Flueggea acicularis (Phyllanthaceae), a narrow endemic species rediscovered in central China

Abstract Flueggea acicularis (Phyllanthaceae) is endemic to the karst region of central China. Male specimens of this species were first collected in 1908. In 1989, female plants of F. acicularis were found for the first time, but misidentified as a new species. Throughout this period the male plants of F. acicularis were mismatched with female plants of other species, and male plants had not been collected since 1908. Then, in March, 2009, the authors rediscovered a wild population of F. acicularis consisting of both male and female plants in Wuxi county, Chongqing municipality, China. Based on field investigation and examination of specimens, we matched the correct female and male plants of this species for the first time since its initial publication a century ago. A complete and accurate morphological description, distribution, habitat and phenology of this species are also provided. Furthermore, the conservation status of F. acicularis is assessed as “Near Threatened” (NT) according to the IUCN Red List criteria.


Introduction
Flueggea (Phyllanthaceae) consists of 16 species, widespread in tropical to warm temperate regions, along with 3 Eurasian narrowly distributed taxa that have been interpreted as relictual. An unusually obligate pollination mutualism (pollination and seed parasite) exists between Epicephala moth and Phyllanthaceae trees (Kawakita 2010, Hu and.  also reported that Epicephala relictella fed on the seeds of F. suffruticosa, but was not pollinating its host. Some secondary products (alkaloids, diterpenoids) that are of medicinal use have been extracted from Flueggea Wang et al. 2010).There are four Flueggea species in China, and Flueggea acicularis is endemic to the karst region of central China. F. acicularis is extremely similar to F. tinctoria in morphology (Webster 1984). However, the geographical disjunction between the Chinese F. acicularis and F. tinctoria in the Iberian Peninsula is one of the most remarkable in the Euphorbiaceae, which might represent the relicts of the flora of Tethys in Tertiary period. But the taxonomic status of F. acicularis is somewhat in doubt.
The English botanist E.H. Wilson collected a male shrub assigned to Euphorbiaceae s.l. in the Three Gorges Area of central China in March, 1908. Hutchinson (1916 misidentified these specimens as Flueggea leucopyra Willd., a species producing berries. Croizat (1940) published a new species Securinega acicularis Croizat based on the three specimens of Wilson. Airy Shaw (1971) accepted this new species and described the morphology of fruits as "a shallowly 3-lobed, depressed-globose, dehiscent capsule, 6-7mm in diam.", but no specimens documenting the fruit were cited. Webster (1984) used a broad generic concept in the taxonomic revision of Flueggea and combined Securinega acicularis Croizat into Flueggea acicularis (Croizat) Webster, but indicated that pistillate flowers and the fruit were not seen. Li (1994) and Li and Gilbert (2008) described this species with "Female flowers: pedicels ca. 3mm; sepals 5,……Berry globose, 6-7 mm in diam, 3-locular". Thus, up to this point, the taxonomic status of F. acicularis and the morphological description of the staminate plant have not been doubted in academia, but the morphological characters of pistillate flowers and capsules have been confused throughout this period.
After a careful examination of the specimens stored under the name of Flueggea acicularis in main herbaria of China, we found that 25 sheets representing ten gatherings collected from the Jinshajiang valley flanking northwestern Yunnan province and southwestern Sichuan province had been misidentified. The whole plants of these specimens are entirely glabrous and bear flowers with 5 sepals, clearly differing from F. acicularis which has hirtellous young branchlets and has 6 sepals in a flower. These misidentified specimens belong to Flueggea virosa (Roxb. ex Willd.) Voigt, F. suffruticosa (Pall.) Baill. and F. leucopyra Willd. Besides, a most recent study of Huang et al. (2020) claimed that diterpenoids have been extracted from the aerial parts of F. acicularis collected in Yunnan. Given that the locality of collection is in Yunnan, it seems that the materials used in their study should be F. leucopyra, instead of F. acicularis.
In August, 1989, three botanists (Mingxi Jiang, Zongqiang Xie and Jinsheng He) collected specimens of the female plants of F. acicularis for the first time, in Luyou-dong, Wushan county, during the vegetation investigation in the Three Gorges Area. But the specimens were not identified, because of their lack of flowers and fruits. In May, 1990, Zongqiang Xie et al. collected specimens of F. acicularis with capsules in Bawuxia located in the midstream of Daning river. However, since most floras in China still confused F. acicularis with F. leucopyra (Fu, 1979), or considered F. acicularis to have berries (Li 1994), the real female specimens of F. acicularis with capsules were misidentified as a new species under a nomen nudum "Securinega wuxiensis" (Chen et al. 1994). Thus, the male plants of F. acicularis remained paired with female plants of other species, and the true female plants of F. acicularis were considered as another species.
In April, 2009, during a field trip to Wuxi county, Chongqing municipality, the authors accidentally discovered a population consisting of shrubs of Phyllanthaceae in a remote area called Jingzhuba. The place is located in the limestone canyon of the headwaters of the Daning river in the northeast of Wuxi county. We collected specimens of both male and female plants containing staminate and pistillate flowers and capsules from the same population. After a careful morphological investigation, we confirmed that this species is F. acicularis. Based on an intensive study of the male and female plants from the same population, the male plant of F. acicularis has finally been matched with the correct female plant of the same species.

Materials
Specimens were collected and photographs were taken in the field of Badong county, Hubei, Wushan county, and Wuxi county, Chongqing municipality, Central China in 1989China in , 1990China in , 1997China in and 2009. Specimens from the main herbaria of China (PE, KUN, IBK, IBSC) and some digital specimen databases (CVH, A, MO, US, K, GH, JSTOR Global Plants) were checked. The morphology of the species was observed and measured based on living plants, dry specimens and preserved materials. All morphological characters were measured with dissecting microscopes and were described using the terminology presented in Harris and Harris (1994).   (Fig. 1); 1.c. 11758 (male plant, 2 sheets, PE!); and 11759 (male plant, 2 sheets, PE!).

Local name. Yang ci.
Habitat and ecology. Three Gorges reservoir area is located in a subtropical region. The annual average rainfall is 1000-1400 mm, mostly in July and August. The annual average temperature is 18.4 °C (average temperature in January: 7.1 °C; average temperature in July: 29.3 °C), and the extreme maximum temperature is up to 44 °C. The relative humidity is 60%-80%. The photoperiod in this area is short, affected by the canyon landform and the foggy environment.
The population of Wushan county. In 1908, Wilson collected specimens of F. acicularis here, but without detailed location. In August, 1989, Mingxi Jiang et al. found  Provisional IUCN conservation assessment. In 2009, the Three Gorges water conservancy project, the largest in the world, was completed, located in Yichang city, Hubei province. The altitudes of the dam base and dam top are 4 m and 185 m respectively, and therefore we calculated the populations of Badong and Wushan of F. acicularis at alt. lower than 185m have been submerged according to altitude. Based on field investigations and specimens, we are confident that F. acicularis is distributed narrowly, and is endemic to the karst region of the Three Gorges Area in Central China. The provisional conservation status is "Near Threatened" (NT) according to the IUCN red list criteria (IUCN 2019).