiwan Forestry Research Institute

References

  1. Chang KC, Wang CC, Deng SL, Kono Y, Lu FY, Peng C-I: Cotoneaster rosiflorus (Rosaceae), a new species from Taiwan. Bot Stud 2011, 52: 211–218.Google Scholar
  2. Chang KC, Wang CM, Deng SL, Wang CC: A new species Cotoneaster chingshuiensis (Rosaceae) from Taiwan. Taiwania 2011, 56: 125–131.Google Scholar
  3. Cheng CY, Yang CS: A synopsis of the Chinese species of Asarum (Aristolochiaceae). J Arnold Arbor 1983, 64: 565–597.Google Scholar
  4. Chiang PY, Hsieh TH: Thismia huangii (Thismiaceae), a new species from Taiwan. Taiwania 2011, 56: 138–142.Google Scholar
  5. Chung SW, Hsu TC, Peng C-I: Phacellanthus (Orobanchaceae), a newly recorded genus in Taiwan. Bot Stud 2010, 51: 531–536.Google Scholar
  6. Erdtman G: Pollen Morphology and Plant Taxonomy: Angiosperm. Stockholm: Almgvist and Wiksell; 1952:20–51.Google Scholar
  7. Hsu TC, Chung SW: Tripterospermum hualiense (Gentiaceae), a new species from Taiwan. Taiwania 2012, 57: 183–187.Google Scholar
  8. Hsu TW, Kono Y, Chiang TY, Peng C-I: Ypsilandra (Melanthiaceae; Lilliaceae sensu lato), a new generic record for Taiwan. Bot Stud 2011, 52: 99–104.Google Scholar
  9. Huang SF, Hsieh TH, Huang TC: Notes on the Flora of Taiwan (21) – The Genus Asarum L. (Aristolochiaceae). Taiwania 1995, 40: 91–120.Google Scholar
  10. Huang SM, Kelly LM, Gilbert MG: Aristolochiaceae. In Flora of China. Volume 5. Edited by: Wu Z-Y, Raven PH. Beijing: Science Press; 2003:246–269. Missouri Botanical Garden Press, St. Louis Missouri Botanical Garden Press, St. LouisGoogle Scholar
  11. IUCN: IUCN red list categories and criteria, ver. 3.1. IUCN, Gland, Switzerland and Cambridge. United Kingdom: IUCN Species Survival Commission; 2001.Google Scholar
  12. Kelly LM: A cladistic analysis of Asarum (Aristolochiaceae) and implications for the evolution of herkogamy. Am J Bot 1997, 84: 1752–1765. 10.2307/2446475View ArticlePubMedGoogle Scholar
  13. Kelly LM: Phylogenetic relationship in Asarum (Aristolochiaceae) based on morphology and ITS sequences. Am J Bot 1998, 85: 1454–1467. 10.2307/2446402View ArticlePubMedGoogle Scholar
  14. Kelly LM: Taxonomy of Asarum section Asarum (Aristolochiaceae). Syst Bot 2001, 26: 17–53.Google Scholar
  15. Lu CT, Wang JC: Three new species of Asarum (section Heterotropa ) from Taiwan. Bot Stud 2009, 50: 229–240.Google Scholar
  16. Lu CT, Chen CW, Wang JC: Asarum yaeyamense Hatusima (Aristolochiaceae) newly found in northern Taiwan. Taiwan J For Sci 2009, 24: 149–157.Google Scholar
  17. Lu CT, Chiou WL, Liu SC, Wang JC: Asarum satsumense F. Maekawa (Aristolochiaceae), a newly recorded species in Taiwan. Taiwania 2010, 55: 396–401.Google Scholar
  18. Maekawa F, Ono M: Karyotype analysis in the genus Hexastylis (Aristolochiaceae). J Fac Sci Univ Tokyo Sec 3: Bot 1965, 9: 151–159.Google Scholar
  19. Mi QW, Yang CS: Pollen morphology of Asarum in China. Acta Phytotax Sin 1981, 29: 164–171.Google Scholar
  20. Niedenberger BA: Molecular phylogeny and comparative pollen morphology of the genus Hexastylis (Aristolochiaceae). Master’s thesis. Boone, North Carolina: Appalachian State University; 2010.Google Scholar
  21. Ono M: Studies on Heterotropa and its related genera with special reference to their karyo-morphology and phylogeny. J Fac Sci Univ Tokyo Sect 3 Bot 1960, 7: 473–499.Google Scholar
  22. Peng C-I, Kono Y, Chen CJ, Hsu TC, Chung SW: Pouzolzia taiwaniana (Urticaceae), a new species from Taiwan. Bot Stud 2012, 53: 387–392.Google Scholar
  23. Shi QF, Wang HC, Li XW, Meng AP, Li JQ: New chromosome counts in Asarum s.l. (Aristolochiaceae) from China. Nord J Bot 2008, 26: 91–95.View ArticleGoogle Scholar
  24. Sugawara T: Taxonomic studies of Asarum sensu lato — I. Karyotype and C-banding pattern in Asarum s. str., Asiasarum and Heterotropa . Bot Mag Tokyo 1981, 94: 225–238. 10.1007/BF02488612View ArticleGoogle Scholar
  25. Sugawara T: Further investigations on karyotype and C-banding patterns in seven species of Heterotropa . J Jpn Bot 1985, 60: 15–23.Google Scholar
  26. Sugawara T: A note on Heterotropa pseudosavatieri and its allied species (Aristolochiaceae). J Jpn Bot 1985, 60: 202–212.Google Scholar
  27. Sugawara T: Taxonomic studies of Asarum sensu lato — III. Comparative floral anatomy. Bot. Mag. Bot Mag Tokyo 1987, 100: 335–348. 10.1007/BF02488853View ArticleGoogle Scholar
  28. Sugawara T: A taxonomic study of Heterotropa nipponica and H. savatieri ssp. pseudosavatieri (Aristolochiaceae) in the Shima Peninsula. Acta Phytotax Geobot 1992, 43: 15–26.Google Scholar
  29. Sugawara T: A taxonomic study of Asarum megacalyx F. Maek. and related taxa (Aristolochiaceae) distributed in Niigata Prefecture and adjacent areas of Japan. Acta Phytotax Geobot 1998, 49: 1–17.Google Scholar
  30. Sugawara T: Morphological and cytological variation in Asarum fauriei (Aristolochiaceae) in central and northern Honshu, Japan. Acta Phytotax Geobot 2003, 54: 149–162.Google Scholar
  31. Sugawara T, Ogisu M: Karyomorphology of 11 species of Asarum (Aristolochiaceae) from Taiwan and mainland China. Acta Phytotax Geobot 1992, 43: 89–96.Google Scholar
  32. Wang JC, Lu CT (Eds): Flora of Taiwan, Second Edition–Supplement. Taipei: National Taiwan Normal University; 2012:414.Google Scholar
  33. Yinger BR: A horticultural monograph of the genus Asarum, sensu lato, in Japan. Master’s thesis. Newark, DE: University of Delaware; 1983.Google Scholar
  34. Yuasa H, Maekawa F: Chromosome of Asarum and Heterotropa (Aristolochiaceae) in the Ryukyu Islands. Kromosomo 1976, II: 8–18.Google Scholar

Copyright

© Lu et al.; licensee Springer. 2013

This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.