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0 Department of Plant Biology and The Photosynthesis Center, Arizona State University, Tempe, Arizona 85287-1601 USA
Received for publication March 23, 1999. Accepted for publication August 26, 1999.
ABSTRACT
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: 7°C day/7°C night, 12°C day/7°C night, and 20°C day/7°C night (18 h/6 h). These daytime temperatures represent suboptimal (7°C), near-optimal (12°C), and supraoptimal (20°C) 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 20°C had greater RGR (relative growth rate) and produced 2.2–3.3 times as much total biomass as plants grown at daytime temperatures of 12° or 7°C. Plants grown at 20°C 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 12° or 7°C. Greater RGR and biomass production at 20°C 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 12°C, and rates of plants grown at 20°C were only 58 (C. quitensis) or 64% (D. antarctica) of the rates in plants grown at 12°C. Thus, lower Pn per leaf area in plants grown at 20°C 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 20°C, 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 8.4° to 10.3° to 11.5°C as daytime growth temperatures increased from 7° to 12° to 20°C. 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 (10°C) 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 12°C were higher than those of plants grown at daytime temperatures of 7° or 20°C, 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: Antarctica • Colobanthus quitensis • Deschampsia antarctica • growth • photosynthesis • respiration • temperature • warming
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 ~2.6°C and mean summer (January–March) temperature rose ~1.5°C at Faraday/Vernadsky Station (65°15' S, 64°16' W) along the Peninsula (King, 1994
; Smith, 1994
; Smith, Stammerjohn, and Baker, 1996
). Additional evidence 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 vegetative 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 13° and 19°C, respectively, and both species maintained considerable rates of Pn (~30% of their maximal Pn) at ~0°C 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 >20°C), rates of Pn in both species in the field were very low (<1 µmol·m-2·sec-1). They also found that the Topt for Pn was relatively low (10° in D. antarctica, and 14°C in C. quitensis), and that they had unusually low high-temperature compensation points (22° in D. antarctica, and 26°C in C. quitensis). The apparent sensitivity of Pn in these species to moderate temperatures (20°C) 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. antarctica 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 (64°47' S; 64°00' 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 -2.3°C, and monthly means range from -7.5°C in July to 2.7°C 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 <6°C. For example, daily temperatures in November, the coldest month of the growing season, range from an average low of -2.7°C to a high of 2.4°C, and daily temperatures in January, the warmest month of the growing season, range from an average low of 0.7°C to a high of 5.1°C. 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 4.3°C, and was <10°C for 86% of diurnal periods, 10°–20°C for 13% of these periods, and >20°C for 1% of these periods (Day et al., 1999
).
Plants were transported in chilled boxes (5°C) to Arizona State University and propagated in growth chambers under a 12°/12°C (day/night) temperature regime with a 12-h photoperiod, during which time they received 400 µmol·m-2·sec-1 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 20°C under 75 µmol·m-2·sec-1 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 x 11 x 11 cm, L x W x 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 x 25 cm, D x H) containing the same soil mixture.
Temperature regime treatments
We examined the response of plants to three temperature regime treatments: 7°/7°C, 12°/7°C, or 20°/7°C day/night (18 h/6 h) temperatures. These three daytime temperatures represent suboptimal (7°C), near-optimal (12°C), and supraoptimal (20°C) 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 temperature 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 µmol·m-2·sec-1 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 60°C 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:
; Hunt, 1990
).
Net photosynthesis and dark respiration
Whole-canopy net photosynthesis (Pn) and dark respiration (Rd) rates of individual 60- to 85-d-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 custom-made clear teflon-lined cylindrical double-walled cuvette (7.5 x 11 cm, ID x 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 7°, 12°, or 20°C 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 µmol·m-2·sec-1 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 µL/L with a CO2 injector system (6400-01, Li-COR). Relative humidity was maintained 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 ~0° to 35°C. 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 (4°C) overnight. The sample was homogenized twice in 4 mL of methanol and the homogenate was filtered through a 25-µm 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 20°C had the greatest RGR, being 0.056 g·g-1·d-1 in C. quitensis and 0.063 g·g-1·d-1 in D. antarctica (Fig. 1A). In contrast, plants grown at 12°C 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 20°C (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), 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).
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On a leaf-area basis, D. antarctica plants grown at a daytime temperature of 12°C 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 7° or 20°C daytime temperatures, rates of Pchamber were only 59 or 64% of those of plants grown at 12°C, respectively. On a whole-canopy basis, plants grown at 20°C 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 12°C 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 (10.2°–10.5°C), 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 7°C when measured at 7°C (6.0 µmol·m-2·sec-1) was similar to that of plants grown at 12°C when measured at 12°C (6.3 µmol·m-2·sec-1) and to that of plants grown at 20°C when measured at 20°C (5.8 µmol·m-2·sec-1; 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 µmol·m-2·sec-1; Fig. 6B, solid symbols). The Q10 values for Rd (calculated from 5° to 15°C) 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 7°, 12°, and 20°C, respectively. In both species, rates of Rd on a whole-canopy basis (per plant) were higher in plants grown at 20°C, than at 7° and 12°C (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 7°C used for all treatments, rates of Rd on a dry-mass basis were highest in plants grown at a daytime temperature of 7°C and lowest in plants grown at a daytime temperature of 20°C (Fig. 7, inset).
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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 20°C than at 7° or 12°C. Greater growth rates at 20°C 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 °C than in plants grown at 12°C. Specifically, rates of Pn in plants grown at 20°C were only 58 (C. quitensis) and 64% (D. antarctica) of rates of plants grown at 12°C, 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.
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 20°C were similar to those in plants grown at 7° and 12°C, when measured at their respective daytime temperatures (Fig. 6, solid symbols). Furthermore, plants grown at a 20°C daytime temperature would have substantially lower nighttime (7°C) rates of Rd, being only ~30 and 41% of the rates of plants grown at the 7° and 12°C, respectively. The relative importance or contribution of this down regulation of canopy Rd to improved plant performance at 20°C 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 20°C.
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 20°C (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 12°C. 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 20°C allocated more biomass to leaves than plants at 12° or 7°C. For example, plants grown at 20°C 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 °C. 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 20°C 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 20°C 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 20°C and those grown at 7° or 12°C was the former plants' ability to produce more leaves, total leaf mass, and total leaf area. Why were the plants grown at 20°C able to produce more leaves than plants at 12°C, 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 12°C? On a leaf-area basis, respiratory losses may have been lower in plants growing at 20°C, because their daytime Rd rates were similar to those of plants in other treatments, while their nighttime rates of Rd (at temperature of 7°C) would be lower than those of plants in other treatments (Fig. 6). However, the much larger leaf area of plants grown at 20°C would lead to high Rd rates per plant; at daytime temperatures Rd rates on a whole-canopy basis would be much higher in plants growing at 20°C, 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 leaf-area 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 6°–8°C 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 (7°C) did not have a higher rate of Pn at 7°C than plants grown at 12°C, and plants grown at high temperature (20°C) did not have a higher rate of Pn at 20°C than plants grown at 12°C. 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 12°C had higher rates of Pn at 7° and 20°C than plants grown at these latter temperatures. Thus, these species appear to possess only a slight (C. quitensis) or negligible (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 14° and 10°C, 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 <6°C 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 7°C when measured at 7°C were similar to rates in plants grown at 12°C when measured at 12°C, and to rates in plants grown at 20°C when measured at 20°C (Fig. 5). As a result, not only did plants grown at a 20°C 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 (7°C) rates of Rd, being only ~30% of the nighttime rate of Rd of plants grown at the 7°C 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 temperatures 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 4.3°–6.5°C, 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 <10°C for 86% of diurnal periods, and diurnal canopy air temperature averages 4.3°C (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 20°C and certainly above 12°C. 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 mat-forming 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 thermal acclimation of Rd. Although Pn on a leaf-area basis was greatest in both species when grown at a daytime temperature of 12°C, plants grown at a daytime temperature of 20°C 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.
FOOTNOTES
1 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: tadday{at}asu.edu
).
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