Photosynthetic acclimation to temperature and drought in the endemic chelan rockmat, Petrophytum cinerascens (Rosaceae).
Two basic mechanisms for plants to survive changes in global temperature are: (1) migration to areas with a suitable environment; and (2) acclimation or adaptation to the changed environment. For example, bristlecone pine (Pinus longaeva) which grows near tree line of the southern White Mountains of California, demonstrates migration to a suitable environment. The presence of dead trees above the current tree line indicates that climate was once warmer, but trees were not able to acclimate to lower temperatures (LaMarche and Mooney, 1967). In contrast, other plant species are able to acclimate to changes in temperature or other climatic factors such as drought. Photosynthesis in the coastal shrub Encelia californica acclimated to either higher or lower growth temperature in as little as 24 h (Mooney and Shropshire, 1967). In addition, the differential ability of plants to acclimate to temperature change was demonstrated in a study using two [C.sub.4] grasses from the genus Bouteloua. The warm environment species B. eriopodia acclimated to changes in growth temperature, whereas the cool environment species B. gracilis did not (Bowman and Turner, 1993).
Endemic plant species tend to be vulnerable to environmental changes. Although many endemic, threatened and rare species may be locally abundant, their populations are limited in number across the landscape. Restricted distribution of plant species may be due to various factors, including geographic isolation or habitat specialization (Holsinger and Gottlieb, 1991). A geographically isolated plant is not able to disperse its seeds beyond some geographic barrier and thus may not be able to migrate to new areas when environmental conditions change. For a habitat specialist, species may go extinct during climate change because they are unable to tolerate changes in precipitation, temperature or other environmental factors. Because these habitat specialists occupy a small niche, such plants become extremely vulnerable to any change in environment. The continued existence of endemic plants during global climate change depends primarily on five factors: (1) the plant's potential to acclimate to environmental changes; (2) the plant's genetic variability; (3) environmental variables which limit plant distribution and dispersal; (4) the extent of direct disturbance by human activity and (5) the geographic dispersion of individual plants and of populations.
Petrophytum cinerascens (Piper) Rydb. (Rosaceae), the Chelan rockmat, is an endemic plant found only along the Columbia River between Wenatchee and Lake Chelan, Washington. This species is associated with cliffs and rock outcrops and is not found on sites with deep soils. Although Hitchcock and Cronquist (1973) described these rock outcrops as basalt, the rocks along this segment of the Columbia River are predominantly composed of gneiss, schist and granite (Alt and Hyndman, 1984). Because of the steep slopes and restricted land use around the rock outcrops, direct human disturbance of the P. cinerascens population is likely to be small. Although all populations of P cinerascens have not been mapped, its distribution and dispersal potential are known to be very limited. Thus, unless P cinerascens can acclimate or adapt to global climate change, this species is susceptible to extinction should global warming occur. The overall goal of this study was to explore potential use of this endemic species as an indicator of climate change by examining the plant's ability to photosynthetically acclimate to increased growth temperature.
Plant collection. - Rooted samples of Petrophytum cinerascens were collected from rock outcrops and soil derived from the Swakane gneiss and schist along a section of the Columbia River N of Wenatchee, Washington (approximately 47 [degrees] 30 [minutes] N, 120 [degrees] 19 [minutes] E, 500 m elevation). Six genets were represented by sampling an individual plant on each of three N- and three S-facing slopes. Six clones were produced from each genet by rooting shoot cuttings in peat moss. We then planted each rooted clone into a 2-liter pot filled with a 3:1 mixture of potting soil to coarse sand. Clones were allowed to establish in the pots for 9 mo under greenhouse conditions, during which time they were well watered and fertilized weekly with 20:20:20 N:P:K. In addition, we applied 3-5 pellets of Temik as needed for aphid control.
Experimental treatments. - We randomly assigned two clones of each genet to three growth chambers (Model E7H, Conviron Inc., Hayward, California). One-thousand watt, metal halide, lamps (G-4 Green House Luminaire fixtures, Energy Techniques, York, Pennsylvania) were hung over each of the sealed growth chambers to provide a greater photosynthetic photon flux density (PPFD) than that provided by the incandescent and fluorescent light bank built into the chambers. Although light intensity inside the chamber at plant height ranged from 740 PPFD [[micro]mol] [m.sup.-2] [s.sup.-1] in the corners to 1150 PPFD [[micro]mol] [m.sup.-2] [s.sup.-1] in the center, we placed plants only near the center of the chamber where PPFD exceeded 785 [[micro]mol] [m.sup.-2] [s.sup.-1]. Differences in light distribution within the chambers were compensated by a double rotation system. Plants were sequentially moved from the back to the front of the chamber as well as from the left to right side every other day. For the first 21 days, all growth chambers were set at 25/18 C day/night temperatures with a 12-h photoperiod. We then adjusted all growth chambers to 30/16 C for 7 days before beginning treatments. During this 28-day period, plants were watered with enough water to saturate the soil, 3 days a week.
Two sets of experimental treatment were imposed: 3 growth temperature treatments and 2 watering treatments. Temperature treatments of 30/16, 34/20 and 38/24 C day/night were assigned randomly to one of the three growth chambers. The base daytime temperature treatment of 30 C was determined from the long-term, average maximum temperature measured in Wenatchee, Washington during June through August The increase of 4 degrees from 30 to 34 C is the average annual increase in temperature within 100 yr from model predictions (Flaschka et al., 1987; Roeckner, 1992). The increase of 8 degrees to 38 C is the maximum that Roeckner (1992) predicted. For the well-watered treatment, plants were watered Monday, Wednesday and Friday with enough water to saturate the soil. Plants subjected to periodic drought conditions were watered Monday and Friday with enough water to saturate the soil. For all chambers, we maintained photoperiod at 12 h. All plants were fertilized and treated with Temik every other week on a scheduled watering day. Fertilization and pest control were stopped 11 days before the initiation of gas exchange measurements. Plants were well watered before gas exchange measurements were performed.
Leaf gas exchange and nitrogen content. - Gas exchange measurements started after plants had experienced experimental treatments for 81 days. Gas exchange measurements were made in a laboratory setting using gas exchange systems similar to that of Field et al. (1982). Because our primary interest was temperature acclimation of photosynthesis, we measured gas exchange at step intervals of leaf temperature, i.e., a temperature response curve. Protocol for the response curve followed that of Bloom et al. (1980). Steady-state measurements of leaf gas exchange were made sequentially at 28, 24, 20, 24, 28, 30, 34, 38, 42, 46, 38, 30 and 28 C. Light for leaf gas exchange was supplied by slide projector bulbs with an irradiance between 1.5 and 2.0 mmol [m.sup.-2] [s.sup.-1]. Dew point and C[O.sub.2] concentration inside the gas exchange cuvette were held constant and near ambient levels; mean [+ or -] standard error for dew point and C[O.sub.2] were 2.3 [+ or -] 0.1 and 358 [[micro]mol] [mol.sup.-1] [+ or -] 0.5, respectively. Net assimilation ([A.sub.net]), transpiration (E), leaf conductance (g) and intercellular C[O.sub.2] ([c.sub.i]) were calculated according to equations from von Caemmerer and Farquhar (1981). Gas exchange measurements occurred over a 31-day period during which experimental treatments were maintained.
Samples for total leaf nitrogen were acquired from leaf material used during gas exchange. Leaf material was dried at 65 C for a minimum of 48 h, then ground using a mortar and pestle. Total leaf N was obtained using a Perkin-Elmer 2400 CHN Elemental Analyzer (Norwalk, Connecticut).
Statistical analysis. - We used SAS System for Personal Computer Software (SAS Institute Inc., 1987) for regression analysis of individual temperature response curves. The first step in the procedure was to detect and delete visual and statistical outliers from within the set of gas exchange measurements that comprised each temperature curve. We detected visual outliers by plotting the residuals against the predicted values. Values that appeared to stray from the main cluster of observations were considered for deletion. To detect statistical outliers that would influence the shape of the curve, the standardized difference between predicted and observed values was calculated (Dffits procedure in PROC REG). Standard differences greater than 0.295 for 14 observations, 0.960 for 13 observations and 1.0 for 12 observations provided the criterion to identify statistically influential observations (Freund and Littell, 1986). To identify noninfluential statistical outliers (points off the curve but not influencing the fit of the curve), we used a more sensitive version of studentized residuals. Values for studentized residuals are given in standard deviations, and any value beyond 2.5 standard deviations is commonly considered an outlier (Freund and Littell, 1986). After identification of potential outliers, we deleted visual and statistical outliers only if we documented difficulties during gas exchange measurements or if gas exchange parameters were not held at proper experimental conditions. However, if deletion of the visual or statistical outlier(s) made only small changes to the fitted curve, we did not delete the observation(s).
After removing appropriate outliers from an individual temperature response curve, three characteristics of the curves were calculated. We used response surface regression analysis in SAS (PROC RSREG) to calculate the optimum temperature for net assimilation ([T.sub.opt]), the high temperature x-axis intercept or compensation point ([T.sub.high]), and the assimilation rate at optimal temperature for assimilation ([A.sub.opt]) for each temperature curve. We then used analysis of variance (PROC GLM) to determine if these characteristics of the curves ([T.sub.opt], [T.sub.high], and [A.sub.opt]) differed among the experimental treatments. The data were analyzed as a 3 x 2 split-plot experimental design. The main effect was growth temperature, and the watering treatment was a split-plot factor. Main effects, interaction terms, and mean comparisons were considered significant if P [less than or equal to] 0.05.
RESULTS AND DISCUSSION
The general response of net assimilation ([A.sub.net]) to leaf temperature for Petrophytum cinerascens [ILLUSTRATION FOR FIGURE 1 OMITTED] was similar to that for many [C.sub.3] plants (Smith and Nowak, 1990). [A.sub.net] increased with increased leaf temperature up to an optimal temperature ([T.sub.opt]), then declined. At all measured leaf temperatures, mean [A.sub.net] of leaves for clones grown at 30/16 C was greater than that at 34/20 C, which in turn was greater than that at 38/24 C.
[TABULAR DATA FOR TABLE 1 OMITTED]
The main effect of growth temperature on the assimilation rate at the optimal temperature for assimilation ([A.sub.opt]) was significant in the AOV (Table 1a). [A.sub.opt] for clones grown at 30/16 and 34/20 C was significantly greater than that at 38/24 C, but the difference in [A.sub.opt] between clones grown at 30/16 and at 34/20 C was not significant (Table 1b). Neither the water split-plot effect nor the interaction term was significant (Table 1a). [A.sub.opt] decreased with increased growth temperature by 58% for well-watered clones and by 23% for clones with periodic drought treatments [ILLUSTRATION FOR FIGURE 2A OMITTED].
[T.sub.high] and [T.sub.opt] were not significantly affected by growth temperature or watering treatment (Table 1a). [T.sub.high] averaged 51 C for clones grown at 30/16 and 34/20 C and 53 C for clones grown at 38/24 C [ILLUSTRATION FOR FIGURE 1 OMITTED]. Although the difference was not significant, [T.sub.high] for the periodic drought treatment was several degrees higher than that for the well-watered clones when grown at 30/16 and 38/24 C [ILLUSTRATION FOR FIGURE 2B OMITTED]. [T.sub.opt] averaged between 24 and 28 C for clones grown at 30/16, 34/20 and 38/24 C [ILLUSTRATION FOR FIGURE 1 OMITTED]. [T.sub.opt] was also similar between watering treatments [ILLUSTRATION FOR FIGURE 2B OMITTED].
We examined g, [c.sub.i] and intrinsic water use efficiency (WUE) from gas exchange measurements at leaf temperatures of 24 and 28 C, which bracketed the optimum temperature for photosynthesis. Leaf conductance was significantly different between clones exposed to periodic drought and those exposed to well-watered conditions at each growth temperature (Table 1a, [ILLUSTRATION FOR FIGURE 3A OMITTED]). However, well-watered clones had no significant difference in g between growth temperatures 30/16 and 34/20, but g was significantly lower for clones grown at 38/24 C (Table 1c). In contrast, g for the periodic drought clones grown at 30/16 C were significantly lower than that at the higher growth temperatures. For both watering treatments, [c.sub.i] for clones grown at 30/16 were also significantly lower than that at the higher growth temperatures (Table 1a, [ILLUSTRATION FOR FIGURE 3B OMITTED]). In addition, well-watered clones had higher [c.sub.i] than clones exposed to periodic drought. Conversely, WUE decreased significantly as growth temperature increased for both well watered and periodic drought clones. WUE for well-watered clones was significantly lower than for clones exposed to periodic drought (Table 1a, [ILLUSTRATION FOR FIGURE 3C OMITTED]).
The decrease in [A.sub.net] with increased growth temperature does not appear to be due to stomatal limitation. Under the periodic drought conditions in our study, the supply of C[O.sub.2] as indicated by g and [c.sub.i] increased with increased growth temperature [ILLUSTRATION FOR FIGURES 3A, B OMITTED]. Although well-watered clones had a significant decrease in g at the highest growth temperature, [c.sub.i] increased, which suggests that the supply of C[O.sub.2] should have been sufficient to maintain photosynthesis [ILLUSTRATION FOR FIGURES 2A, 3A, B OMITTED]. Thus although the association of stomatal conductance with assimilation has been well documented (Chavez, 1991; Comstock and Ehleringer, 1984; Ehleringer and Cook, 1984) and conductance may limit assimilation under certain conditions (Nowak et al., 1988; Anderson et al., 1995), stomates of Petrophytum cinerascens were sufficiently open to maintain an adequate supply of C[O.sub.2] for photosynthesis.
An alternative to stomatal limitation of the C[O.sub.2] supply for photosynthesis is a biochemical or photochemical limitation that decreases the capacity of leaves to utilize C[O.sub.2]. Ghosh et al. (1994) found that a decline in [A.sub.net] with increased growth temperature was associated with a reduction in the synthesis of ribulose-1, 5-bisphosphate carboxylase (RUBISCO) for a variety of species. However, we do not have any direct evidence to substantiate such chemical limitations. Leaf nitrogen content is well correlated with [A.sub.net] and RUBISCO content (Fitter and Hay, 1995), and thus serves as an indirect index of biochemical/photochemical potential for [A.sub.net]. Unfortunately, our data on the nitrogen content of Petrophytum cinerascens leaves does not provide rigorous statistical support for a biochemical/photochemical limitation: although leaf nitrogen content tended to decrease with increased growth temperature [ILLUSTRATION FOR FIGURE 4 OMITTED], the main effect of growth temperature and the temperature by water treatment interaction term were not significant in the AOV (Table 1a). Note that other mechanisms, such as greater amounts of inactive RUBISCO or redistribution of N to enzymes other than RUBSCO, also cannot be excluded by our data.
The general lack of highly significant effects of the watering treatment on [A.sub.opt], [T.sub.opt], and [T.sub.high] is likely due to the short duration of the drought cycles in our experiment. Chavez (1991) suggests that mesophyll photosynthetic capacity does not decline in water stressed plants until severe levels of water stress are reached. The advantage for plants is that [A.sub.net] has the ability to rapidly recover after a short period of drought. The purpose of the watering treatments was to impose two levels of drought stress and was not to mimic natural conditions. Pot size, which was limited by the size of the growth chambers, precluded a long-term, dry-down drought treatment. Nonetheless, the periodic drought treatment is likely to be more representative of natural conditions. Summer droughts are common in Wenatchee, Washington: mean precipitation over the 3-mo period of June through August is 35 mm, which is 16% of the mean annual precipitation of 220 mm.
The lack of change in [T.sub.high] and [T.sub.opt] suggests that Petrophytum cinerascens is not able to photosynthetically acclimate to increased growth temperature. In fact, the large decrease in [A.sub.opt] with increased growth temperature suggests that increased global temperature may be detrimental. This large depression of photosynthesis with increased growth temperature (over 20% for the periodic drought treatment and almost 60% for well-watered clones), especially if coupled with increased respiration that typically occurs in many species (Osmond et al., 1980), will likely have adverse effects on the plant's carbon balance and growth. Consequently, we speculate that decreases in population size and increases in plant mortality are likely to occur with climate warming. Although the extrapolation of ecophysiological results to population dynamics may be confounded by factors such as intraspecific genetic diversity, we did not find any statistical differences among clones used in this experiment (data not shown). Nonetheless, any demographic changes of P. cinerascens will be easy to monitor because of its restricted distribution. Thus, P. cinerascens may serve as a sensitive indicator of climate change.
Acknowledgments. - This research was supported in part from funds provided by the U.S. Forest Service, Pacific Northwest Research Station (Cooperative Agreement PNW 92-0200) with additional support from Nevada Agriculture Experiment Station. We thank Dr. Richard Everett for helping us initiate the study. We also thank Sandy Lawrence for assistance with the gas exchange measurements.
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|Author:||Moore, Darrin J.; Nowak, Robert S.; Nowak, Cheryl L.|
|Publication:||The American Midland Naturalist|
|Date:||Apr 1, 1998|
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