American Journal of Botany 87(5): 700–710. 2000.
PHOTOSYNTHETIC
AND RESPIRATORY ACCLIMATION
AND GROWTH RESPONSE OF
ANTARCTIC
VASCULAR
PLANTS TO CONTRASTING TEMPERATURE REGIMES1
FUSHENG S. XIONG, ERIN C. MUELLER,
AND
THOMAS A. DAY2
Department of Plant Biology and The Photosynthesis Center, Arizona State University, Tempe, Arizona 85287-1601 USA
Air temperatures have risen over the past 50 yr along the Antarctic Peninsula, and it is unclear what impact this is having
on Antarctic plants. We examined the growth response of the Antarctic vascular plants Colobanthus quitensis (Caryophyllaceae) and Deschampsia antarctica (Poaceae) to temperature and also assessed their ability for thermal acclimation, in
terms of whole-canopy net photosynthesis (Pn) and dark respiration (Rd), by growing plants for 90 d under three contrasting
temperature regimes: 78C day/78C night, 128C day/78C night, and 208C day/78C night (18 h/6 h). These daytime temperatures
represent suboptimal (78C), near-optimal (128C), and supraoptimal (208C) temperatures for Pn based on field measurements
at the collection site near Palmer Station along the west coast of the Antarctic Peninsula. Plants of both species grown at a
daytime temperature of 208C had greater RGR (relative growth rate) and produced 2.2–3.3 times as much total biomass as
plants grown at daytime temperatures of 128 or 78C. Plants grown at 208C also produced 2.0–4.1 times as many leaves,
3.4–5.5 times as much total leaf area, and had 1.5–1.6 times the LAR (leaf area ratio; leaf area:total biomass) and 1.1–1.4
times the LMR (leaf mass ratio; leaf mass:total biomass) of plants grown at 128 or 78C. Greater RGR and biomass production
at 208C appeared primarily due to greater biomass allocation to leaf production in these plants. Rates of Pn (leaf-area basis),
when measured at their respective daytime growth temperatures, were highest in plants grown at 128C, and rates of plants
grown at 208C were only 58 (C. quitensis) or 64% (D. antarctica) of the rates in plants grown at 128C. Thus, lower Pn per
leaf area in plants grown at 208C was more than offset by much greater leaf-area production. Rates of whole-canopy Pn
(per plant), when measured at their respective daytime growth temperatures, were highest in plants grown at 208C, and
appeared well correlated with differences in RGR and total biomass among treatments. Colobanthus quitensis exhibited only
a slight ability for relative acclimation of Pn (leaf-area basis) as the optimal temperature for Pn increased from 8.48 to 10.38
to 11.58C as daytime growth temperatures increased from 78 to 128 to 208C. There was no evidence for relative acclimation
of Pn in D. antarctica, as plants grown at all three temperature regimes had a similar optimal temperature (108C) for Pn.
There was no evidence for absolute acclimation of Pn in either species, as rates of Pn in plants grown at a daytime temperature
of 128C were higher than those of plants grown at daytime temperatures of 78 or 208C, when measured at their respective
growth temperatures. The poor ability for photosynthetic acclimation in these species may be associated with the relatively
stable maritime temperature regime during the growing season along the Peninsula. In contrast to Pn, both species exhibited
full acclimation of Rd, and rates of Rd on a leaf-area basis were similar among treatments when measured at their respective
daytime growth temperature. Our results suggest that in the absence of interspecific competition, continued warming along
the Peninsula will lead to improved vegetative growth of these species due to (1) greater biomass allocation to leaf-area
production (as opposed to improved rates of Pn per leaf area) and (2) their ability to acclimate Rd, such that respiratory
losses per leaf area do not increase under higher temperature regimes.
Key words:
ature; warming.
Antarctica; Colobanthus quitensis; Deschampsia antarctica; growth; photosynthesis; respiration; temper-
Rising concentrations of greenhouse gases have heightened concerns about the impacts of warming on biological processes (Hinckley and Tierney, 1992; Ennis and
Marcus, 1996). Most general circulation models predict
that initial warming will be most evident in polar regions
(Mitchell et al., 1990), and a warming trend is already
apparent along the west coast of the Antarctic Peninsula.
From 1945 to 1990, mean annual air temperature rose
;2.68C and mean summer (January–March) temperature
rose ;1.58C at Faraday/Vernadsky Station (658159 S,
648169 W) along the Peninsula (King, 1994; Smith, 1994;
Smith, Stammerjohn, and Baker, 1996). Additional evi-
dence of regional warming comes from the retreat of ice
shelves along the west coast of the Peninsula over this
period (Vaughan and Doake, 1996).
Colobanthus quitensis (Kunth) Bartl. (a cushion-forming member of the Caryophyllaceae) and Deschampsia
antarctica Desv. (a prostrate tussock grass) are the only
two vascular plant species native to Antarctica, where
they are limited to the maritime region along the west
coast of the Peninsula (Smith, 1996). Recent increases in
both the size and number of populations of these species
have been documented along the Peninsula and have been
suggested to be due to improved reproductive performance as the result of longer, warmer growing seasons
associated with the recent warming trend (Fowbert and
Smith, 1994; Smith, 1994; Grobe, Ruhland, and Day,
1997). In support of these suggestions, Day et al. (1999)
found that warming naturally growing plants along the
Peninsula for two growing seasons accelerated the development of reproductive structures and improved seed
production in both species. However, they found that veg-
1 Manuscript received 23 March 1999; revision accepted 26 August
1999.
The authors thank Tuyetlan Nguyen for laboratory assistance. This
research was supported by NSF grants OPP-9596188 and OPP-9615268
(TAD) and an NSF Graduate Research Traineeship (DGE-9553456)
supporting ECM. This is publication number 410 from The Photosynthesis Center at Arizona State University.
2 Author for correspondence (e-mail: [email protected]).
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ET AL.—TEMPERATURE RESPONSE OF
etative growth of C. quitensis was improved under warming, whereas vegetative growth of D. antarctica was reduced.
It remains unclear what mechanisms are responsible
for changes in their performance under warming, since
few studies have addressed their physiological responses
to higher temperatures. Edwards and Smith (1988) investigated the photosynthetic temperature response of
these species after propagating them in greenhouses and
outdoor plots in the summer near Cambridge, UK. They
found that photosynthesis of both species appeared well
adapted to low temperatures, as the temperature optimum
(Topt) for net photosynthesis (Pn) in detached leaves of D.
antarctica and C. quitensis was 138 and 198C, respectively, and both species maintained considerable rates of
Pn (;30% of their maximal Pn) at ;08C leaf temperature.
However, there was a sharp decline in Pn at supraoptimal
leaf temperatures in both species, suggesting that Pn
might be sensitive to higher temperatures in the field.
Xiong, Ruhland, and Day (1999) recently examined the
photosynthetic temperature response of naturally growing
plants along the Peninsula and found that whole-canopy
Pn appeared quite sensitive to higher field temperatures.
On warm days (canopy air temperature .208C), rates of
Pn in both species in the field were very low (,1
mmol·m22·sec21). They also found that the Topt for Pn was
relatively low (108 in D. antarctica, and 148C in C. quitensis), and that they had unusually low high-temperature
compensation points (228 in D. antarctica, and 268C in
C. quitensis). The apparent sensitivity of Pn in these species to moderate temperatures (208C) suggests that they
might be susceptible to rising air temperatures along the
Peninsula.
Predicting the growth response of these species to
warming based solely on their photosynthetic temperature
response is difficult because the relationship between
rates of leaf-area based Pn and whole-plant growth is
complex and often poor (Pereira, 1995; Lambers, Chapin,
and Pons, 1998). Furthermore, it is unclear how these
species might acclimate photosynthetically to rising temperatures. Photosynthetic temperature acclimation refers
to a plant’s ability to adjust its photosynthetic temperature
response so that Pn is improved with a change in its temperature regime (Billings et al., 1971; Berry and Björkman, 1980). The ability to acclimate photosynthetically
to a change in temperature regime varies among species,
as well as among populations or ecotypes within species
(Mooney and West, 1964; Berry and Björkman, 1980).
For example, in comparisons of inland vs. coastal populations of the shrub Atriplex lentiformis (Pearcy, 1976,
1977), and alpine vs. arctic populations of the forb Oxyria digyna (Billings et al., 1971), the former inland and
alpine populations had a much greater ability to acclimate
photosynthetically to changing temperature regimes than
the latter populations of these species. The acclimation
ability of Antarctic vascular plants is unknown, which
makes predicting their photosynthetic response to continued regional warming difficult.
In view of the strong warming trend along the Antarctic Peninsula and the paucity of information on how Antarctic vascular plants might respond to this trend, our
main objective in this study was to assess the growth and
biomass production response of C. quitensis and D. an-
ANTARCTIC
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701
tarctica to contrasting temperature regimes. Additionally,
we examined whether rates of Pn and dark respiration (Rd)
could explain differences in their growth responses and
also assessed whether these species could acclimate, in
terms of Pn and Rd, to contrasting temperature regimes.
MATERIALS AND METHODS
Collection site and plant material—Young plants of C. quitensis and
D. antarctica were collected in March 1996 from the easternmost island
of Stepping Stones (648479 S; 648009 W), a group of three small islands
3 km southeast of Palmer Station along the west coast of the Antarctic
Peninsula. The climate is maritime Antarctic, being relatively mild, humid, and moderate by Antarctic standards (Smith, 1996). Mean annual
air temperature at Palmer Station is 22.38C, and monthly means range
from 27.58C in July to 2.78C in January (Smith, Stammerjohn, and
Baker, 1996). Although weather records at Palmer Station only extend
back to 1974 and are incomplete over this period, Smith, Stammerjohn,
and Baker (1996) found a very strong linear correlation (P , 0.001)
between temperature records from Palmer Station and Faraday/Vernadsky Station (52 km south of Palmer Station), implying that warming is
also occurring in the Palmer Station area. The maritime influence and
frequent cloud cover in the area strongly moderate temperatures, and
the daily range in air temperature during the growing season is usually
,68C. For example, daily temperatures in November, the coldest month
of the growing season, range from an average low of 22.78C to a high
of 2.48C, and daily temperatures in January, the warmest month of the
growing season, range from an average low of 0.78C to a high of 5.18C.
Regarding plant microclimate, over two growing seasons (November–
March 1995–1996 and 1996–1997) at the Stepping Stones field site,
diurnal canopy air temperature averaged 4.38C, and was ,108C for 86%
of diurnal periods, 108–208C for 13% of these periods, and .208C for
1% of these periods (Day et al., 1999).
Plants were transported in chilled boxes (58C) to Arizona State University and propagated in growth chambers under a 128/128C (day/night)
temperature regime with a 12-h photoperiod, during which time they
received 400 mmol·m22·sec21 photosynthetically active radiation (PAR)
from a combination of cool white fluorescence tubes (F72T12/CW/
VHO, Sylvania, Danvers, Massachusetts, USA) and incandescent bulbs
(60 W XL, Sylvania, St. Marys, Pennsylvania, USA). After 14 mo,
seeds were collected from C. quitensis plants and used to propagate
experimental plants. Seeds were germinated at 208C under 75
mmol·m22·sec21 PAR in a mixture of commercial potting soil:perlite:
vermiculate (2:1:1, v:v:v). Twenty days after germination we transplanted 105 C. quitensis seedlings of similar size (8.5–9.5 mm cushion diameter, containing 9–11 leaves) into square pots (11 3 11 3 11 cm, L
3 W 3 H), containing the above potting soil mixture. At the same time,
we transplanted 105 young tillers of D. antarctica (3–4 cm total length,
containing 4–5 leaves) into torpedo pots (4.2 3 25 cm, D 3 H) containing the same soil mixture.
Temperature regime treatments—We examined the response of
plants to three temperature regime treatments: 78/78C, 128/78C, or 208/
78C day/night (18 h/6 h) temperatures. These three daytime temperatures represent suboptimal (78C), near-optimal (128C), and supraoptimal
(208C) temperatures for whole-canopy Pn (leaf-area basis) of these species at the collection site based on the findings of Xiong, Ruhland, and
Day (1999). In this study we choose to keep nighttime temperatures
similar among treatments so as to simplify our interpretation of temperature effects. Of the 105 plants of each species, 30 seedlings of C.
quitensis and 30 tillers of D. antarctica were randomly assigned to each
of the three temperature regime treatments. Fifteen plants of each species in a treatment were used for growth analysis, while the other 15
plants were used for gas-exchange measurements. The remaining 15
plants of the 105 in each species at the beginning of the experiment
were used for an initial growth analysis harvest (see below). Each tem-
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perature regime treatment was assigned to a growth chamber, and plants
and treatments were rotated among the three growth chambers every
14 d during the 90-d growth period. Plants received 400 mmol·m22·sec21
PAR for 18 h each day and were watered every other day and fertilized
every 20 d with Miracle-Gro Fertilizer (Marysville, Ohio, USA). Soil
temperatures of pots were not controlled in the chambers and were
allowed to fluctuate with changes in air temperature. When air temperature changed from the daytime to nighttime temperature or vice versa
in a chamber, soil temperature in pots reached a new steady-state temperature (equal to air temperature) within 3 h in all treatments.
Growth analysis and biomass allocation—The influence of temperature regime on growth was determined over a 90-d treatment period
using growth analysis following Hunt (1990) and Evans (1972). At the
beginning of the experiment, 15 plants of each species were harvested
immediately to provide initial growth values for the 15 plants to be
subsequently used for the final growth-analysis harvest in each treatment. At 30-d intervals we made nondestructive measurements on the
latter plants; we measured the total number of leaves, branches, and
cushion diameter of C. quitensis, and the total number of tillers, leaves,
and length of the longest tiller of D. antarctica. After 90 d these plants
were harvested. Plants were divided into roots and aboveground parts,
and the latter were further divided into vegetative and reproductive
parts. Soil was washed from roots by hand. Biomass was determined
after oven drying at 608C for 72 h. Specific leaf mass (SLM) was determined by measuring leaf areas of a subsample from each plant (containing ;25% of the total leaves) and oven drying. Plants from the
initial and the final harvests were paired randomly, and the relative
growth rate (RGR) and net assimilation rate (NAR) of each pair of
plants were estimated using the equations:
RGR 5
NAR 5
E
E
1
t2 2 t1
1
t2 2 t1
w2
d(ln W) 5
w1
t2
t1
ln w2 2 ln w1
t2 2 t1
1 dW
(w2 2 w1 )(ln s2 2 ln s1 )
dt 5
s dt
(s2 2 s1 )(t2 2 t1 )
(1)
(2)
where w1 and s1 are plant dry mass and total leaf area, respectively, at
the initial time (t1), and w2 and s2 are plant dry mass and total leaf area
at the final harvest (t2) (Evans, 1972; Hunt, 1990).
Net photosynthesis and dark respiration—Whole-canopy net photosynthesis (Pn) and dark respiration (Rd) rates of individual 60- to 85d-old plants were measured with an open infra-red gas analyzer (IRGA)
system (LI-6400, Li-COR, Lincoln, Nebraska, USA). Prior to measurements, dead leaves were removed and the plant was sealed in a custommade clear teflon-lined cylindrical double-walled cuvette (7.5 3 11 cm,
ID 3 H). The cuvette was attached between the IRGA sensor-head
sample line and the console. A fan mounted inside the top of the cuvette
insured well-stirred air. Two fine-wire thermocouples were used to measure air and leaf temperatures inside the cuvette with the latter being
attached to an external thermocouple adapter (6400-13, Li-COR) on the
IRGA console. The exposed soil around the base of the plant was sealed
off with teflon tape and putty. Temperature inside the cuvette was controlled by circulating coolant (polyethylene glycol:H2O, 1:1, v:v)
through the cuvette jacket from a refrigerating water bath. A thermocouple was inserted into the center of the pot to measure soil temperature. Water from an additional water bath was circulated through insulated plastic tubing that was coiled tightly around the pot to maintain
soil temperature at 78, 128, or 208C to match the plant’s daytime temperature in the growth chamber. A metal-halide lamp (1000 W, Crawfordsville, Indiana, USA) adjusted with neutral density filters provided
750 mmol·m22·sec21 PAR at the plant surface, as measured with a quantum sensor (LI-190SA), which was saturating for whole-canopy Pn at
all temperatures (Xiong, Ruhland, and Day, 1999). Air entering the
cuvette was maintained at a CO2 concentration of 350 mL/L with a CO2
injector system (6400-01, Li-COR). Relative humidity was maintained
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at 70–75% by adjusting the proportion of air that flowed through a
desiccant tube vs. a bubbler in a water-filled flask, which were placed
in parallel upstream of the console intake. Each plant to be measured
was removed from its growth chamber 2–3 h into a photoperiod and
was immediately placed in the cuvette for gas-exchange measurements.
Temperature response measurements were initiated at the lowest temperature and proceeded in a step-wise manner from ;08 to 358C. At
each measurement temperature, the plant was kept in the dark until a
steady-state Rd was obtained and recorded. Saturating PAR was applied
and Pn was recorded after a steady-state rate was attained, which took
10–45 min, depending on temperature. Afterward, the plant was harvested and the leaf area was determined with an area meter (CI-202,
CID, Vancouver, Washington, USA). Whole-canopy Pn and Rd were
calculated using the equations of von Caemmerer and Farquhar (1981)
and were examined on a total one-sided leaf area basis, leaf dry-mass
basis, and whole-canopy or per-plant basis. For each species, Pn and Rd
responses were measured on eight plants that were randomly selected
from the 15 plants available for gas-exchange measurements in each
treatment. We estimated Topt for Pn by drawing curves through the points
of each plant’s response curve by eye and estimating the temperature
of maximum Pn.
We attribute changes in Pn and Rd to differences in temperature in
the cuvette, but should note that air vapor pressure deficits (VPD) also
increased with measurement temperature since relative humidity was
maintained at 70–75%. The same can be said of VPD in the different
daytime temperature regimes of the growth chambers. Indirect evidence
supporting our assumption that the main cause for reductions in Pn at
supraoptimal temperatures was higher temperatures, not higher VPD,
comes from our observation that there was no evidence for an increase
in stomatal limitations to Pn at supraoptimal temperatures, since intercellular CO2 concentrations did not decline at supraoptimal temperatures. A VPD-induced reduction in Pn at supraoptimal temperatures
would likely involve an increase in the stomatal limitation to Pn.
Total chlorophyll and carotenoid concentrations—During the final
growth-analysis harvest, an ;0.1-g (fresh mass) sample was collected
from a fully expanded leaf on each plant for pigment analysis. The leaf
area of the sample was measured, and it was placed in 5 mL of methanol
in a dark refrigerator (48C) overnight. The sample was homogenized
twice in 4 mL of methanol and the homogenate was filtered through a
25-mm mesh screen. Total chlorophyll (Chl) and carotenoid concentrations were calculated by measuring absorbance of the extract with a
spectrophotometer (Lambda2, PerkinElmer, Norwalk, Connecticut,
USA) and using the extinction coefficients of Porra, Thompson, and
Kriedemann (1989).
Statistical analyses—One-way ANOVAs were used to examine
growth-temperature effects, and the LSD (Least Significant Difference)
test was used to compare treatment means. Treatment effects were considered significant at the P , 0.05 level.
RESULTS
In both species, plants grown at a daytime temperature
of 208C had the greatest RGR, being 0.056 g·g21·d21 in
C. quitensis and 0.063 g·g21·d21 in D. antarctica (Fig.
1A). In contrast, plants grown at 128C had the highest
NAR (Fig. 1B). Along with RGR, leaf area ratio (leaf
area per total biomass; LAR) and total leaf area were
highest in plants grown at 208C (Fig. 1C, D). We further
assessed allocation to leaves by examining the leaf mass
ratio (leaf mass:total biomass; LMR). In both species,
LMR increased with daytime growth temperature (Fig.
1D, insets). The canopy architecture of plants in all treatments was generally similar to those of many plants
found at the field collection site. Leaf area index (LAI),
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ET AL.—TEMPERATURE RESPONSE OF
Fig. 1. (A) Relative growth rate (RGR), (B) net assimilation rate
(NAR), (C) leaf area ratio (LAR), and (D) total leaf area of C. quitensis
and D. antarctica grown in the three temperature treatments (7/78C, 12/
78C, 20/78C, 18 h day/6 h night) for 90 d. The insets show (D) leaf
mass ratio (LMR). Horizontal axis refers to daytime growth temperature
(nighttime temperatures were 78C in all treatments). Values are means
6 1 SE (N 5 15).
calculated using only the area under plant canopies (not
bare soil areas in pots), ranged from 6.9 to 11.8 in C.
quitensis and 1.3 to 3.4 in D. antarctica in growth chamber plants, which are similar to values found in plant
canopies at the field site; LAI of C. quitensis at Stepping
Stones can range from 2 to 10 while that of D. antarctica
can range from 1 to 4 (T. A. Day, unpublished data, Arizona State University).
Consistent with the trends in RGR, LAR, total leaf
area, and LMR, plants grown at a daytime temperature
of 208C produced the most total biomass, aboveground
vegetative biomass, and root mass (Fig. 2). Trends in reproductive biomass were not as apparent, although repro-
ANTARCTIC
PLANTS
703
Fig. 2. (A) Total, (B) aboveground, (C) root, and (D) reproductive
biomass of C. quitensis and D. antarctica grown in the three temperature treatments for 90 d. The insets show (C) ratios of root:shoot biomass, where shoot biomass is all aboveground biomass and (D) reproductive:aboveground vegetative biomass. Horizontal axis refers to daytime growth temperature. Values are means 6 1 SE (N 5 15).
ductive biomass tended to increase with growth temperature (Fig. 2D). We assessed allocation to reproductive
structures by examining the ratio of reproductive:aboveground vegetative biomass. This ratio was greatest at
128C in both species (Fig. 2D, insets). The root:shoot
ratio (where shoot biomass is all aboveground biomass)
declined with increasing growth temperature in D. antarctica, while there were no significant differences in
this ratio among treatments in C. quitensis (Fig. 2C, insets).
Along with biomass production, leaf production increased with growth temperature in both species and was
greatest in plants grown at 208C (Fig. 3A). These treatment differences in leaf production were particularly ev-
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Fig. 3. Number of (A) leaves and (B) branches, and (C) cushion
diameter of C. quitensis, and number of (A) leaves and (B) tillers, and
(C) longest tiller length of D. antarctica grown in the three temperature
treatments over the 90-d growth period. Symbol key refers to daytime
growth temperature of each treatment. Values are means 6 1 SE (N 5
15).
ident over the 60- to 90-d growth period (Fig. 3A). Shoot
production in C. quitensis and tiller production in D. antarctica were also greatest in plants grown at 208C (Fig.
3B). Cushion diameter of C. quitensis and length of the
longest tiller in D. antarctica were greatest in plants
grown at 208C (Fig. 3C), but unlike the other parameters
they tended to increase linearly over the 90-d growth period, as opposed to exponentially. We attribute the decline
in length of the longest tiller over the initial 30-d growth
period in D. antarctica at 78 and 128C (Fig. 3C) to the
death of the initial (longest) tiller over this period; at 208C
this initial tiller had already been replaced by a longer
tiller.
On a leaf-area basis, C. quitensis plants grown at a
daytime temperature of 128C had the highest rates of Pn,
when measured at their respective daytime growth temperature (Pchamber; Fig. 4A, solid symbols and inset). When
grown at 78 or 208C daytime temperatures, rates of Pchamber
were only 37 or 58% of those of plants grown at 128C,
respectively. On a whole-canopy basis, plants grown at
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208C had the highest rates of Pn (per plant) when measured at their respective daytime growth temperature
(Fig. 5A, solid symbols). On a leaf dry-mass basis, plants
grown at 128 and 208C had higher rates of Pn than plants
grown at 78C, when measured at their respective daytime
growth temperature (Fig. 5A, solid symbols in inset).
Colobanthus quitensis showed a slight, but significant,
ability for photosynthetic temperature acclimation (LSD,
P , 0.05). The Topt for Pn (leaf-area basis) shifted from
8.48C in plants grown at a daytime temperature of 78C,
to 10.38C in plants grown at 128C, and to 11.58C in plants
grown at 208C (Fig. 4A). Differences in the shapes of the
response curves also suggest some acclimation, as the
slope of the curves at supraoptimal temperatures was
lowest in plants grown at 208C, demonstrating slightly
improved Pn at supraoptimal temperatures in these plants.
Similarly, the slope of the curves at suboptimal temperatures was lowest in plants grown at 78C.
On a leaf-area basis, D. antarctica plants grown at a
daytime temperature of 128C also had the highest rates
of Pn, when measured at their respective daytime growth
temperature (Pchamber; Fig. 4B, solid symbols and inset).
When grown at 78 or 208C daytime temperatures, rates
of Pchamber were only 59 or 64% of those of plants grown
at 128C, respectively. On a whole-canopy basis, plants
grown at 208C had the highest rates of Pn (per plant),
when measured at their respective daytime growth temperature (Fig. 5B, solid symbols). On a leaf dry-mass
basis, plants grown at 128C had the highest rates of Pn,
when measured at their respective daytime growth temperature (Fig. 5B, solid symbols in inset).
Deschampsia antarctica did not appear to acclimate
photosynthetically to changing temperatures. Plants from
the different temperature regimes had similar Topt for Pn
(10.28–10.58C), and the shapes of their response curves
were similar (Fig. 4B).
Both species demonstrated full thermal acclimation of
leaf-area based Rd. For example, the Rd of C. quitensis
plants grown at 78C when measured at 78C (6.0
mmol·m22·sec21) was similar to that of plants grown at
128C when measured at 128C (6.3 mmol·m22·sec21) and
to that of plants grown at 208C when measured at 208C
(5.8 mmol·m22·sec21; Fig. 6A, solid symbols). Similar acclimation of Rd was observed in D. antarctica, with rates
among plants from different temperature regimes similar
when measured at their respective daytime temperatures
(;7 mmol·m22·sec21; Fig. 6B, solid symbols). The Q10
values for Rd (calculated from 58 to 158C) increased with
growth temperature, being 1.9, 2.0, and 2.5 for C. quitensis and 1.7, 1.9, and 2.3 for D. antarctica when grown
at daytime temperatures of 78, 128, and 208C, respectively. In both species, rates of Rd on a whole-canopy basis
(per plant) were higher in plants grown at 208C, than at
78 and 128C (Fig. 7). On a leaf dry-mass basis, rates of
Rd were similar among plants grown at different temperature regimes, when measured at their respective daytime
temperatures (Fig. 7, inset). When measured at the nighttime temperature of 78C used for all treatments, rates of
Rd on a dry-mass basis were highest in plants grown at
a daytime temperature of 78C and lowest in plants grown
at a daytime temperature of 208C (Fig. 7, inset).
In both species, plants grown at a daytime temperature
of 128C had significantly higher leaf total Chl concentra-
May 2000]
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705
Fig. 4. Temperature response of net photosynthesis (Pn) on a leaf-area basis in (A) C. quitensis and (B) D. antarctica grown in the three
temperature treatments for 60–85 d. Symbol key refers to daytime growth temperature of each treatment. The filled symbols denote the Pn rate of
plants in each temperature treatment measured at their respective daytime temperature (i.e., Pchamber). The insets show the optimal temperature (Topt)
for Pn and Pchamber of plants in each temperature treatment. Values are means 6 1 SE (N 5 8).
tions (leaf-area basis) than plants grown at 78 or 208C
(Fig. 8A). Growth temperature regime had no effect on
leaf carotenoid concentrations, or the ratios of Chl a:b or
carotenoids:total Chl (data not shown). Leaf total Chl
concentrations on a dry-mass basis were significantly
higher in plants of both species grown at 128 compared
to 208C, but were not significantly higher than concentrations in plants grown at 78C (data not shown). In both
species, plants grown at 128C had significantly higher
specific leaf mass (SLM) than plants grown at 78C, and,
Fig. 5. Temperature response of net photosynthesis (Pn) on a whole-canopy or per-plant basis in (A) C. quitensis and (B) D. antarctica grown
in the three temperature treatments for 60–85 d. Symbol key refers to daytime growth temperature of each treatment. The filled symbols denote
the Pn rate of plants in each temperature treatment measured at their respective daytime growth temperature (i.e., Pchamber). The insets show the Pn
on a leaf dry-mass basis, with the filled symbols denoting Pchamber rates. Values are means 6 1 SE (N 5 8).
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Fig. 6. Temperature response of dark respiration (Rd) on a leaf-area basis in (A) C. quitensis and (B) D. antarctica grown in the three temperature
treatments for 60–85 d. Symbol key refers to daytime growth temperature of each treatment. The filled symbols denote the Rd rate of plants in
each temperature treatment measured at their respective daytime growth temperature. Values are means 6 1 SE (N 5 8).
in the case of C. quitensis, than plants grown at 208C as
well (Fig. 8B). We also recalculated Pn on a total leafChl basis and found that the rates of Pn per total Chl
were greatest at each measurement temperature in plants
grown at 208C and lowest in plants grown at 78C (data
not shown).
DISCUSSION
Relative growth rate and biomass production increased
with daytime growth temperature in both species and
were substantially higher in plants grown at a daytime
temperature of 208C than at 78 or 128C. Greater growth
Fig. 7. Temperature response of dark respiration (Rd) on a whole-canopy or per-plant basis in (A) C. quitensis and (B) D. antarctica grown in
the three temperature treatments for 60–85 d. Root respiration was not measured. Symbol key refers to daytime growth temperature of each
treatment. The filled symbols denote the Rd rate of plants in each temperature treatment measured at their respective daytime temperature. The
insets show the Rd on a leaf dry-mass basis, with the filled symbols denoting Rd rates at their respective daytime growth temperature. Values are
means 6 1 SE (N 5 8).
May 2000]
XIONG
ET AL.—TEMPERATURE RESPONSE OF
Fig. 8. (A) Leaf total chlorophyll concentration and (B) specific leaf
mass (SLM) of C. quitensis and D. antarctica grown in the three temperature treatments for 90 d. Horizontal axis refers to daytime growth
temperature. Values are means 6 1 SE (N 5 15).
rates at 208C could result from these plants having (1)
higher Pn per unit leaf area, (2) lower Rd per unit leaf
area, (3) lower SLM, and/or (4) greater biomass allocation to leaves (higher LMR).
Concerning the first point (Pn per unit leaf area), rates
were substantially lower, not higher, in plants grown at
20 8C than in plants grown at 128C. Specifically, rates of
Pn in plants grown at 208C were only 58 (C. quitensis)
and 64% (D. antarctica) of rates of plants grown at 128C,
when measured at their respective daytime growth temperatures (Fig. 4, solid symbols and inset). This is not
surprising since the relationship between growth and photosynthesis, when expressed on a leaf-area basis, is often
poor (Pereira, 1995; Lambers, Chapin, and Pons, 1998).
In contrast to leaf-area based Pn, rates of Pn per plant
appeared well correlated with growth and biomass among
the three treatments. For example, linear least-squares
correlation analyses of the rate of Pn per plant at daytime
growth temperatures (Fig. 5, solid symbols) vs. total biomass (Fig. 2A) gave coefficients of determination (r2) of
0.99 (C. quitensis) and 0.92 (D. antarctica). Obviously,
these strong correlations between Pn per plant and biomass production were due to the large differences in the
leaf areas of plants grown at different temperatures (i.e.,
allocation; see below), and not to differences in Pn per
unit leaf area.
ANTARCTIC
PLANTS
707
Regarding the second point (Rd), both species exhibited
full acclimation of Rd, such that rates of Rd per unit leaf
area in plants grown at 208C were similar to those in
plants grown at 78 and 128C, when measured at their respective daytime temperatures (Fig. 6, solid symbols).
Furthermore, plants grown at a 208C daytime temperature
would have substantially lower nighttime (78C) rates of
Rd, being only ;30 and 41% of the rates of plants grown
at the 78 and 128C, respectively. The relative importance
or contribution of this down regulation of canopy Rd to
improved plant performance at 208C is difficult to assess
because we have no information on root respiration or on
canopy respiration rates in the light. However, this acclimation of Rd would improve the plant carbon balance of
plants growing at higher temperatures by helping to
maintain respiratory carbon losses per leaf area at levels
similar to or lower than those of plants growing at lower
temperatures; thus, this should be partly responsible for
the improved growth of these plants at 208C.
Concerning the third point (SLM), higher RGR is often
correlated with higher SLM (Grace, 1988; Poorter, 1989;
Pereira, 1995; Lambers, Chapin, and Pons, 1998), and
this usually leads to higher rates of Pn on a leaf-mass
basis. However, we found plants grown at a daytime temperature of 208C (highest RGR) had lower SLM (Fig. 8B)
and similar or lower rates of Pn per leaf mass, when measured at their daytime growth temperatures (Fig. 5, insets)
than plants grown at 128C. Thus, differences in SLM do
not appear to explain the differences in growth rates that
we observed at different temperatures in these species.
With respect to the fourth point (leaf allocation), plants
grown at a daytime temperature of 208C allocated more
biomass to leaves than plants at 128 or 78C. For example,
plants grown at 208C had 1.1–1.3 times the LMR, 1.6
times the LAR, and produced 3.4–3.7 times as much leaf
area (Fig. 1), and 2 (D. antarctica) to 4 (C. quitensis)
times as many leaves (Fig. 2) as plants grown at 12 8C.
High RGR has been linked to enhanced partitioning to
leaf production and leaf area in other species (Potter and
Jones, 1977; Patterson, Meyer, and Quinby, 1978). In the
case of D. antarctica, greater biomass allocation to leaves
at 208C was also accompanied by less allocation to roots
(i.e., lower root:shoot ratio; Fig. 2C). This trend has been
noted in several surveys; at optimal temperatures for
RGR and total biomass production, allocation to roots
and root:shoot ratios are typically at a minimum (Davidson, 1969; Bowen, 1991; Lambers, Chapin, and Pons,
1998). In conclusion, greater biomass allocation to leaf
production by plants grown at 208C more than compensated for their reduced Pn per leaf area and resulted in
much greater total biomass production.
It would appear that the major difference between the
more productive plants grown at a daytime temperature
of 208C and those grown at 78 or 128C was the former
plants’ ability to produce more leaves, total leaf mass,
and total leaf area. Why were the plants grown at 208C
able to produce more leaves than plants at 128C, when
their daytime rates of Pn per unit leaf area were only 58
(C. quitensis) and 64% (D. antarctica) of the rates in
plants at 128C? On a leaf-area basis, respiratory losses
may have been lower in plants growing at 208C, because
their daytime Rd rates were similar to those of plants in
other treatments, while their nighttime rates of Rd (at tem-
708
AMERICAN JOURNAL
perature of 78C) would be lower than those of plants in
other treatments (Fig. 6). However, the much larger leaf
area of plants grown at 208C would lead to high Rd rates
per plant; at daytime temperatures Rd rates on a wholecanopy basis would be much higher in plants growing at
208C, while nighttime whole-canopy Rd rates appear to
be similar among the different temperature treatments
(Fig. 7). As previously mentioned, the relationship between growth and photosynthesis, particularly on a leafarea basis, is usually poor; this apparent discrepancy reflects a complex, poorly understood relationship between
these two processes (Poorter, 1989; Poorter and Remkes,
1990; Lambers and Poorter, 1992; Pereira, 1995; Lambers, Chapin, and Pons, 1998). In addition to the large
difference in the time scales between instantaneous photosynthetic measurements and long-term growth, growth
is controlled by several other processes in addition to
carbon acquisition. While the underlying mechanisms
and constraints on growth remain unclear in many situations, in the case of low-temperature limitations, leaf
elongation and plant growth are generally more sensitive
to temperature than the rate of Pn, and growth processes
appear to have a higher temperature optima than Pn
(Thorne, Ford, and Watson, 1967; Forde, Whitehead, and
Rowley, 1975; Woodward, Körner, and Crabtree, 1986;
Körner and Woodward, 1987; Grace, 1988; Körner and
Larcher, 1988; Pollock and Eagles, 1988). For example,
plants from cold regions can have low-temperature
thresholds for leaf extension that are 68–88C higher than
photosynthetic thresholds (Woodward, Körner, and Crabtree, 1986; Körner and Woodward, 1987; Körner and
Larcher, 1988). Our findings on Antarctic species certainly support this idea that the temperature optima for
growth are considerably higher than those for Pn.
Relative acclimation of photosynthesis refers to an increase (or decrease) in Topt of Pn when plants are grown
at a higher (or lower) temperature (Mooney, Björkman,
and Collatz, 1978; Berry and Björkman, 1980). In contrast, absolute acclimation refers to a shift in the photosynthetic temperature response, such that the rate of Pn
is improved at the new growth temperature. For example,
plants grown at a higher temperature display absolute acclimation if their rate of Pn at this higher growth temperature is greater than it was originally (when measured
at this higher temperature). In terms of carbon balance,
the ability for absolute acclimation should be more important than relative acclimation when considering the
performance of a species under a new temperature regime. Colobanthus quitensis showed a slight degree of
relative acclimation in that Topt shifted slightly in response to different temperature regimes (Fig. 4A). However, there was no evidence for absolute photosynthetic
acclimation in C. quitensis, as plants grown at low temperature (78C) did not have a higher rate of Pn at 78C
than plants grown at 128C, and plants grown at high temperature (208C) did not have a higher rate of Pn at 208C
than plants grown at 128C. Regarding D. antarctica, there
was no evidence for relative acclimation as plants grown
at all temperatures had similar Topt. There was also no
evidence for absolute acclimation in this species as plants
grown at 128C had higher rates of Pn at 78 and 208C than
plants grown at these latter temperatures. Thus, these species appear to possess only a slight (C. quitensis) or neg-
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[Vol. 87
ligible (D. antarctica) ability for relative acclimation, and
probably more importantly, no ability for absolute acclimation of Pn to temperature. Further evidence for their
low photosynthetic acclimation potential comes from the
similarity of the Topt in these chamber-grown plants with
that of plants growing at the field site in Antarctica,
where C. quitensis and D. antarctica had whole-canopy
Topt for Pn of 148 and 108C, respectively (Xiong, Ruhland,
and Day, 1999).
Species native to habitats with large temperature variations during their growing season generally display a
strong ability to acclimate photosynthetically, whereas
species from habitats with relatively stable thermal regimes over the growing season tend to possess a poor
ability for such acclimation (Berry and Björkman, 1980;
Björkman, 1981; Öquist, 1983). For example, Pearcy
(1976, 1977) found that the Atriplex lentiformis plants
native to coastal regions with a moderating maritime influence displayed less ability for photosynthetic acclimation compared to their inland desert counterparts. Similarly, Billings et al. (1971) found that populations of Oxyria digyna native to the arctic, where summer temperatures are relatively stable, had less ability for
photosynthetic acclimation than alpine populations. The
inability for photosynthetic acclimation in C. quitensis or
D. antarctica may be correlated with the very stable temperature regime along the Antarctic Peninsula, where the
diel range in temperature averages ,68C during the growing season.
Although thermal acclimation of Rd has received far
less attention than acclimation of Pn, the ability for acclimation of Rd also appears to vary greatly among species, as well as among populations and ecotypes within
species (Mooney, Wright, and Strain, 1964; Billings et
al., 1971; Körner and Larcher, 1988; Larigauderie and
Körner, 1995; Arnone and Körner, 1997). While some
species show no ability for acclimation of Rd, others show
full or complete acclimation such that their rates of Rd,
when measured at their respective growth temperatures,
are similar. Although it is unclear whether plants from
cold climates have a greater ability for thermal acclimation of Rd than plants from warmer climates (Larigauderie
and Körner, 1995), acclimation appears to be very common in plants from cold climates (Körner and Larcher,
1988) and both C. quitensis and D. antarctica displayed
full acclimation of Rd. Rates of Rd in plants grown at 78C
when measured at 78C were similar to rates in plants
grown at 128C when measured at 128C, and to rates in
plants grown at 208C when measured at 208C (Fig. 5).
As a result, not only did plants grown at a 208C daytime
temperature have daytime rates of Rd that were similar to
those of plants growing at the lower temperatures, but
they also would have substantially lower nighttime (78C)
rates of Rd, being only ;30% of the nighttime rate of Rd
of plants grown at the 78C daytime temperature. Interestingly, we found that plants displayed full acclimation
to their prevailing daytime temperature regime as opposed to their prevailing median or mean diel temperature. It is unclear whether different nighttime temperature
regimes would have altered their acclimation response
since nighttime temperatures were similar in all treatments. In any case, the respiratory acclimation response
shown by these species to prevailing daytime tempera-
May 2000]
XIONG
ET AL.—TEMPERATURE RESPONSE OF
tures would improve plant carbon balance by reducing
respiratory carbon losses and would be beneficial under
continued regional warming along the Peninsula.
Relatively rapid increases in the size and numbers of
populations of C. quitensis and D. antarctica along the
Peninsula have recently been documented, and these increases have been suggested to be due to improved reproductive performance as the result of longer, warmer
growing seasons associated with the recent warming
trend (Fowbert and Smith, 1994; Smith, 1994; Grobe,
Ruhland, and Day, 1997). In support of these suggestions,
Day et al. (1999) passively warmed naturally growing
plants at the Stepping Stones field site for two growing
seasons, raising diurnal canopy air temperatures from a
growing-season average of 4.38–6.58C, and found that
warming accelerated the development of reproductive
structures and led to substantial increases in seed production of both species during both field seasons. However, the influence of warming on vegetative growth under field conditions was less clear. Warming led to greater
leaf and shoot production and foliar cover of C. quitensis,
whereas it led to shorter leaves and less leaf production
and foliar cover in D. antarctica. Day et al. (1999) suggested that C. quitensis may have outcompeted D. antarctica under field warming treatments. In contrast to
these field results, based on our present growth-chamber
results we would suspect that the vegetative performance
of both species, not only C. quitensis, would be improved
under field warming treatments. Prevailing air temperatures during the growing season are usually suboptimal
for Pn and growth in these species. For example, hourly
mean canopy air temperatures at the Stepping Stones field
site are ,108C for 86% of diurnal periods, and diurnal
canopy air temperature averages 4.38C (Day et al., 1999).
Thus, warming would usually bring these species closer
to their Topt for Pn, and also raise diurnal canopy air temperatures closer to their optima for growth, which our
current results suggest are probably close to 208C and
certainly above 128C. We do not interpret the differences
in the warming response of D. antarctica in our previous
field study and the present growth-chamber study to be
in conflict because there was no plant competition in the
growth-chamber study. In contrast, in the treatment plots
at the Stepping Stones field site competition between
these species was probably high as they were growing in
close proximity with one another; plots were placed over
tussocks of D. antarctica that made up patches of prostrate turf up to several square meters in area and matforming cushions of C. quitensis were interspersed
throughout the turf. While we suspect that interspecific
competition is important in these more developed communities and that it can influence the growth response of
these species to warming, we also suspect that our current
growth-chamber results are also applicable to many communities along the Peninsula because D. antarctica often
occurs in the absence of C. quitensis. In a survey of 116
locations containing vascular plants along the west coast
of the Peninsula, 58% contained only D. antarctica (Komárková, Poncet, and Poncet, 1985).
In conclusion, Antarctic vascular plants exhibited a
weak or negligible ability for Pn acclimation to temperature, which may stem from the relatively stable thermal
regime along the Peninsula. Both species exhibited full
ANTARCTIC
PLANTS
709
thermal acclimation of Rd. Although Pn on a leaf-area
basis was greatest in both species when grown at a daytime temperature of 128C, plants grown at a daytime temperature of 208C produced far more biomass, which appeared primarily due to enhanced leaf-area production.
We suspect that continued regional warming will generally improve the performance of these species along the
Antarctic Peninsula, particularly in communities where
interspecific competition between these vascular plants is
less developed or lacking.
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