全 文 ：海拔对高山栎光合气体交换和叶性状的影响*
张石宝1, 周浙昆1,2, 许摇 琨2
(1 中国科学院西双版纳热带植物园热带植物生态学重点实验室, 云南 昆明摇 650223;
2 中国科学院昆明植物研究所, 云南 昆明摇 650204)
摘要: 理解影响植物分布的式样及过程是生态学研究的中心内容之一, 但对许多物种而言, 限制其分布的
原因还不清楚。 为了认识高山栎分布与生理生态特性的关系, 我们在不同海拔的 4 个观测点研究了帽斗栎
的光合气体交换、 叶氮含量、 叶绿素含量和比叶重。 由于高的水气压亏缺和气温, 帽斗栎的光合作用和蒸
腾作用在午间表现出明显的降低现象。 帽斗栎的饱和光合速率、 水分利用效率、 最大羧化速率、 最大电子
传递速率和氮利用效率在海拔中部比低海拔或高海拔处的为高。 不同海拔的叶氮含量在 5 月份有差异, 8
月份则没有明显不同。 叶片厚度随海拔增加, 但叶绿素含量及光合最适温度随海拔升高而降低。 帽斗栎光
合作用的海拔变化与叶片的生化效率和氮含量有关, 而与比叶重无关。 研究结果说明, 温度的海拔变化对
高山栎的光合作用和叶性状有明显影响, 最适宜帽斗栎光合碳获取及生长的海拔范围是 3 180 ~ 3 610 m。
关键词: 帽斗栎; 光合作用; 叶绿素荧光; 叶性状; 高山生境; 生态适应
中图分类号: Q 945摇 摇 摇 摇 摇 摇 文献标识码: A摇 摇 摇 摇 摇 摇 摇 摇 文章编号: 2095-0845(2011)02-214-11
Effects of Altitude on Photosynthetic Gas Exchange and
the Associated Leaf Trait in an Alpine Oak,
Quercus guyavifolia (Fagaceae)
ZHANG Shi鄄Bao1, ZHOU Zhe鄄Kun1,2, XU Kun2
(1 Key Laboratory of Tropical Plant Ecology, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences,
Kunming 650223, China; 2 Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650204, China)
Abstract: Understanding the pattern and process governing the distribution is a central goal of ecology, yet for many
species the causes of distribution limit are unknown. To understand the relationship between altitudinal distribution
of alpine oak and ecophysiological trait, leaf nitrogen content, chlorophyll content, leaf mass per unit area and pho鄄
tosynthetic gas exchange of Quercus guyavifolia were investigated at four sites along an altitudinal gradient from 2 650
to 3 920 m in the Hengduan Mountains. Q. guyavifolia showed a significant midday depression in photosynthesis and
transpiration at all sites due to high vapour pressure deficit and temperature. Both in May and August, this species
had higher light鄄saturated photosynthesis, water use efficiency, maximum RuBP rate of carboxylation, light saturated
rate of electron transport and photosynthetic nitrogen use efficiency at the middle altitude than at the lowest or highest
location. Leaf nitrogen content was different in May among altitudes, but remained relatively constant in August.
Leaf thickness increased with altitude while chlorophyll content and photosynthetic optimum temperature decreased.
The altitudinal trend in photosynthesis of Q. guyavifolia could be linked to leaf biochemical efficiency and nitrogen
content, but not leaf mass per unit area. The variation in temperature along the altitudinal gradient imposed a con鄄
植 物 分 类 与 资 源 学 报摇 2011, 33 (2): 214 ~ 224
Plant Diversity and Resources摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 DOI: 10. 3724 / SP. J. 1143. 2011. 10159
* Foundation items: The National Natural Science Foundation of China (30770226) and West Light Foundation of Chinese Academy of Sciences
Received date: 2010-09-15, Accepted date: 2010-12-15
作者简介: 张石宝 (1970-) 男, 博士, 副研究员, 主要从事植物生理生态学研究。 E鄄mail: zhangsb@ xtbg. org. cn
straint on photosynthesis and leaf trait. The altitudinal range from 3 180 m to 3 610 m would be optimal for the photo鄄
synthetic carbon gain and growth of Q. guyavifolia.
Key words: Quercus guyavifolia; Photosynthesis; Chlorophyll fluorescence; Leaf traits; Alpine environment; Eco鄄
logical adaptation
Introduction
Every species is limited both geographically and
ecologically to a range of available habitats. Under鄄
standing the pattern and process governing the distri鄄
bution is a central goal of ecology, yet for many spe鄄
cies the causes of distribution limit are unknown
(Angert, 2006). This question is particularly im鄄
portant today because of the potential sensitivity of
distribution boundary of tree to climate change (Bro鄄
dersen et al., 2006; Lenoir et al., 2008). Species忆
altitudinal range limit may, in part, be due to meta鄄
bolic limitation on growth that ultimately decreases
survival and limits reproduction ( Angert, 2006 ),
because altitudinal change in environments has an
important effect on plant physiology and morphology
(Hovenden and Brodribb, 2000). Previous studies
showed that leaf thickness, leaf nitrogen content and
photosynthetic capacities of alpine plants are higher
than those of lowland plants (Hultine and Marshall,
1999; Cordell et al., 1999; Qi et al., 2007). How鄄
ever, the contradictory data provided by several au鄄
thors ( Rada et al., 1998; Cabrera et al., 1998;
Bowman et al., 1999) showed that there is no gen鄄
eral trend in photosynthesis across altitudes, as the
altitudinal variation in photosynthesis can be caused
by multiple factors, such as environmental condi鄄
tion, genetic trait of plant, leaf anatomy and physi鄄
ology. It is believed that alpine environments are
very sensitive to global changes, but it is unclear
whether alpine plants are sensitive to global change.
Consequently, the physiological ecology, and partic鄄
ularly the leaf gas exchange of plant at high altitude,
has attracted increasing attention ( Pelfini et al.,
2006). However, data on the physiological ecology
of plants over altitude of 3 000 m is limited (Li et
al., 2006; Zhang et al., 2007), especially for the
alpine plants in the Hengduan Mountains, located at
the eastern end of the Himalayan range (Li et al.,
2006). Consequently, little is known about the alti鄄
tudinal patterns in ecophysiological traits of alpine
plants at high elevations, and how alpine plants
adapt to their environments in the Hengduan Moun鄄
tains. This information is essential for understanding
the rich diversity of species in the Hengduan Moun鄄
tains and predicting the response to alpine plants to
climate change.
Quercus sect. Heterobalanus, distributed from alt.
1 700-4 800 m, is the dominant component of ever鄄
green sclerophyllous oak forests in the Hengduan
Mountains, and plays an important role in preventing
soil erosion and water loss, as well as in maintaining
ecological stability (Zhou et al., 2003). Their large
ranges of habitats across different elevations imply a
strong adaptation to different environments, and
would be beneficial for understanding the relationship
between altitude and ecophysiological trait of plant.
Usually, evergreen sclerophyllous oaks occur in
the xerothermic zone of the world, but the oaks of
Quercus Sect. Heterobalanus are distributed in the
cold and moist habitats of the Hengduan Mountains,
and there still remain obvious xerophytic characters,
such as dense hairs and low stomatal density (Zhou
et al., 2003). Temperature is thought to be one of
the primary determinants of species distribution and
growth along altitudinal gradients ( Cabrera et al.,
1998; K觟rner, 1998). Previous studies suggested
that Quercus Sect. Heterobalanus can adapt to alpine
environments due to their xerothermic characters and
unique genetic structure, and the altitudinal ranges
from 2 400 m to 3 600 m are their optimum distribu鄄
tion zone ( Zhou et al., 2003 ). Zhang et al.
(2005) showed that photosynthetic capacity of Q.
pannosa decreases from 3 240 m to 4 170 m in the
Hengduan Mountains, while Li et al. (2006) sug鄄
5122 期摇 摇 摇 ZHANG Shi鄄Bao et al. : Effects of Altitude on Photosynthetic Gas Exchange and the Associated Leaf …摇 摇 摇
gested that near 2 800 m altitude is the optimum zone
for growth of Q. aquifolioides. Obviously, the physi鄄
ological mechanisms concerning the altitudinal distri鄄
bution of alpine evergreen sclerophyllous oak in the
Hengduan Mountains have not been studied suffi鄄
ciently, and relevant data are fragmentary.
The photosynthesis and leaf traits of Q. guyavi鄄
folia were studied at four sites of different altitudes
in the Hengduan Mountains. The aims were ( i) to
characterize the photosynthetic adaptation of alpine
evergreen sclerophyllous oak to environment; (ii) to
investigate the differences in chlorophyll content,
leaf N content and leaf mass per unit area affecting
photosynthetic performance along the altitudinal gra鄄
dient; ( iii) to understand the relationship between
altitudinal distribution of Q. guyavifolia and photo鄄
synthetic gas exchange and leaf trait.
Materials and methods
Material and study sites
The research was conducted at four sites along
an altitudinal gradient in the Hengduan Mountains of
southwestern China: site A (99毅26. 69忆E, 28毅07. 57忆
N), site B (99毅34. 90忆E, 27毅57. 99忆N), site C (99毅
36. 81忆E, 27毅56. 03忆N) and site D (99毅39. 77忆E, 27毅
53. 01忆N) at altitudes of 2 650, 3 180, 3 610 and
3 920 m respectively. As the atmospheric pressure
deceases with increasing elevation, the partial pres鄄
sure of CO2 at site A, site B, site C and site D are
25. 8, 24. 2, 22. 9 and 21. 9 Pa, respectively. The
long鄄term climatic data of study sites are unavaila鄄
ble, but the climatic data in Zhongdian weather sta鄄
tion nearby site B is available. The air temperatures
at study sites were calculated from the altitudinal
lapse rate of 7. 1益 / 1 000 m in this region (Zhang,
1998). The annual pattern of temperature was given
in Fig. 1. May to October is the rainy season with
87% of annual rainfall, while the dry season occurs
from November to April. The soil at all four sites are
brown soils with pH values of 6. 2-6. 9.
Quercus guyavifolia L佴vl. is an evergreen broa鄄
dleaf tree that occurs in the mountain oak forests or
Fig. 1摇 Seasonal variations of air temperature at four study sites. Based
the climatic data from Zhongdian weather station nearby site B, the
air temperatures at study sites were calculated from the altitudinal
lapse rate of 7. 1益 / 1 000 m in the Hengduan Mountains
pine鄄oak mixed forests at altitudes between 2 500 m
and 4 000 m in southwestern China. The new leaves
emerge from April to May, and are retained for 2-3
years. The trees blossom from April to May and their
fruits ripen between October and November. Obser鄄
vations at four open sites were conducted in May and
August 2003. Five trees of 4 - 5 m height of Q.
guyavifolia were selected at each site for measure鄄
ments.
Measurement of photosynthesis and chlorophyll
fluorescence
Diurnal gas exchange variations were measured
in May 2003. Five fully expanded leaves from the
upper position facing east of five sampling trees per
site were selected from sampling trees for hourly
measurements from 08:00 h to 19:00 h on the clear
days in May 17-20, 2003. Photosynthetic rate (A),
transpiration rate (E), stomatal conductance ( gs)
and intercellular CO2 partial pressure (C i) were re鄄
corded using a portable infrared gas analyser with a
leaf chamber type PLC鄄B (CIRAS鄄1, PP Systems,
UK) under ambient conditions. Meanwhile, a Li鄄
1400 data logger (Li鄄Cor, NE, USA) was used to
record irradiance and air temperature at 1鄄hour inter鄄
val. Leaf and air temperature and relative humidity
were used to calculate leaf鄄to鄄air vapour pressure
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deficit (VPD). Water use efficiency (WUE) was
calculated as the ratio between A and E.
The photosynthetic responses to CO2, light and
temperature were measured both in May and August
2003. Photosynthetic responses to photosynthetic
photon flux density (PPFD) were measured by using
a CIRAS鄄1 infrared gas analyser at ambientCO2 par鄄
tial pressure and 20益 leaf temperature. After the
initial measurement at 2 000 滋mol m-2 s-1, PPFD
was decreased to produce 13 subsequent levels at
which photosynthetic rates were recorded. Data were
fit by a non鄄rectangular hyperbola (Prioul and Char鄄
tier, 1977). Using this function, apparent quantum
efficiency (AQE) and light鄄saturated photosynthetic
rate ( Amax ) were estimated by Photosyn Assistant
software (v1. 1, Dundee Scientific, UK).
Following A鄄PPFD curves, the CO2 responses
of photosynthesis were determined with a range of
CO2 partial pressure at PPFD of 1 200 滋mol m-2 s-1
and 20益 . CO2 was injected into the circuit using
the built鄄in injection system of the gas analyser. Af鄄
ter the initial measurements at ambient partial pres鄄
sure, CO2 partial pressure was reduced to 0 Pa and
then increased in steps to produce CO2 response
curves. Using A鄄C i curves, the maximum carboxyla鄄
tion rate by Rubisco (Vcmax) and light鄄saturated e鄄
lectron transport (Jmax) were calculated by Photosyn
Assistant software that applied the biochemical mod鄄
el of von Caemmerer and Farquhar (1981). The in鄄
tercellular CO2 partial pressures at different altitudes
were calibrated according to the differences in air
pressure. Relative stomatal limitation (Ls) of photo鄄
synthesis, an estimate of proportion of the reduction
in photosynthesis attributable to CO2 diffusion from
atmosphere to intercellular space, was calculated
from A鄄C i curves using the method of Farquhar and
Sharkey (1982).
The dependence of photosynthesis on tempera鄄
ture was examined with five fully expanded leaves
from five sampling trees using an infrared gas analy鄄
ser between 08:00 h and 11:00 h in the morning.
Leaf temperature was adjusted using the internal
heating / cooling system. Measurements were made
between 10益 and 35益 at ambient CO2 partial pres鄄
sure and PPFD 1 200 滋mol m-2 s-1 . After the initial
measurements at 20益, leaf temperature was re鄄
duced to 10益 and then increased to 35益 . Each
temperature maintained 5 min. A second鄄order poly鄄
nomial equation was used to fit the photosynthetic
optimum temperature (Topt).
Five expanded leaves per site were selected
from sampling trees for hourly measurements from
08:00 h to 19:00 h. Chlorophyll fluorescence was
measured on dark鄄acclimated leaf (30 min) with a
FMS鄄2 pulse modulated fluorometer ( Hanstech,
Norfolk, UK). After the minimal fluorescence (Fo)
was determined by a weak modulated light, A 0. 8 s
saturating light of 8 000 滋mol m-2s-1 was used to de鄄
termine the maximal fluorescence (Fm). Then the
leaf was illuminated by an actinic light of 1 200 滋mol
m-2 s-1 . After 5 min, the steady鄄state fluorescence
(Fs) was recorded and a second 0. 8 s saturating
light of 8 000 滋mol m-2 s-1 was given to determine
the maximal fluorescence (Fm忆) on the light鄄accli鄄
mated leaf. The fluorescence parameters were calcu鄄
lated as Fv / Fm = (Fm -Fo) / Fm and 椎PSII = 1-Fs /
Fm忆. The second鄄degree polynomial equation was
used to assess the relationship between temperature
and chlorophyll fluorescence.
Leaf traits
Twenty leaves nearby the leaves used in photo鄄
synthetic measurements were harvested from the up鄄
per part of sampling trees. In the laboratory, leaf ar鄄
eas were measured using a Li鄄3000A leaf area meter
(Li鄄Cor, NE, USA), and then the leaves were
dried to a constant mass at 70益 for 48 h to measure
the dry mass and calculate leaf mass per unit area
(LMA). The nitrogen concentration of these leaves
were analysed using a Leco FP鄄428 CHN analyser
(Leco Corporation, MI, USA). Leaf nitrogen con鄄
tent per unit area (Na ) was calculated by leaf N
concentration per unit mass multiplying LMA. Pho鄄
tosynthetic nitrogen use efficiency (PNUE) was cal鄄
culated as the ratio between Amax and Na . Chloro鄄
7122 期摇 摇 摇 ZHANG Shi鄄Bao et al. : Effects of Altitude on Photosynthetic Gas Exchange and the Associated Leaf …摇 摇 摇
phyll content was extracted from 20 leaf disk (0. 38
cm2 per disk) on the leaves nearby the the leaves
used in photosynthetic measurements in the sampling
trees with N, N鄄Dimethylformamide, and stored in
the dark at 4益 for 5 -7 days. Chlorophyll content
was analyzed with a UV鄄2550 spectrophotometer
( Shimadzu, Japan) and calculated using the method
of Inskeep and Bloom (1985).
Statistical analysis
Statistical analysis was performed using SPSS
version 13. 0 (SPSS Inc., Chicago, USA). Differ鄄
ences in leaf morphological and physiological varia鄄
bles among altitudes were determined using one鄄way
analysis of variance ( ANOVA) and LSD test for
multiple comparisons, and between May and August
by independent samples t鄄test.
Results
Diurnal of environmental factors and gas ex鄄
change
At all sites, the maximum PPFD, temperature
and VPD were observed around 14:00 h (Fig. 2).
There was no statistical difference in average daily
PPFD among altitudes ( F = 0. 503, P > 0. 05).
However, both air temperature (F = 11. 868, P<
0. 001) and VPD (F= 4. 894, P<0. 01) decreased
as altitude increased.
The maximum gs occurred in the early morning,
decreased towards midday and increased in the after鄄
noon (Fig. 3). The diurnal variation of gs was similar
to that of relative humidity (data not presented), an
opposite trend to VPD. Although the gs values of plants
at the altitudes of 3 180 m and 3610 m were higher than
at the altitudes of 2 650 m and 3 920 m, there was no
significant difference (F=1. 482, P>0. 05).
Diurnal variations of E and A of Q. guyavifolia
showed a significant midday depression. The mini鄄
mum value of E was observed around noon, and E
decreased with increasing altitude. The average A of
5 leaves at all sites peaked rapidly after dawn, be鄄
fore subsiding in the middle of the day, and reached
maximum values at about 10:00 h, then reached a
second鄄peak in the late afternoon ( Fig. 3 ). The
plants had higher daily mean photosynthetic rate at
the altitudes of 3 180 m and 3 610 m than at the alti鄄
tudes of 2 650 m and 3 920 m (F=3. 173, P<0. 05).
The diurnal variation of WUE was similar to A, and
the plants at altitude of 3 610 m had the highest
WUE among altitudes (F=8. 015, P<0. 001).
Effects of light and temperature on photosynthesis
The photosynthesis of Q. guyavifolia was satu鄄
rated around the light intensity of 1 000 滋mol m-2s-1
(Fig. 4). There was no significant difference in light
compensation point among sites in August (F=0. 574,
P>0. 05), but the plants at altitude of 3 610 m in
May had lower light saturation points than at other
three sites (F=9. 934, P<0. 01). The photosynthetic
Fig.2摇 Diurnal variations of photosynthetic photon flux density (PPFD),
air temperature (Ta) and leaf鄄to鄄air vapor pressure deficit (VPD)
on the clear day in May 2003. Data are means依1SE (n=5)
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Fig. 3摇 Diurnal patterns of stomatal conductance (gs), transpiration
rate (E), net photosynthesis (A) and water use efficiency (WUE)
of Q. guyavifolia at ambient temperature, light intensity and
CO2 partial pressure in May 2003. Each point is a mean
of 5 measurements. Bars represent依1 SE
light saturation point at altitude of 3 920 m was high鄄
er than at other three sites in May (F=19. 954, P<
0. 001) or August (F=6. 489, P<0. 05).
The optimum temperatures for photosynthesis
(Topt) of Q. guyavifolia were between 18益 and 22益
Fig. 4摇 Photosynthetic responses of Q. guyavifolia to photosynthetic
photon flux density (PPFD) at ambient CO2 partial pressure and
leaf temperature of 20益 in May (a) and August (b) . Vertical
bars indicate standard errors of means for five measurements
at all sites in May, and between 20益 and 23益 in
August. Topt decreased with the increasing altitude
both in May and August ( Fig. 5). The Topt of Q.
guyavifolia in August were higher than in May at all
sites. The temperature range attaining above 90%
Amax was reduced with increasing altitude. There was
a drastic decrease in photosynthesis when leaf tem鄄
perature was greater than 25益 . The data of chloro鄄
phyll fluorescence of Q. guyavifolia at all sites was
analysed together using a second鄄degree polynomial
equation to address the relationship between chloro鄄
phyll fluorescence and temperature ( Fig. 6 ). Be鄄
tween 18益 and 22益, Q. guyavifolia had highest
Fv / Fm and 椎PSII values.
Altitudinal changes in photosynthetic capacity
The light鄄saturated photosynthesis (Amax) of Q.
guyavifolia at the middle attitudes (alt. 3 180 m and
alt. 3 610 m) was higher at the upper altitude (alt.
3 920 m) and lower altitude (alt. 2 650 m) in both
May and August (Table 1). From May to August,
9122 期摇 摇 摇 ZHANG Shi鄄Bao et al. : Effects of Altitude on Photosynthetic Gas Exchange and the Associated Leaf …摇 摇 摇
Fig. 5摇 Effects of leaf temperature on photosynthesis of Q. guyavifolia
at ambient CO2 partial pressure and photosynthetic photon flux
density of 1 200 滋mol m-2s-1 in May (a) and August (b). Vertical
bars indicate standard errors of means for five measurements
Fig. 6摇 Effects of temperature on maximum photochemical
efficiency (Fv / Fm) and quantum yield of PSII
(椎PSII) of Q. guyavifolia across all the
trees and all the sites
Table 1摇 Comparison of photosynthetic parameters of Quercus guyavifolia at different altitudes and seasons
Altitude (m)
2 650 m (site A) 3 180 m (site B) 3 610 m (site C) 3 920 m (site D) p
May 10. 93依0. 43a 13. 27依0. 55b 13. 77依0. 58b 10. 13依0. 43a **
Amax August 11. 70依0. 45a 14. 77依0. 55bc 15. 63依0. 75b 13. 47依0. 66ac **
p ns ns ns *
May 0. 031依0. 003a 0. 035依0. 001ab 0. 041依0. 002b 0. 027依0. 002a **
AQE August 0. 033依0. 001a 0. 045依0. 002b 0. 051依0. 003b 0. 038依0. 002a ***
p ns * ns **
May 34. 23依1. 53a 39. 03依2. 40ab 44. 57依1. 30b 34. 73依1. 36a **
Vcmax August 36. 73依1. 30a 41. 77依1. 87a 51. 73依2. 87b 36. 37依2. 12a **
Sig. ns ns ns ns
May 103. 07依4. 33a 111. 07依4. 27ab 121. 07依4. 22b 89. 33依5. 60a **
Jmax August 119. 33依5. 18a 130. 67依3. 71a 150. 67依7. 97b 120. 33依5. 55a *
p ns * * *
May 3. 01依0. 01a 2. 85依0. 07b 2. 71依0. 02b 2. 56依0. 06g ***
Jmax / Vcmax August 3. 25依0. 07a 3. 14依0. 11a 2. 91依0. 02a 3. 32依0. 10a ns
p ns ns ** **
May 30. 51依1. 62a 19. 55依0. 70摇 23. 88依1. 33c 24. 29依0. 24c ***
Ls August 18. 43依0. 24ab 21. 07依0. 93ab 14. 69依3. 18b 22. 51依2. 19a *
p ** ns ns ns
Data are means依 1SE. Significance: ns, no significant difference; * P<0. 05; ** P<0. 01; *** P<0. 001. The same letters in a row indicate
no significant difference. Amax, light鄄saturated photosynthetic rate (滋mol m-2 s-1); AQE, apparent quantum efficiency (mol CO2 mol-1 photon);
Vcmax, maximum RuBP saturated rate of carboxylation (滋mol m-2 s-1); Jmax, light saturated rate of electron transport (滋mol m-2 s-1); Ls, rela鄄
tive stomatal limitation (% )
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Amax increased at all sites, but the increment at the
upper altitude was the highest among four sites. The
altitudinal trend in AQE of Q. guyavifolia was similar
to that of Amax .
Photosynthetic parameters from the A鄄C i curves
also suggested that the photosynthetic capacity of Q.
guyavifolia at the middle altitudes were higher than
at the upper and lower altitude ( Fig. 7 and Table
1). Except for the plants at the lowest altitude (alt.
2 650 m), Jmax of the plants at other three sites were
lower in May than in August, but there were no sta鄄
tistical differences in Vcmax between in May and Au鄄
gust at all sites. The ratio of Jmax to Vcmax decreased
with increasing altitude in May, but they were not
significantly different among altitudes in August.
The plants in May had lower Jmax / Vcmax ratio than in
August.
Altitudinal and seasonal trends in leaf traits
High鄄altitude Q. guyavifolia had lower chloro鄄
phyll content than those at lower altitudes ( Table
2). The chlorophyll contents of plants in May were
lower than those in August. LMA of Q. guyavifolia
increased with increasing altitude. However, leaf N
content per unit area (Na) at altitude of 3 610 m was
higher than at other sites in May, but there was no
significant difference among altitudes in August.
Quercus guyavifolia at lower altitudes had higher
PNUE that those at the upper and lower altitude.
Fig. 7摇 Photosynthetic responses of Q. guyavifolia to intercellular
CO2 partial pressure (Ci) at photosynthetic photon flux density
of 1 200 滋mol m-2 s-1 and leaf temperature of 20益 in May
(A) and August (B). Vertical bars indicate standard errors
of means for five measurements
Table 2摇 Comparison of leaf traits of Quercus guyavifolia at different altitudes and seasons in the Hengduan Mountains
Altitude (m)
2 650 m (site A) 3 180 m (site B) 3 610 m (site C) 3 920 m (site D) p
May 40. 48依0. 83a 35. 45依1. 47b 31. 03依1. 41bc 27. 18依1. 02c ***
Chl August 44. 58依3. 96a 40. 96依2. 36a 36. 44依1. 98ab 33. 77依2. 54b ns
p ns ns ns ns
May 215. 5依6. 4a 218. 2依9. 9a 250. 8依7. 7b 253. 3依12. 9b *
LMA August 207. 5依4. 5a 202. 5依5. 2a 239. 6依7. 9b 243. 6依11. 5b *
p ns ns ns **
May 2. 533依0. 117a 2. 687依0. 167ab 2. 893依0. 348b 2. 628依0. 207ab *
Na August 2. 467依0. 122a 2. 883依0. 136b 摇 2. 997依0. 268b 2. 863依0. 077b ns
p ns ns ns ns
May 4. 320依0. 143ab 4. 960依0. 168b 摇 4. 803依0. 366b 3. 887依0. 195a *
PNUE August 4. 773依0. 349a 摇 5. 127依0. 052ab 5. 260依0. 619b 4. 701依0. 127a *
p ns ns ns *
Data are means依1SE. Significance: ns, no significant difference; *P<0. 05; **P<0. 01; ***P<0. 001. The same letters in a row indicate no
significant difference. Chl, chlorophyll content per unit area (滋g cm-2); LMA, leaf mass per unit area (gm-2); Na, leaf N content per unit area
(gm-2); PNUE, photosynthetic N use efficiency (滋mol CO2 g-1 s-1 N)
1222 期摇 摇 摇 ZHANG Shi鄄Bao et al. : Effects of Altitude on Photosynthetic Gas Exchange and the Associated Leaf …摇 摇 摇
Discussion
Diurnal variation in photosynthesis
In the present study, Quercus guyavifolia experi鄄
enced a pronounced midday depression in photosyn鄄
thesis. This was similar to the responses reported for
Mediterranean oaks Q. suber and Q. ilex (Tenhunen et
al., 1984). The photosynthetic rate of Q. guyavifo鄄
lia did not substantially decrease under high PPFD
conditions, provided temperature was favourable
(Fig. 4). When leaf temperature went over 25益,
which typically occurred from 11:00 h to 15:00 h,
the photosynthesis of Q. guyavifolia decreased dra鄄
matically. The inactivation of photosynthesis can be
induced by high temperature (Berry and Bj觟rkman,
1980). Present study also provided evidence for the
important role of high temperature on photosynthetic
depression of Q. guyavifolia at midday.
Seasonal variation in photosynthesis
In this study, the Topt of Q. guyavifolia not only
shifted by about 1益 -3益 higher from May to Au鄄
gust, but also decreased with increasing altitude ir鄄
respective of seasons. The variation in growth tem鄄
perature can cause a shift in the optimum tempera鄄
ture of photosynthesis (Topt), which allows plants to
perform more efficiently at new growth temperatures
( Battaglia et al., 1996). This change in optimal
temperature would be related to the change in the
temperature dependence of Rubisco activity as RuBP
carboxylation and RuBP regeneration have different
temperature dependence (Ishikawa et al., 2007).
Seasonal changes in environmental factors had a
significant effect on photosynthetic capacity. At all
sites, the parameters describing photosynthetic ca鄄
pacity in August were higher than those in May (Ta鄄
ble 1). Previous study suggested that the change in
the ratio of Jmax / Vcmax would be responsible for some
parts of seasonal changes in photosynthesis. Howev鄄
er, the response of the Jmax / Vcmax ratio to temperature
was different among species (Onoda et al., 2005).
The Jmax / Vcmax ratio of Q. guyavifolia increased with
growth temperature which indicated the relative pro鄄
portion of Jmax in the photosynthetic proteins de鄄
creased under low鄄temperature conditions. The re鄄
duction in Jmax indicated that the photosynthetic elec鄄
tron transport of Q. guyavifolia in May and at the
high鄄altitude sites would be limited by cold stress.
Altitudinal patterns in photosynthesis and leaf traits
This study showed that Q. guyavifolia growing
at altitudes of 3 180 m and 3 610 m displayed higher
photosynthetic capacity (Amax) than at altitudes of
3 920 m and 2 650 m. Angert (2006) suggested that
two Mimulus species attain the greatest biomass,
photosynthetic rate and effective quantum yield of
PSII when grown under temperature characteristics of
the altitudinal range centre. The highest Amax of Pi鄄
nus sylvestris is found in the middle parts of the dis鄄
tribution and decreased towards both ends of the
transect ( Luoma, 1997). Previous studies showed
that leaf N content (Na) in Metrosideros polymorpha
increased from sea level to treeline (Cordell et al.,
1999), but leaf N content per unit area in seven
populations of Frasera speciosa did not change with
altitude along a 1 700 m gradient (Bowman et al.,
1999). For Q. guyavifolia, the plants had higher Na
at the middle altitude than at the lower and upper al鄄
titude in May, but Na remained relatively constant in
August. The photosynthetic N use efficiencies at the
middle altitudes were higher than at the upper and
lower altitude. Altitudinal variation of Na appeared
to be largely attributable to variation in LMA
(K觟rner and Diemer, 1987), but the LMA of Q.
guyavifolia was not correlated with Na and Amax . An鄄
other reason was that plants with higher LMA limited
the supply of CO2 to chloroplast site because the dif鄄
fusive path in thicker leaf became longer (Kao and
Chang, 2001).
The gs of Q. guyavifolia at altitudes of 3 180 m
and 3 650 m were higher than those at altitudes of
2 650 m and 3 920 m. However, Kumar et al.
(2005) found that the stomatal conductance increa鄄
ses with altitude. According to the data from A鄄C i
response curves, photosynthetic rate of Q. guyavifo鄄
lia was limited likely by stomatal limitation, since
the temperatures at different elevations dramatically
222摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 植 物 分 类 与 资 源 学 报摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 摇 第 33 卷
affects CO2 diffusion and the ratio of chloroplast CO2
partial pressure to ambient CO2 partial pressure (Shi
et al., 2006).
Several authors suggested that temperature is
likely to be critical for the limitation on growth, car鄄
bon balance, resource usage and reproduction
(K觟rner, 1998; Cavieres et al., 2000). Zhou et
al. (2003) suggested that sclerophyllous oaks have
the highest species richness in the altitudinal range
from 2 400 and 3 600 m. Q. aquifolioides has higher
genetic variability at altitudes of 2 400-3 300 m (Li
et al., 1998 ). In this study, the plants of Q.
guyavifolia at the middle altitudes had higher CO2
assimilation rate than at lower altitude and higher al鄄
titude. In the optimum distribution range, alpine
oaks have higher resource use efficiency (Zhang et
al., 2007). By contrary, the unfavourable environ鄄
ments at the low or high altitudes would limit carbon
assimilation, growth and survival of plants ( Zu et
al., 1998).
Comparison of ecophysiological traits of Q. guyav鄄
ifolia with Mediterranean oaks
Usually sclerophyllous oaks are distributed in
the xerothermic regions, but Q. guyavifolia occurs in
the relatively cold habitats in the Hengduan Moun鄄
tains. Morphological and genetic evidences sugges鄄
ted that alpine evergreen sclerophyllous oaks in the
Hengduan Mountains have closely phylogenetic rela鄄
tionship with Mediterranean oaks ( Zhou et al.,
2003). Present study showed that the photosynthetic
capacity and WUE of Q. guyavifolia were similar to
those of Mediterranean oaks, but the latter had a
lower LMA (Gratani et al., 2000). LMA of Q. ilex
was higher in the colder sites (Ogaya and Pe倬uelas,
2007). We speculated that lower temperature in the
Hengduan Mountains reduced leaf extension of Q.
guyavifolia and resulted in thicker leaves.
Compared with the result of Gratani et al.
(2000), the Topt of Q. guyavifolia was lower than that
of Mediterranean oak (18益 -23益 vs 25益 -30益).
Q. semicarpifolia, another alpine oak in the Hengduan
Mountains, can resist temperature down to - 15益
(Sakai, 1981). The photosynthetic adaptation of Q.
guyavifolia to low temperature could be confirmed by
fluorescence analysis, as Fv / Fm and 椎PSII can be
used as the sensitive indicators of plant photosynthetic
performances (Maxwell and Johnson, 2000). Both
Fv / Fm and 椎PSII of Q. guyavifolia were higher be鄄
tween 18益 and 22益, and deceased above 25益 rap鄄
idly. This indicated that Q. guyavifolia is well adap鄄
ted to low temperature rather than high temperature.
In conclusion, altitude had an important effect
on leaf morphology and physiology of Q. guyavifolia.
LMA increased with altitude while chlorophyll con鄄
tent decreased. The highest Amax were found at mid鄄
dle altitude. This altitudinal trend in photosynthesis
may be linked to biochemical efficiency and Na . The
altitudinal range from 3 180 to 3 610 m would be op鄄
timal for the photosynthetic carbon gain and growth
of Q. guyavifolia. These results would be beneficial
for understanding the relationship between altitudinal
distribution of alpine oak and ecophysiological traits.
References:
Angert AL, 2006. Growth and leaf physiology of monkey flowers with
different altitude ranges [J] . Oecologia, 148: 183—194
Battaglia M, Beadle C, Loughhead S, 1996. Photosynthetic tempera鄄
ture responses of Eucalyptus globulus and Eucalyptus nitens [ J] .
Tree Physiology, 16: 81—89
Berry JA, Bj觟rkman O, 1980. Photosynthetic response and adaptation
to temperature in higher plants [ J] . Annual Review of Plant
Physiology, 3: 491—543
Bowman WD, Keller A, Nelson M, 1999. Altitudinal variation in leaf
gas exchange, nitrogen and phosphorus concentrations, and leaf
mass per area in populations of Frasera speciosa [ J] . Arctic,
Antarctic, and Alpine Research, 31: 191—195
Brodersen CR, Germino MJ, Smith WK, 2006. Photosynthesis during
an episodic drought in Abies lasiocarpa and Picea engelmannii
across an alpine treeline [J] . Arctic, Antarctic, and Alpine Re鄄
search, 38: 34—41
Cabrera HM, Rada F, Cavieres L, 1998. Effects of temperature on
photosynthesis of two morphologically contrasting plant species a鄄
long an altitudinal gradient in the tropical high Andes [ J] .
Oecologia, 114: 145—152
Cavieres LA, Rada F, Azocar A et al., 2000. Gas exchange and low
temperature resistance in two tropical high mountain tree species
from Venezuelan Andes [J] . Acta Oecologia, 21: 203—211
Cordell S, Goldstein G, Meinzer FC et al., 1999. Allocation of nitro鄄
3222 期摇 摇 摇 ZHANG Shi鄄Bao et al. : Effects of Altitude on Photosynthetic Gas Exchange and the Associated Leaf …摇 摇 摇
gen and carbon in leaves of Metrosideros polymerpha regulates car鄄
boxylation capacity and 啄13C along an altitudinal gradient [ J] .
Functional Ecology, 13: 811—818
Farquhar GD, Sharkey TD, 1982. Stomatal conductance and photosyn鄄
thesis [J]. Annual Review of Plant Physiology, 33: 317—345
Gratani L, Pesoli P, Crescente MF et al., 2000. Photosynthesis as a
temperature indicator in Quercus ilex L [ J ] . Global Planet
Change, 24: 153—163
Hovenden JM, Brodribb T, 2000. Altitude of origin influences stoma鄄
tal conductance and therefore maximum assimilation rate in
Southern Beech, Nothofagus cunninghamii [ J ] . Australian
Journal of Plant Physiology, 27: 451—456
Hultine KR, Marshall JD, 2000. Altitude trends in conifer leaf mor鄄
phology and stable carbon isotope composition [ J] . Oecologia,
23: 32—40
Inskeep WR, Bloom PR, 1985. Extinction coefficients of chlorophyll
a and b in N, N鄄dimethylformamide and 80% acetone [ J] .
Plant Physiology, 77: 483—485
Ishikawa K, Onoda Y, Hikosaka K, 2007. Intraspecific variation in
temperature dependence of gas exchange characteristics among
Plantago Asiatica ecotypes from different temperature regimes
[J] . New Phytologist, 176: 356—364
Kao WY, Chang KW, 2001: Altitudinal trends in photosynthetic rate
and leaf characteristics of Miscanthus populations from central
Taiwan [J] . Australian Journal of Botany, 49: 509—514
K觟rner C, 1998. A re鄄assessment of high elevation treeline positions
and their explanation [J] . Oecologia, 115: 445—459
K觟rner C, Diemer M, 1987. In situ photosynthetic responses to light,
temperature and carbon dioxide in herbaceous plants from low and
high altitude [J] . Functional Ecology, 1: 179—184
Kumar N, Kumar S, Ahuja PS, 2005. Photosynthetic characteristics
of Hordeum, Rumex, and Trifolium species at contrasting alti鄄
tudes [J] . Photosynthetica, 43: 195—201
Lenoir J, G佴gout JC, Marquet PA et al., 2008. A significant upward
shift in plant species optimum elevation during the 20th century
[J] . Science, 320: 1768—1771
Li C, Zhang XJ, Liu XL et al., 2006. Leaf morphological and physi鄄
ological responses of Quercus aquifolioides along an altitudinal
gradient [J] . Silva Fennica, 40: 5—13
Li J, Chen KY, Li BS, 1998. The variation of genetic diversity of
Quercus aquifolioides in different elevations [ J] . Acta Botanica
Sinica, 40: 761—767
Luoma S, 1997. Geographical pattern in photosynthetic light response
of Pinus sylvestris in Europe [ J] . Functional Ecology, 11:
273—281
Maxwell K, Johnson GN, 2000. Chlorophyll fluorescence鄄a practical
guide [J] . Journal of Experimental Botany, 51: 659—668
Ogaya R, Pe倬uelas J, 2007. Leaf mass per area ratio in Quercus ilex
leaves under a wide range of climatic conditions. The importance
of low temperatures [J] . Acta Oecologica, 31: 168—173
Onoda Y, Hikosaka H, Hirose T, 2005. The balance between RuBP
carboxylation and RuBP regeneration: a mechanism underlying
the interspecific variation in acclimation of photosynthesis to sea鄄
sonal change in temperature [ J] . Functional Plant Biology,
32: 903—910
Pelfini M, Leonelli G, Santilli M, 2006. Climatic and environmental
influences on mountain pine ( Pinus montana Miller) growth in
the central Italian Alps [ J] . Arctic, Antarctic, and Alpine Re鄄
search, 38: 614—623
Prioul JL, Chartier P, 1977. Partitioning of transfer and carboxylation
components of intracellular resistance to photosynthetic CO2 fixa鄄
tion: a critical analysis of the methods used [J] . Annals of Bota鄄
ny, 41: 789—800
Qi J, Ma KM, Zhang YX, 2007. The altitudinal variation of leaf
traits of Quercus liaotungensis and associated environmental expla鄄
nations [J] . Acta Ecologica Sinica, 27: 930—937
Rada F, Azocar A, Gonzalez J et al., 1998. Leaf gas exchange in Es鄄
peletia schultzii, a giant caulescent rosette species, along an alti鄄
tudinal gradient in the Venezuelan Andes [J] . Acta Oecologia,
19: 73—79
Sakai A, 1981. Winter hardiness of tree species at high altitudes in
the East Himalayas, Nepal [J] . Ecology, 62: 1288—1298
Shi Z, Liu S, Liu X et al., 2006. Altitudinal variation in photosyn鄄
thetic capacity, diffusional conductance and 啄13C of butterfly bush
(Buddleja davidii) plants growing at high elevations [J] . Phys鄄
iologia Plantarum, 128: 722—731
Tenhunen JD, Lange OL, Gebel J et al., 1984. Changes in photosyn鄄
thetic capacity, carboxylation efficiency, and CO2 compensation
point associated with midday stomatal closure and midday depres鄄
sion of net co2 exchange of leaves of Quercus suber [J] . Planta,
162: 193—203
Zhang SB, Zhou ZK, Hu H et al., 2005. Photosynthetic perform鄄
ances of Quercus pannosa vary with altitude in the Hengduan
Mountains, Southwest China [ J] . Forest Ecology and Manage鄄
ment, 212: 291—301
Zhang SB, Zhou ZK, Hu H et al., 2007. Gas exchange and resource
utilization in two alpine oaks at different altitudes in the Hengdu鄄
an Mountains [ J] . Canadian Journal of Forest Research, 37:
1184—1193
Zhang YG, 1998. Several issues concerning vertical climate of the
Hengduan Mountains [J] . Resource Science, 20: 12—14
Zhou ZK, Pu STBZ, Chen WY, 2003. Relationships between the dis鄄
tributions of Quercus sect. Heterobalanus and uplift of Himalayas
[J] . Advances in Earth Science, 18: 884—890
Zu YG, Yan XF, Zhang WH et al., 1998. Gas exchange and water
use efficiency of Adenophora lobophylla at different altitudes on
the east boundary of Qing鄄Zang Plateau [J] . Acta Botanica Sin鄄
ica, 40: 947—954
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