Diversity xxx (2016) 1e8

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Plant Diversity

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How to conserve threatened Chinese plant species with extremely small populations?

* Sergei Volis

Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, 650204, China article info abstract

Article history: The Chinese flora occupies a unique position in global plant diversity, but is severely threatened. Received 27 December 2015 Although biodiversity conservation in China has made significant progress over the past decades, many Received in revised form wild plant species have extremely small population sizes and therefore are in extreme danger of 27 January 2016 extinction. The concept of plant species with extremely small populations (PSESPs), recently adopted and Accepted 27 January 2016 widely accepted in China, lacks a detailed description of the methodology appropriate for conserving Available online xxx PSESPs. Strategies for seed sampling, reintroduction, protecting PSESP locations, managing interactions with the local human population, and other conservation aspects can substantially differ from those Keywords: Biodiversity commonly applied to non-PSESPs. The present review is an attempt to provide a detailed conservation Endangered methodology with realistic and easy-to-follow guidelines for PSESPs in China. PSESP Copyright © 2016 Kunming Institute of Botany, Chinese Academy of Sciences. Publishing services by in situ Elsevier B.V. on behalf of KeAi Communications Co., Ltd. This is an open access article under the CC BY- ex situ NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). quasi in situ Conservation actions Conservation guidelines Chinese plant conservation Nature reserves

1. Introduction of natural habitats in virtually all biomes of China are the most important causes of plant extinction. I will not go into the history of China is a globally recognized biodiversity center, harboring plant conservation in China as this subject is beyond the scope of more than 30,000 higher plant species of which approximately this paper. Nor will I cover the current situation with protection of 10,000 are endemics (Yang et al., 2005). Besides tremendous di- threatened species in China as this information can be found versity and high endemism, the Chinese flora contains a large elsewhere (Liu et al., 2003; Lopez-Pujol et al., 2006; Huang, 2011). number of relic lineages of plant taxa. All these features give the Instead, my goal here is to present an analysis of current conser- Chinese flora a unique position in global plant diversity. Unfortu- vation practices in China, make a rough estimation of their effec- nately, rapid economic development, population growth, intensive tiveness, and, after identifying the problems, to propose some agriculture and the over-harvesting of timber and medicinal plants possible solutions. have led to serious destruction or alteration of the natural envi- The major document regulating plant conservation in China is ronment which has resulted in the extinction or decline of many China's Strategy for Plant Conservation (China's Strategy for Plant species. At least 200 species have become extinct over the past 50 Conservation Editorial Committe, 2008), which formulated the years (Chinese State Report on Biodiversity Editorial Committee, nation's commitment to plant conservation and established targets 1998) and c. 5000 species are currently threatened or on the to reduce the ongoing loss of plant diversity. Implementation of this verge of extinction, making China one of the highest priorities for plan is coordinated by the Chinese Academy of Sciences, State global biodiversity conservation. Destruction and/or fragmentation Forestry Administration and the Ministry of Environmental Pro- tection. The strategy serves as a framework for Chinese plant con- servation and includes 16 targets. The two targets most relevant for conservation of endangered plant species aim to protect ~90% of * þ Tel./fax: 86 871 5223170. China's national key protected plants through in situ efforts (Target E-mail address: [email protected]. Peer review under responsibility of Editorial Office of Plant DiversityAbstract. 7), and to reintroduce 10% of China's threatened plant species to http://dx.doi.org/10.1016/j.pld.2016.05.003 2468-2659/Copyright © 2016 Kunming Institute of Botany, Chinese Academy of Sciences. Publishing services by Elsevier B.V. on behalf of KeAi Communications Co., Ltd. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

Please cite this article in press as: Volis, S., How to conserve threatened Chinese plant species with extremely small populations?, Plant Diversity (2016), http://dx.doi.org/10.1016/j.pld.2016.05.003 2 S. Volis / Plant Diversity xxx (2016) 1e8 their natural habitats and establish monitoring programs to track emphasis on international cooperation and public education”. management success (Target 8). However, the progress of plant Some of the listed measures can be easily understood and are un- conservation in China is impeded by several factors. First, the questionably very important, e.g., “combining habitat protection criteria for prioritizing species to be protected are unclear. Second, and habitat restoration”. Others are equally important but require detailed methodological conservation guidelines that can be effi- some explanation and more details. For example “improving the ciently applied to threatened species in China are absent. network of nature reserves and focusing on in situ conservation” is In 1999, the State Council of China promulgated a list of National indeed an important task, but how should the network be Key Protected Wild Plants (First Group) of 419 species to be legally improved: by an increase in number of reserves, changes in reserve managed and protected by the central government. In 2004, Wang management, closer coordination between the reserves or some- and Xie (2004) published the China Species Red List (Vol. 1) based on thing else? Unfortunately, this is not explained. An urgent necessity IUCN classifications and academic experts recommendations, for properly described conservation methodology for PSESPs which substantially differed from the National Key Protected Wild motivated this study. The present review is an attempt to provide a Plants list. Unfortunately, only plant species listed in the latter list detailed conservation methodology with realistic and easy-to- have been subject to conservation actions (Ma et al., 2013). The follow guidelines for PSESPs in China. incongruence between the two lists has left many threatened species out of active conservation. In addition, the IUCN Red List 2. Identification of the species protection category approach has recognized limitations (Possingham et al., 2002; de Grammont and Cuaron, 2006; Miller et al., 2007; Mace et al., The IUCN Red List Categories and Criteria are intended to be an 2008; Harris et al., 2012) as will be discussed below. easily and widely understood system for classifying species at high In 2012, the State Forestry Administration of China formulated risk of global extinction. However, although the general aim of the the ‘‘Conservation Program for Wild Plants with Extremely Small system is to provide an explicit, objective framework for the clas- Population in China’’ as their 2012e2015 operational plan. The term sification of the broadest range of species according to their ‘‘extremely small population’’ refers to a population having a nar- extinction risk, the system criteria do not work well when applied row geographical distribution which has resulted from some to PSESPs. The IUCN Red List Criteria assume that the populations negative external factors over a long time, and whose numbers are exhibit a normal demographic structure in which all the life cycle smaller than the minimum required to prevent extinction (State stages are present. This, however, is rather the exception than the Forestry Administration of China, 2012). This was an important rule with Chinese PSESPs. The fact that the species is represented by stage in Chinese plant conservation. Indeed, most endangered a very small population(s) is already an alarm that something is Chinese plant species are represented by very small populations wrong with its demographic structure. Indeed, virtually all species (hereafter PSESPs), and must be the first priority for conservation. A with extremely small population sizes have abnormal population survey conducted by the State Forestry Administration between demographic structures. Some lack saplings, others lack seedlings 1997 and 2003 identified 189 national key protected wild plant or produce no seeds. Application of the IUCN rules related to species, most of which have fewer than 5000 individuals, with 11 decrease in area of occurrence/occupancy or population size has no having fewer than 10 individuals in natural populations. It should meaning if most or all the individuals comprising a population be noted that these numbers do not distinguish reproducing and cannot reproduce or the seeds produced do not germinate. This non-reproducing adults, and may also include very young plants means that for many, if not most, of the PSESPs the current pro- that will never reach adult stage. tection status is misleading and these species are actually at the Surprisingly, the newly formulated Chinese policy focus on very verge of extinction. For example, Davidia involucrata is not PSESPs (Ren et al., 2012) has not been followed by amendments to even included on the list of threatened Chinese plants, but all the the routinely applied plant conservation methodology. Although natural populations of this species show no signs of regeneration. PSESPs have received much attention in the recent literature (Ren The majority of the plants in natural populations of this species are et al., 2012; Ma et al., 2013; Ma and Sun, 2015; Sun and Han, old (>50 years old) and no seedlings/saplings have been 2015; Yang et al., 2015b), no publications have provided a observed in these populations for the last few decades (Ma and Li, detailed description of the methodology appropriate for conserving 2005; Zhang et al., 2008). The seeds produced are viable, but they PSESPs. The conservation methods appropriate for PSESPs are do not germinate under natural conditions. On the other hand, briefly presented in Ma et al. (2013). Undoubtedly, all the steps the thousands of D. involucrata trees have been produced artificially for authors propose are appropriate and important, but details on how landscaping in cities and many have been planted in Botanical they should be performed are not provided. Strategies for seed Gardens and Arboreta. Has the artificial production and planting sampling, reintroduction, protecting PSESP locations, and interac- helped the species recover? There are no indications that it has. tion with the local population can substantially differ from those This example shows that neither reduction in the area occupied by routinely applied to non-PSESPs. Ren et al. (2012) summarize the a population or the population size itself can provide a reliable appropriate conservation strategies for PSESPs in China as estimate of how endangered the species is. Similarly, Li et al. (2012) involving: “(1) initiating the national key protected wild plants showed that lack of naturally regenerated seedlings in Metasequoia resources survey and established resource information systems; (2) glyptostroboides calls into question the criteria used to define con- improving the network of nature reserves and focusing on in situ servation program success, and suggested that the criteria for conservation; (3) establishing networks for national botanical delisting species should not be based solely on the number of gardens and strengthening near-in situ conservation and ex situ extant plants and their distribution ranges. Other examples of conservation; (4) increasing the construction of breeding centers species for which no seedlings have been observed in natural and combining in situ and ex situ conservation; (5) combining populations include Magnolia sinica (Wang et al., 2015), Camellia habitat protection and habitat restoration; (6) improving and changii (Ren et al., 2014), Acer yangbiense (Weibang Sun, personal expanding the species' living space; (7) rationally combining con- communication), Quercus (Cyclobalanopsis) sichourensis, Pinus servation, germplasm preservation, and sustainable utilization; and squamata, Nyssa yunnanensis, Annamocarya sinensis, Malania olei- (8) conservation may also include overall planning; government fora, Camellia fascicularis, Glyptostrobus pensilis, Diploknema yun- guidance, participation and cooperation by scientists, government, nanensis, and Euryodendron excelsum (Sun, 2013). I propose that and the public in creating realistic policies and regulations, and distorted population demographic structure must be adopted as

Please cite this article in press as: Volis, S., How to conserve threatened Chinese plant species with extremely small populations?, Plant Diversity (2016), http://dx.doi.org/10.1016/j.pld.2016.05.003 S. Volis / Plant Diversity xxx (2016) 1e8 3 the most important indicator that the species is really endangered. landscaping due to their high decorative value (e.g., Breitshneidera Thus, we must first recognize the extreme danger of extinction for sinensis, C. changii and many Magnoliaceae). High demand dictates these species, make them the top priority for conservation, fol- their high market price which in turn stimulates people to regularly lowed that with IMMEDIATE action; and second, we must visit the wild populations, collect seeds and dig out seedlings. concentrate our efforts on understanding why the seeds do not Even a rough population demographic survey and assessment of germinate under natural conditions or why the seedlings do not anthropogenic disturbance can reveal the major threats for popu- develop into saplings as opposed to producing artificially seedlings/ lation viability. Habitat destruction and over-exploitation have saplings for landscaping, which has nothing to do with the real been and, for many species, continue to be the main threats. conservation of the species. The immediate actions must include However, in some cases low population viability can be due to /seed collecting, mapping all the reproducing adults, and a genetic or demographic processes, such as low pollinator visitation preliminary survey of the population demographic structure. These or inbreeding depression, which are associated with small (effec- first immediate actions must be followed by properly organized tive) population size. In other cases, biotic interactions vital for the study of the species habitat, long-term observations on population species can be disrupted, for example, the disappearance of demography and setting an Action Plan for the species recovery. frugivorous animals, leading to no seed germination in situ. The In general, conservation of every threatened species should start level of “clearance” of Chinese territory from wild animals is dra- with proper mapping of its range, an inventory of its existing matic, producing true “empty forests” (Redford, 1992). An under- populations and a population demographic survey, but this is standing of the role of frugivory and zoohory in the biology of especially critical for PSESPs. This information is crucial for defining endangered plant species is something that is urgently needed the species conservation status and its critical habitat, under- because, for many endangered species, especially those having standing factors determining species range, and for future decisions large , seed germination under natural conditions is extremely about species in situ conservation. Most PSESPs, although wide- rare or not observed. Defaunation has been recognized as a very spread in the past, currently fall into the category of rare species significant conservation problem not only for animal species but that have a very narrow ecological niche or occupy (micro)habitats also for plants (Redford, 1992; Terborgh et al., 2008; Beaune et al., that are rare by themselves (due to almost complete destruction of 2013; Harrison et al., 2013; Caughlin et al., 2015). Reduced overall their natural habitats). This implies that the suitable habitat for sapling recruitment, increased recruitment of species dispersed by such species is probably not randomly distributed, but uncommon abiotic means and altered relative abundances of species occur in (Maschinski et al., 2012). Unfortunately, in China, there are many an empty forest (Terborgh et al., 2008). more studies of genetic variation in threatened species than studies Identification of a threat requires at least basic knowledge of the of their ecological niche or population demography. For most species biology, viz. mode of pollination and seed dispersal, PSESPs we only have information about the populations' locations breeding structure, presence of seed dormancy, age at maturity and and rough estimates of their sizes, but almost never their de- pattern of fruit/seed production. Genetic studies such as analysis of mographic structure, not to mention population viability analysis. extent and structure of genetic variation, estimation of pattern of gene flow among and within populations and identification of 3. Identification of a threat evolutionarily significant units can provide very useful information for conservation, but their importance should not be over- There is no doubt that human activity has been and continues to estimated. In terms of money allocation and urgency, demographic be the major threat to Chinese plant biodiversity. Loss of natural and ecological studies should have priority. Typically, active man- habitats due to agriculture and logging started in ancient times but agement of genetic diversity is not necessary for the majority of rose dramatically after mass-scale forest clear-cutting in the rare species (Holsinger and Gottlieb, 1991). 1950se1960s. The destructive clear-logging was followed by land conversion into forest plantations or agricultural fields. As a result, 4. Habitat protection continuously distributed primeval forests became patches of sec- ondary forests that survived within complex mosaics of land use. Habitat protection has a crucial role in plant conservation Some of these forest remnants are relatively large and less damaged because it prohibits activities that can damage, destroy or modify than others due to their low accessibility and remoteness; these the habitats recognized as critical for the species survival. In China, areas have preserved many species that disappeared elsewhere. to date, there are a total of 2349 nature reserves including 265 However, alteration of the native forests by human activity has national nature reserves (of which 132 are wild plant nature re- never stopped and is continuing as local logging, firewood cutting, serves), covering an area of 2,260,000 ha. However, the efficiency of charcoal production, agricultural development, overgrazing and the existing Chinese network of nature reserves should not be uncontrolled harvesting of wild plants. Of the 8000 and shrub overestimated, because it has been created without an adequate taxa in China, about 2000 are timber species (World Bank, 2001), conceptual foundation or systematic planning. Furthermore, it does and small-scale illegal commercial logging still occurs, with esti- not have centralized management/coordination, and many reserves mated 80 million m3 being illegally logged nationwide every year have no clear boundaries, no management teams, and no staff (Liu (SEPA (State Environmental Protection Administration), 2002). et al., 2003). On top of this, continued legal and illegal activities by Cutting of trees for firewood is widespread and intensive in China local residents living in nature reserves have detrimental effects on because fuel wood still serves as the main source of heating in rural the “protected” environment (Liu et al., 2001). For example, even in mountain areas. Many plant species are harvested because of their a flagship protected area such as Wolong Nature Reserve, which medicinal or horticultural properties. As more than 11,000 species was established to protect the world-renowned, endangered giant are used in Chinese traditional medicine (Hamilton, 2004), the ef- pandas, the rate of high-quality habitat loss after the reserve's fect of over-collecting can be extremely severe for natural pop- establishment was much higher than before its creation, and was ulations. Even widespread cultivation does not stop continuous even higher than in unprotected areas adjacent to the reserve (Liu depletion of wild populations of commercially important species et al., 2001). (e.g. Panax ginseng and regia). In some cases widespread Besides these recognized problems with nature reserves, the cultivation even encourages local people to deplete wild pop- situation with PSESPs is worsened by the fact that only some ulations. For example, many rare tree species are used for PSESPs are located within the reserves, while many other

Please cite this article in press as: Volis, S., How to conserve threatened Chinese plant species with extremely small populations?, Plant Diversity (2016), http://dx.doi.org/10.1016/j.pld.2016.05.003 4 S. Volis / Plant Diversity xxx (2016) 1e8 populations are situated in unprotected environments. As a rule, 6. ex situ: seed collections these populations occupy very small territory and in many cases are surrounded by completely or partially altered environment that has At present in China, there are about 180 botanical gardens, no conservation value. In light of this, it is difficult to agree with the having in their collections 22,000 higher plant species native to conclusion that “the current network of protected areas in north- China, and three national germplasm banks. However, the effi- western Yunnan is adequate to protect much of floral diversity in ciency of this impressive infrastructure for the conservation of the region (Ma et al., 2007)”. One solution for protecting PSESPs is threatened species seems to be low. For example, the China the creation of small-scale reserves or Plant Micro-Reserves (PMR; Germplasm Bank of Wild Species based at Kunming Institute of Laguna, 2001; Laguna et al., 2004). Small reserves were long ago Botany, which has the largest seed bank collection, not only in recognized as an efficient way to protect plant-rich flora in a frag- China, but the whole Asia, stores in total 8855 species. However, mented landscape (Reznicek, 1987; Cowling and Bond, 1991; only 47 (less than 0.6%) are species from critically endangered, Falkner and Stohlgren, 1997; Gotmark€ and Thorell, 2003), and endangered and vulnerable categories. became part of the designs of regional and national strategies for For ex situ collections to be useful in conservation of threatened protected areas (Cowling et al., 2003; Draper et al., 2003; Kadis species, they must be explicitly oriented towards conservation, i.e. et al., 2013). the collections must not only adequately represent the species PMRs are small land plots (up to 20 ha) given legal protection genetic diversity during storage but also ensure availability of status with the aim of long term monitoring and conservation of stored germplasm for future in situ recovery efforts. For species plant species and their habitat. Within PMRs, active management of with extremely small populations, all reproducing adults must be plant populations is allowed, including seed collection and estab- sampled, and sampling should be done repeatedly over several lishing living collections, population reinforcements and in- years because i) sampling large quantities of seeds is impossible troductions, herbivore exclusion, scrub clearance, and restoration when the population is small and seed production is limited, of suitable environmental conditions. Of course, the small reserves infrequent or varies among seasons; and ii) relatively small but are not an alternative to large protected areas, but a complement to more frequent samples are less harmful for a population than larger them, being the only option available to protect natural fragments samples taken more infrequently (Menges et al., 2004). surrounded by land unavailable for conservation purposes. For rare and endangered species, and especially for PSESPs, In China, small protected areas designated for a particular collecting seeds from individual plants and keeping their seeds function, so called mini nature reserves (MNR) or “in situ conser- separately as maternal lines (families) is preferable to bulk collec- vation sites” (“bahu xiaoqu” in Chinese), are sometimes established tions. The reason is that seed banks of rare and endangered species outside nature reserves. For example, two MNRs have been estab- must be useful for in situ actions, and for these actions genetic lished to protect orchids (Liu et al., 2015). identity of the seeds can be very important. For example, specific genotypes may be needed to ensure sexual reproduction in a 5. Environmental education population, or genetic enrichment may be necessary to prevent the negative effects of genetic drift and inbreeding. Furthermore, only Over-collecting is a very serious threat to many plant species in collections organized by family can be used for analyses of the China, and addressing this threat should include but not be limited species' genetic structure, identification of evolutionarily signifi- to a prohibition on the collection of seeds and other parts of en- cant units, assessments of gene flow and other important genetic dangered plants. Environmental education should also be information. improved, especially in local communities, where one of the main Even for relatively large populations the number of source causes of ongoing species loss is the lack of true awareness or plants and quantities of seeds per plant can be well below target appreciation of the value these species possess beyond their prac- levels. For PSESPs with infrequent and/or limited seed production, tical use. Conservation policies have been proposed for ornamental the quantities required for successful reintroduction cannot be and decorative species that encourage artificial breeding programs collected in natural populations even after multiple visits and by state or private entities for commercial use. For medicinal plant require an intermediate step of propagation. Thus, a good approach species, where consumers prefer wild-gathered materials, policies would be to distinguish short- and long-term seed collections have been proposed that encourage a combination of artificial (Volis, 2015). The goal of the long-term collection is to create a cultivation and cultivation in natural habitats (Ren et al., 2014; Liu “strategic” source of germplasm that can be used for studying et al., 2015). This is unlikely to work without a comprehensive species biology, propagation and renewal, but not for in situ actions. educational campaign that starts from primary school, or even The seeds stored in short-term collection, on the contrary, will be kindergarten, and which teaches children to enjoy nature without used exclusively for in situ actions either directly or after committing harmful acts, such as picking flowers or digging out propagation. plants. Such a campaign was launched in Israel during the 1960s and was a phenomenal success. Today in Israel, picking wild plants 7. ex situ: living collections is no longer a threat to species with attractive flowers. In China, where many orchid species are severely threatened by collecting, Living collections are an important element of modern conser- such a campaign is urgently needed. The key factors explaining the vation programs and botanical gardens are the major depositories tremendous success of the Israeli “Go Out to the Landscape, but of valuable living material for conservation. The Chinese Academy Don't Pick” campaign included targeting children in compulsory of Sciences has drafted and, in 2002, began implementation of a 15- kindergartens, pre- and elementary schools, and the availability of year ex situ master plan to conserve the diversity of native Chinese an alternative, inexpensive flower supply (Tal, 2002). plants in botanical gardens. Its main goals include increasing the Secondly, there is rapidly accumulating evidence that environ- number of native protected species to 21,000, enhancing garden mental education can inspire citizens to be involved in conserva- collections of rare and endangered plants, as well as the creation of tion actions (Brewer, 2006; Jordan et al., 2011; Chen et al., 2015). five new regional and nine specialized gardens (Huang et al., 2002). Thus educational campaigns in villages neighboring populations of There are several living collections strongly oriented towards threatened species can turn destroyers into conservation sup- endangered and rare species in China, such as Xishuangbanna porters and helpers. Tropical Botanical Garden, South China Botanical Garden and

Please cite this article in press as: Volis, S., How to conserve threatened Chinese plant species with extremely small populations?, Plant Diversity (2016), http://dx.doi.org/10.1016/j.pld.2016.05.003 S. Volis / Plant Diversity xxx (2016) 1e8 5

Kunming Botanical Garden. These and 13 smaller Chinese gardens Use of seeds for introduction is known to be ineffective provide shelter to the threatened species and participate in species- compared with seedlings (Guerrant and Kaye, 2007; Godefroid oriented conservation programs. For example, A. yangbiense, rep- et al., 2011). Raising large number of seedlings from seeds in resented in nature by only five individuals, has been planted, hand- botanical gardens or nurseries may not always be possible for lo- pollinated and the resulting seeds used to produce more than 1600 gistic reasons. To obtain large quantities of seedlings required for in saplings now growing in the Kunming Botanical Garden (Yang et al., situ actions, two approaches can be used. “In situ seedling banks” 2015a). Similarly, 1300 saplings of Q. sichourensis, 400 saplings of (Pritchard et al., 2014) are created by sowing seeds and maintaining Manglietia ventii and 100 saplings of M. sinica represented by seedlings in the forest understory in a convenient, reduced space. eleven, ~200 and 52 individuals in nature, respectively, were pro- This approach has certain advantages which make it easy to apply, duced in the Kunming Botanical Garden and have been used in including the wide range of forests that can be used, e.g., natural, different conservation actions (Wang et al., 2015; Weibang Sun, degraded or planted forests, not excluding monoculture tree plan- personal communication). Another example is Vatica guangxiensis, tations. The critical points for this approach are high seed viability an endangered species for which about 90 individuals from three and germination rate, and low requirements for successful germi- remaining populations were successfully transplanted to Xish- nation. The other limitations of this approach are that seedlings uangbanna Tropical Botanical Garden (Li et al., 2002). cannot withstand a long time in the shady understorey and advance However, utility and overall capacity of botanical gardens for to saplings, and intense seedling herbivory (Benitez-Malvido et al., maintaining living collections of threatened species should not be 2005). Another approach is to use wildlings. Although this overestimated. One known problem is poor management, e.g. method cannot be applied to those PSESPs that suffer from germi- representation of species by only a few individuals, lack of infor- nation failure, it can be useful for other PSESP species. For example, mation on accession sampling locality and mislabeling (Hurka, intensive seed production of Liriodendron chinense trees planted in 1994). Another potential problem is the risk of spontaneous hy- Gaowangjie Nature Reserve along a local road gave rise to dense bridization when related species, sub-species or ecotypes are stands of seedlings and saplings in proximity to the mother plants. grown in close physical proximity in the garden. The latter seriously These wildlings can be used for the creation of new populations of L. undermines utilization of botanic garden ex situ collections for chinense in this area. Phoebe bournei, which is represented by many propagation because open-pollinated offspring may lack genetic reproducing trees planted and maintained by farmers in a village of integrity and harbor maladaptive gene combinations (Maunder Baojing County, provides another example. The fruits produced are et al., 2004). Finally, botanical gardens have obvious limitations in dispersed by birds into the surrounding village forest, where they the number of individuals per species they can maintain. These readily germinate and grow to seedlings. However, due to apparent issues strongly limit the utility of botanical garden living collections anthropogenic disturbance (grazing and cutting for firewood), for conservation. Space limitations usually preclude achieving even which has altered the forest's environmental conditions, the seed- the minimum recommended sample size of 15 individuals neces- lings do not develop into saplings. Thus, P. bournei wildlings, which sary to capture an acceptable level of genetic variation (Namoff have no future in this environment, can be used for creation of new et al., 2010). populations in a more suitable natural location. Propagation of material for threatened species outside botanical 8. Integration of ex situ and in situ gardens in China is currently done at the national field germplasm nurseries and plant introduction bases established by National The utility of ex situ collections via storage and propagation of Environmental Protection Agency specifically for this purpose plant material that can later be used for in situ actions has been (Division of Plant Conservation of the State Forestry recognized, but the obvious space and logistical limitations of ex Administration, 2005). Currently, there are 32 germplasm nurs- situ collections present well-known challenges (Hamilton, 1994; eries and 255 introduction bases. However, there is a very limited Schoen and Brown, 2001; Maunder et al., 2004; Volis and recognition of the importance of living collections in semi-natural Blecher, 2010). This has motivated a search for an efficient inte- and natural environments that serve both as depositories preser- gration of these two approaches by creating living collections of ving species genetic variation and sites for seed propagation (but needed capacity under natural, semi-natural or artificial conditions. see Sun, 2013). The only such conservation project in China I am Two concepts of integrative conservation that suit PSESPs are aware of is the reintroduction program on M. ventii. In this project, “forest gene banks” (Uma Shaanker and Ganeshaiah, 1997; Uma after propagation in the nursery, 300 saplings were planted in a Shaanker et al., 2001; Uma Shaanker et al., 2002) and “quasi in semi-natural environment near natural population in Pingbian situ” (Volis and Blecher, 2010; Volis, 2015). The former concept (Honghe prefecture, Yunnan province) (Weibang Sun, personal proposes use of a particular existing population as an in situ sink communication). into which genetic material from several source sites is introduced and maintained. Thus the genetically diverse sink population 9. in situ management serves as a repository of the species gene pool and, at the same time, allows for random interbreeding. Although this approach The Convention on Biological Diversity (CBD, 1994)defines in cannot be used in cases when introduction of non-locals may lead situ conservation as “the maintenance and recovery of viable to outbreeding depression, in situations where plants originate populations of species in their natural surroundings”. A naive and from the same climatic zone and similar biotic environments it can over simplistic view that once dominated among conservation 1) greatly improve the local population's genetic variation and biology practitioners was that if populations are legally protected eliminate inbreeding depression; and 2) provide a large quantity of their long-term survival is guaranteed. This, however, turned out to vigorous seedlings (due to heterosis) for creating new and rein- be far from true due to the fact that virtually all natural systems forcing existing populations. The second concept proposes the preserved in nature reserves represent some degree of human- creation of new, as opposed to existing populations, as depositories induced changes that disrupted previously existing species in- of genetically variable source material. The site for such living teractions and ecological processes. Apart from this, fragmentation collections should contain individuals from populations sharing the and environmental degradation reduced population sizes of many same climatic zone and biotic/abiotic environment, have natural or species below the viability threshold. Such populations are doomed semi-natural conditions and be protected. to extinction even under the strictest protection in a reserve. Thus,

Please cite this article in press as: Volis, S., How to conserve threatened Chinese plant species with extremely small populations?, Plant Diversity (2016), http://dx.doi.org/10.1016/j.pld.2016.05.003 6 S. Volis / Plant Diversity xxx (2016) 1e8 for in situ conservation to be effective it must be based on proper reintroduced population can be misleading, because their extant understanding of ecological processes within an ecosystem and populations can be located in fragmented and degraded environ- population dynamics of threatened species. If necessary, actions ments that do not support positive or stable population growth must be implemented, including reestablishment of extinct or (Maschinski and Wright, 2006). In such cases, the reintroduction/ reinforcement of critically declined populations. But in many cases translocation decisions must be based on detailed knowledge of even this is not enough. When a population can no longer sustain historic species range, the ecological requirements of the species its existence this indicates that the habitat has deteriorated and and habitat conditions at potential reintroduction sites. Valuable requires action, too. For example, analysis of regeneration in the information for estimating suitability of a potential site for the only natural population of M. glyptostroboides revealed that in the endangered PSESPs can provide, on one hand, a comparison of last 41 years, habitat changes caused by detrimental activities of ecological factors in locations still occupied by the species and lo- human residents (cultivation of profitable plants in the understory, cations where the species went extinct, and, on the other hand, a selective cutting and harvesting of wood for fuel) have effectively comparison of these factors in locations with PSESPs and in loca- ended recruitment of M. glyptostroboides (Tang et al., 2011). The tions where the population size exceeds viability threshold (if the latter means that neither strict protection nor reinforcement ac- latter still exist). Identification of the habitats most suitable for the tions will rescue this population. Without restoring conditions that target species can utilize species distribution modeling, experi- once were present in this habitat and under which natural germi- mental introduction, or both. Distribution modeling is useful for nation was occurring normally (as evidenced by Chu and Cooper, broad categorizations of potential habitat, but for species with very 1950), the population has no chance of survival. Thus, in situ con- limited distribution, where the importance of microhabitat condi- servation of threatened species requires identifying the habitats in tions is apparent and there is a shortage of information on prior which they can maintain viable populations, and then protecting distribution (as the case with many PSESPs), only actual introduc- both the habitat and the species through carefully designed man- tion can efficiently identify the species' realized niche. Thus, for agement. This especially applies to PSESPs. Modern conservation in PSESPs we strongly recommend the experimental approach, i.e. situ includes not only protection of the population or group of experimental introduction across multiple (micro)sites within the populations within a protected area or habitat, but also involves, current or documented historic species range (reintroduction), or after identification of a threat, the preparation and implementation within the presumed ecological niche of the species (translocation) of management plans to eliminate the threat and recover the (Fiedler and Laven, 1996; Falk et al., 1996; Maschinski et al., 2004; population(s). Maschinski and Wright, 2006; Guerrant and Kaye, 2007; Volis For most of the threatened species with PSESPs, reinforcement et al., 2010, 2011; Rünk et al., 2014). (IUCN, 1998), i.e. supplementation of existing populations to For threatened PSESPs, source material for reintroduction or enhance population viability (increase in population growth rate translocation should come from more than one population to and decrease in probability of extinction) would be the optimal prevent inbreeding depression, and these populations' locations option, but only if the remaining populations are located in pro- should have close environmental and ecological similarity with the tected and non-degraded areas. If these locations are unprotected recipient locations. A match of donor and recipient locations crucial they are almost inevitably doomed to disappearance as a result of for successful introduction can be difficult to recognize with cer- continuing anthropogenic disturbance. Supplementation must be tainty. For example, sites that appeared suitable based on expert- aimed at restoring or improving reproduction and regeneration, for opinion at the time of introduction turned out to differ in ecolog- which necessary measures can be the introduction of plants of ical similarity, and as a result success of the introduction varied particular gender to correct the sex ratio in a population, and of (Noel€ et al., 2011). adults needed to increase the pollinator visitation rates, or seed- Based on the latest theoretical developments in estimating safe lings/saplings to rejuvenate the degraded populations. The material number of introduced families and individuals, the effective pop- for reinforcement must originate either from the same location or ulation sizes should be at least 100 families and 1000 individuals, from geographically closest population(s) within the same habitat with a ratio for conversion of effective into census population size and be genetically diverse. of 0.1e0.2 as the first approximation (Frankham et al., 2014). For Reintroduction, i.e., placement of plant material into an area many PSESPs this required number of families will be impossible to where it occurred in the past, should be used for the species that achieve due to the small number of reproducing adults in extant went extinct in the wild, or for which natural populations are populations, but the required number of individuals located in unprotected and rapidly deteriorating environments, (5000e10,000), derived from all available mother plants, can be while locations with suitable environments for these species exist achieved following proper propagation. in protected areas within the known species range. Translocation, It must be noted that efficient conservation of a threatened i.e. movement of plant material to a seemingly suitable area with no species is impossible without preparing some kind of Action Plan documented past history of its existence, is the conservation action specifying all the types of intervention needed for species recovery, used to prevent species extinction when there is no remaining area such as population reinforcement, translocation or habitat resto- left within a species' historic range able to sustain viable pop- ration. The level of management intervention will depend on the ulation(s) (IUCN, 1998; Hoegh-Guldberg et al., 2008). Habitats nature and degree of the threats to which the populations/habitats suitable for the species may exist outside of the species' recorded are exposed, ranging from just monitoring to intensive recovery distribution but be unoccupied due to dispersal limitations or se- actions. These interventions can include weeding, eradication of vere fragmentation of previously continuous habitat. In both rein- exotic species, assisted pollination to increase seed set, removing troduction and translocation, creation of viable new populations risks to seedling recruitment, predator and pest control, aug- requires prior knowledge of the species' biology, including its menting dispersers, and reinforcement of populations by artificially reproduction, demography, environmental requirements and or naturally propagated material (Heywood, 2015). ecological interactions. In both actions the major criteria for eval- uating the suitability of a site for reintroduction are ecological 10. Information sharing similarity with locations of extant populations and protection. For many PSESPs, however, the assumption that similarity to extant Good knowledge of the species distribution is a prerequisite for populations is the best criterion for successful establishment of a efficient conservation of threatened species. The Global

Please cite this article in press as: Volis, S., How to conserve threatened Chinese plant species with extremely small populations?, Plant Diversity (2016), http://dx.doi.org/10.1016/j.pld.2016.05.003 S. Volis / Plant Diversity xxx (2016) 1e8 7

Biodiversity Information Facility (GBIF, http://www.gbif.org/), conservation related information, e.g. species management- which collates occurrence records of species from hundreds of or- related manuscripts, reports, and expert opinions. ganizations, is an easily searchable database that should be adopted as the major database for depositing data on PSESP distribution. Acknowledgment However, although important, occurrence data is only a part of the information needed for an Action Plan. Other crucial information This work was supported by the CAS/SAFEA International Part- includes population demographic structure, species biology, and nership Program for Creative Research Teams. I am grateful to descriptions of the species habitat. Equally important is access to a Weibang Sun and two anonymous reviewers for their comments geo-referenced database of nature reserves and other types of and Linda Olsvig-Whittaker for editing the manuscript English. protected areas (Wu et al., 2011). 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