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Potential Challenges of Climate Change to Orchid
Conservation in a Wild Orchid Hotspot
in Southwestern China
Hong Liu
1,2,3,8
&Chang-Lin Feng
4
&Yi-Bo Luo
5
&
Bao-Shan Chen
3
&Zhong-Sheng Wang
6
&
Hong-Ya Gu
7
1
Department of Earth and Environment, Florida International University, 11200 SW 8th Street, Miami, FL
33199, USA
2
Center for Tropical Plant Conservation, Fairchild Tropical Botanic Garden, Coral Gables, FL, USA
3
Guangxi Key Laboratory of Subtropical Bioresources Conservation and Utilization, Guangxi University,
Nanning, China
4
Experimental Center of Tropical Forestry, Chinese Academy of Forestry, Pingxiang, China
5
State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of
Sciences, Beijing, China
6
Laboratory of Forest Ecology and Global Changes, School of Biological Sciences, Nanjing University,
Nanjing, China
7
College of Biological Sciences, Beijing University, Beijing, China
8
Author for Correspondence; e-mail: hliu@fiu.edu
Published online: 26 March 2010
#The New York Botanical Garden 2010
Abstract Southwestern China including Guangxi Province is one of nine world
hotspots for orchid. Warming in the region in the past century was around 0.5°C,
slightly lower than the global average of 0.7°C, while rainfall has remained the
same. It is projected that the warming trend will continue for the next two centuries,
while precipitation will increase slightly, and soil moisture level will decrease. We
identify a number of threats due to climate changes to orchid community in the
Yachang Orchid Nature Reserve in Guangxi (hereafter refer to as Yachang Reserve),
a good representative of the region. Firstly, decreased soil moisture is likely to have
a negative effect on growth and survival of orchids, especially terrestrial and
saprophytic ones. Sixty eight (50%) orchid species in the Yachang Reserve are in
this category. Secondly, the greater majority of the orchids in Yachang Reserve
(72%) have populations on or close to the limestone mountain tops. These
populations are likely to shrink or even become extinct as the warming continues
because they have no higher places to which they are able to migrate. Natural
poleward migration is unlikely for these populations because of the complex terrain,
small size of the reserve and human-dominated surroundings. Species with narrow
distributions (14%) and/or small population sizes (46%) will be the most vulnerable.
In addition, populations represent the southern limit of the species (24%) are also
prone to local extinction. Thirdly, extreme rainfall events are projected to occur more
frequently, which can exacerbate erosion. This may impact orchid populations that
grow on steep cliffs. Fifty seven species (42%) of the orchids in Yachang have cliff
populations. Fourthly, the majority of orchid species have specialized insect
Bot. Rev. (2010) 76:174–192
DOI 10.1007/s12229-010-9044-x
pollination systems. It is unknown whether the change or lack of change in plant
phenology will be in synchrony with the potential phenological shifts of their
pollinators. Fifty four (40%) orchid species in Yachang Reserve flower in the spring
and are potentially subject to this threat. Finally, mycorrhizal fungi are vital for seed
germination for all orchids and important for post-seedling growth for some species. Yet
there is a lack of knowledge of the nature of mycorrhiza on all orchids in the region, and
little is known on the responses of these vital symbiotic relationships to temperature and
soil moisture. Overall, 15% of the orchid species and a quarter of the genera bear high
risk of population reduction or local extinction under the current projection of climate
change. While studies on predicting and documenting the consequences of climate
change on biodiversity are increasing, few identified the actual mechanisms through
which climate change will affect individual species. Our study provides a unique
perspective by identifying specific threats to a plant community.
Keywords Biodiversity .Climate Change .Global Change .Nature Reserve .
Orchids .Phenology .Plant Conservation .Rare Species
Introduction
The Southwestern China Orchid Hotspot and its Conservation Status
Southwestern China, consisting of Yunnan, Guangxi and Guizhou Provinces, is one
of the nine world orchid hotspots (Cribb et al., 2003). Orchid conservation issues in
the region, however, are acute. In addition to threats from rapid habitat destruction
and alteration associated with rapid economic growth and rural development during
the past three decades, Chinese wild orchids are facing destructive collecting
pressures due to large cultural, horticultural and ethnobotanical demands and the
primitive horticultural techniques in the country (Luo et al., 2003; Liu et al., 2009).
In 2004 several Chinese botanists discovered more than 100 species of orchids, some
of which with extremely large, relatively undisturbed populations, in a 220 km
2
state
forestry reserve in a remote area in northwestern Guangxi Zhuang Autonomous
Region. This area was made a provincial nature reserve soon after the discovery and
more recently, it was elevated to the status of national nature reserve, namely the
Yachang Orchid Nature Reserve (Liu & Luo, 2010). Yachang is the first nature reserve
in China, and second of its kind in the world defined by a national government
primarily on the basis of protecting wild orchids. Protection of the rich orchid resources
in Yachang, however, is not without problems, especially with the projected rapid
global climate change. In this paper we identify a few specific challenges that may be
posed by the current and projected climate changes as well as potential solutions.
The Challenges of Current Climate Change to Biological Conservation
In the past 2.5 million years, cycles of climate change driven by natural factors have
occurred over periods of decades, centuries, and millennia (Wright, 1989; Bond et
al., 1997,2001; Diaz & Markgraf, 2000). For example, over 40 glacial/interglacial
cycles were detected using oxygen-isotope analysis of ice cores from the Greenland
Potential Challenges of Climate Change to Orchid Conservation 175
ice sheet (Wright, 1989). These cycles were driven by variations in primary orbital
cycles of the Earth (Zachos et al., 2001). Abundant evidence worldwide indicates
that life on earth had responded to climate change at each of these scales in the past
(Jackson et al., 1987; Thompson, 1990; Grayson, 1993).
Darwin speculated that species migration in response to climate change had
proceeded in an orderly manner and that entire communities had shifted poleward
together as a unit (Darwin, 1859). However, studies of pollen and fossils during the
past glacial and inter glacial periods tell a different story (Miller & Brubaker, 2006).
Species responses were individualistic such that population increases or decreases did
not appear to be in synchrony with climate change, especially when climate changes
were extreme and abrupt, and non-analog ecological communities (i.e., communities
that do not exist in present time) were common (Miller & Brubaker, 2006).
How species or population respond to climate change depends on the species biology
and the geographic location of the population. In general, populations in a relatively flat
terrain migrated poleward during a warming period (Jackson et al., 1987), while those in
mountainous areas with mild slopes migrated upward along an elevational gradient
(Thompson, 1990; Grayson, 1993). However, in regions where habitats were complex,
highly patchy, and with steep and discontinuous gradients, species, especially rare
species, responded primarily with shrinking in population sizes, minor geographic
range shifts, or local extinctions (Heusser, 2000;Maschinskietal.,2006).
The current anthropogenic driven climate changes are worrisome to conservation
biologistsbecause the projected warming inthe next 100 years will result in an earth that
is hotter than most extant species have ever seen (Barnosky, 2009). In addition, the rate
of warming is at least twice as fast as what nature has experienced in the past (Davis &
Shaw, 2001;Barnosky,2009). It is therefore questionable whether current species
migration can keep up with the speed and magnitude of the warming. A case in point,
upward migrations of Andean cloud forest tree communities due to warming in the
past 5 years has been approximately 2 m/yr, less than 4 times slower than is required
to keep pace with the speed of warming (Kenneth J Feeley, Florida International
University, pers. com.). Finally current natural habitats are highly fragmented and
isolated by anthropogenic landscapes such as cities, farmlands, pastures and so on
(Barnosky, 2009). Such landscape features make natural migration, one of the main
responses to climate change, challenging if not impossible.
Hypotheses on how plants will respond to climate change are largely derived from
studies on forest canopy species, especially those with wind dispersed pollen (Miller &
Brubaker, 2006). Modern phenological monitoring also focuses primarily on common
tree species, because they are easy to observe and can be compared across a wide
range of locations (Schwartz, 2003; Chen, 2003; Zhu & Wan, 1983; Wan, 1986,
1987). The response of herbaceous understory species to climate change are, however,
largely unknown. These plants include orchids, many of which are rare and threatened.
Current and Projected Climate Change in Southwest China and its Challenges
to Orchid Conservation
The Yachang Orchid Nature Reserve is situated between 24°44′16″to 24° 53′58″N,
and 106° 11′31″to 106° 27′04″and is influenced by the subtropical climate—as is the
176 H. Liu, et al.
case with most of southwestern China (Corlett, 2009). In this region, there are
pronounced seasonal variations in both rainfall and temperature (Corlett & Lafrankie,
1998; Huang et al., 2008), with nearly 60% of the rainfall occurring in the hot summer
months and less than 10% in the cold winter months (Huang et al., 2008). Phenology
of woody plants in southwestern China is characterised by regular, annual cycles at the
individual, population, and community level (Corlett & Lafrankie, 1998; Wan, 1986,
1987), probably triggered by temperature and/or water availability (Corlett &
Lafrankie, 1998).
Records indicate that warming in southwestern China in the past 100 years was
around 0.5°C, slightly lower than the global average of 0.7°C (IPCC, 2007; Huang
et al., 2005), and the warming has been largely due to increase in winter, spring and
fall temperatures (Chen et al., 2008; He et al., 2007; Wang et al., 2008). Total annual
rainfall, on the other hand, has remained the same or has increased slightly for the
region (Huang et al., 2005; Bates et al., 2008). It is projected that the warming trend
will continue during the next two centuries in Southwest China (Jiang et al., 2005;
IPCC, 2007; Xu et al., 2009). Precipitation, on the other hand, is projected to
increase only slightly (Bates et al., 2008; Jiang et al., 2005; Xu et al., 2009), but will
not keep pace with the increase in evaporation rates due to warming (Bates et al.,
2008). As such a slight decrease in soil moisture is predicted (Bates et al., 2008).
Challenge 1—Lower Soil Moisture
Orchids are notorious for their stringent habitat requirements, a factor contributing to
their rarity (Cribb et al., 2003). The projected increase in precipitation and
evaporation rate will result in a lower level of soil moisture (Bates et al., 2008).
This will likely to impact mostly the terrestrial orchids. Sixty eight (50%) of the
orchids in Yachange are either terrestrial or saprophytic.
Challenge 2—Geographical Barriers and Limits to Natural Migration
Complex terrain and habitat fragmentation and non-availability may hinder natural
poleward migration. The Yachang Orchid Nature Reserve, as in adjacent areas in
southwestern China, is characterized by many low to medium height limestone hills
(elevations of 1,200 m or less), separated by steep valleys or rivers. Species in such
complex terrain are expected to respond primarily by shrinking in population size
(Heusser, 2000). This may happen to more than 100 species of orchids in Yachang
(73%), since they are currently growing on the mountain tops (Table 1), with no
higher places to migrate to. The most extraordinary feature in Yachang is that
populations of some orchid species are extremely large (Shi et al., 2007b; Liu et al.,
2009). Conservation of these unusually large populations is one of the conservation
priorities for the Yachang Reserve. Most of these large populations are located on or
near the hill tops. Thus, the projected warming in the region will likely threaten the
long-term persistence of these large populations unless these populations possess a
high micro-evolutionary potential which will enable them to evolve in accordance to
the environmental changes related to climate changes (Holt, 1990). This group of
species includes several species with horticultural importance or potentials, e.g.
Bulbophyllum andersonii, Coelogyne fimbriata,Cymbidium cyrprefolium, Eria
Potential Challenges of Climate Change to Orchid Conservation 177
Table 1 List of Orchids (139 species in 47 genera) in Yachang Orchid Nature Reserve
a,b
and Potential Threats from Climate Change
Species Terrestrial
c
Narrow
endemic
d
Spring
flower
e
Mountain top
population
f
Cliff
population
g
Very small
population
h
South
most
range
Risk score Genus mean
score
Acanthephippium sylhetense Lindl. Yes No Yes No No Yes No 3 3
Anoectochilus elwesii (Clarke ex Hook. f.) King &
Pnatl.
Yes No No Yes No No Yes 3 3.3
Anoectochilus moulmeinensis (Par. et Rchb. f.)
Seidenf.
Yes No No Yes No Yes No 3
Anoectochilus roxburghii (Wall.) Lindl. Yes No No Yes Yes No Yes 4
Aphyllorchis montana Rchb. f. Yes (S) No No No No Yes No 2 2
Bletilla formosana (Hayata.) Schltr. Yes No Yes Yes No Yes Yes 5 4.3
Bletilla ochracea Schltr Yes No No Yes No Yes Yes 4
Bletilla striata (Thunb. ex A. Murray) Rchb. f. Yes No Yes Yes No No Yes 4
Bulbophyllum ambrosia (Hance) Schltr. No No Yes Yes No Yes No 3 3
Bulbophyllum andersonii (Hook. f.) J. J. Smith No No Yes Yes Yes No No 3
Bulbophyllum kwangtungense Schltr. No No No Yes Yes No No 2
Bulbophyllum longibrachiatum Z. H. Tsi No Yes No Yes Yes No No 3
Bulbophyllum odoratissimum (J. E. Smith) Lindl. No No Yes Yes Yes No No 3
Bulbophyllum tianguii k. Y. Lang et D. Luo No Yes No Yes Yes Yes No 4
Calanthe argentro-striata C. Z. Tang et S. S. Ying Yes No Yes Yes Yes No No 4 3.5
Calanthe davidii Franch Yes No No No No Yes Yes 3
Calanthe hancockii Rolfe Yes Yes Yes No No Yes Yes 5
Calanthe reflexa (Kuntze) Maxim Yes No No Yes No Yes Yes 4
Calanthe sylvatica (Thouars) Lindl. No No Yes No No Yes No 2
Calanthe triplicata (Willem.) Ames Yes No Yes No No Yes No 3
178 H. Liu, et al.
Table 1 (continued)
Species Terrestrial
c
Narrow
endemic
d
Spring
flower
e
Mountain top
population
f
Cliff
population
g
Very small
population
h
South
most
range
Risk score Genus mean
score
Cephalanthera longifolia (L.) Fritsch Yes No No Yes Yes Yes No 4 4
Cheirostylis chinensis Rolfe Yes No Yes Yes No No No 3 2.5
Cheirostylis yunnanensis R. Yes No Yes No No No No 2
Cleisostoma menghaiense Z.H.Tsi No Yes No Yes Yes Yes No 4 2
Cleisostoma nangongense Z. H. Tsi No Yes No No No Yes No 1
Cleisostoma paniculatum (Ker-Gawl.) Garay No No No Yes No No No 1
Cleisostoma williamsonii (Rchb. f.) Garay No No Yes Yes No No No 2
Coelogyne fimbriata Lindl. No No No Yes Yes No No 2 3
Coelogyne flaccida Lindl. No No Yes Yes Yes Yes No 4
Cremastra appendiculate (D. Don) Makino Yes No No Yes No Yes No 3 3
Cymbidium bicolor subsp. obtusum Du Puy & Cribb Yes No Yes No Yes No No 3 3.3
Cymbidium cyperifolium Wall. et Lindl. Yes No No Yes No No No 2
Cymbidium aloifolium (L.) Sw. No No No No Yes No Yes 2
Cymbidium ensifolium (L.) Sw. Yes No No Yes No No No 2
Cymbidium faberi Rolfe Yes No Yes Yes No Yes Yes 5
Cymbidium floribundum Lindl. Yes (semi) No Yes Yes Yes No No 4
Cymbidium goeringii (Rchb. f.) Rchb. f. Yes No Yes Yes No Yes Yes 5
Cymbidium goeringii var. serratum (Schltr.) Y.S.Wu
et S.C.Chen
Yes No Ye s Ye s N o Ye s Ye s 5
Cymbidium kanran Makino Yes No No Yes No Yes No 3
Cymbidium lancifolium Hook. Yes (semi) No No Yes Yes No No 3
Cymbidium macrorhizon Lindl. Yes (S) No No Yes No No No 2
Potential Challenges of Climate Change to Orchid Conservation 179
Table 1 (continued)
Species Terrestrial
c
Narrow
endemic
d
Spring
flower
e
Mountain top
population
f
Cliff
population
g
Very small
population
h
South
most
range
Risk score Genus mean
score
Cymbidium nanulum Y. S. Wu et S. C. Chen Yes No No No No Yes No 2
Cymbidium qiubeiensis K. M. Feng et H. Li Yes Yes No Yes No No No 3
Cymbidium sinense (Jackson ex Andr.) Willd. Yes No No Yes No Yes No 3
Cymbidium tortisepalum var. longibracteatum (Y. S.
Wu & S. C. Chen) S. C. Chen & Z. J. Liu
Yes Yes Yes Yes No Yes Yes 6
Cymbidium tracyanum L. Castle No No No Yes Yes No No 2
Cypripedium henryi Rolfe Yes No Yes Yes No Yes Yes 5 5
Dendrobium aduncum Wall et Lindl. No No No No Yes No No 1 2.9
Dendrobium aphyllum (Roxb) C. E. C. Fisch No No Yes Yes No No No 2
Dendrobium aurantiacum Rchb. F. Var. denneanum
(kerr) Z. H. Tsi.
No No Yes Yes Yes No No 3
Dendrobium chrysanthum Lindl. No No No Yes No No No 1
Dendrobium devonianum Paxt No No Yes Yes Yes Yes No 4
Dendrobium fimbriatum Hook. No No Yes Yes Yes No No 3
Dendrobium hancockii Rofle No No No Yes Yes Yes Yes 4
Dendrobium henryi Schltr. No No No Yes Yes Yes No 3
Dendrobium hercoglossum Rchb. f. No No No No Yes Yes No 2
Dendrobium lindleyi Stendel No No Yes No No No No 1
Dendrobium loddigesii Rolfe No No Yes Yes Yes No No 3
Dendrobium lohohense T. Tang & F. T. Wang No No No Yes Yes Yes Yes 4
Dendrobium nobile Lindl. No No Yes Yes Yes Yes No 4
Dendrobium officinale Kimura et Migo No No Yes Yes No Yes Yes 4
Dendrobium williamsonii Day & Rchb. f. No No Yes Yes Yes Yes No 4
Epipactis helleborine (L.) Crantz. Yes No No Yes No Yes No 3 3
Eria clausa King et Pantl. No No Yes Yes Yes Yes No 4 3
Eria Corneri Rchb. f. No No No No Yes No No 1
Eria coronaria (Lindl.) Rchb. f. No No Yes Yes Yes No No 3
180 H. Liu, et al.
Table 1 (continued)
Species Terrestrial
c
Narrow
endemic
d
Spring
flower
e
Mountain top
population
f
Cliff
population
g
Very small
population
h
South
most
range
Risk score Genus mean
score
Eria lasiopetala (Willd.) Ormerod No No Yes Yes Yes No No 3
Eria obvia W.W.Smith No No Yes Yes Yes Yes No 4
Eria rhombodalis T. Tang et F. T. Wang No No Yes Yes Yes No No 3
Eria spicata (D. Don) Hand.-Mazz. No No No Yes Yes Yes No 3
Eulophia bracteosa Lindl. Yes No Yes No No Yes No 3 2.7
Eulophia flava (Lindl.) Hook. F. Yes No Yes No No No No 2
Eulophia zollingeri (Rchb. f.) J. J. Smith Yes (S) No Yes Yes No No No 3
Flickingeria albopurea Seidenf No No No Yes Yes No No 2 2.7
Flickingeria angustifolia (Bl.)Hawkes No No No Yes Yes Yes No 3
Flickingeria calocephala Z. H. Tsi et S. C. Chen No Yes No Yes Yes No No 3
Galeola lindleyana (Hook. f. et Thoms.) Rchb. f. Yes (S) No No Yes No No Yes 3 3
Gastrodia eleta Bl. Yes (S) No No Yes No No Yes 3 3
Geodorum densiflorum (Lam.) Schltr. Yes No No No No No No 1 1.7
Geodorum eulophioides Schltr. Yes Yes No No No Yes No 3
Geodorum recurvum (Roxb.) Alston Yes No No No No No No 1
Goodyera henryi Rolfe Yes No No No No No No 1 1.5
Goodyera schlechtendaliana Rchb. f. Yes No No Yes No No No 2
Habenaria ciliolaris Kraenzl. Yes No No Yes No No No 2 2.6
Habenaria davidii Franch. Yes No No Yes No Yes Yes 4
Habenaria dentata (Sw.) Schltr Yes No No Yes No No No 2
Habenaria fordii Rolfe Yes Yes No Yes No No No 3
Habenaria petelotii Gagnep. Yes No No No No Yes No 2
Potential Challenges of Climate Change to Orchid Conservation 181
Table 1 (continued)
Species Terrestrial
c
Narrow
endemic
d
Spring
flower
e
Mountain top
population
f
Cliff
population
g
Very small
population
h
South
most
range
Risk score Genus mean
score
Herminium bulleyi (Rolfe) Tang et Wang Yes Yes No Yes No Yes Yes 5 3.5
Herminium lanceum (THunb.) Vuijk Yes No No Yes No No No 2
Kingidium braceanum (Hook. f.) Seidenf. No Yes No Yes No Yes No 3 3
Lecanorchis multiflora J. J. Smith Yes (S) No No No No Yes No 2 2
Liparis bootanensis Griff. No No No No Yes Yes No 2 2.2
Liparis cordifolia Hook. f. Yes No No Yes No No Yes 3
Liparis distans C. B. Clarke No No Yes Yes Yes No No 3
Liparis esquirolii Schltr. No Yes No Yes Yes Yes Yes 5
Liparis inaperta Finet No No No Yes Yes No No 2
Liparis japonica (Miq.)Maxim. No No No No Yes Yes Yes 1
Liparis nervosa (Thunb.ex A. Murray) Lindl. No No Yes No Yes Yes No 3
Liparis nigra Seidenf. No No Yes Yes No No No 2
Liparis stricklandiana Rchb.f. No No No No No Yes No 1
Liparis viridiflora (Bl.) Lindl. No No Yes No Yes No No 2
Luisia teres (Thunb. ex A. Murray.) Bl. No No Yes Yes No No No 2 2
Malaxis acuminata D. Don Yes No No Yes No No No 2 2
Malaxis biaurita (Lindl.) Kuntze Yes No No Yes No No No 2
Malaxis latifolia J. E. Smith Yes No No Yes No No No 2
Malaxis monophyllos (L.) Sw. Yes No No No No Yes Yes 3
Malaxis purpurea (Lindl.) Kuntze Yes No No No No No No 1
Nervilia fordii (Hance) Smitin Yes No No No No No No 1 1.5
Nervilia plicatao (Andr.) Schltr. Yes No No Yes No No No 2
Oberonia ensiformis (J. E. Smith) Lindl. No No No Yes Yes No No 2 2
Oberonia myosurus (Forst. f.) Lindl. No No No Yes Yes No No 2
Pachystoma pubescens Bl. Yes No Yes No No Yes No 3 3
Panisea cavalerei Schltr. No Yes Yes Yes Yes No No 4 4
Paphiopedilum dianthum T. Tang et F.T.Wang No Yes No Yes Yes Yes No 4 4.3
182 H. Liu, et al.
Table 1 (continued)
Species Terrestrial
c
Narrow
endemic
d
Spring
flower
e
Mountain top
population
f
Cliff
population
g
Very small
population
h
South
most
range
Risk score Genus mean
score
Paphiopedilum hirsutissimum (Lindl. et Hook.) Stein Yes (semi) No Yes Yes Yes No No 4
Paphiopedilum micranthum T. Tang et F. T. Wang Yes (semi) Yes Yes Yes Yes Yes No 6
Peristylus affinis (D.Don) Seidenf. Yes No No No No Yes No 2 2.7
Peristylus flagellifer (Makino) Ohwi No Yes No Yes No Yes Yes 4
Peristylus mannii (Rolfe) Makerjee No No No Yes No Yes No 2
Phaius flavus (Bl.) Lindl. Yes No No Yes No No No 2 2.5
Phaius tankervilleae (Banks ex L’herit.) Bl. Yes No Yes Yes No No No 3
Pholidota cantonensis Rolfe No No Yes Yes Yes No No 3 3
Pholidota leveilleana Schltr. No Yes No Yes Yes Yes No 4
Pholidota missionariorum Gagnep. No Yes No Yes Yes No No 3
Pholidota yunnanensis Rolfe No No No Yes Yes No No 2
Pleione yunnanensis (Rolfe) Rolfe Yes No Yes Yes No No No 3 3
Pogonia japonica R. Yes No No No No Yes Yes 3 3
Robiquetia succisa (Lindl) Seidenf. No No No No Yes No No 1 1
Spathoglottis pubescens Lind. Yes No No Yes No Yes No 3 3
Spiranthes sinensis (Pers.) Ames Yes No No Yes Yes No No 3 3
Tainia angustifolia (Lindl.) Benth. et Hook. f. Yes No No Yes No Yes No 3 3
Potential Challenges of Climate Change to Orchid Conservation 183
Table 1 (continued)
Species Terrestrial
c
Narrow
endemic
d
Spring
flower
e
Mountain top
population
f
Cliff
population
g
Very small
population
h
South
most
range
Risk score Genus mean
score
Tainia macrantha Hook. f. Yes Yes No No No Yes No 3
Thelasis pygmaea Hook. f. No No Yes Yes Yes Yes No 4 4
Vanda concolor Bl. No No Yes No No No No 1 1
Vandopsis gigantea (Lindl.) Pfitz No No Yes No No No No 1 1
Vanilla siamensis Rdfe ex Downie No No Yes Yes Yes No No 3 3
Zeuxine goodyeroides Lindl. Yes No No Yes No Yes No 3 3.5
Zeuxine strateumatica Yes No Yes Yes No Yes No 4
Number of species (%) 72
(51.8%)
20
(14.4%)
55
(39.6%)
101
(72.7%)
58 (41.7%) 65 (46.8%) 34
(24.5%)
33 (23.7%
with a score
≥4)
7 (14.9% with
a score ≥4)
a
Species list were complied based on “The Comprehensive Investigation Report of Guangxi Yachang Orchids Natural Reserve”by The Comprehensive Scientific Investiation
Team of Guangxi Yachang Orchid Nature Reserve (2007), “Picture book of Wild Orchids in Guangxi Yachang”by Luo et al. (2008), and Feng et al. unpublished data
b
Information on global distribution is derived from “Flora of China, Orchidaceae”by Chen et al. (2009b)
c
Saprophytes are considered terrestrial. (S) indicates Saprophytes, and (semi) indicate populations in Yachang are found to be both terrestrial and epiphytic
d
A species is considered a narrow endemic if its current range include only Guangxi, Guizhou, Yunnan and northern Vietnam or fewer areas because these areas are adjacent to
one another and share similar limestone and climatic characteristics
e
Spring flower species are those whose flowering periods include any month from January to April
f
Populations found at 1,200 m or above is considered mountain top populations because the geographical feature of Yachang Reserve, i.e. the area is composed of many low- and
mid-elevation mountains
g
Species with cliff populations are those grow on steep rocky surfaces in Yachang Reserve
h
Species are found in less than 3 locations within the Yachang Reserve and each has less than 100 reproducing plants
184 H. Liu, et al.
coronaria, Liparis viridiflora, L. chapaensis, L. cordifolia, Oberonia myosurus,
Paphiopedilum hirsutissimum,Panisea calalerei, Pholidota yunnanensis, and
Vanilla siamensis.
Sixty five orchid species (47%) currently consist of very small populations in
Yachang, and 20 species (14%) have narrow distributional ranges. These orchids, which
face high risk of extinction without the climate change (Rabinowitz, 1981), may also
face high level of threat from climate change, especially if they are found on hill tops.
Species in this category include Bulbophyllum tianguii, Cymbidium goeringii,C.
longibracteatum,C. nanulum,C. tracyanum,Dendrobium officinale,P. micranthum
(Table 1). In addition, populations that represent the southern limit of the species
distributions (34 orchid species or 25% in Yachang) are also vulnerable to local
extinction (Lavergne et al., 2006). Yachang Orchid Nature Reserve is located in
transitional zone of warm subtropical to cool subtropical climate and harbors some
southern-most populations of temperate orchid species (Table 1). For example, Yachang
is one of the few places where Paphiopedilum, a genus of tropical lady’sslipper
orchids, co-occur with the temperate lady’s slipper orchids, Cypripedium species. The
only Cypripedium species in Yachang, C. henryi are found in very small numbers on a
hill top. This population, being small, on hill top, and at the south limit of the species’
distribution, is certainly the one most vulnerable to local extinction (Table 1).
Challenge 3—Erosion Induced by Extreme Weather
Extreme rainfall events are predicted to occur more frequently even though overall
rainfall has been and is projected to increase only slightly in the region (IPCC, 2007,
Chen Yegou, Guangxi Meteorology Bureau, pers. comm.). Extreme rainfall event
can accelerate erosion. Nearly half of the orchid species in Yachang (42%) have
populations on steep cliffs (Table 1) that have probably adapted to the disturbance
caused by frequent runoffs associated with rain and occasional erosions. However,
increased degree and frequency in erosion may negatively affect the cliff
populations. Orchids in this category include Coelogyne fimbriata,Eria coronaria,
E. rhomboidalis,E. spicata,Paphiopedilum dianthum,P. hirsutissimum,Pholidota
yunnanensis,Oberonia ensiformis, O. myosurus.
Challenge 4—Flowering Responses to Climate Change
The fourth challenge for orchid conservation in the region relating to climate
changes is the potential mismatches in phenology between orchids and their
pollinators due to spring warming.
The majority of orchid species have specialized insect pollination system, relying
on one to a few pollinator species (Cingel, 2001; Tremblay et al., 2005). This is
likely to be the case for orchids in Yachang. Pollination systems of 10 orchid species
in Yachang have been studied and all are pollinated by a single species of pollinator
(Cheng et al., 2007,2009; Shi et al., 2007a,2008,2009; Shangguan et al., 2008; Luo
et al., unpubl data). One species (Geodorum densiflora) can also self-pollinate,
possibly requiring the assistance of rain (Liu et al., unpbl. data).
Long-term phenological data are rare for orchid species (Willis et al., 2008).
However, fluctuations in flowering time due to fluctuations in spring temperatures
Potential Challenges of Climate Change to Orchid Conservation 185
have been well documented for many temperate woody species and a limited
number of herbaceous species (Wan, 1986,1987; Chen, 2003; Dose & Menzel,
2006). Early initiation of flowers and other spring events due to the current global
warming has also been reported for many temperate species (Fitter & Fitter, 2002;
Menzel et al., 2006; Miller-Rushing & Primack, 2008). Little data is available on the
response of subtropical species response to global climate change. Nevertheless,
phenology of some subtropical species can be temperature driven, especially in areas
with pronounced annual fluctuation in temperature (Corlett & Lafrankie, 1998; Feng
et al., unpbl. data). Warming in winter and spring are therefore likely to affect the
flowering phenology of some orchid species in southwestern China, including those
in the Yachang Reserve.
The majority of orchid pollinators are insects (Pemberton, 2010). Yet, our
knowledge of insect responses to current climate change is just beginning to
accumulate. There is evidence that some butterflies and moths have migrated
poleward or upwards within the past 5 decades in responding to the warming
(Parmesan et al., 1999; Chen et al., 2009a). European honey bees (Apis mellifera)
have been reported to respond to spring temperature fluctuations by coming out of
their annual dormancy either early or late in the warm or cool springs, respectively,
in temperate China (Wan, 1986,1987). There is a need for studies to determine
whether the Chinese honey bee (A. cerana), a major orchid pollinator in
southwestern China, and other insect pollinators have similar responses to changes
in spring temperatures.
The ability to track global warming varies among species (Miller-Rushing &
Primack, 2008). It is unknown whether the change or lack of change in plant
flowering phenology will be in synchrony with its pollinator’s activity. A simulation
of the impacts of global warming on generalist plant-pollinator webs indicated
disruptions and even extinction of some of these crucial interactions (Memmott et
al., 2007). Climate change might have induced asynchronized shifts in space and
time between peak flowering of the British orchids and the peak flight times of the
orchid’s pollinators (David Roberts, Kew, pers. comm.). It is logical to expect that
specialized pollination relationships, such as the ones borne by orchids and their
pollinators, will be more vulnerable to such mismatch than the more generalist
interactions (Ashworth et al., 2004; Dixon, 2009). This vulnerability is due in part to
the skewed relationships between orchids and pollinators, with the orchid being
much more dependent on the pollinators than vice versa (Dixon, 2009; Pemberton,
2010; Vereecken et al., 2010). Fifty five species or 40% of orchids in Yachang
flower in the Spring and are therefore likely to be impacted the most (Table 1), these
include Cymbidium faberi, C. floribundum, C.goeringii, C. longibracteatum,
Geodorum densiflora, G. eulophioides, G. recurvum,Paphiopedilum hirsutissimum,
and P. micranthum, to name a few.
Challenge 5—Lack of Knowledge on Response of Orchid-Fungi Mycorrhizal
Relationship to Climate Changes
The symbiotic relationship between orchid and mycorrhizal fungi is considered to be
critical in natural seed germination and seedling growth of all orchid species
(Rasmussen & Rasmussen, 2009). This relationship is also essential in post-seedling
186 H. Liu, et al.
growth in many orchid species (Dearnaley, 2007; Rasmussen & Rasmussen, 2009;
Liu et al., 2010, this volume). However, despite the significant advance made on
orchid mycorrhiza research in the past two decades (Rasmussen & Rasmussen,
2009), our knowledge on orchid-mycorrhizal fungi relationships is limited,
particularly in the case of Chinese wild orchids (Liu et al., 2010, this volume).
The function and stability of orchid mycorrhiza can be sensitive to environmental
factors (Batty et al., 2001). However, it is not known whether and how the role of
mycorrhizal fungi in orchid germination and growth will be maintained with rising
temperature and reduced soil moisture.
Potential Solutions
A number of actions can be taken to alleviate the threats imposed by climate change
on orchids in this orchid hotspot.
Ranking Vulnerability of Species Due to Climate Change
Prioritizing the species based on vulnerability of wild orchids to climate change can
be performed using their habit, flowering time, population size, distribution patterns
in elevational range as well as their geographic range as indicators. We attempted
such a ranking system in Table 1. We first assigned a value of 1 to each positive
answer of the threatening factors listed, and then summed the values for each
species. Species with a score of four or greater in this exercise were considered
highly vulnerable. Overall, nearly a quarter of the species facing high risk and they
spread across 19 genera. Each of these threats impacts 14% to 72% of the species,
and each species is threatened by at least one of these factors (Table 1).
We also calculate the average risk for each genus in Yachang Reserve to see
whether there is a risk pattern in this higher taxonomic level. There are 7 genera
whichhaveameanscoreof4orhigher,withBletilla,Cypripedium,and
Pahiopedilum most at risk (risk scores of 4.3 and above). Both Dendrobium and
Cymbidium, two genera of high market values for horticultural and Chinese
medicinal use, respectively, are not at particularly high risk, yet, but some members
in these genera are (Table 1). Whether a species is subject to high collecting pressure
can influence the species’extinction probability. We did not list this factor because it
is independent of climate change. One could also weigh each of the factors
differently based on the degree of its potential impacts on population dynamics.
Restoration experiments should be started on the most vulnerable species.
Establishing Long-Term Phenological Monitoring for Plants and Pollinators
Currently, rangers are assigned to patrol areas where large populations of orchids
occur. These rangers may be trained to collect phenological data using data sheet
designed by, and under the supervision of, conservation ecologists. Some rangers
have already been trained to assist in long-term population monitoring of large
populations in Yachang Reserve. This can also be supplemented by phenological
studies from the herbarium specimens. If there are indeed mismatches in
Potential Challenges of Climate Change to Orchid Conservation 187
phenological responses to spring temperature fluctuations between orchids and their
pollinators, it will be useful to know the magnitude of the mismatch and how this
may contribute to the overall population decline.
Assisted Migrations
As mentioned earlier, natural poleward or upward migration of orchids, especially
mountain top species, would be very difficult if not impossible for orchids in the
Yachang Reserve because, like many other protected areas in the world, it is of small
size (18 km south-north, by 26 km west-east), and surrounded by, or interspersed
with, disturbed or human-dominated landscapes. In addition, there are 89 mountains
of elevation 1,000 m or higher. However, only 19 of these are above 1,500 m.
Nevertheless, all hills are not equally occupied by orchids. Thus, micro- and macro-
habitat analyses, including using remote sensing data, will be useful to determine
what are suitable and projected suitable sites and vegetation successional stages.
Projected suitable but unoccupied sites can be used as experimental artificial
planting or restoration sites. Such restoration approach can provide opportunity to
determine how orchids in the area can better cope with the predicted climate
changes.
Before a network of protected areas in this orchid-rich region are established,
human-assisted migration of selected orchids to protected areas in Guizhou (to the
north of the Reserve) or to Yunnan (to the west, more inland, and with higher
mountains) provinces may be required. Human-assisted migration (alternatively
referred to as “assisted colonization”,“artificial transplantation”,or“managed
translocation”) of rare and endangered species in relation to climate change has been
advocated and implemented elsewhere (Fox, 2007; McLachlan et al., 2007; Zimmer,
2007; Hoegh-Guldberg et al., 2008; Richardson et al., 2009). However, such efforts
will also require co-ordination among provinces, which can be challenging. In
addition, habitat destruction is worse in Guizhou than in the other two neighboring
provinces and it is questionable whether appropriate habitat can be identified there.
Nevertheless, this measure, along with assisted migration to locations within
Yachang with higher elevations, may be a good option for the narrow endemic
species, such as Bulbophyllum tianguii,Geodorum eulophioides, and Paphiopadi-
lum dianthum. Following the general rules of temperature gradient along elevational
or latitudinal gradients (Colwell et al., 2008; Jump et al., 2009), a 500 m upward or
500 km pole-ward migration will be sufficient for a species to track the 2.5°C
projected change in southwestern China for the next century (Jiang et al., 2005;
IPCC, 2007; Xu et al., 2009).
Orchid Restoration Using Symbiotic Seed Germination and Seedling Growth
Before human-assisted migration is conducted, mycorrhiza relationships should be
studied in detail for selected orchid species in Yachang Reserve. Besides identifying
the orchid mycorrhizal fungi partners and determining their roles in orchid
population dynamics, the effects of temperature and moisture on these relationships
should be investigated with other environmental variables. Transplanting symbiotic
plants (e.g. seedlings inoculated with appropriate mycorrhizal fungi) are expected to
188 H. Liu, et al.
overcome impediment from lack of adequate symbiotic fungi. Therefore, knowledge
on the identities and roles of mycorrhizal fungi of orchids will determine in part
whether such a restoration project will be successful (Dearnaley, 2007; Swarts &
Dixon, 2009, Liu et al., 2010).
Intra-Species Hybridization
Another possible tool in conservation of the orchid species is to hybridize plants
from warmer areas of a species’distribution with those in Yachang. This may
improve the heat tolerance of the local populations (Fox, 2007). However, the
microevolutionary potential of the spectacularly large populations of certain orchid
species in Yachang should be investigated before taking the hybridization approach.
Concluding Remarks
We acknowledge that some of the potential conservation measurements are
controversial. Yet, depending on the objectives of the Yachang Reserve, e.g.
preventing species from extinction, and maintaining the large populations unique
to the Reserve, they may be the best options to accomplish these goals in light of
the projected climate change. In addition to in-situ conservation options proposed
here, ex-situ conservation measures, especially seed banking of highly vulnerable
species, should be implemented to buffer species extinction (Seaton et al., 2010).
Other non-climate change related conservation measures, such as conserving
resources that pollinators depend on (Pemberton, 2010; Vereecken et al., 2010;
Bernhardt & Meier, 2010), should be promoted. For example, a wasp species
(Vespula sp.) was found to be the sole pollinator for Coelogyne fimbriata (Cheng et
al., 2009), however the wasp itself is collected by the local people for consumption.
Regulated exploitation of the wasp is one obvious measure that could be pursued by
the Reserve.
Climate change is considered to be one of the biggest threats to diversity. But in
most studies the actual mechanisms through which climate change will affect
individual species have remained ambiguous or undefined. Here we identified seven
specific threats that climate change may pose to the orchids of the Yachang Reserve
and the specific species that are most likely to be impacted. Although there are
potentially more that we did not look at, this study provides a scientific framework
for conservation workers in the southwestern China orchid hotspot to prioritize their
conservation efforts.
Acknowledgements We wish to thank Vice Governor of Guangxi, Dr. Chen Zhangliang, for his vision
to convene the Guangxi International Orchid Symposium, which stimulated this synthesis. We are indebt
to the staff of Yachang, especially Wu Tiangui and Luo Dun for their logistic support of the conservation
research in Yachang Reserve. Graduate students Lin Wuying and Ma Xiaokai from the Institute of Botany,
Chinese Academic of Sciences, Yachang staff Liu Shiyong, Deng Zhenhai, Wei Xinlian, Lan Yutian, and
Huanglan are acknowledged for their excellent field assistance. Travel support to HL, HYG, and YBL
from the Guangxi Forestry Bureau and research support to HL, YBL, BSC, ZSW and HYG from the
Guangxi Science and Technology Bureau (Chairman’s Foundation grant # 09203-04) are greatly
appreciated. Financial supports from The Mohamed bin Zayed species conservation fund (0905324) to
HL and YBL, and the Social Welfare Research Project (2005DIB6J144) of the Ministry of Science and
Potential Challenges of Climate Change to Orchid Conservation 189
Technology of the People’s Republic of China to CLF help to cover partial costs of research related to this
project. Drs. Amots Dafni, Philip Seaton, David Roberts, Richard Primack, Robert Pemberton, and
Kenneth J. Feeley provided critical reviews on earlier drafts of the ms.
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