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New discoveries of cycads and advancement of conservation of cycads in China.

 I. Abstract
 II. Introduction
 III. Cycas debaoensis Y. C. Zhong & C. J. Chen
 IV. Cycas changfiangensis N. Liu
 V. The First Discovery of Cycas szechuanensis in the Wild in Fujian
 VI. Advancement of the Conservation of Cycads in China
 VII. Acknowledgment
VIII. Literature Cited


II. Introduction

Following extensive field studies of cycads in China in the first half of 1990s (Zhou et al., 1990; Turner, 1993; Chen & Yang, 1994a, 1994b, 1994c; Shen et al., 1994; Hill & Chen, 1994; Walters & Yang, 1994; Yang & Yang, 1994; Chang & Zhong, 1995; Chang et al., 1995; Chen & Wang, 1995; Deng & Huang, 1995; Wang & Peng, 1995; Zhong, 1995; Zhou & Liang, 1995; Guan & Zhou, 1996; Chen, 1999), other detailed field and herbarium studies of cycads in China were made in the last half of 1990s. The main cycad expeditions were: 1) to Hainan by N. Liu and his group in 1997; 2) to Hainan by C. J. Chen, N. Li, Q. Wei, and L. S. Qu in 1997; 3) to Debao, Guangxi, by C. J. Chen, N. Li, L. S. Qu, z. F. Lu, and Y. C. Zhong in 1997; 4) to Guangxi by C. J. Chen, Ken Hill, Stan Walkley, and Y. C. Zhong in 1998; and 5) to Fujian by C. J. Chen, R. S. Fu, and X. P. Zhang in 1999. More knowledge of Chinese cycads has been obtained. Two new cycads, Cycas debaoensis Y. C. Zhong & C. J. Chen, from western Guangxi, and C. changjiangensis N. Liu, from Hainan, have been described. Another 11 new species, which were described in 1997 and 1998, were treated as synonyms (Chen & Stevenson, 1999). Fortunately, useful detailed field observations and studies were sufficient to recognize the species C. segmentifida D. Y. Wang & C. Y. Deng in northwestern Guangxi and southern Guizhou (Wang & Deng, 1995; Wang et al., 1996) as a good species, with previous material being misidentified as C. guizhouensis Lan & R. F. Zou by the authors (Chen & Wang, 1995) or as C. siamensis Miquel by C. Y. Deng (1995).

The original native locality of Cycas szechuanensis W. C. Cheng & L. K. Fu is not in the Nanpanjiang River Valley but in southeastern Fujian, southeastern China (Zhou et al., 1998). Our recent fieldwork has verified this conclusion. In the 1970s this cycad species was still common there, but now only a few wild individuals survive in remote mountain forests in the Shaxi River Valley in the center of Fujian Province. With these data it is clear that C. guizhouensis should be treated as a good species and not as a synonym of C. szechuanensis, as treated by Chen and Wang (1995), de Laubenfels and Adema (1998), and Chen and Stevenson (1999). Our field cycad studies in Guangxi and Fujian have also verified that C. szechuanensis differs from C. taiwaniana Carruth., though it is similar to the latter in some aspects of vegetative morphology. In order to thoroughly clarify the resources of cycads in China, more studies, especially those based on fieldwork, are necessary.

In China, ca. 60% of the native cycad populations and individuals are estimated to have been lost over the past century, especially with the growth of flower and ornamental plant markets throughout China in 1980s. Fortunately, since 1994 the decline of native cycads in China has been much slower, and populations in some cycad reserves have declined much less than in the past. A new local cycad reserve, the Honghe Cycad Nature Reserve, was established to protect Cycas multipinnata, C. hongheensis, and other cycads in southeastern Yunnan in 1996. But protection of cycad diversity is far from adequate in China. If no valid measures are taken in time, about half of the native cycads will disappear in China within the next half-century. Thus, the rescue of cycads and their habitat is a very urgent task for China.

III. Cycas debaoensis Y. C. Zhong & C. J. Chen

Cycas debaoensis Y. C. Zhong & C. J. Chen in Acta Phytotax. Sin 35(6): 571. 1997; C. J. Chen & D. W. Stevenson, Fl. China 4: 3. 1999. TYPE: CHINA. Debao: 106[degrees]14' E, 23[degrees]30' N, alt. 850 m, 27-08-1997, Y C. Zhong 8762 (HOLOTYPE: PE; ISOTYPE: GZF).

Historical notes: This interesting cycad was discovered only recently. In 1984 Hua Qin and Guo-bao Zhao, at the Nursery Station of Bose Department of Forestry in Guangxi Autonomous Region (Province), first found a cycad that looked like a fern but with spines on the petiole at Fuping village, Fuping town in Debao County, Guangxi, when conducting fieldwork on palms in the area. They called this cycad "Fencha Cycad" (forked cycad). In August 1997 Ye-Chong Zhong (one of the authors for this new cycad) and An-Ding Zhou, at the Forest Surveying and Designing Institute of Guangxi in Nanning, did cycad fieldwork in Bose District and were told about this forked-leafleted cycad by H. Qin, Y. C. Zhong, and Z. F. Lu, who were also interested in this cycad and doing fieldwork in Debao. Soon afterward, Zhong informed the first author of the present article (Chia Jui Chen) that Cycas multipinnata also occurred in Guangxi. Having examined the material, it was determined that this cycad differs from C. multipinnata in Yunnan, so it was described as a new species, C. debaoensis Y. C. Zhong & C. J. Chen.

Description: Trunk almost subterranean, to 40(-70) cm tall, 25(-40) cm diam. aboveground, sometimes clumped. Leaves (3-)5-11(-15), 1.5-2.7 m long, 0.5-1.2 m wide, 3-pinnate, openly keeled in cross-section at 110-150[degrees] between pinnae (leaflets); petiole obovate-orbicular in cross-section, 0.6-1.3 m long, 1.5-3 cm across, tomentose when young, later glabrescent except at the base, spiny except at the base, spines 20-55 along adaxial part of each side, 1-4.5 cm apart, conical, 3-4 mm long; primary pinnae in 6-14 pairs, 3-12 cm apart, middle pinnae subopposite, longest 40-60 cm long, 20-27 cm wide, openly keeled in cross-section at 70-90[degrees] between secondary pinnae, basal pinnae alternate, not gradually reducing to spines, 20-30 cm long; secondary pinnae in 3-5 pairs, dichotomously 2- or 3-forked, 12-25 cm long with petiolule 0.5-2 cm long; segments (ultimate leaflets) 3-5, green and shiny above, light green below, linear, 10-22(-28) cm long, 0.8-1.5 cm wide, thickly papery, glabrous, base decurrent, apex long-attenuate or long-acuminate, margin fiat or somewhat undulate, midrib raised on both surfaces. Cataphylls narrowly triangular, 6-8 cm long, 1.5-2 cm wide, densely brown tomentose, apex attenuate, somewhat soft. Pollen cones ovoid and golden tomentose initially, fusiform-cylindric cream, and glabrescent at maturity, 20-49 cm long (including peduncle 3-4 cm long), 6-10 cm across; microsporophylls narrowly cuneate, 3-3.5 cm long, 1.2-1.6 cm wide, apical sterile part semiorbicular, wavy, and slightly revolute, apex broadly rounded with very short, upcurved mucro. Megasporophylls 30-50, laxly grouped, forming an oblate group 15-21 cm high, 18-25 cm diam.; sterile blade green, subcordate or subflabellate, 6-9 cm long, 5-10 cm wide, tomentose on central part abaxially, deeply divided into 39-51 filiform lobes 3-6 cm long, terminal lobe 4-5 cm long; stalk 9-12 cm long; ovules 2-3 on each side, glabrous. Seeds 3-4, subglobose, slightly compressed, 2.5-3.5 cm diam.; sarcotesta green to yellowish and smooth, brown and wrinkled when dry; sclerotesta finely verrucose.

Phenology: Pollination in March-April, seed maturity in November.

Distinguishing features: This recently described species is most similar to Cycas multipinnata in its 3-pinnate leaf structure but differs in its more numerous and much shorter leaves, with segments long-attenuate or long-acuminate at the apex; its megasporophylls, with more and filiform lobes; and its dry and sunny habitat.

Distribution and ecology: This cycad is very rare and endemic to Guangxi, China, restricted to a narrow area only in Fuping village, Fuping town, Debao County, northwestern Guangxi, at 106[degrees]14' E, 23[degrees]30' N. It grows on a red soil derived from limestone and sandstone at pH 5-6.5 and in thickets and sparse forests on sunny, open slopes of hills at alt. 700-1000 m. The average annual temperature is 19.5[degrees]C, with 11.1[degrees]C in the coldest month (January) and 25.7[degrees]C in the hottest month (July). The absolute minimum is -2.6[degrees]C; the absolute maximum; 37[degrees]C. The total annual rainfall averages about 1461 mm, of which 75% falls between June and August. It is dry in winter and spring.

Population status and threat: In 1997, this endangered cycad consisted of only one population with ca. 1500 individuals, covering a total of ca. 15 ha. Unfortunately, in January 2000 the population consisted of only ca. 500 individuals (including 200 reproductively mature plants), mainly because of unlawful digging for commerce. Among the adult individuals, 20% are female and 80% are male. Only two or three female plants in the population produce seeds in any given year. Therefore, this cycad is already severely depleted, and it is regarded as endangered. Recently, the Debao Cycad Nature Reserve was established by the local government, partly with the assistance of American friends.

IV. Cycas changjiangensis N. Liu

Cycas changjiangensis N. Liu in Acta Phytotax. Sin. 36(6): 552, f. 1. 1998; C. J. Chen & D. W. Stevenson, Fl. China 4: 6. 1999. TYPE: CHINA. Changjiang: 10-06-1997, N. Liu 97002 (HOLOTYPE: IBSC; ISOTYPE: PE).

Description: Trunk often subterranean, cylindric or flask-shaped, sometimes moniliform, to 50 cm tall, 15 cm diam., base abruptly swollen to 25 cm diam., apex almost glabrous; bark gray, nearly smooth toward the base of the trunk. Leaves 25-45, 1-pinnate, 60-120 cm long; petiole 10-40 cm long, with 9-16 spines 2 mm long on each side throughout the length; leaflets 40-70 pairs longitudinally inserted 0.8-1.8 cm apart at 55-65[degrees] to rachis, straight, 10-17(-23) cm long, 4-7(-9) mm wide, leathery, glabrous, base attenuate and slightly decurrent, apex attenuate, pungent, margin flat or slightly recurved, midrib prominent on both surfaces, especially strongly so above when dry. Cataphylls triangular-lanceolate, 5-7 cm long, 1-1.3 cm wide, densely yellow-brown tomentose, apex long-attenuate, somewhat soft at the tip. Pollen cones conical-cylindric, 15-25 long, 4-6 cm across; microsporophylls cuneate or broadly cuneate, 1.5-2 cm long, 0.6-1 cm wide, apical sterile part subrhombic, margin subentire, with short, upcurved mucro. Megasporophylls 40-60, tightly grouped, 8-13 cm long, densely yellowish brown silky tomentose; sterile blade broadly ovate or flabellate, 5-6 cm long, 4-8 cm wide, with 17-35 lobes 2-3.8 cm long, terminal lobe broadly lanceolate, 1.5-3.5 cm long, with some irregular denticles; ovules 1-2 on each side of the distal part of the stalk, glabrous. Seeds 2-4, green to yellowish brown, broadly obovoid or subglobose, ca. 2 cm diam.; sarcotesta not spongy or fibrous.

Phenology: Pollination in April-May, seed maturity in October-November.

Distinguishing features: This species is similar to Cycas siamensis Miquel in its gray and abruptly swollen trunk base but is quite different from that species in its strongly adaxially raised midrib and small seeds with sarcotesta neither spongy nor fibrous.

Distribution and ecology: This cycad is endemic to Hainan Island, China, restricted to a narrow area at Bawanling, Changjiang County, western Hainan. It grows on a fulious loam soil at pH 7.1 on rocky slopes of hills among grass and low shrubs or in open broad-leaved forests with a tropical climate of hot, wet summers and hot, dry winters at alt. 750-900 m. The average annual temperature is 24.3[degrees]C, with 39.7[degrees]C in the hottest month (June) and 4.2[degrees]C in the coldest month (January). The total annual precipitation averages 1480 mm.

Population status and threat: Although this cycad occurs in the Bawanling Natural Reserve in Changjiang County, western Hainan, its habitat is continually being degraded, and the number of plants in each population is decreasing. This cycad survives in only two populations in ca. 200 ha and with ca. 3000 individuals, respectively. It is regarded as endangered.

V. The First Discovery of Cycas szechuanensis in the Wild in Fujian

Cycas szechuanensis was described by W. C. Cheng and L. K. Fu (1975) on the basis of a cultivated specimen that Xiong Ji-hua et al. 33221 (holo PE) had collected at Fuhu Temple, Emei Mountain, Sichuan. Plants of this cycad in Sichuan are cultivated, and all of them are female (Fu et al., 1978; Zhou et al., 1981). In South China, especially in Fujian, Guangdong, Guangxi, this cycad is also commonly cultivated and again almost all female. The recurring question for the past 30 years has been, Where does this species occur naturally? D. Y. Wang and H. Peng (1995) concluded that the original distribution of C. szechuanensis should be in the southern area of China other than Sichuan, based on the fact that the female individual of this cycad cultivated in the Fairy Lake Botanical Garden bore 17 seeds that were successfully pollinated by a male introduced from South China in 1993. Chen et al. (1995) and Chen and Stevenson (1999) concluded that this cycad occurred along the Nanpanjiang River in southwestern Guizhou, northwestern Guangxi, and eastern Yunnan, based on the fact that C. szechuanensis and C. guizhouensis from the Nanpanjiang River have many common morphological characters; thus they treated C. guizhouensis as a synonym of C. szechuanensis. Zhong and Zhou (1999) reported that C. szechuanensis is found in Hexian, Fuchuan, Gongcheng, and Zhaoping Counties in eastern Guangxi. In 1998 G. S. Zhou, of the Laizhou Forestry Farm in Nanping, Fujian, did fieldwork and reported that C. szechuanensis occurs in eastern and southern Fujian Province but that male individuals are less than 1% of the populations. In October 1999 one of the current authors, C. J. Chen, and S. S. Fu, of the Sanming Institute of Forestry, Sanming, Fujian, again conducted fieldwork on the cycads in Fujian Province and came to the following conclusions:

1. Cycas szechuanensis is very common in cultivation in Fujian, especially in Fuqing, Putian, Yongtai, in the southern part, in Luoyuan, Lianjiang, in the eastern part, and in Nanping, Sha County, in central Fujian. On Taojingshan Hill, Sha County and adjacent areas, there are many old cultivated populations of this cycad, some of which have been cultivated for ca. 800 years. Some of the individual plants were originally introduced from nearby wild populations. The adult females cone almost every year, but they bear no viable seeds in cultivation because there are no male plants, or very rarely coning males plants, in the population.

2. A few females of Cycas szechuanensis can bear seeds under artificial pollination; for example, C. J. Chen 99011 (PE), collected from the coning plant of C. szechuanensis in the Fuzhou Arboretum pollinated by a male of "C. taiwaniana" on May 20, 1999. This fertilized megasporophyll cone of C. szechuanensis was 44 cm in diameter and produced ca. 250 mature seeds.

3. A wild population of Cycas szechuanensis was first found at Chendazhen, Sanming County, in the middle valley of the Shaxi River of central Fujian. The plants grow on sandy soil in shaded Pinus massoniana--Castanea henryi mixed forest on a vertical face of the mountain by a stream at alt. 400 m. The population consisted of 3 clumps with about 20 female individuals but without male plants. Unfortunately, the adult plants were moved by a farmer of the village from the wild onto his farmland in February 1999. It was from here that the specimen C. J. Chen 99001 (PE) was collected. Fortunately, some young cycad plants still remained in the wild population, and it is said that another population exists nearby in the wild. In the meantime, G. S. Zhou, of the Laizhou Forestry Farm, Fujian, reported that there was also a wild population in Yongan County, along the Shaxi River.

The fact mentioned above has preliminarily proved that the original distribution of Cycas szechuanensis should be in Fujian. In 1998 N. Liu, of the South China Botanical Garden, Chinese Academy of Sciences, reported that some individuals of C. szechuanensis cultivated at the garden had been introduced from Yingfu Lake, Shenzhen, in the 1970s. If the cycad in Shenzhen is in the wild, how to explain its disjunctive distribution pattern? This must remain unanswered until more fieldwork is conducted on the distribution, reproductive biology, and species related to C. szechuanensis. However, our current knowledge of C. szechuanensis, C. guizhouensis, and C. segmentifida along the Nanpanjiang River in southwestern China indicate that all should be considered good species (Chen & Liu, 1999).

VI. Advancement of the Conservation of Cycads in China

China has a diverse cycad flora, with at least 20 species of Cycas, representing three sections within four sections of the genus worldwide. Recently, new cycad species and new records were discovered from China in rapid succession. Unfortunately, in the past half-century wild cycads in China have dwindled markedly in number. About 60% of their populations and individuals have disappeared, mainly because overcollecting for horticultural purposes and cutting of forests for farmland have resulted in plant and habitat destruction. A few species are almost extinct in the wild in China: for example, C. revoluta and C. szechuanensis, in Fujian; and C. hongheensis, in Yunnan. A small population of forked cycad (? C. micholitzii) in Xinlong, Hainan Province, has probably disappeared. In the past three years C. multipinnata, C. diannanensis, and C. debaoensis individuals have been drastically reduced in number, by about 20-30%.

The Panzhihua Cycad Natural Reserve was upgraded from the local level to the state level in 1996. The people who lived in the reserve were relocated, and the management of the reserve has been strengthened and improved. To date, the number of cycad individuals in the reserve has increased from 150,000 in 1990 to 230,000 in 2002. In early 1995 a project was undertaken to restore cycads in abandoned mining sites, covering ca. 41,000 [m.sup.2] in the reserve (Yang et al., 1999). About 2000 cycad individuals have survived in the sites. The coverage of vegetation has been restored to about 30% of its original cover.

The Honghe Cycad Nature Reserve was established in Yunnan in 1996. Several cycads, Cycas multipinnata, ? C. micholitzii, C. diannanensis, and C. hongheensis, are in the reserve.

The Debao Cycad Nature Reserve was established in Guangxi in 1999. Unfortunately, the cycad resources in both this reserve and the Honghe Cycad Reserve are continually draining away because of funding shortages.

As for ex situ conservation of cycads, the Qingxiushan Cycad Garden in Nanning, Guangxi, one of the largest cycad gardens in China, was established in 1998. The area of the cycad garden is about 5 ha, and it contains about 25 cycad species. The largest and best cycad garden in China is the Shenzhen Cycad Garden in Shenzhen Fairy Lake Botanical Garden. It is about 5 ha and has ca. 130 species from 5 genera, representing 3 families from all over the world. The other main cycad gardens in China are: Panzhihua Cycad Garden in Panzhihua, about 3 ha with 50 species and a large nursery; the cycad garden of the South China Botanical Garden, Chinese Academy of Sciences, in Guangzhou, the oldest one in China, ca. 2 ha with 30 species, especially those from South China; the cycad garden of Fuzhou Arboretum in Fujian, 1 ha with ca. 20 species; Xiamen Botanical Garden, 1 ha cycad garden with ca. 30 species. Some large cycad nurseries are in Fujing and Guangdong. The cycad gardens and nurseries mentioned above are the main bases for ex situ cycad conservation in China.

VII. Acknowledgment

This project was supported by the National Natural Science Foundation of China (No. 39770061).

VIII. Literature Cited

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Zhong, Y. C. 1995. Resources of cycads in Guangxi. Chinese Bull. Bot. 12 (Suppl.): 26-27.

-- & D. A. Zhou. 1999. The distribution of Cycas szechuanensis in Guangxi Province. Pp. 70-72 in C.-J. Chen (ed.), Biology and conservation of cycads: Proceedings of the Fourth International Conference on Cycad Biology, held in Panzhihua, Sichuan, China, 1-5 May 1996. International Academic Publishers, Beijing.

Zhou, G. S., S. X. Jiang, W. Zhou, Y. S. Kang & N. D. Chen. 1998. Abstracts of 2nd Cycad Symposium of China, Shenzhen: 4-5.

Zhou, L., S. Y. Yang, L. K. Fu & S. Z. Cheng. 1981. Two new species of Cycas from Sichuan. Acta Phytotax. Sin. 19(3): 335-338.

-- & Z. Zhou. 1990. Investigation of the natural community of Cycas panzhihuaensis L. Memoirs New York Bot. Gard. 57: 148-151.

Zhou, L. S. & Q. S. Liang. 1995. Field investigation and cultivated observation on Cycas micholitzii Dyer. Chinese Bull. Bot. 12 (Suppl.): 63-66.

CHIA JUI CHEN

Institute of Botany

Chinese Academy of Sciences

Beijing 100093, China

AND

NIAN LIU

South China Botanical Garden

Chinese Academy of Sciences

Guangzhou 510520, China
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Author:Chen, Chia Jui; Liu, Nian
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Date:Jan 1, 2004
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