全 文 ：温度和湿度对草果花柱卷曲的影响*
杨耀文1,2,3, 钱子刚3, 李爱荣1, 普春霞1,2,3, 刘小莉3, 管开云1**
(1 中国科学院昆明植物研究所, 云南 昆明摇 650201; 2 中国科学院大学, 北京摇 100049;
3 云南中医学院中药材优良种苗繁育中心实验室, 云南 昆明摇 650500)
摘要: 草果 (Amomum tsaoko) 为姜科植物, 有花柱卷曲机制。 研究表明温度和湿度均影响草果上举型花
和下垂型花的花柱卷曲, 相对恒定的低温和高湿可促使花柱的同步卷曲。 当 8 颐 00-19 颐 30 期间的平均温度
小于 18 益、 平均湿度大于 90%时, 花柱卷曲没有滞后现象, 卷曲的同步性较好。 当平均温度大于 18 益、
平均湿度小于 90%时, 随着温度的升高和湿度的降低, 花柱卷曲滞后愈加明显。 和上举型花相比, 下垂
型花的花柱卷曲对湿度变化更为敏感; 可能两种花型之间存在一定的分化。 居群初花期 19. 17 ~ 19. 52 益
的平均温度和 51. 00% ~ 51. 44%的平均湿度, 导致单朵下垂型花的寿命由 1 d 延长为 2 d。 温度和湿度变
化对花柱卷曲的影响导致在居群水平上没有完全形成功能上的雌雄异株, 可能影响草果的繁育和降低其适
合度。 从不同角度对花柱卷曲机制的深入研究, 有助于更好的探索其起源和进化。
关键词: 草果; 温度; 湿度; 花柱卷曲; 花期延迟
中图分类号: Q 944摇 摇 摇 摇 摇 摇 文献标识码: A摇 摇 摇 摇 摇 摇 摇 文章编号: 2095-0845(2013)05-613-08
The Influence of Temperature and Humidity on Stylar
Curvature in Amomum tsaoko (Zingiberaceae)*
YANG Yao鄄Wen1,2,3, QIAN Zi鄄Gang3, LI Ai鄄Rong1, PU Chun鄄Xia1,2,3,
LIU Xiao鄄Li3, GUAN Kai鄄Yun1**
(1 Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, China; 2 University of Chinese
Academy of Sciences, Beijing 100049, China; 3 The Center for Reproducing Fine Varieties of Chinese
Medicinal Plants, Yunnan College of TCM, Kunming 650500, China)
Abstract: Flexistyly is a floral mechanism involving extreme curving of the style first described in Amomum tsaoko
Crevost & Lemarie. We examined the influence of temperature and humidity on stylar curvature in this species. Al鄄
though floral behavior was similar to that reported previously in this species and other flexistylous gingers, there was
a delay in stylar movement in two morphs, which differed strikingly from previous observations. When mean temper鄄
ature and humidity between 8 颐 30 and 19 颐 30 hrs were below 18 益 and above 90% , respectively, style movement of
both morphs was not delayed; however, there was a delay in style movement when temperature was increased above
18 益 and humidity fell below 90% . Stylar curvature of cataflexistylous flowers was more sensitive to change of hu鄄
midity than anaflexistylous ones. When mean temperature and humidity were between 19. 17-19. 52 益 and 51. 00%
-51. 44% , respectively, the anthesis of a single cataflexistylous flower was prolonged from 1 day to 2 days, and sty鄄
lar curvature downwards was asynchronous. The asynchronous stylar movement did not ensure complete functional di鄄
oecy within a population, which would decrease successful cross鄄fertilization (outcrossing) between the two different
植 物 分 类 与 资 源 学 报摇 2013, 35 (5): 613 ~ 620
Plant Diversity and Resources摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 DOI: 10. 7677 / ynzwyj201312171
*
**
Funding: Science and Technology Projects of Yunnan Province (2009CD078) and the Science Foundation of Yunnan Education Bureau
(2010Z097)
Author for correspondence; E鄄mail: guanky@ mail. kib. ac. cn
Received date: 2012-12-17, Accepted date: 2013-02-21
作者简介: 杨耀文 (1967-) 男, 副教授, 主要从事药用植物资源保护方面的教学和科研工作。 E鄄mail: yangyaowen@ mail. kib. ac. cn
forms, and affect the breeding and fitness of plants. Flexistyly is a special form of heterodichogamy, which requires
further study to fully understand its origin and evolution.
Key words: Amomum tsaoko; Temperature; Humidity; Stylar movement; Prolonged flowering
摇 Flexistyly is a unique and motile sexual dimor鄄
phism first found in Amomum tsaoko Crevost &
Lemarie (Cui et al., 1995a, b) and then in Alpinia
Roxb. species (Li et al., 2001a, b, 2002; Zhang
et al., 2003; Takano et al., 2005; Wang et al.,
2005a, b). In a flexistylous species, there are two
floral morphs ( anaflexistylous and cataflexistylous)
with styles behaving oppositely and differing in the
time of stigma receptivity and pollen release during
anthesis. Through active stylar curvature, each mor鄄
ph changes from one sexual phase to the other in the
middle of the 1鄄d flowering period, and the two mor鄄
phs form a reciprocal cooperation between stigmas
and anthers to promote outcrossing ( Li et al.,
2001a; Zhang and Li, 2002). The sexual organs
are separated temporarily and spatially by active sty鄄
lar curvature, thus interference of male and female
functions may reduce to small extent ( Li et al.,
2001a, b; Barrett, 2002; Zhang and Li, 2002;
Zhang et al., 2003; Zhang, 2004).
As a special form of heterodichogamy, flexistyly
mechanism was observed in several genera of Zingib鄄
eraceae, such as Alpinia, Amomum, Etlingera, and
Paramomum (Ren et al., 2007). This mechanism
was found in all Alpinia species which have been ob鄄
served so far; however, not all species in Amomum
have this mating strategy. Therefore, Amomum is an
ideal model for discussing flexistyly phylogeny and
flexistyly in this genus is worth to be studied in de鄄
tails (Ren et al., 2007). Weather condition affect鄄
ed the speed of stylar movement of Alpinia species
(Li et al., 2001a). Rainy weather would delay the
stylar movement of Alpinia (Zhang and Li, 2002).
These researches imply that temperature and humidi鄄
ty would influence the stylar movement. The influ鄄
ence of weather conditions on the flexistylous move鄄
ment of style of A. tsaoko has not been reported yet.
To fully understand the origin and evolution of this
unique floral mechanism, studying flexistyly in Amo鄄
mum from various aspects are need. In this sense,
we reported the influence of temperature and humidi鄄
ty on the stylar movement of A. tsaoko, and also dis鄄
cussed its effect on the breeding of this species in
this research.
1摇 Material and method
1. 1摇 Research species
Amomum tsaoko Crevost et Lemaire is a peren鄄
nial herb of Zingiberaceae, usually 2-3 m in height.
Inflorescence consists of a densely flowered spike
that arises from rhizomes. The showy yellow label鄄
lum with red nectar guide is fused with the single
stamen to form a tube, the free part of which forms
an expanded landing platform for visitors. An appar鄄
ent anther appendage (ca. 4 mm伊11 mm) forms an
arch at the top of the anther and surrounds the stig鄄
ma. Flowering occurs from April to June, capsules
are ripe from September to December (Wu and Ra鄄
ven, 2000).
Amomum tsaoko distributes in Yunnan Prov鄄
ince, southwest China (Wu and Raven, 2000), but
now its wild (or natural) population is almost extinct
in Yunnan. Since its fruit is used as common materi鄄
a medica ( Chinese Pharmacopoeia Commission,
2010) and a food condiment in China, it is cultivat鄄
ed as economic plant in Yunnan.
1. 2摇 Study site
The study was conducted from 24 to 26 in May,
2007, and from 10 to 13 in May, 2009, at the Gao鄄
ligong Mountain, Yunnan Province, southwest Chi鄄
na. In the study site, primary forest is kept as a part
of natural reserve, and A. tsaoko inhabits understory
of broad鄄leaved forest and its fruits are collected by
local villagers. Population 1 (24毅50. 289忆 N, 98毅
46. 501忆 E, 2 070 m in altitude) is about 3 km away
from population 2 (25毅3. 702忆 N, 98毅30. 129忆E,
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2 219 m in altitude). Both populations have been
cultivated for more than 20 years. Flowering of pop鄄
ulation 1 and 2 occurred from late April to early June
and from early May to June, respectively.
1. 3摇 Field observations
In the two populations, all flowers that random鄄
ly selected from two morphs were subjected to obser鄄
vations. For each flower, the following traits were
observed and recorded every 30 min from 08 颐 30 to
19 颐 30: movement of style ( upward or downward
curving), position of stigma ( above or below an鄄
ther) and anther dehiscence.
We observed 243 flowers from 23 individuals,
including 117 flowers from 10 cataflexistylous indi鄄
viduals and 126 flowers from 13 anaflexistylous indi鄄
viduals, respectively. In population 1, we observed
four individuals of each morph and 57 flowers (22
anaflexistylous flowers +35 cataflexistylous flowers)
over three days in 2007. Two to four flowers were
selected at random from the same individual and ob鄄
served every day. Nine anaflexistylous individuals
and 104 flowers from these individuals were observed
over two days in 2009. Six to ten flowers were se鄄
lected at random every day. In population 2, there
were only 6 cataflexistyled individuals that came
into anthesis on May 10-11, 2009, there were 60
open flowers on May 10, and 22 open flowers on
May 11.
The temperature and humidity were monitored
and recorded every 30 min at the center of each pop鄄
ulation, of where the degree of shading was moderate
and presenting the average level of temperature and
humidity across population.
1. 4摇 Statistical analyses
Frequency of stylar movement of the same mor鄄
ph in different time of one鄄day anthesis was counted
out by proportion of flowers which stylar movement
had occurred to the total flowers observed in corre鄄
sponding time. The style of both floral morphs didn爷t
obviously curve downwards or upwards until 19 颐 30,
the stigma was still above the anther and wasn爷t in
its receptive position ( for cataflexistylous morph),
or the stigma was still below the anther and wasn爷t
far away from the insect visiting channel ( for
anaflexistylous morph), which were termed delay of
stylar movement. Percentage of stylar delay of the
same floral morph in one鄄day anthesis was counted
out by proportion of flowers which stylar movement
delayed to the total flowers observed.
Date on temperature and humidity were checked
by Homogeneity of variance test, then compared by
one鄄way analysis of variance ( ANOVA) in SPPS
(13. 0 version). Student Newman Keuls Test (S鄄N鄄K
test) was used to analyze the variances among the
seven days. Correlation was tested by Bivariate Corre鄄
lation and Partial Correlate in SPSS (13. 0 version).
2摇 Results
2. 1 摇 Significant difference of temperature and
humidity
Homogeneity of variance test showed that the
variances of both temperature and humidity were e鄄
qual (P = 0. 000 <0. 01). Among the seven days,
both temperature (df= 6, F = 13. 170, P = 0. 000)
and humidity (df=6, F=68. 161, P=0. 000) from
8 颐 30 to 19 颐 30 were significant different. By S鄄N鄄K
test ( 琢 = 0. 05), the temperature and humidity of
these days were divided into 4 and 3 subsets respec鄄
tively (Table 1).
2. 2摇 Stylar movement and prolonged flowering
Despite the resemblance in floral behavior there
were still some differences between the previous
studies and ours. In population 1, both floral morphs
changed asynchronously from one sexual stage to an鄄
other on May 24-26, 2007 (Fig. 1). The analogous
phenomena were also observed on May 12 and 13,
2009, the styles of anaflexistyled flowers didn爷t bend
upward strictly synchronously on the same day (Fig.
2). In population 2, we observed that the longevity
of a single cataflexistyled flower was lengthened from
1 d to 2 d, and their corollas withered and closed till
11 颐 00-13 颐 00 of the next day. The most cataflexi鄄
styled flowers opened on May 10 were in their male
stage on the first day (May 10) because their styles
5165 期摇 摇 摇 摇 YANG Yao鄄Wen et al. : The Influence of Temperature and Humidity on Stylar Curvature in …摇 摇 摇 摇 摇
remained upwards, and their styles curved downwards
and they were in their female stage on the second day
(May 11). The same case was observed in flowers
opened on May 11. In the process of these cataflexi鄄
styled flowers opening, their styles curved downwards
asynchronously on the same day (Fig. 3).
Although the styles of two morphs didn爷t curve
strictly simultaneously during our observation days
(2007 and 2009), there was a time when the styles
curved convergently. The styles of anaflexistyled
flowers curved upwards mainly from 16 颐 00 to 18 颐 30,
and styles of cataflexistyled flowers curved down鄄
wards mainly from 15 颐 30 to 16 颐 00 and from 17 颐 30
to 19 颐 30 (Fig. 1-3).
Delay of stylar movement was observed in the
five days with exception of May 24 and May 26. The
delay of stylar movement of two morphs was more se鄄
rious in 2009 than 2007, with significant difference
of both temperature and humidity between these two
years (Table 1).
Table 1摇 Delay of stylar movement and the changes of temperature and humidity during the field observations
Day
Percentage of
stylar delay of
anaflexistylous
flower / %
Percentage of
stylar delay of
cataflexistylous
flower / %
8 颐 00-19 颐 30
Temperature / 益 Humidity / %
(Mean依SD)
Subset
(琢=0. 05)
by S鄄N鄄K test
(Mean依SD)
Subset
(琢=0. 05)
by S鄄N鄄K test
May 24, 2007 0. 00 0. 00 16. 65依1. 03 1 95. 74依0. 81 3
May 26, 2007 0. 00 0. 00 17. 22依1. 59 1 90. 87依6. 86 3 or 2
May 25, 2007 14. 29 4. 76 18. 13依1. 58 1 or 2 87. 22依4. 82 2
May 11, 2009 data missing 77. 27 19. 52依3. 29 2 or 3 51. 44依13. 19 1
May 10, 2009 data missing 83. 33 19. 17依2. 85 2 or 3 51. 00依14. 05 1
May 13, 2009 21. 74 data missing 21. 04依2. 98 3 or 4 57. 26依14. 42 1
May 12, 2009 25. 71 data missing 22. 35依4. 12 4 55. 91依17. 84 1
Fig. 1摇 The frequency of stylar movement of A. tsaoko during 1鄄d anthesis (May 24-26, 2007)
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Fig. 2摇 The frequency of stylar upward curvature of the anaflexistyled flowers during 1鄄d anthesis (May 12-13, 2009)
Fig. 3摇 The frequency of stylar downward curvature of the cataflexistyled flowers and prolonged flowering (May 10-11, 2009)
2. 3摇 Influence of temperature and humidity on
stylar movement
The result of Bivariate Correlation analysis indi鄄
cated that significant correlations occurred between
percentage of stylar delay of anaflexistylous flower
and some climatic factors, viz. mean temperature
from 8 颐 30 to 19 颐 30 (df=3, r=0. 948, P=0. 014<
0. 05), standard deviation of temperature (df = 3, r
7165 期摇 摇 摇 摇 YANG Yao鄄Wen et al. : The Influence of Temperature and Humidity on Stylar Curvature in …摇 摇 摇 摇 摇
= 0. 886, P = 0. 046 <0. 05), and mean humidity
from 8 颐 30 to 19 颐 30 (df=3, r= -0. 921, P=0. 026
<0. 05). Accordingly, significant correlations were
tested out between percentage of stylar delay of cat鄄
aflexistylous flower and some climatic factors, viz.
mean temperature from 8 颐 30 to 19 颐 30 (df = 3, r =
0. 918, P = 0. 028 <0. 05), standard deviation of
temperature (df=3, r = 0. 953, P = 0. 012<0. 05),
mean humidity from 8 颐 30 to 19 颐 30 (df = 3, r = -
0. 994, P = 0. 001 <0. 01), standard deviation of
humidity (df=3, r=0. 924, P=0. 025<0. 05).
The result of Partial Correlation analysis indica鄄
ted that significant correlations occurred between
percentage of stylar delay of cataflexistylous flower
and mean humidity from 8 颐 30 to 19 颐 30 (df=2, r=
-0. 989, P = 0. 011 <0. 05) by control variable of
mean temperature.
3摇 Discussion
There are numerous examples of floral or repro鄄
ductive polymorphisms maintained within a popula鄄
tion ( Pannell et al., 2005 ), displaying diverse
strategies of plant reproduction ( Barrett, 2002 ).
Flexistyly is a genetic polymorphism to promote out鄄
crossing and reduce interference between male and
female function through active stylar curvature.
When stigma was already located above the anther,
the flower was in its male stage, oppositely while
stigma was below the anther, the flower was in its fe鄄
male stage. Both floral morphs change almost syn鄄
chronously from one sexual stage to another without
gender overlap (Ren et al., 2007), exhibiting tem鄄
poral dioecy, which prevents not only self鄄pollination
within a flower and within the same inflorescence,
but also among individuals of the same floral morph
in a population, thus in natural condition, pollina鄄
tion can only occur between different morphs (Ren
et al., 2007). Sex expression enhances sexual re鄄
production through an optimal model of bisexual re鄄
source allocation ( Charnov, 1979 ). For a flexi鄄
stylous ginger, the stylar movement seems to play an
important role during the bisexual resource alloca鄄
tion, and the speed of stylar movement is an impor鄄
tant factor in the process.
By comparison of the analysis results, the stylar
movement was more synchronous from May 24-26,
2007 than from May 10-13, 2009; the stylar move鄄
ment was more asynchronous on May 25 than May 24
and May 26. Both temperature and humidity were
significantly different among these days. The corre鄄
lation analysis indicated that change of the tempera鄄
ture and humidity from 8 颐 30 to 19 颐 30 would influ鄄
ence the stylar movement. When the mean tempera鄄
ture from 8 颐 30 to 19 颐 30 was below 18 益, the style
movement of both morphs didn爷 t delay. When the
mean temperature was above 18 益, the stylar move鄄
ment of two morphs delayed, and more high the
mean temperature, the more delay of the stylar
movement. When the mean humidity from 8 颐 30 to
19 颐 30 was above 90% , the stylar movement of two
morphs didn爷t delay. When the mean humidity was
below 90% , the stylar movement of both morphs de鄄
layed, and more lower the mean humidity, the more
delay of the stylar movement.
If the style of cataflexistylous flower didn爷t bend
downward to its receptive position until 19 颐 30, op鄄
portunity of the stigma accepting pollen would be
greatly reduced. Since the stigma of anaflexistylous
flower was already located above the anther, far from
the insect visiting channel, then its pollen sacs be鄄
gan to dehisce; if the style of anaflexistylous flower
didn爷t curve above the anther until 19 颐 30, opportu鄄
nity of the pollen releasing from anther would also be
greatly reduced, and the pollen would fall and accu鄄
mulate on the labellum when we tore open these fa鄄
ded flowers in the next morning. Delay of stylar
movement was more obvious and asynchronization of
stylar movement was more serious. Our studies indi鄄
cated that both temperature and humidity affected the
stylar movement of both floral morphs of A. tsaoko,
displaying a tendency that steady low temperature
(< 18 益) would lead the stylar movement toward
more synchronization than the mean temperature of 18
-22 益, and steady high humidity ( >90%) would
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lead the stylar movement toward more synchroniza鄄
tion than changeable low humidity (<58% ).
The similar asynchronous stylar movement was
reported in Alpinia hainanensis (Wang et al., 2005a).
The asynchronous stylar movement of A. tsaoko might
be caused by photoperiod (Cui et al., 1995a). Dif鄄
ferent light intensity and duration would cause differ鄄
ent temperature and humidity. The degree of sha鄄
ding was changing across a day, which would result
in alteration of temperature and humidity within popu鄄
lation. During field observations, we observed that
the stylar movement was more asynchronous on the
sunny days than the cloudy days, because the hetero鄄
geneity of environmental factors across the same popu鄄
lation was smaller on cloudy day than sunny day.
The synchronous stylar movement ensured that
there was completely functional dioecy within a popu鄄
lation, which insured successful cross鄄fertilization
(outcrossing) only occurs between the two different
forms (Li et al., 2001a). Synchronous stylar move鄄
ment of a flexistylous species could increase pollen
export during their male phase by reducing levels of
within鄄 and between鄄flower interference (Sun et al.,
2011). Cui et al. (1996) indicated that A. tsaoko
was self鄄compatible. Self鄄fertilization would lead to
inbreeding depression due to expression of deleteri鄄
ous recessive genes ( Charlesworth and Charles鄄
worth, 1987, 1999). The peak of stylar movement
of the two morphs would promote that the outcrossing
would occur mainly between the two different forms.
The heterogeneity of environmental factors in a popu鄄
lation could cause some asynchronous stylar move鄄
ment, which would influence on the breeding of popu鄄
lation, and discount fitness of the plant.
Style movement appeared to have asymmetrical
effects, in contrast to male function, female function
appeared to be affected weakly by stigma movement
(Sun et al., 2007, 2011). The analysis also indi鄄
cated that the stylar movement of the cataflexistylous
flowers was more sensitive to change of humidity
than the anaflexistyled ones. There might be some
differentiation between the two morphs. The fruit set
of the anaflexistylous individual was significantly
higher than the cataflexistylous one ( unpublished
observation). It was likely correlative of the differ鄄
entiation between the two morphs. Both stylar move鄄
ment and breeding of the cataflexistylous morph ap鄄
peared to be affected greatly by weather condition in
contrast to the anaflexistylous morph.
The sex expression of plants was regarded as a
quantitative character, which was termed as pheno鄄
typic gender and functional gender, phenotypic gen鄄
der was usually measured by the morphological fea鄄
ture of flowering ( Lloyd, 1979). Floral longevity
was assumed to reflect a balance between the benefit
of increased pollination success and the cost of flow鄄
er maintenance ( Ashman and Schoen, 1994;
Schoen and Ashman, 1995), and long floral longe鄄
vity was advantageous to both female and male fitness
in Hedychium villosum var. villosum ( Gao et al.,
2009). Reproductive assurance would be a self鄄pro鄄
tecting mechanism or strategy ( Baker, 1955). In
population 2, all the flowers were cataflexistylous
during the early flowering, both temperature (19. 17
-19. 52 益) and humidity (51. 00-51. 44% ) might
influence on the floral behavior: the anthesis of a
single flower was prolonged from 1 d to 2 d, and
their stylar downward movement was asynchronous.
These cataflexistyled flowers mainly acted as func鄄
tionally male flowers at the first day, and as func鄄
tionally female flowers at the second day; outcros鄄
sing would occur between the same morphs for repro鄄
ductive assurance. So the prolonged flowering would
help to improve the both of female and male fitness
for reproductive assurance on special occasions. Al鄄
though the similar example was reported in Alpineae
oxyphylla (Wang et al., 2005b), it was observed
for the first time in A. tsaoko.
Heterodichogamy is understood to come from
synchronous dichogamy and is heading towards dio鄄
ecy (Renner, 2001). Flexistyly is a special hete鄄
rodichogamy, further insight into which would be
worth studying in details to fully understand its origin
and evolution.
9165 期摇 摇 摇 摇 YANG Yao鄄Wen et al. : The Influence of Temperature and Humidity on Stylar Curvature in …摇 摇 摇 摇 摇
Acknowledgements: We thank Dr. Yu Wen鄄bin for his crit鄄
ical reading of the paper and good advice.
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