Rescuing Magnolia Sinica (Magnoliaceae), a Critically Endangered Species Endemic to Yunnan, China

Rescuing Magnolia sinica (Magnoliaceae), a Critically Endangered species endemic to Yunnan, China

B IN W ANG,YONGPENG M A ,GAO C HEN,CONGREN L I Z HILING D AO and W EIBANG S UN

Abstract Magnolia sinica, a Critically Endangered tree en- Chinese botanists refer to the species as M. sinicum and demic to Yunnan, China, is one of the  plant species with also use its common name huagaimu (Sun et al., ). extremely small populations approved by the Yunnan gov- The species is categorized as Critically Endangered on the ernment for urgent rescue action before . Information IUCN Red List, based on limited data suggesting a popula- on the geographical distribution and population size of tion of ,  mature individuals (Wang & Xie, ; Cicuzza this species had not previously been reported, hindering ef- et al., ; Zheng et al., ). The term ‘plant species with fective conservation. We therefore carried out a survey of extremely small populations’ is used to describe species that the literature and of herbarium specimens, followed by a de- are restricted to a narrow geographical distribution, have tailed field survey and morphological measurements and been subjected to disturbance and other external stress fac- observations of surviving individuals. We located  indivi- tors over a long period of time, and whose population size duals in the wild, in eight localities. Two distinguishing has decreased below a critical threshold necessary to prevent morphological characters (tepal colour and tepal number) extinction (Ren et al., ; State Forestry Administration of were revised based on observations of all remaining wild in- China, ; Ma et al., ). Magnolia sinica is one such dividuals that produced flowers and on one -year-old species, and it has been targeted as one of the  such species flowering plant in Kunming Botanical Garden. The survival approved by the Yunnan government for urgent rescue ac- rate of individuals propagated from seed for ex situ conser- tion before . Here we () update distribution data for M. vation at the Garden was % over  years; of  indivi- sinica and reassess the number of wild individuals, () revise duals transplanted to each of two reinforcement sites,  the species’ main floral characteristics, and () examine the and , respectively, were alive after  years. We propose conservation of the species. two groups of measures to protect M. sinica:() in situ con- We firstly gathered information covering most of servation, population monitoring, and public engagement, Yunnan Province, with a focus on the south-east (including and () ex situ conservation with reinforcement or almost all counties in Wenshan, Honghe: Maguan, Xichou, reintroduction. Malipo, Jinping and Hekou/Pingbian prefectures). We re- viewed Flora Reipublicae Popularis Sinicae (Law, ), Keywords Ex situ conservation, extremely small popula- Flora Yunnanica (Law, ) and Flora of China (Xia tions, in situ conservation, Magnolia sinica, morphological et al., ) for information on the species, and examined revision, reinforcement, species distribution all M. sinica specimens in the three major herbaria of the Chinese Academy of Sciences (KUN, IBSC, PE) to identify To view supplementary material for this article, please visit potential sites for field verification. We then surveyed for http://dx.doi.org/./S M. sinica during –, using field measurements and participatory rural appraisal (Chambers, , ; Upjohn et al., ). We interviewed  people (five mem- agnolia sinica (Law) Noot. (Magnoliaceae), a tree bers of staff at each of four reserves), in particular regarding endemic to China, was first described as M factors affecting the vulnerability of the species. During the Manglietiastrum sinicum Law (Law, ); the type locality field surveys several previously unrecorded individuals of is in broadleaved evergreen forest near Fadou village, M. sinica were discovered, bringing the total number of Xichou County, in south-east Yunnan Province. Most known individuals in the wild to , scattered throughout the prefectures of Wenshan and Honghe in Yunnan (Fig. ) at altitudes of ,–, m. Thirty-six of the BIN WANG*, YONGPENG MA,GAO CHEN,CONGREN LI,ZHILING DAO (Corresponding remaining individuals are in Wenshan prefecture (Table ). author) and WEIBANG SUN (Corresponding author) Kunming Botanical Garden,  Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, 650201 We collected morphological data for each of the indivi- Yunnan, China. E-mail [email protected], [email protected] duals, and grouped them into eight categories, based on height *Also at: University of Chinese Academy of Sciences, 100049 Beijing, China (H) for smaller individuals and diameter at breast height ,  $  Received  November . Revision requested  December . (DBH) for larger individuals: I (H cm), II (H cm, Accepted  March . First published online  May . and individuals for which DBH can be measured with DBH

Oryx, 2016, 50(3), 446–449 © 2015 Fauna & Flora International doi:10.1017/S0030605315000435 Downloaded from https://www.cambridge.org/core. IP address: 170.106.33.42, on 26 Sep 2021 at 04:57:35, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0030605315000435 Rescuing Magnolia sinica 447

FIG. 1 Known locations of Magnolia sinica in China, with the total number of individuals at each location and, in parentheses, the number of these that are within nature reserves. New records are indicated in blue, and previously known populations in black. The shaded rectangle on the inset shows the location of the main map in China.

,. cm), III (DBH .–. cm), IV (DBH .–. cm), nursery affiliated with Kunming Botanical Garden. After  V(DBH.– cm), VI (DBH –. cm), VII (DBH years of nursery growth  saplings of each batch were .– cm) and VIII (DBH $  cm). There was consider- transplanted to Shangchang (SC and SC) and another able variation in size, implying differences in age. There were  saplings of each batch to Xiaoqiaogou (XQG and no seedlings near those adult trees that could have produced XQG). These two reinforcements were monitored by seeds (Fig. ). The height of adult trees (V–VIII) was –. local rangers, who recorded the height, basal diameter and m, and DBH was .– cm; the height of immature trees crown breadth of the saplings. Saplings were also trans- (III–IV) was – m, and DBH was – cm. Our revision of planted to Kunming Botanical Garden, batch  (KBG) the floral traits of M. sinica is provided in Supplementary after  years of nursery growth and batch  (KBG) after  Material . years of nursery growth, and both batches were monitored Magnolia sinica in Kunming Botanical Garden can be to record annual growth. Beginning in June  we mea- traced to a single introduction event in . Of the  indi- sured the growth of batches KBG ( individuals) and viduals introduced to the garden in  for ex situ conser- KBG () annually. In June  the survival rate of both vation the first flowering (of an individual  m in height) batches was %. In  the numbers of surviving indivi- occurred in March . During the flowering period duals at the reinforcement sites were  (SC) and  (March–April) in  we performed bagged pollination (XQG) after  years, and  (SC) and  (XQG) after  treatments to assess seed-set from self-pollination (n =  years. We believe that the low survival rate of these two flowers) and outcrossing (cross-pollination with pollen batches of reintroduced seedlings is attributable to inappro- from a wild tree in Jinping County, n =  flowers); as a con- priate handling of the saplings during transplanting (c. % trol  flowers were untreated and accessible to natural pol- of the saplings were planted directly without removing the linators. None of the flowers open to pollinators produced plastic bags in which they had been grown, thus hindering any fruit, whereas all hand-pollination experiments showed the young plants from taking root). The annual increments seed-set of .–.% (calculated as the number of suc- of height, basal diameter and crown breadth are in cessfully fertilized ovules producing seed relative to the Supplementary Table S. total number of ovules per flower). The eight follicles that re- Although the species is protected at the national level as sulted from the pollination experiments contained a total of well as locally in Yunnan, it is on the brink of extinction in  seeds. At least some of these seeds were viable, as several the wild. The low number of saplings and young trees is lim- germinated after incubation in humid sand for  months. iting the potential for regeneration, and the surviving indi- Seeds were collected for ex situ conservation and propa- viduals all occur in remnant populations that are gation from four trees at the type locality in Fadou village, fragmented and comprise too few individuals for natural re- Xichou County, in  (Batch ) and in  (Batch ; covery. As M. sinica is unlikely to recover naturally, effective Zhang et al., ). Both batches of seeds were sown in a conservation of this species requires intervention.

TABLE 1 Records of Magnolia sinica in the wild, with locality, geographical coordinates, altitude, and number of individuals in categories III–IV (DBH .–. cm and .–. cm, respectively) and V–VIII (DBH .– cm, –. cm, .– cm and $  cm, respectively).

No. of individuals Localities (village/reserve, Category Category county)1 Geographical coordinates Altitude (m) III–IV V–VIII Wenshan Zhuang & Miao Autonomous Prefecture Fadou, Xichou3 23°21′37″−23°22′43″N, 104°45′59″–104°47′16″E 1,490–1,573 4 6 Pingzhai, Xichou2 23°21′17″–23°21′18″N, 104°46′46″–104°46′47″E 1,366 1 1 Xiaoqiaogou, Xichou2 23°21′43″–23°21′44″N, 104°41′57″–104°42′02″E 1,528–1,584 1 4 Heba, Xichou2 23°21′24″–23°21′37″N, 104°41′28″–104°41′58″E 1,572–1,639 0 2 Dalishu, Maguan2 23°01′54″–23°02′44″N, 104°12′21″–104°13′30″E 1,605–1,707 1 4 Miechang, Maguan4 22°51′15″–22°51′48″N, 104°01′19″–104°02′38″E 1,420–1,509 2 8 + 25 Honghe Hani & Yi Autonomous Prefecture Daweishan, Hekou/ 22°54′00″–22°55′41″N, 103°37′51″–103°40′52″E 1,403–1,570 0 5 + 45 Pingbian2 Maandi, Jinping2 22°40′27″–22°46′32″N, 103°29′50″–103°32′26″E 1,339–1,437 0 7

 The individuals in Xichou are all in nature reserves. Two individuals in Dalishu, Maguan are in state-owned forest. The individuals in Hekou are all in non-commercial forest.  New records  Records include seven previously known individuals  Records include three previously known individuals  Based on information provided by local people

education, establishing better cooperation between local governments and research institutes, including universities and environmental organizations, is needed for long-term monitoring and research and to develop strategies for the conservation of M. sinica. () The seeds cultivated in Kunming Botanical Garden and used for reinforcement of wild populations were from only one site (Xichou). It is essential to collect seeds from other sites and individuals to increase the genetic diversity of the seed pool for further ex situ conservation and for reinforcement or reintroduction (Ren et al., ). One of the criteria for judging the success of ex situ conservation is whether the  FIG. 2 Numbers of wild M. sinica individuals in each of eight transplanted plants can produce offspring (Law et al., ), size categories, defined in the text. Information provided by local and M. sinica has done so in Kunming Botanical Garden. people about six individuals is not included.

Acknowledgements We therefore propose two groups of measures to protect M. sinica:() in situ conservation, population monitoring, We gratefully acknowledge Yuan Zhou, Jing Yang, Tiancai Bo, and public engagement, and () ex situ conservation with Wulong Jiang, Guoyun Li, Hongliang Liu, Li Ma, Enjun reinforcement or reintroduction. Wang, Yongjun Wang, Ziqing Yuan, Xiangyuan Zeng and () Many of the individuals remaining in the wild ( of Yingliang Zhao for their help during fieldwork, Fauna & , in three populations) are outside protected areas, and Flora International, Botanic Gardens Conservation therefore expansion of reserves or establishment of new International, and the State Forestry Administration of sites for in situ conservation is necessary (Shen et al., China for their support for this study, the local forestry au- ). Local governments and nature reserves could limit thorities (including Maguan, Xichou, Hekou and Jinping) any further habitat destruction by reducing cultivation of for assistance in field work, all interviewees for their valuable amomum, rubber and banana, which are grown in former information about the distribution of M. sinica, Drs Tobias M. sinica habitat, and renaturalization of farmland could and Jane Marczewski for reviewing the text and for drafting create new habitat for reinforcement or reintroduction. To Fig. , two anonymous reviewers for their invaluable com- bridge the gap between scientific research and public ments and suggestions, and Xingfeng Zhao for providing

photographs. This study was supported by the National Unpublished report. State Forestry Administration of China, China. Science Foundation of China–Yunnan (Grant no. U [In Chinese]  to WS). SUN, W.B., ZHOU, Y., LI, X.Y., YANG, H.B. & TAO,P.Y.( ) Population reinforcing program for Magnolia sinica, a critically endangered endemic tree in southeast Yunnan province, China. References In Plant Reintroduction in a Changing Climate (eds J. Maschinski & K.E. Haskins), pp. –. Island Press, Washington, DC, USA. CHAMBERS,R.() The origins and practice of participatory rural UPJOHN, M.M., ATTWOOD, G.A., LEROTHOLI, T., PFEIFFER, D.U. & appraisal. World Development, , –. VERHEYEN, K.L.P. () Quantitative versus qualitative CHAMBERS,R.() From PRA to PLA and Pluralism: Practice and approaches: a comparison of two research methods applied to Theory. Working Paper . Institute of Development Studies, identification of key health issues for working horses in Lesotho. Brighton, UK. Preventive Veterinary Medicine, , –. CICUZZA, D., NEWTON,A.&OLDFIELD,S.() The Red List of WANG,S.&XIE,Y.() China Species Red List. Volume . Higher Magnoliaceae. Fauna & Flora International, Cambridge, UK. Education Press, Beijing, China. LAW,Y.W.() A new genus of Magnoliaceae from China. Acta XIA, N.H., LIU, Y.H. & NOOTEBOOM, H.P. () Magnoliaceae. In Phytotaxonomica Sinica, , –. Flora of China, pp. –. Science Press, Beijing, China & Missouri LAW,Y.W.() Magnoliaceae. In Flora Reipublicae Popularis Botanical Garden Press, St. Louis, USA. Sinicae, pp. –. Science Press, Beijing, China. ZHANG, A.L., SHEN, S.K. & WANG, Y.H. () Conservation and LAW,Y.W.() Magnoliaceae. In Flora Yunnanica, pp. –. reintroduction of the Vulnerable plant Apterosperma oblata in Science Press, Beijing, China. China. Oryx, , . LAW, Y.W., ZHOU, R.Z. & ZENG, Q.W. () Ex-situ conservation of ZHENG, Y.L., SUN, W.B. & ZHAO, X.F. () Seed dormancy and Magnoliaceae including its rare and endangered species. Journal of germination of Manglietiastrum sinicum Law, a globally critical Tropical and Subtropical Botany, , –. endangered plant in China. Plant Physiology Communications, , MA, Y.P., CHEN, G., GRUMBINE, R.E., DAO, Z.L., SUN, W.B. & –. GUO, H.J. () Conserving plant species with extremely small populations (PSESP) in China. Biodiversity and Conservation, , –. REN, H., JIAN, S.G., CHEN, Y.J., LIU, H., ZHANG, Q.M., LIU, N. et al. () Distribution, status, and conservation of Camellia changii Ye (Theaceae), a Critically Endangered plant endemic to southern Biographical sketches China. Oryx, , –. REN, H., ZHANG, Q.M., LU, H.F., LIU, H.X., GUO, Q.F., WANG, J. et al. B IN WANG has a particular interest in seed ecology and conservation () Wild plant species with extremely small populations require of threatened endemic plants, especially of the family Magnoliaceae. conservation and reintroduction in China. Ambio, , –. Y ONGPENG M A ’s main research interest is the evolutionary signifi- SHEN, S.K., WANG, Y.H., ZHANG, A.L., WU, F.Q., JIANG, L.J. & JIANG, cance of natural hybridization. G AO C HEN’s main research interest L.N. () Conservation and reintroduction of a Critically is the relationships between plants and insects. C ONGREN L I carries Endangered plant Euryodendron excelsum. Oryx, , –. out field investigations that focus on introducing and cultivating seed- STATE FORESTRY ADMINISTRATION OF CHINA () The Saving and lings of threatened endemic plants. Z HILING D AO and W EIBANG Conservation Program on Extremely Small Populations in China. S UN’s main research interests are in conservation biology.