全 文 ：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
a r t i c l e i n f o
Article history:
Received 27 December 2015
Received in revised form
27 January 2016
Accepted 27 January 2016
Available online 20 May 2016
Keywords:
Biodiversity
Endangered plants
PSESP
in situ
ex situ
quasi in situ
Conservation actions
Conservation guidelines
Chinese plant conservation
Nature reserves
a b s t r a c t
The Chinese flora occupies a unique position in global plant diversity, but is severely threatened.
Although biodiversity conservation in China has made significant progress over the past decades, many
wild plant species have extremely small population sizes and therefore are in extreme danger of
extinction. The concept of plant species with extremely small populations (PSESPs), recently adopted and
widely accepted in China, lacks a detailed description of the methodology appropriate for conserving
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
commonly applied to non-PSESPs. The present review is an attempt to provide a detailed conservation
methodology with realistic and easy-to-follow guidelines for PSESPs in China.
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/).
1. Introduction
China is a globally recognized biodiversity center, harboring
more than 30,000 higher plant species of which approximately
10,000 are endemics (Yang et al., 2005). Besides tremendous di-
versity and high endemism, the Chinese flora contains a large
number of relic lineages of plant taxa. All these features give the
Chinese flora a unique position in global plant diversity. Unfortu-
nately, rapid economic development, population growth, intensive
agriculture and the over-harvesting of timber and medicinal plants
have led to serious destruction or alteration of the natural envi-
ronment which has resulted in the extinction or decline of many
species. At least 200 species have become extinct over the past 50
years (Chinese State Report on Biodiversity Editorial Committee,
1998) and c. 5000 species are currently threatened or on the
verge of extinction, making China one of the highest priorities for
global biodiversity conservation. Destruction and/or fragmentation
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
plant conservation in China as this subject is beyond the scope of
this paper. Nor will I cover the current situation with protection of
threatened species in China as this information can be found
elsewhere (Liu et al., 2003; L
opez-Pujol et al., 2006; Huang, 2011).
Instead, my goal here is to present an analysis of current conser-
vation practices in China, make a rough estimation of their effec-
tiveness, and, after identifying the problems, to propose some
possible solutions.
The major document regulating plant conservation in China is
Chinas Strategy for Plant Conservation (Chinas Strategy for Plant
Conservation Editorial Committe, 2008), which formulated the
nations commitment to plant conservation and established targets
to reduce the ongoing loss of plant diversity. Implementation of this
plan is coordinated by the Chinese Academy of Sciences, State
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
Chinas national key protected plants through in situ efforts (Target
7), and to reintroduce 10% of Chinas threatened plant species to
* Tel./fax: þ86 871 5223170.
E-mail address: volis@mail.kib.ac.cn.
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Plant Diversity 38 (2016) 45e52
their natural habitats and establish monitoring programs to track
management success (Target 8). However, the progress of plant
conservation in China is impeded by several factors. First, the
criteria for prioritizing species to be protected are unclear. Second,
detailed methodological conservation guidelines that can be effi-
ciently applied to threatened species in China are absent.
In 1999, the State Council of China promulgated a list of National
Key Protected Wild Plants (First Group) of 419 species to be legally
managed and protected by the central government. In 2004, Wang
and Xie (2004) published the China Species Red List (Vol. 1) based on
IUCN classifications and academic experts recommendations,
which substantially differed from the National Key Protected Wild
Plants list. Unfortunately, only plant species listed in the latter list
have been subject to conservation actions (Ma et al., 2013). The
incongruence between the two lists has left many threatened
species out of active conservation. In addition, the IUCN Red List
approach has recognized limitations (Possingham et al., 2002; de
Grammont and Cuaron, 2006; Miller et al., 2007; Mace et al.,
2008; Harris et al., 2012) as will be discussed below.
In 2012, the State Forestry Administration of China formulated
the ‘‘Conservation Program for Wild Plants with Extremely Small
Population in China’’ as their 2012e2015 operational plan. The term
‘‘extremely small population’’ refers to a population having a nar-
row geographical distribution which has resulted from some
negative external factors over a long time, and whose numbers are
smaller than the minimum required to prevent extinction (State
Forestry Administration of China, 2012). This was an important
stage in Chinese plant conservation. Indeed, most endangered
Chinese plant species are represented by very small populations
(hereafter PSESPs), andmust be the first priority for conservation. A
survey conducted by the State Forestry Administration between
1997 and 2003 identified 189 national key protected wild plant
species, most of which have fewer than 5000 individuals, with 11
having fewer than 10 individuals in natural populations. It should
be noted that these numbers do not distinguish reproducing and
non-reproducing adults, and may also include very young plants
that will never reach adult stage.
Surprisingly, the newly formulated Chinese policy focus on
PSESPs (Ren et al., 2012) has not been followed by amendments to
the routinely applied plant conservation methodology. Although
PSESPs have received much attention in the recent literature (Ren
et al., 2012; Ma et al., 2013; Ma and Sun, 2015; Sun and Han,
2015; Yang et al., 2015b), no publications have provided a
detailed description of the methodology appropriate for conserving
PSESPs. The conservation methods appropriate for PSESPs are
briefly presented in Ma et al. (2013). Undoubtedly, all the steps the
authors propose are appropriate and important, but details on how
they should be performed are not provided. Strategies for seed
sampling, reintroduction, protecting PSESP locations, and interac-
tion with the local population can substantially differ from those
routinely applied to non-PSESPs. Ren et al. (2012) summarize the
appropriate conservation strategies for PSESPs in China as
involving: “(1) initiating the national key protected wild plants
resources survey and established resource information systems; (2)
improving the network of nature reserves and focusing on in situ
conservation; (3) establishing networks for national botanical
gardens and strengthening near-in situ conservation and ex situ
conservation; (4) increasing the construction of breeding centers
and combining in situ and ex situ conservation; (5) combining
habitat protection and habitat restoration; (6) improving and
expanding the species living space; (7) rationally combining con-
servation, germplasm preservation, and sustainable utilization; and
(8) conservation may also include overall planning; government
guidance, participation and cooperation by scientists, government,
and the public in creating realistic policies and regulations, and
emphasis on international cooperation and public education”.
Some of the listed measures can be easily understood and are un-
questionably very important, e.g., “combining habitat protection
and habitat restoration”. Others are equally important but require
some explanation and more details. For example “improving the
network of nature reserves and focusing on in situ conservation” is
indeed an important task, but how should the network be
improved: by an increase in number of reserves, changes in reserve
management, closer coordination between the reserves or some-
thing else? Unfortunately, this is not explained. An urgent necessity
for properly described conservation methodology for PSESPs
motivated this study. The present review is an attempt to provide a
detailed conservation methodology with realistic and easy-to-
follow guidelines for PSESPs in China.
2. Identification of the species protection category
The IUCN Red List Categories and Criteria are intended to be an
easily and widely understood system for classifying species at high
risk of global extinction. However, although the general aim of the
system is to provide an explicit, objective framework for the clas-
sification of the broadest range of species according to their
extinction risk, the system criteria do not work well when applied
to PSESPs. The IUCN Red List Criteria assume that the populations
exhibit a normal demographic structure in which all the life cycle
stages are present. This, however, is rather the exception than the
rulewith Chinese PSESPs. The fact that the species is represented by
a very small population(s) is already an alarm that something is
wrong with its demographic structure. Indeed, virtually all species
with extremely small population sizes have abnormal population
demographic structures. Some lack saplings, others lack seedlings
or produce no seeds. Application of the IUCN rules related to
decrease in area of occurrence/occupancy or population size has no
meaning if most or all the individuals comprising a population
cannot reproduce or the seeds produced do not germinate. This
means that for many, if not most, of the PSESPs the current pro-
tection status is misleading and these species are actually at the
very verge of extinction. For example, Davidia involucrata is not
even included on the list of threatened Chinese plants, but all the
natural populations of this species show no signs of regeneration.
The majority of the plants in natural populations of this species are
old (>50 years old) trees and no seedlings/saplings have been
observed in these populations for the last few decades (Ma and Li,
2005; Zhang et al., 2008). The seeds produced are viable, but they
do not germinate under natural conditions. On the other hand,
thousands of D. involucrata trees have been produced artificially for
landscaping in cities and many have been planted in Botanical
Gardens and Arboreta. Has the artificial production and planting
helped the species recover? There are no indications that it has.
This example shows that neither reduction in the area occupied by
a population or the population size itself can provide a reliable
estimate of how endangered the species is. Similarly, Li et al. (2012)
showed that lack of naturally regenerated seedlings inMetasequoia
glyptostroboides calls into question the criteria used to define con-
servation program success, and suggested that the criteria for
delisting species should not be based solely on the number of
extant plants and their distribution ranges. Other examples of
species for which no seedlings have been observed in natural
populations include Magnolia sinica (Wang et al., 2015), Camellia
changii (Ren et al., 2014), Acer yangbiense (Weibang Sun, personal
communication), Quercus (Cyclobalanopsis) sichourensis, Pinus
squamata, Nyssa yunnanensis, Annamocarya sinensis, Malania olei-
fora, Camellia fascicularis, Glyptostrobus pensilis, Diploknema yun-
nanensis, and Euryodendron excelsum (Sun, 2013). I propose that
distorted population demographic structure must be adopted as
S. Volis / Plant Diversity 38 (2016) 45e5246
the most important indicator that the species is really endangered.
Thus, we must first recognize the extreme danger of extinction for
these species, make them the top priority for conservation, fol-
lowed that with IMMEDIATE action; and second, we must
concentrate our efforts on understanding why the seeds do not
germinate under natural conditions or why the seedlings do not
develop into saplings as opposed to producing artificially seedlings/
saplings for landscaping, which has nothing to do with the real
conservation of the species. The immediate actions must include
fruit/seed collecting, mapping all the reproducing adults, and a
preliminary survey of the population demographic structure. These
first immediate actions must be followed by properly organized
study of the species habitat, long-term observations on population
demography and setting an Action Plan for the species recovery.
In general, conservation of every threatened species should start
with proper mapping of its range, an inventory of its existing
populations and a population demographic survey, but this is
especially critical for PSESPs. This information is crucial for defining
the species conservation status and its critical habitat, under-
standing factors determining species range, and for future decisions
about species in situ conservation. Most PSESPs, although wide-
spread in the past, currently fall into the category of rare species
that have a very narrow ecological niche or occupy (micro)habitats
that are rare by themselves (due to almost complete destruction of
their natural habitats). This implies that the suitable habitat for
such species is probably not randomly distributed, but uncommon
(Maschinski et al., 2012). Unfortunately, in China, there are many
more studies of genetic variation in threatened species than studies
of their ecological niche or population demography. For most
PSESPs we only have information about the populations locations
and rough estimates of their sizes, but almost never their de-
mographic structure, not to mention population viability analysis.
3. Identification of a threat
There is no doubt that human activity has been and continues to
be the major threat to Chinese plant biodiversity. Loss of natural
habitats due to agriculture and logging started in ancient times but
rose dramatically after mass-scale forest clear-cutting in the
1950se1960s. The destructive clear-logging was followed by land
conversion into forest plantations or agricultural fields. As a result,
continuously distributed primeval forests became patches of sec-
ondary forests that survived within complex mosaics of land use.
Some of these forest remnants are relatively large and less damaged
than others due to their low accessibility and remoteness; these
areas have preserved many species that disappeared elsewhere.
However, alteration of the native forests by human activity has
never stopped and is continuing as local logging, firewood cutting,
charcoal production, agricultural development, overgrazing and
uncontrolled harvesting of wild plants. Of the 8000 tree and shrub
taxa in China, about 2000 are timber species (World Bank, 2001),
and small-scale illegal commercial logging still occurs, with esti-
mated 80 million m3 being illegally logged nationwide every year
(SEPA (State Environmental Protection Administration), 2002).
Cutting of trees for firewood is widespread and intensive in China
because fuel wood still serves as the main source of heating in rural
mountain areas. Many plant species are harvested because of their
medicinal or horticultural properties. As more than 11,000 species
are used in Chinese traditional medicine (Hamilton, 2004), the ef-
fect of over-collecting can be extremely severe for natural pop-
ulations. Even widespread cultivation does not stop continuous
depletion of wild populations of commercially important species
(e.g. Panax ginseng and Juglans regia). In some cases widespread
cultivation even encourages local people to deplete wild pop-
ulations. For example, many rare tree species are used for
landscaping due to their high decorative value (e.g., Breitshneidera
sinensis, C. changii and many Magnoliaceae). High demand dictates
their highmarket pricewhich in turn stimulates people to regularly
visit the wild populations, collect seeds and dig out seedlings.
Even a rough population demographic survey and assessment of
anthropogenic disturbance can reveal the major threats for popu-
lation viability. Habitat destruction and over-exploitation have
been and, for many species, continue to be the main threats.
However, in some cases low population viability can be due to
genetic or demographic processes, such as low pollinator visitation
or inbreeding depression, which are associated with small (effec-
tive) population size. In other cases, biotic interactions vital for the
species can be disrupted, for example, the disappearance of
frugivorous animals, leading to no seed germination in situ. The
level of “clearance” of Chinese territory from wild animals is dra-
matic, producing true “empty forests” (Redford, 1992). An under-
standing of the role of frugivory and zoohory in the biology of
endangered plant species is something that is urgently needed
because, for many endangered species, especially those having
large fruits, seed germination under natural conditions is extremely
rare or not observed. Defaunation has been recognized as a very
significant conservation problem not only for animal species but
also for plants (Redford, 1992; Terborgh et al., 2008; Beaune et al.,
2013; Harrison et al., 2013; Caughlin et al., 2015). Reduced overall
sapling recruitment, increased recruitment of species dispersed by
abiotic means and altered relative abundances of species occur in
an empty forest (Terborgh et al., 2008).
Identification of a threat requires at least basic knowledge of the
species biology, viz. mode of pollination and seed dispersal,
breeding structure, presence of seed dormancy, age at maturity and
pattern of fruit/seed production. Genetic studies such as analysis of
extent and structure of genetic variation, estimation of pattern of
gene flow among and within populations and identification of
evolutionarily significant units can provide very useful information
for conservation, but their importance should not be over-
estimated. In terms of money allocation and urgency, demographic
and ecological studies should have priority. Typically, active man-
agement of genetic diversity is not necessary for the majority of
rare species (Holsinger and Gottlieb, 1991).
4. Habitat protection
Habitat protection has a crucial role in plant conservation
because it prohibits activities that can damage, destroy or modify
the habitats recognized as critical for the species survival. In China,
to date, there are a total of 2349 nature reserves including 265
national nature reserves (of which 132 are wild plant nature re-
serves), covering an area of 2,260,000 ha. However, the efficiency of
the existing Chinese network of nature reserves should not be
overestimated, because it has been created without an adequate
conceptual foundation or systematic planning. Furthermore, it does
not have centralizedmanagement/coordination, andmany reserves
have no clear boundaries, no management teams, and no staff (Liu
et al., 2003). On top of this, continued legal and illegal activities by
local residents living in nature reserves have detrimental effects on
the “protected” environment (Liu et al., 2001). For example, even in
a flagship protected area such as Wolong Nature Reserve, which
was established to protect the world-renowned, endangered giant
pandas, the rate of high-quality habitat loss after the reserves
establishment was much higher than before its creation, and was
even higher than in unprotected areas adjacent to the reserve (Liu
et al., 2001).
Besides these recognized problems with nature reserves, the
situation with PSESPs is worsened by the fact that only some
PSESPs are located within the reserves, while many other
S. Volis / Plant Diversity 38 (2016) 45e52 47
populations are situated in unprotected environments. As a rule,
these populations occupy very small territory and inmany cases are
surrounded by completely or partially altered environment that has
no conservation value. In light of this, it is difficult to agree with the
conclusion that “the current network of protected areas in north-
western Yunnan is adequate to protect much of floral diversity in
the region (Ma et al., 2007)”. One solution for protecting PSESPs is
the creation of small-scale reserves or Plant Micro-Reserves (PMR;
Laguna, 2001; Laguna et al., 2004). Small reserves were long ago
recognized as an efficient way to protect plant-rich flora in a frag-
mented landscape (Reznicek, 1987; Cowling and Bond, 1991;
Falkner and Stohlgren, 1997; G€otmark and Thorell, 2003), and
became part of the designs of regional and national strategies for
protected areas (Cowling et al., 2003; Draper et al., 2003; Kadis
et al., 2013).
PMRs are small land plots (up to 20 ha) given legal protection
status with the aim of long term monitoring and conservation of
plant species and their habitat. Within PMRs, activemanagement of
plant populations is allowed, including seed collection and estab-
lishing living collections, population reinforcements and in-
troductions, herbivore exclusion, scrub clearance, and restoration
of suitable environmental conditions. Of course, the small reserves
are not an alternative to large protected areas, but a complement to
them, being the only option available to protect natural fragments
surrounded by land unavailable for conservation purposes.
In China, small protected areas designated for a particular
function, so called mini nature reserves (MNR) or “in situ conser-
vation sites” (“bahu xiaoqu” in Chinese), are sometimes established
outside nature reserves. For example, two MNRs have been estab-
lished to protect orchids (Liu et al., 2015).
5. Environmental education
Over-collecting is a very serious threat to many plant species in
China, and addressing this threat should include but not be limited
to a prohibition on the collection of seeds and other parts of en-
dangered plants. Environmental education should also be
improved, especially in local communities, where one of the main
causes of ongoing species loss is the lack of true awareness or
appreciation of the value these species possess beyond their prac-
tical use. Conservation policies have been proposed for ornamental
and decorative species that encourage artificial breeding programs
by state or private entities for commercial use. For medicinal plant
species, where consumers prefer wild-gathered materials, policies
have been proposed that encourage a combination of artificial
cultivation and cultivation in natural habitats (Ren et al., 2014; Liu
et al., 2015). This is unlikely to work without a comprehensive
educational campaign that starts from primary school, or even
kindergarten, and which teaches children to enjoy nature without
committing harmful acts, such as picking flowers or digging out
plants. Such a campaign was launched in Israel during the 1960s
and was a phenomenal success. Today in Israel, picking wild plants
is no longer a threat to species with attractive flowers. In China,
where many orchid species are severely threatened by collecting,
such a campaign is urgently needed. The key factors explaining the
tremendous success of the Israeli “Go Out to the Landscape, but
Dont Pick” campaign included targeting children in compulsory
kindergartens, pre- and elementary schools, and the availability of
an alternative, inexpensive flower supply (Tal, 2002).
Secondly, there is rapidly accumulating evidence that environ-
mental education can inspire citizens to be involved in conserva-
tion actions (Brewer, 2006; Jordan et al., 2011; Chen et al., 2015).
Thus educational campaigns in villages neighboring populations of
threatened species can turn destroyers into conservation sup-
porters and helpers.
6. ex situ: seed collections
At present in China, there are about 180 botanical gardens,
having in their collections 22,000 higher plant species native to
China, and three national germplasm banks. However, the effi-
ciency of this impressive infrastructure for the conservation of
threatened species seems to be low. For example, the China
Germplasm Bank of Wild Species based at Kunming Institute of
Botany, which has the largest seed bank collection, not only in
China, but the whole Asia, stores in total 8855 species. However,
only 47 (less than 0.6%) are species from critically endangered,
endangered and vulnerable categories.
For ex situ collections to be useful in conservation of threatened
species, they must be explicitly oriented towards conservation, i.e.
the collections must not only adequately represent the species
genetic diversity during storage but also ensure availability of
stored germplasm for future in situ recovery efforts. For species
with extremely small populations, all reproducing adults must be
sampled, and sampling should be done repeatedly over several
years because i) sampling large quantities of seeds is impossible
when the population is small and seed production is limited,
infrequent or varies among seasons; and ii) relatively small but
more frequent samples are less harmful for a population than larger
samples taken more infrequently (Menges et al., 2004).
For rare and endangered species, and especially for PSESPs,
collecting seeds from individual plants and keeping their seeds
separately as maternal lines (families) is preferable to bulk collec-
tions. The reason is that seed banks of rare and endangered species
must be useful for in situ actions, and for these actions genetic
identity of the seeds can be very important. For example, specific
genotypes may be needed to ensure sexual reproduction in a
population, or genetic enrichment may be necessary to prevent the
negative effects of genetic drift and inbreeding. Furthermore, only
collections organized by family can be used for analyses of the
species genetic structure, identification of evolutionarily signifi-
cant units, assessments of gene flow and other important genetic
information.
Even for relatively large populations the number of source
plants and quantities of seeds per plant can be well below target
levels. For PSESPs with infrequent and/or limited seed production,
the quantities required for successful reintroduction cannot be
collected in natural populations even after multiple visits and
require an intermediate step of propagation. Thus, a good approach
would be to distinguish short- and long-term seed collections
(Volis, 2015). The goal of the long-term collection is to create a
“strategic” source of germplasm that can be used for studying
species biology, propagation and renewal, but not for in situ actions.
The seeds stored in short-term collection, on the contrary, will be
used exclusively for in situ actions either directly or after
propagation.
7. ex situ: living collections
Living collections are an important element of modern conser-
vation programs and botanical gardens are the major depositories
of valuable living material for conservation. The Chinese Academy
of Sciences has drafted and, in 2002, began implementation of a 15-
year ex situ master plan to conserve the diversity of native Chinese
plants in botanical gardens. Its main goals include increasing the
number of native protected species to 21,000, enhancing garden
collections of rare and endangered plants, as well as the creation of
five new regional and nine specialized gardens (Huang et al., 2002).
There are several living collections strongly oriented towards
endangered and rare species in China, such as Xishuangbanna
Tropical Botanical Garden, South China Botanical Garden and
S. Volis / Plant Diversity 38 (2016) 45e5248
Kunming Botanical Garden. These and 13 smaller Chinese gardens
provide shelter to the threatened species and participate in species-
oriented conservation programs. For example, A. yangbiense, rep-
resented in nature by only five individuals, has been planted, hand-
pollinated and the resulting seeds used to produce more than 1600
saplings nowgrowing in the Kunming Botanical Garden (Yang et al.,
2015a). Similarly, 1300 saplings of Q. sichourensis, 400 saplings of
Manglietia ventii and 100 saplings of M. sinica represented by
eleven, ~200 and 52 individuals in nature, respectively, were pro-
duced in the Kunming Botanical Garden and have been used in
different conservation actions (Wang et al., 2015; Weibang Sun,
personal communication). Another example is Vatica guangxiensis,
an endangered species for which about 90 individuals from three
remaining populations were successfully transplanted to Xish-
uangbanna Tropical Botanical Garden (Li et al., 2002).
However, utility and overall capacity of botanical gardens for
maintaining living collections of threatened species should not be
overestimated. One known problem is poor management, e.g.
representation of species by only a few individuals, lack of infor-
mation on accession sampling locality and mislabeling (Hurka,
1994). Another potential problem is the risk of spontaneous hy-
bridization when related species, sub-species or ecotypes are
grown in close physical proximity in the garden. The latter seriously
undermines utilization of botanic garden ex situ collections for
propagation because open-pollinated offspring may lack genetic
integrity and harbor maladaptive gene combinations (Maunder
et al., 2004). Finally, botanical gardens have obvious limitations in
the number of individuals per species they can maintain. These
issues strongly limit the utility of botanical garden living collections
for conservation. Space limitations usually preclude achieving even
the minimum recommended sample size of 15 individuals neces-
sary to capture an acceptable level of genetic variation (Namoff
et al., 2010).
8. Integration of ex situ and in situ
The utility of ex situ collections via storage and propagation of
plant material that can later be used for in situ actions has been
recognized, but the obvious space and logistical limitations of ex
situ collections present well-known challenges (Hamilton, 1994;
Schoen and Brown, 2001; Maunder et al., 2004; Volis and
Blecher, 2010). This has motivated a search for an efficient inte-
gration of these two approaches by creating living collections of
needed capacity under natural, semi-natural or artificial conditions.
Two concepts of integrative conservation that suit PSESPs are
“forest gene banks” (Uma Shaanker and Ganeshaiah, 1997; Uma
Shaanker et al., 2001; Uma Shaanker et al., 2002) and “quasi in
situ” (Volis and Blecher, 2010; Volis, 2015). The former concept
proposes use of a particular existing population as an in situ sink
into which genetic material from several source sites is introduced
and maintained. Thus the genetically diverse sink population
serves as a repository of the species gene pool and, at the same
time, allows for random interbreeding. Although this approach
cannot be used in cases when introduction of non-locals may lead
to outbreeding depression, in situations where plants originate
from the same climatic zone and similar biotic environments it can
1) greatly improve the local populations genetic variation and
eliminate inbreeding depression; and 2) provide a large quantity of
vigorous seedlings (due to heterosis) for creating new and rein-
forcing existing populations. The second concept proposes the
creation of new, as opposed to existing populations, as depositories
of genetically variable source material. The site for such living
collections should contain individuals from populations sharing the
same climatic zone and biotic/abiotic environment, have natural or
semi-natural conditions and be protected.
Use of seeds for introduction is known to be ineffective
compared with seedlings (Guerrant and Kaye, 2007; Godefroid
et al., 2011). Raising large number of seedlings from seeds in
botanical gardens or nurseries may not always be possible for lo-
gistic reasons. To obtain large quantities of seedlings required for in
situ actions, two approaches can be used. “In situ seedling banks”
(Pritchard et al., 2014) are created by sowing seeds andmaintaining
seedlings in the forest understory in a convenient, reduced space.
This approach has certain advantages which make it easy to apply,
including the wide range of forests that can be used, e.g., natural,
degraded or planted forests, not excluding monoculture tree plan-
tations. The critical points for this approach are high seed viability
and germination rate, and low requirements for successful germi-
nation. The other limitations of this approach are that seedlings
cannotwithstand a long time in the shady understorey and advance
to saplings, and intense seedling herbivory (Benitez-Malvido et al.,
2005). Another approach is to use wildlings. Although this
method cannot be applied to those PSESPs that suffer from germi-
nation failure, it can be useful for other PSESP species. For example,
intensive seed production of Liriodendron chinense trees planted in
Gaowangjie Nature Reserve along a local road gave rise to dense
stands of seedlings and saplings in proximity to the mother plants.
Thesewildlings can be used for the creation of new populations of L.
chinense in this area. Phoebe bournei, which is represented by many
reproducing trees planted andmaintained by farmers in a village of
Baojing County, provides another example. The fruits produced are
dispersed by birds into the surrounding village forest, where they
readily germinate and grow to seedlings. However, due to apparent
anthropogenic disturbance (grazing and cutting for firewood),
which has altered the forests environmental conditions, the seed-
lings do not develop into saplings. Thus, P. bourneiwildlings, which
have no future in this environment, can be used for creation of new
populations in a more suitable natural location.
Propagation of material for threatened species outside botanical
gardens in China is currently done at the national field germplasm
nurseries and plant introduction bases established by National
Environmental Protection Agency specifically for this purpose
(Division of Plant Conservation of the State Forestry
Administration, 2005). Currently, there are 32 germplasm nurs-
eries and 255 introduction bases. However, there is a very limited
recognition of the importance of living collections in semi-natural
and natural environments that serve both as depositories preser-
ving species genetic variation and sites for seed propagation (but
see Sun, 2013). The only such conservation project in China I am
aware of is the reintroduction program on M. ventii. In this project,
after propagation in the nursery, 300 saplings were planted in a
semi-natural environment near natural population in Pingbian
(Honghe prefecture, Yunnan province) (Weibang Sun, personal
communication).
9. in situ management
The Convention on Biological Diversity (CBD, 1994) defines in
situ conservation as “the maintenance and recovery of viable
populations of species in their natural surroundings”. A naive and
over simplistic view that once dominated among conservation
biology practitioners was that if populations are legally protected
their long-term survival is guaranteed. This, however, turned out to
be far from true due to the fact that virtually all natural systems
preserved in nature reserves represent some degree of human-
induced changes that disrupted previously existing species in-
teractions and ecological processes. Apart from this, fragmentation
and environmental degradation reduced population sizes of many
species below the viability threshold. Such populations are doomed
to extinction even under the strictest protection in a reserve. Thus,
S. Volis / Plant Diversity 38 (2016) 45e52 49
for in situ conservation to be effective it must be based on proper
understanding of ecological processes within an ecosystem and
population dynamics of threatened species. If necessary, actions
must be implemented, including reestablishment of extinct or
reinforcement of critically declined populations. But in many cases
even this is not enough. When a population can no longer sustain
its existence this indicates that the habitat has deteriorated and
requires action, too. For example, analysis of regeneration in the
only natural population of M. glyptostroboides revealed that in the
last 41 years, habitat changes caused by detrimental activities of
human residents (cultivation of profitable plants in the understory,
selective cutting and harvesting of wood for fuel) have effectively
ended recruitment of M. glyptostroboides (Tang et al., 2011). The
latter means that neither strict protection nor reinforcement ac-
tions will rescue this population. Without restoring conditions that
once were present in this habitat and under which natural germi-
nation was occurring normally (as evidenced by Chu and Cooper,
1950), the population has no chance of survival. Thus, in situ con-
servation of threatened species requires identifying the habitats in
which they can maintain viable populations, and then protecting
both the habitat and the species through carefully designed man-
agement. This especially applies to PSESPs. Modern conservation in
situ includes not only protection of the population or group of
populations within a protected area or habitat, but also involves,
after identification of a threat, the preparation and implementation
of management plans to eliminate the threat and recover the
population(s).
For most of the threatened species with PSESPs, reinforcement
(IUCN, 1998), i.e. supplementation of existing populations to
enhance population viability (increase in population growth rate
and decrease in probability of extinction) would be the optimal
option, but only if the remaining populations are located in pro-
tected and non-degraded areas. If these locations are unprotected
they are almost inevitably doomed to disappearance as a result of
continuing anthropogenic disturbance. Supplementation must be
aimed at restoring or improving reproduction and regeneration, for
which necessary measures can be the introduction of plants of
particular gender to correct the sex ratio in a population, and of
adults needed to increase the pollinator visitation rates, or seed-
lings/saplings to rejuvenate the degraded populations. Thematerial
for reinforcement must originate either from the same location or
from geographically closest population(s) within the same habitat
and be genetically diverse.
Reintroduction, i.e., placement of plant material into an area
where it occurred in the past, should be used for the species that
went extinct in the wild, or for which natural populations are
located in unprotected and rapidly deteriorating environments,
while locations with suitable environments for these species exist
in protected areas within the known species range. Translocation,
i.e. movement of plantmaterial to a seemingly suitable areawith no
documented past history of its existence, is the conservation action
used to prevent species extinction when there is no remaining area
left within a species historic range able to sustain viable pop-
ulation(s) (IUCN, 1998; Hoegh-Guldberg et al., 2008). Habitats
suitable for the species may exist outside of the species recorded
distribution but be unoccupied due to dispersal limitations or se-
vere fragmentation of previously continuous habitat. In both rein-
troduction and translocation, creation of viable new populations
requires prior knowledge of the species biology, including its
reproduction, demography, environmental requirements and
ecological interactions. In both actions the major criteria for eval-
uating the suitability of a site for reintroduction are ecological
similarity with locations of extant populations and protection. For
many PSESPs, however, the assumption that similarity to extant
populations is the best criterion for successful establishment of a
reintroduced population can be misleading, because their extant
populations can be located in fragmented and degraded environ-
ments that do not support positive or stable population growth
(Maschinski and Wright, 2006). In such cases, the reintroduction/
translocation decisions must be based on detailed knowledge of
historic species range, the ecological requirements of the species
and habitat conditions at potential reintroduction sites. Valuable
information for estimating suitability of a potential site for the
endangered PSESPs can provide, on one hand, a comparison of
ecological factors in locations still occupied by the species and lo-
cations where the species went extinct, and, on the other hand, a
comparison of these factors in locations with PSESPs and in loca-
tions where the population size exceeds viability threshold (if the
latter still exist). Identification of the habitats most suitable for the
target species can utilize species distribution modeling, experi-
mental introduction, or both. Distribution modeling is useful for
broad categorizations of potential habitat, but for species with very
limited distribution, where the importance of microhabitat condi-
tions is apparent and there is a shortage of information on prior
distribution (as the case with many PSESPs), only actual introduc-
tion can efficiently identify the species realized niche. Thus, for
PSESPs we strongly recommend the experimental approach, i.e.
experimental introduction across multiple (micro)sites within the
current or documented historic species range (reintroduction), or
within the presumed ecological niche of the species (translocation)
(Fiedler and Laven, 1996; Falk et al., 1996; Maschinski et al., 2004;
Maschinski and Wright, 2006; Guerrant and Kaye, 2007; Volis
et al., 2010, 2011; Rünk et al., 2014).
For threatened PSESPs, source material for reintroduction or
translocation should come from more than one population to
prevent inbreeding depression, and these populations locations
should have close environmental and ecological similarity with the
recipient locations. A match of donor and recipient locations crucial
for successful introduction can be difficult to recognize with cer-
tainty. For example, sites that appeared suitable based on expert-
opinion at the time of introduction turned out to differ in ecolog-
ical similarity, and as a result success of the introduction varied
(No€el et al., 2011).
Based on the latest theoretical developments in estimating safe
number of introduced families and individuals, the effective pop-
ulation sizes should be at least 100 families and 1000 individuals,
with a ratio for conversion of effective into census population size
of 0.1e0.2 as the first approximation (Frankham et al., 2014). For
many PSESPs this required number of families will be impossible to
achieve due to the small number of reproducing adults in extant
populations, but the required number of individuals
(5000e10,000), derived from all available mother plants, can be
achieved following proper propagation.
It must be noted that efficient conservation of a threatened
species is impossible without preparing some kind of Action Plan
specifying all the types of intervention needed for species recovery,
such as population reinforcement, translocation or habitat resto-
ration. The level of management intervention will depend on the
nature and degree of the threats to which the populations/habitats
are exposed, ranging from just monitoring to intensive recovery
actions. These interventions can include weeding, eradication of
exotic species, assisted pollination to increase seed set, removing
risks to seedling recruitment, predator and pest control, aug-
menting dispersers, and reinforcement of populations by artificially
or naturally propagated material (Heywood, 2015).
10. Information sharing
Good knowledge of the species distribution is a prerequisite for
efficient conservation of threatened species. The Global
S. Volis / Plant Diversity 38 (2016) 45e5250
Biodiversity Information Facility (GBIF, http://www.gbif.org/),
which collates occurrence records of species from hundreds of or-
ganizations, is an easily searchable database that should be adopted
as the major database for depositing data on PSESP distribution.
However, although important, occurrence data is only a part of the
information needed for an Action Plan. Other crucial information
includes population demographic structure, species biology, and
descriptions of the species habitat. Equally important is access to a
geo-referenced database of nature reserves and other types of
protected areas (Wu et al., 2011). In the case of PSESPs, access to this
information is vital as decisions making must be quick to prevent
species extinction. Information on active or completed conserva-
tion programs is very important for coordination of conservation
efforts and for interactive learning. Poor information sharing due to
an inadequate system for disseminating/obtaining information
may significantly hinder conservation of PSESPs (Meek et al., 2015).
One solution is the creation of a searchable database and repository
for conservation-related information, e.g., species management-
related manuscripts, reports, and expert opinions.
11. Conclusions and recommendations
1. Defining conservation status of PSESPs must not be based either
on population decline or extant species range, because this in-
formation can be misleading. Instead, the decisions must be
based on population sizes (number of reproducing individuals)
and population demographic structure (whether it is viable or
not).
2. Identification of a threat requires a preliminary demographic
survey and assessment of anthropogenic disturbance followed
by properly organized studies of population demography and
the ecological requirements of the species.
3. Establishment of small-scale reserves or Plant Micro-Reserves
must be recognized as the most appropriate approach for in
situ conservation of PSESPs, although large nature reserves
should be given priority whenever possible.
4. A strong environmental education campaign aimed at local
communities (especially children) is needed to create awareness
and appreciation of rare species value beyond their practical
use.
5. ex situ collections must not only represent well the species ge-
netic diversity during storage but also ensure availability of
stored germplasm in future in situ recovery efforts. Collecting
from individual plants and keeping their seeds separately as
maternal lines (families or accessions) should be strongly
encouraged over bulk collections.
6. Seed banks and botanical gardens must allocate more resources
and space to PSESPs and more actively participate in PSESP
conservation programs.
7. Usage of integrated ex situ e in situ approaches must be a norm
in every conservation project. The living collections in natural or
semi-natural environments must serve as depositories preser-
ving species genetic variation, and as seed propagation sites.
8. in situ conservation must be based on proper understanding of
ecological processes within an ecosystem and population dy-
namics of PSESPs. After identifying the habitats in which a
species can maintain viable populations, an Action Plan must
follow, specifying the carefully designed management needed
for protecting both the habitat and the species. The latter can
include population reinforcement, translocation or habitat
restoration.
9. There must be a proper sharing of information on species
occurrence, and active or completed programs for coordination
of conservation efforts and for interactive learning. The latter
requires the creation of a searchable database and repository for
conservation related information, e.g. species management-
related manuscripts, reports, and expert opinions.
Acknowledgment
This work was supported by the CAS/SAFEA International Part-
nership Program for Creative Research Teams. I am grateful to
Weibang Sun and two anonymous reviewers for their comments
and Linda Olsvig-Whittaker for editing the manuscript English.
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