Nordic Journal of Botany 35: 681–686, 2017 doi: 10.1111/njb.01656, ISSN 1756-1051 © 2017 The Authors. Nordic Journal of Botany © 2017 Nordic Society Oikos Subject Editor: Xiang-Yun Zhu. Editor-in-Chief: Torbjörn Tyler. Accepted 1 September 2017

Primula zhui () sp. nov. from south Yunnan, southwest China

Bin Yang, Hong-Bo Ding, Zhi-Hong Li and Yun-Hong Tan

B. Yang, H.-B. Ding and Y.-H. Tan (http://orcid.org/0000-0001-6238-2743) ([email protected]), Southeast Asia Biodiversity Research Inst., Chinese Academy of Sciences, Yezin, Nay Pyi Taw, Myanmar. BY, HBD and YTH also at: Center for Integrative Conservation, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Menglun, Mengla, Yunnan, P. R. China. Z.-H. Li, Management Dept of Puer National Park, Pu’er, Yunnan, P. R. China.

Primula zhui a new species of Primula endemic to the Yunnan Province, China, is described and illustrated. It is morphologically similar to P. intanoensis from Thailand, and P. calyptrata from southeast Yunnan, affiliated to Primula sect. Carolinella (Hemsl.) Pax. However, it is easily distinguished from the Thailand species by its longer corolla tube and distylous flowers, and it differs from the Chinese species by its leaf ovate to ovate-elliptic blade and distylous flowers.

The genus Primula L. is the largest genus in Primulaceae 1999, Gong and Fang 2003, Richards 2003, Yu et al. 2015, (Hu and Kelso 1996, Richards 2003), and consists of more Xu et al. 2016d). than 500 species. It is mainly distributed in the North During our recent field expedition to survey Temperate Zone and alpine region. Southwestern China diversity in south Yunnan, specimens of Primula were col- is one of the diversity centers of Primula, with more than lected. Based on detailed examination of the morphologi- 300 species, most of which occur in the alpine regions of cal and anatomical characters of our material and closely western Sichuan, northwestern Yunnan, and eastern Xizang related species (Yamazaki 1988, Hu 1990b, 1999, Gong (Hu 1990a, Hu and Kelso 1996, Hu 1998, Richards 2003). and Fang 2003, Richards 2003), concluded that the species Primula as currently circumscribed is polyphyletic as revealed we collected in Yunnan belong to a species new to science, by molecular phylogeny evidence, with genera like Cortusa Primula zhui Y.H. Tan & B. Yang, affiliated toPrimula sect. L., Dodecatheon L. and Dionysia Fenzl embedded within it Carolinella (Hemsl.) Pax, which is hereby described and (Mast et al. 2001, 2006, Trift et al. 2002). illustrated. In recent years, after the ‘Flora of China’ was published, many new species of Primula have been described from Primula zhui Y.H. Tan & B. Yang sp. nov. (Fig. 1–2) China (Fang 1998, Gong and Fang 2003, Hu and Geng 2003, Li and Hu 2009, Hu and Hao 2011, Wu et al. 2013, A species similar to P. intanoensis T. Yamaz. from Thailand Xu et al. 2014a, 2014b, 2015a, 2015b, 2016a, 2016b, and P. calyptrata X. Gong & R.C. Fang from China, but 2016c, 2016d, Yu et al. 2015, He et al. 2017, Li et al. easily distinguished from the former by its longer corolla 2017, Yuan et al. 2017). Three of these species, i.e.Primula tube (1.4–1.6 cm long, 2.0–2.5 times as long as the calyx) calyptrata (Gong and Fang 2003), P. hunanensis (Yu et al. and distylous flowers, and from the latter by its ovate to 2015) and P. undulifolia (Xu et al. 2016d), belong to Prim- ovate-elliptic leaf blade and distylous flowers. ula sect. Carolinella (Hemsl.) Pax. The key character of P. sect. Carolinella (Hemsl.) Pax is its calyptrate capsules, Type: China. Yunnan: Pu’er, Simao, Yixiang, 101°07ʹE, which are also found in other genera of the family, i.e. 22°37ʹN, terrestrial perennial herbs in subtropical evergreen Pomatosace Maximowicz, Anagallis L., Soldanella L., and broadleaf forests, 1359 m a.s.l., 18 Apr 2017, B. Yang and Bryocarpum Hooker f. & Thomson (Pax and Knuth 1905, H.B. Ding 0001(holotype: HITBC). Gong and Fang 2003). Primula sect. Carolinella encom- passes ca 14 species, is generally narrowly distributed in Description southeastern Yunnan, western Guangxi, southern Hunan Perennial herb, 12–20 cm tall, efarinose, with a short, com- and northern Guangdong, but with a few members extend- paratively red stout rhizome and numerous fibrous roots. ing to the border of Vietnam and Thailand (Hu 1990b, Leaves forming a spreading rosette; petiole 3–10 cm long,

681 Figure 1. Primula zhui sp. nov. (A) habit, (B) thrum flower, (C) pin flower, (D) persistent calyx of pin flower, (E) persistent calyx of thrum flower, (F) corolla of pin flower, (G) corolla of thrum flower. Drawn by Zheng-Meng Yang, from the holotype.

682 Figure 2. Primula zhui sp. nov. (A) and (B) habit, (C) thrum flowers in anterior view, (D) pin flowers in anterior view, (E) inflorescence, showing the persistent calyx, (F) inflorescence in lateral view, showing the corolla tube, (G) pin and thrum flowers, (H) leaf blade in adaxial view, (I) leaf blade in abaxial view. Photographed by H. B. Ding.

683 stained white or tawny pilose and with sparse short glan- Distribution and habitat dular hairs; leaf blade ovate to ovate-elliptic, 6.5–13.5 3 Primula zhui is endemic to south Yunnan, southwest China, 4–8 cm, rounded at apex, cordate at base, slightly undulate only known from its type locality, Yixiang, Simao, Pu’er. or irregularly crenulate along margins, membranous when Here it grows in the understory of subtropical evergreen dry, adaxial aparsley pubescent, abaxially pubescent, dis- broadleaf forests, at 1300–1500 m a.s.l. tinctly pilose and with sparse short glandular hairs along the veins; lateral veins 5–7 pairs, raised and prominent. Conservation status Scape slender, 8–15 cm tall, slightly longer than the leaves, Primula zhui is here assesed as ‘Critically Endangered’ (CR densely covered by white pubescence and short glandular B1abiii, IUCN 2012). In our preliminary field survey in hairs, carrying an umbel of 8–15 flowers. Bracts 4–11 mm, Simao county we found only 3 populations and less than linear, sparsely pilose. Pedicels 8–12 mm, sparsely pilose 50 individuals in the type locality of about 4 km2 area in and with short glandular hairs. Flowers distylous; calyx Yixiang. Forests are severely fragmented in this region. The 6–8 mm, narrowly proculiform or campanulate, sub- species is endangered due to the increasing deforestation and prominently 5-veined, with stained white hairs on the out- habitat fragmentation. side, conspicuous on the veins and dense at the base, split to one third with triangular to ovate-triangular lobes that are Similar species 2–3 mm long. Corolla white to pink, exannulate, pubes- With the inclusion of the species described here, Primula cent at throat; limb 1.6–1.8 cm in diameter; lobes obovate, sect. Carolinella encompasses 14 species (Gong and Fang emarginate at apex; tube 1.4–1.6 cm, 2.0–2.5 times as long 2003, Richards 2003, Yu et al. 2015, Xu et al. 2016d). as the calyx, sparsely pilose and with short glandular hairs; This section is believed to be a primitive group inPrimula pin flowers: stamens inserted ca 5 mm above base of corolla (Hu 1994, 1998, Yan et al. 2010). Although members of tube, their style ca 1.2 cm; thrum flowers: stamens inserted Carolinella are unique in Primula with their calyptrate cap- near throat of corolla tube, 1.3 cm above base of corolla sule with a circum-scissile lid (Pax and Knuth 1905, Hu tube, their style ca 2.5–3.0 mm. Ovary globose. 1990b, Gong and Fang 2003), specimens in flowering stage, without mature capsules, may be confused with members Phenology of P. sect. Obconicolisteri Balf. f. which are similar in habit Primula zhui flowers from April to May. Capsule not seen. and vegetative characters (such as calyx, leaf blade and its indumentum) (Hu 1990b). That’s whyPrimula intanoensis has been assigned to P. sect. Obconicolisteri (Yamazaki 1988) Etymology although it is the most similar species of Primula zhui. Primula The species epithetzhui honors Professor Zhu Hua from the intanoensis is a species known from Thailand (Yamazaki Xishuangbanna Tropical Botany Garden, Chinese Academy 1988, Hu 1999). These species have similar leaf shape and of Sciences, who worked on plant and biogeog- indumentum. The two species differ, however, in the flower raphy and made great contributions to the tropical flora in structures. The flowers ofP. zhui are distylous, whereas China, especially in south Yunnan. those of P. intanoensis are homostylous. The corolla tube of P. zhui is 1.4–1.6 cm long, 2.0–2.5 times as long as the calyx, Vernacular name whereas the corolla tube of P. intanoensis is 5–6 mm long, Zhu hua bao chun (朱华报春) (Chinese). 1.0–1.5 times as long as the calyx (Table 1, Fig. 1–2).

Table 1. Morphological comparison between Primula zhui sp. nov. and closely related species.

P. zhui P. intanoensis P. calyptrata Leaf blade ovate to elliptic, 6.5–13.5 3 4–8 cm ovate-elliptic to sub-orbicular, sub-orbicular, 4–6 3 3–5 cm 2.8–4.0 3 2.6–3.8 cm Lateral veins 5–7 pairs 4–5 pairs 4 pairs Petiole (cm) 3–10 3–5 2.5–5.5 Scape (cm) 8–15 8–12 12–18 Inflorescence 8–15 flowers 2–6 flowers 1–2 super imposed umbels with 2–5 flowers in each Pedicels (mm) 8–12 5–10 2–4 Bracts (mm) 4–11 3–5 4–6 Flower heterostylous homostylous homostylous Calyx ca 6–8 mm, narrowly proculiform or 4–5 (to 7 mm in fruit) mm, 5–6 mm, campanulate; lobes campanulate; lobes triangular to ovate- campanulate; lobes triangular, ovate-triangular, 2–3 mm triangular, ca 2–3mm 1.0–1.5 mm Corolla white to pink, exannulate, pubescent at throat, white, annulate, ca 1 cm in diameter purple, hairy annulate, 1.6–1.8 cm in diameter 1.5–1.8 cm in diameter Corolla tube 1.4–1.6 cm, 2.0–2.5 times as long as the calyx 5–6 mm, 1.0–1.5 times as long as the 1.7 cm long, 3 times as long calyx as the calyx Style and stamens pin flower: stamens 5 mm, inserted at the base stamens with anthers 1.6 mm long, stamens inserted in throat; of corolla tube, style ca 1.2 cmthrum flower: inserted near middle of corolla tube style ca 1.7 cm stamens inserted near throat of corolla tube, 2.5–3.0 mm; style ca 2.3 mm, 1.3 cm above base of corolla tube, style ca reaching the level of the stamens 2.5–3.0 mm

684 Figure 3. Primula zhui sp. nov. and Primula calyptrata. (A)–(D) P. zhui, (E)–(J) P. calyptrata. Photographed by H. B. Ding, Bin Yang and Lei Wu.

Primula zhui is also closely related to P. calyptrate, known of P. zhui are distylous, whereas those of P. calyptrata are from southeast Yunnan, China (Gong and Fang 2003). homostylous. (Table 1, Fig. 3). These species share inflorescence structure and corolla shape. The two species differ, however, in the shape of the leaves and in flowers structure. The leaves ofP. zhui are ovate to Additional specimens examined (paratype) elliptic, whereas those of P. calyptrata are ovate-orbicular to The same locality as holotype, 18 Apr 2017, B. Yang and sub-orbicular, with purple abaxial surface, and the flowers H. B. Ding 0002 (HITBC).

685 Acknowledgements – We thank Zheng-Meng Yang for the illustration Mast, A. R. et al. 2001. Phylogenetic relationships in Primula L. and Cheng Du for providing the photos. and related genera (Primulaceae) based on noncoding chloro- Funding – This work was financially supported by a project of the plast DNA. – Int. J. Plant Sci. 162: 1381–1400. southeast Asia biodiversity research institute, Chinese Academy of Mast, A. R. et al. 2006. Are any primroses (Primula) primitively Sciences (Y4ZK111B01). monomorphic? – New Phytol. 171: 605–616. Pax, F. and Knuth, R. 1905. Primulaceae. – In: Engler, A. (ed.), Das Pflanzenreich. Vol. 27. Verlag von Wilhelm Engelmann, References pp. 1–15. Richards, J. 2003. Primula, 2nd ed. – Timber Press, pp. 1–346. Fang, D. 1998. Two new taxa of Primula Linn. (Primulaceae) from Trift, I. et al. 2002. The monophyly ofPrimula (Primulaceae) Guangxi, China. – J. Trop. Subtrop. Bot. 6: 49–51. evaluated by analysis of sequences from the chloroplast gene Gong, X. and Fang, R. C. 2003. Primula calyptrata, a new species rbcL. – Syst. Bot. 27: 396–407. in section Carolinella (Primulaceae) from Yunnan, China. Wu, X. et al. 2013. Primula mianyangensis (Primulaceae), a new – Novon 13: 193–195. species from Sichuan, China. – Phytotaxa 131: 49–52. He, X. et al. 2017. Primula jiugongshanensis sp. nov. (Primulaceae) Xu, Y. et al. 2014a. Primula pelargoniifolia (Primulaceae), a from China, based on morphological and molecular evidence. new species from Chongqing, China. – Ann. Bot. Fenn. 51: – Nord. J. Bot. 35: 328–333. 125–127. Hu, C. M. 1990a. Primula. – In: Chen, F. H. and Hu, C. M. (eds), Xu, Y. et al. 2014b. Primula dejuniana (Primulaceae), a new species Flora Reipublicae Popularis Sinicae. Vol. 59. Science Press, from Sichuan, China. – Ann. Bot. Fenn. 51: 372–374. pp. 1–277. Xu, Y. et al. 2015a. A new species of Primula (Primulaceae) from Hu, C. M. 1990b. A new species of Primula from Thailand with Sichuan, China. – J. Trop. Subtrop. Bot. 23: 147–150. critical notes on the section Carolinella. – Nord. J. Bot. 10: Xu, Y. et al. 2015b. Primula anthemifolia (Primulaceae), a 399–401. new species from Sichuan, China. – Ann. Bot. Fenn. 52: Hu, C. M. 1994. On the geographical distribution of the 373–375. Primulaceae. – J. Trop. Subtrop. Bot. 2: 1–14. Xu, Y. et al. 2016a. Primula persimilis sp. nov. (Primulaceae) from Hu, C. M. 1998. Diversity and distribution of Primula in China. Sichuan, China. – Nord. J. Bot. 34: 409–412. – In: Qiu, S. T. and Peng, J. Y. (eds), Plant diversity Xu, Y. et al. 2016b. Primula wawushanica sp. nov. (Primulaceae) and conservation by the cross-strait. Natl Mus. Nat. Sci., from Sichuan southwestern China. – Nord. J. Bot. 34: pp. 24–27. 156–158. Hu, C. M. 1999. Primulaceae. – In: Santisuk, T. and Larsen, K. Xu, Y. et al. 2016c. Primula scopulicola (Primulaceae), a new species (eds), Flora of Thailand. Vol. 7, part 1. Diamond printing Co. from Sichuan, southwestern China. – Ann. Bot. Fenn. 53: Ltd, pp. 155–168. 277–279. Hu, C. M. and Geng, Y. Y. 2003. Two new species of Primula Xu, Y. et al. 2016d. Morphological and molecular phylogenetic (Primulaceae) from China. – Novon 13: 196–199. data reveal a new species of Primula (Primulaceae) from Hunan, Hu, C. M. and Hao, G. 2011. New and noteworthy species of China. – PLoS one 11: e0161172.doi:10.1371/journal. Primula from China. – Edinb. J. Bot. 68: 297–300. pone.0161172 Hu, C. M. and Kelso, S. 1996. Primulaceae. – In: Wu, Z. Y. and Yamazaki, T. 1988. A new species of Primula from Thailand. – J. Raven, P. H. (eds), Flora of China. Vol. 15. Science Press; Miss. Jap. Bot. 63: 211–213. Bot. Gard. Press, pp. 39–78. Yan, H. F. et al. 2010. Circumscription of Primula subgenus IUCN 2012. IUCN red list categories and criteria, ver. 3.1, 2nd Auganthus (Primulaceae) based on chloroplast DNA sequences. ed. – IUCN Species Survival Commission. – J. Syst. Evol. 48: 123–132. Li, R. and Hu, C. M. 2009. Primula lihengiana (Primulaceae), a Yu, X. L. et al. 2015. Primula hunanensis sp. nov. (Primulaceae) new species from Yunnan, China. – Ann. Bot. Fenn. 46: from Hunan, south – central China. – Nord. J. Bot. 33: 130–132. 381–384. Li, X. et al. 2017. Primula hubeiensis (Primulaceae), a new species Yuan, S. et al. 2017. Primula chimingiana sp. nov. (Primulaceae) from central China. – Novon 25: 162–165. from Sichuan, China. – Nord. J. Bot., in press.

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