Oecologia DOI 10.1007/s00442-011-2021-1
G L O B A L C H A N G E E C O L O G Y - O RI G I N A L P A P E R
Seasonal photosynthetic gas exchange and water-use eYciency in a constitutive CAM plant, the giant saguaro cactus (Carnegiea gigantea) Dustin R. Bronson · Nathan B. English · David L. Dettman · David G. Williams
Received: 29 September 2010 / Accepted: 9 May 2011 © Springer-Verlag 2011
Abstract Crassulacean acid metabolism (CAM) and the capacity to store large quantities of water are thought to confer high water use eYciency (WUE) and survival of succulent plants in warm desert environments. Yet the highly variable precipitation, temperature and humidity conditions in these environments likely have unique impacts on underlying processes regulating photosynthetic gas exchange and WUE, limiting our ability to predict growth and survival responses of desert CAM plants to climate change. We monitored net CO2 assimilation (Anet), stomatal conductance (gs), and transpiration (E) rates periodically over 2 years in a natural population of the giant columnar cactus Carnegiea gigantea (saguaro) near Tucson, Arizona USA to investigate environmental and physiological controls over carbon gain and water loss in this ecologically important plant. We hypothesized that seasonal changes in daily integrated water use eYciency (WUEday) in this constitutive CAM species would be driven largely by stomatal regulation of nighttime transpiration
and CO2 uptake responding to shifts in nighttime air temperature and humidity. The lowest WUEday occurred during time periods with extreme high and low air vapor pressure deWcit (Da). The diurnal with the highest Da had low WUEday due to minimal net carbon gain across the 24 h period. Low WUEday was also observed under conditions of low Da; however, it was due to signiWcant transpiration losses. Gas exchange measurements on potted saguaro plants exposed to experimental changes in Da conWrmed the relationship between Da and gs. Our results suggest that climatic changes involving shifts in air temperature and humidity will have large impacts on the water and carbon economy of the giant saguaro and potentially other succulent CAM plants of warm desert environments. Keywords Crassulacean acid metabolism · CAM · Columnar cactus · Sonoran desert · Transpiration · Stomatal conductance · Humidity
Introduction Communicated by Robert Pearcy. D. R. Bronson (&) · D. G. Williams Departments of Renewable Resources and Botany, University of Wyoming, 1000 E. University Dr., Laramie, WY 82071, USA e-mail:
[email protected] N. B. English Earth and Environmental Sciences Division, Los Alamos National Laboratory, MS J495, Los Alamos, NM 87545, USA D. L. Dettman Department of Geosciences, University of Arizona, 4810 E. 4th St., Bldg #77, Tucson, AZ 85721, USA
Crassulacean acid metabolism (CAM) plants use phosphoenolpyruvate carboxylase (PEPc) to Wx CO2 and temporarily store the Wxed C as malate inside cell vacuoles at night. The malate is then decarboxylated during the day, releasing CO2 at high concentrations inside photosynthetic tissues (Osmond 1976). This unique CO2 concentrating mechanism allows CAM plants in warm desert environments to carry out carboxylation and Calvin cycle reactions during daytime periods while maintaining relatively low daytime stomatal conductance and transpiration rates. As a result, many CAM species in warm deserts achieve relatively high water use eYciencies (WUE; CO2 uptake/H2O lost) compared to plants that utilize the more common C3 and
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C4 photosynthetic pathways (Larcher 1995). Assuming that all or most photosynthetic gas exchange in constitutive CAM plants occurs at night, WUE will then be a function of nighttime carboxylation and transpiration rates determined by stomatal conductance to water vapor and CO2, nighttime tissue-to-air vapor pressure diVerence, and PEPc activity. Constitutive CAM plants are assumed to Wx the majority of their carbon at night, but stomata may open for short periods during the day allowing for direct CO2 uptake from the atmosphere (Osmond 1976). Daytime CO2 uptake typically occurs only under very favorable moisture conditions (Hartsock and Nobel 1976). More commonly, daytime CO2 exchange involves some net loss of CO2 to the atmosphere from photosynthetic tissues because of the high CO2 partial pressure gradients between photosynthetic cells and the atmosphere that develop during periods of malate decarboxylation (Despain et al. 1970; Pimienta-Barrios et al. 2000). Yet it is generally assumed that very low daytime stomatal conductances ensure minimal daytime CO2 loss and transpiration during daytime periods, so that high WUE can be maintained despite high CO2 and water vapor partial pressure gradients that develop between photosynthetic tissues and the atmosphere. However, considerable variation in the magnitude of daytime CO2 loss and transpiration has been observed in constitutive CAM species (Despain et al. 1970; Nobel 1977; Lajtha et al. 1997; Pimienta-Barrios et al. 2000, 2002; Nobel and De la Barrera 2002, 2004). The impact of variable and occasionally high daytime CO2 loss and transpiration on WUE and productivity of constitutive CAM plants and the environmental and physiological factors that drive high daytime CO2 loss have not been fully resolved. High daytime CO2 loss might result from incomplete stomatal closure coupled with high internal CO2 partial pressure. It is important, therefore, to fully understand the environmental and physiological regulation of stomatal conductance and its coordination with the CAM biochemical cycle in constitutive CAM plants of desert environments. Stomatal conductance variation during nighttime and daytime strongly inXuences patterns of photosynthetic gas exchange in CAM plants. Herppich (1997) showed that stomatal conductance of the CAM species Plectranthus marrubioides responded directly to variations in nighttime water–vapor partial-pressure gradient between the leaf and air, and when highly water limited, CAM was inhibited by low air humidity. Lange and Medina (1979) concluded that nighttime air humidity was responsible for changes in stomatal conductance for the CAM species Tillandsia recurvata, thereby aVecting net assimilation rate. If changes in climate aVect stomatal conductance then WUE may also change with varying climate conditions. Therefore, variation and change in humidity is likely to be an important
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determinant of CAM function in water-limited environments. Desert ecosystems are thought to be particularly sensitive to climate change (Smith et al. 1992; Weltzin et al. 2003). Air temperature, air vapor pressure deWcit (Da), and the amount and seasonal pattern of precipitation potentially will change in deserts as a result of increased greenhouse gas concentrations in the global atmosphere (Brown et al. 1997; Houghton et al. 2007). Climate models currently predict changes in the timing and magnitude of precipitation events (Easterling et al. 2000), with a transition to even more arid conditions across the desert regions of North America (Seager et al. 2007). Such changes are likely to inXuence the physiology and ecology of succulent CAM plants, and particularly the processes regulating plant carbon and water balance. The Sonoran desert of North America has already experienced steady increases in minimum temperature since 1948 (Weiss and Overpeck 2005), which by itself could alter photosynthetic gas exchange and water balance of succulent CAM species of this region. The saguaro (Carnegiea gigantea) is a massive, longlived, columnar cactus distributed throughout southwestern Arizona and western Sonora, Mexico (Turner et al. 1995). Saguaro and other large CAM succulents are vital to the functioning of Sonoran desert ecosystems. SigniWcant amounts of water, nutrients and energy are provided to consumers from Xowers, fruits, seeds and stems of these large succulents (e.g., Goad and Mannan 1987; Markow et al. 2000; Wolf and Martinez del Rio 2003). For this reason, ecosystem functioning and trophic structure in many parts of the Sonoran desert are shaped disproportionately by saguaro and associated columnar cacti, establishing their critical role in the Sonoran desert. CAM and the capacity to store large quantities of water are thought to confer high WUE and survival in saguaro. While maintaining a high WUE may be important for saguaro success, daily and seasonal patterns of WUE and the environmental factors inXuencing photosynthetic gas exchange in saguaro have not been well documented. Despain et al. (1970) examined photosynthetic CO2 exchange in saguaro seedlings and found that daytime CO2 loss exceeded nighttime CO2 uptake after environmental temperature was experimentally increased to 31 from 26°C. The temperature dependence of CO2 exchange helps explain recruitment of saguaro seedlings and the role of nurse plants, or canopy cover, under natural Weld conditions. We monitored net assimilation (Anet), stomatal conductance (gs), and transpiration (E) rates over 2 years in a natural population of saguaro near Tucson, Arizona, USA, and in a controlled environment experiment. Our goal was to investigate environmental and physiological controls over carbon gain and water loss in this ecologically important species. We hypothesized that seasonal changes in
Oecologia
photosynthetic gas exchange and WUE would be driven largely by shifts in nighttime air temperature and humidity through impacts on nighttime transpiration and stomatal regulation of CO2 uptake, and that daytime CO2 release, if it occurred, would not substantially inXuence daily net carbon gain or WUE in this constitutive CAM species.
Materials and methods We conducted Weld and controlled environment studies on saguaro to characterize seasonal patterns of photosynthetic gas exchange and WUE under a broad range of environmental conditions. Field measurements of gas exchange were conducted from June 2008 to August 2009 on a natural population of saguaro at the Tumamoc Hill Desert Laboratory, in Tucson, AZ, USA (32.22°N, 111.00°W). Mean January and June temperatures at Tumamoc Hill are 14 and 33°C, respectively, with approximately 284 mm of total annual precipitation. A controlled environment study involving experimental manipulations of daytime and nighttime humidity was conducted on potted saguaro plants speciWcally to investigate how stem-to-air vapor pressure diVerence (Ds) inXuences daytime and nighttime stomatal conductance and CO2 gas exchange. Field study Meteorological data were collected at Tumamoc Hill using an Onset (Pocasset, MA, USA) micrologger and sensors including the S-LIA-M003 photosynthetically active radiation (PAR) sensor, S-THB-M002 temperature/humidity sensor, and S-RGB-M002 rain gauge. Correlation analysis using data collected at the University of Arizona’s campus meteorological station, located nearby, allowed us to Wll data gaps during brief periods of sensor malfunction. Ten single-stemmed saguaro plants were chosen for measurements on Tumamoc Hill. The ten cacti were divided into three diVerent height classes: 4 m (n = 4). The ten saguaro plants were located on a north-facing slope, and were all within 500 m of each other. Measurements were conducted in June before the onset of the North American Monsoon (the “premonsoon”), a time when saguaro plants likely experience the greatest level of soil and atmospheric water deWcit; during the North American Monsoon in August; and in February, a typically cool, moist period before the onset of the premonsoon. One tall saguaro was Wtted with thermocouple type-T sensors near the top third of the stem, »3 m from soil surface. Thermocouples were inserted approximately 2 mm into the chlorenchyma tissue on both the north and south sides. Temperature data was recorded using a Campbell ScientiWc 10£ datalogger (Logan, UT, USA).
Stem diameter measurements Stem diameter for individual plants taller than 2 m were measured at breast height (1.37 m) using large calipers. Plants less than 2 m height were measured at the widest portion of their stem. Small markings on the saguaro stems ensured measurements were made in the same position over time. Changes in stem diameter over time indicate gains or losses, in relation to stem water volume (English et al. 2007). Plant gas exchange measurements Net CO2 assimilation (Anet), transpiration (E) and stomatal conductance (gs) rates were measured using a custom cuvette attached to a LI-6200 portable infrared gas analyzer (Li-Cor Biosciences, Lincoln, NE, USA). Cuvette dimensions over the exchange surface were 20 £ 4 cm; a cuvette depth of 5 cm provided space for a small fan to mix the cuvette air during measurements and a Wne-wire thermocouple to measure cuvette air temperature. The cuvette design maximized the surface area of the measured cactus stem relative to the cuvette volume. A small thermocouple thermometer (model no. 15-078 k; Fisher ScientiWc) was inserted approximately 2 mm into the stem tissue adjacent to the attached cuvette to measure chlorenchyma temperature (Tchlor) during each gas exchange measurement. A 6-cm-wide plate aYxed with a strip of closed-cell foam around the periphery of the cuvette provided good contact with the cactus stem, minimizing leaks. Saguaro spines were carefully removed from the stem segments to facilitate contact between stem and cuvette and further minimize leaks. Air gaps at the top and bottom of the cuvette exchange face created by the pleated saguaro stems were wedged with closed-cell foam and sealant (Qubit Systems, Kingston, Ontario, Canada) to provide an airtight seal. Leak checks were performed prior to each measurement by breathing air around the surfaces of the cuvette and monitoring changes in [CO2]. Gas exchange measurements were made at various heights and aspects for each individual cactus. Individual cacti in our tallest height class (>4 m) had measurements on their south sides at the top, middle and bottom third of the cactus. Measurements were only made on the south side of saguaro in the tallest height class due to the diYculty of moving tall ladders to measure multiple aspects. Saguaro individuals of the middle height class had measurement locations on both their south and north sides, at two heights near the top and bottom. Saguaros in the smallest height class had measurements on both north and south sides, but at only one height location near the middle of the cactus. Measurements were avoided on segments of the stem that appeared damaged or unhealthy. Gas exchange measurements were conducted at speciWc times
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during the diurnal to capture all four phases of CAM physiology (Osmond 1976). Frequency of gas exchanges measurements varied slightly between each measurement period due to weather and logistical support. Daily-integrated water use eYciency (WUEday; mmol CO2 uptake/mol H2O lost) was calculated using diurnal gas exchange observations for each saguaro individual. Linear models were created between each gas exchange value across the diurnal measurement. Integrals were calculated for each linear model, allowing for carbon gain, carbon loss and transpiration for every cactus between each measurement period over the diurnal cycle. Observations of WUEday across all individuals were averaged for each measurement period. Statistical analysis Analysis of variance (ANOVA) was performed using measurement period, aspect (north or south), height class and height of measurement as main eVects. These main eVects were analyzed to better understand and account for variation across saguaro individuals and locations of gas exchange measurements. An ANOVA was also performed using measurement period as a main eVect for explaining diVerences in WUEday. An alpha value of 0.05 was used to determine signiWcance. Statistical analyses were performed in R version 2.7.2 statistical software (http://www.r-project.org). Controlled environment study Four 1-m-tall, greenhouse-grown, potted saguaros were exposed to experimental changes in Da using a Conviron growth chamber (Winnipeg, MB, Canada) located at the USDA-ARS Crops Research Laboratory in Fort Collins, CO. Potted saguaros were initially purchased at Bach’s Cactus Nursery (Tucson, AZ, USA) in 2007. The potted saguaros were cared for at the University of Wyoming greenhouse until they were transported to the USDA facility in early 2009. Four potted saguaros were used, as that was the maximum number of individuals that could Wt in the growth chamber. The growth chamber did not control [CO2] and reXected ambient values of the room, which varied between 500 and 600 ppm. The light conditions were set to approximate a natural photoperiod with darkness for 9 h, then a stepwise increase in photosynthetically active radiation (PAR) over 2 h, until maximum light intensity was reached, which was approximately 600 (mol m¡2 s¡1) at the top of the saguaro stems. In the evening, light intensity decreased stepwise over 2 h until PAR equaled 0 (mol m¡2 s¡1). The potted saguaros had been well watered every 2 weeks prior to the experiment and we continued the same watering schedule throughout the experi-
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ment. Air temperature inside the growth chamber was set to 25°C throughout the entire experiment, day and night. Da was initially set at 2.78 kPa and held for 2 weeks. Plants were allowed to acclimate for 2 weeks under the set humidity conditions before the Wrst diurnal gas exchange measurements were made. After the diurnal gas exchange measurements, humidity was then increased to produce a Da of approximately 0.32 kPa. This low Da was held for another 2 weeks, allowing plants to acclimate before a second set of diurnal gas exchange measurements were made. Finally, the humidity in the chamber was returned to the original low value, producing Da values of 2.78 kPa for the Wnal 2 weeks of the 6-week experiment and a Wnal set of diurnal gas exchange measurements were made. Gas exchange measurements were made using a Li-Cor 6200 and the same cuvette used for Weld measurements. Only one height position on the potted cactus stems was measured. Stems were prepared for gas exchange measurements using the same methods described for measurements on Weld plants.
Results Field study Meteorological conditions Air temperature at our Weld site on Tumamoc Hill in Tucson, AZ, ranged from 2.6 to 36.8°C during the time of this study (June 2008 through August 2009), with the highest air temperature occurring in early July, 2009 and lowest air temperature occurring in late December, 2008 (Fig. 1). Saguaro stem temperature had observable diVerences between the north and south sides when measured using long-stem thermometers during gas exchange measurements as well as continuous thermocouple measurements (Fig. 2a, b). Maximum nighttime and daytime Da varied seasonally due to changes in air temperature and incursions of moist monsoonal air in the late summer (Fig. 3). While Da during our measurements in June was similar between 2008 and 2009, Da during measurements in August 2008 were substantially lower than that in August 2009, producing the greatest contrast in Da across all measurement periods. Precipitation is variable in this region of Arizona, both in total amount and in timing. The majority (75%) of the 244 mm total precipitation during 2008 came during the summer monsoon period, starting in late June and continuing through the end of August. In contrast, little precipitation occurred during this typical monsoon period in 2009. Only 134 mm of precipitation was recorded through DOY 271 in 2009, compared to 211 mm of precipitation through the same day in 2008.
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Fig. 1 Meteorological data for 2008 and 2009. Data includes air temperature, air vapor pressure deWcit (Da), photosynthetic photon Xux density (PPFD), total daily rainfall and percent of maximum stem diameter. The majority of data were collected at the Tumamoc Hill meteorological station. Air temperature and humidity data, used to calculate Da, was not available from the Tumamoc station on days 220–261 of 2008 so data from the University of Arizona campus meteorological station was used. The University of Arizona campus meteorological station was found to be in good agreement with the Tumamoc station during times when both stations were operating. The triangles located along the x-axis indicate the dates of gas exchange measurements in relation to the meteorological data
Fig. 2 Chlorenchyma temperature of cactus stems between north and south aspects. a The average chlorenchyma temperature per aspect, over all measurement periods presented in this study, for each hour measured. b Data for one typical day (February 4, 2010) from a permanent chlorenchyma temperature data logger with thermocouples inserted at 3 m into a 4-m-tall cactus
Plant stem diameter The change in stem diameter for the saguaro plants was similar across all saguaro individuals whether stem diameter was increasing after a precipitation event or decreasing due to transpirational water loss (Table 1). Stem diameters were smallest during the dry, pre-monsoon period, and increased after precipitation events, reaching their maximum diameter at the end of the monsoon. Saguaro stems varied in diameter in 2008 and 2009 by 21 and 16%, respectively. Plant gas exchange In general, the gas exchange pattern for our measured saguaros was controlled by gs. Maximum gs occurred in the early morning before dawn, this is also the time with the greatest Anet and E for the 24 h period. As the early morning
progresses into midday gs decreases; however, gs never equals zero and as a result CO2 and water are lost from the saguaro stem to the atmosphere. After sunset, gs increases along with increasing Anet and E until they reach maximum values before dawn. There was a signiWcant diVerence (P < 0.01) in instantaneous rates of Anet between the north and south sides of cactus stems, although aspect did not signiWcantly explain variation in E or gs. Average instantaneous nighttime and daytime Anet, over the Wve measurement periods, was 1.01 § 0.11 and ¡0.33 § 0.04 mol m¡2s¡1 for the north sides, respectively, and 1.65 § 0.14 and ¡0.46 § 0.06 mol m¡2s¡1 for the south sides, respectively. No signiWcant diVerences were observed for Anet when the diVerent heights of gas exchange measurement positions were compared, nor were any signiWcant diVerences detected across the three diVerent height classes. The temperature of
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the stem photosynthetic surface (chlorenchyma temperature; Tchlor) was a signiWcant explanatory variable (P < 0.0001) in accounting for variation in Anet. Of the variation in Anet, 23% was explained by aspect and Tchlor. Even though gs was low over most of the daytime period, net CO2 exchange over daytime periods was always negative, indicating a net loss of CO2 from stems to the atmosphere. The diurnal CO2 uptake pattern was similar over the Wve measurement periods, in that uptake was constrained to nighttime or within the Wrst hour of sunrise. While the general diurnal CO2 uptake pattern was similar across measurement periods, corresponding maximum and minimum values varied (Table 2). Diurnal gas exchange measurements for the June and August 2008 measurement periods are presented graphically (Fig. 4) to illustrate the photosynthetic responses across highly contrasting environmental conditions. Overall, instantaneous Anet was not statistically diVerent across the Wve measurement periods, due to large variance between saguaro individuals, even though there
Fig. 3 Air vapor pressure deWcit (Da) during the diurnal gas exchange measurements
were observable diVerences. Under very humid conditions in August, 2008, gs was relatively high early in the evening, allowing for greater carbon uptake over the nighttime during this monsoon period compared to that during other relatively dry measurement periods. Values for nighttime and daytime E and gs in August, 2008, a period of low Da, were substantially greater than those recorded on other measurement dates. Daytime instantaneous gas exchange rates were sensitive to the vapor pressure diVerence between the cactus stem and air (Ds) (Fig. 5). An asymptotic decline in gs with increasing Ds was observed across all measurement periods. Daily integrated water use eYciency (WUEday) was calculated from cumulative carbon gain and water loss over entire 24 h measurement periods. Considerable variation in WUEday was observed within and across the Wve measurement periods (Table 2). High variance within measurement periods was partly attributed to negative WUEday values for some individuals. A negative WUEday is possible when cumulative daytime CO2 release was greater than the cumulative nighttime CO2 uptake. Negative WUEday values were observed in one individual in February 2009 and three individuals in August 2009, both humid periods. The lowest WUEday values were recorded in August 2008 and 2009, although the cause for the low WUEday during these two periods was diVerent. Low WUEday values in August 2008 resulted from high cumulative transpirational losses combined with moderately high daytime CO2 release, whereas in August 2009 low WUEday resulted primarily from low cumulative carbon gain associated with low nighttime CO2 uptake and relatively high daytime CO2 release. High cumulative CO2 uptake and low cumulative transpirational losses in February 2009 accounted for the highest calculated WUEday. However, WUEday was not statistically diVerent among measurement periods (P > 0.1; ANOVA) because of high inter-plant variance.
Table 1 Diurnal gas exchange data reported by month and year Month/year n
Tair
Da
Stem diam. Total CO2 gain Daytime CO2 loss
Fraction of CO2 loss
Anet
E
WUEday
Jun 2008
10 17.7 1.01/6.91 28.2 (1.4)
74.88 (14.4)
9.0 (0.7)
12% (4%)
65.88 (15.13)
46.30 (7.18)
1.4 (0.32)
Aug 2008
10 22.1 0.33/1.92 34.0 (1.4)
61.31 (9.2)
18.36 (2.6)
30% (7%)
47.52 (9.93)
131.98 (9.17)
0.36 (0.08)
Feb 2009
10 12.5 1.27/4.13 32.2 (1.5)
67.14 (18.5)
8.208 (3.0)
12% (3%)
59.04 (19.21)
9.9 (2.00)
6.0 (1.15)
Jun 2009
9
19.4 1.90/5.88 28.5 (1.5)
95.4 (19.4)
20.88 (12.7)
22% (5%)
74.52 (32.10)
25.56 (2.45)
2.92 (1.43)
Aug 2009
9
26.4 2.60/7.89 30.9 (1.5)
22.14 (5.9)
65% (4%)
11.88 (5.42)
27.55 (4.95)
0.43 (0.24)
33.80 (7.3)
Air temperature (Tair) is the minimum air temperature recorded during the measurement period. Air vapor pressure deWcit (Da; kPa) is reported as the minimum and maximum value for each measurement period. Saguaro stem diameter (Stem diam; cm) is the mean diameter for each measurement period. Total CO2 gain is the gross CO2 uptake averaged across all measured saguaros. Daytime CO2 loss is the daily CO2 lost averaged across all saguaro individuals. Fraction of CO2loss is the proportion of daytime CO2 loss (mmol m¡2 day¡1) to total CO2 gain (mmol m¡2 day¡1). Reported net assimilation (Anet; mmol CO2 m¡2 day¡1) is the calculated integral over the diurnal measurement. Transpiration (E; mol H2O m¡2 day¡1) reported is the calculated integral over the diurnal measurement. Daily-integrated water use eYciency (WUEday) is the ratio of daily summed Anet (mmol CO2 m¡2 day¡1) to daily summed E (mol H2O m¡2 day¡1). Standard errors are provided in parentheses for all averages
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Fig. 4 Diurnal gas exchange data for all measurement periods. Gas exchange parameters are net assimilation (Anet), transpiration (E), and stomatal conductance (gs). Shaded portions represent nighttime periods. Data were averaged across all cacti, bars represent standard error
Table 2 Instantaneous gas exchange rates reported are the maximum and minimum recorded averages of all ten saguaros measured within the diurnal period Gas exchange
Jun 2008
Aug 2008
Feb 2009
Jun 2009
Aug 2009
Anet max
3.70 (0.48)
2.66 (0.27)
1.22 (0.40)
3.67 (0.38)
1.39 (0.01)
E max
1.20 (0.10)
1.79 (0.11)
0.16 (0.05)
0.66 (0.05)
0.62 (0.29)
gs max Anet min
0.05 (0.01) ¡0.28 (0.16)
0.70 (0.07) ¡1.43 (0.002)
0.02 (0.004) ¡0.36 (0.07)
0.06 (0.01) ¡0.81 (0.39)
0.03 (0.11) ¡0.72 (0.001)
E min
0.10 (0.02)
0.39 (0.10)
0.04 (0.004)
0.12 (0.06)
0.22 (0.03)
gs min
0.001 (0.0002)
0.01 (0.003)
0.001 (0.0001)
0.002 (0.001)
0.003 (0.0007)
Net assimilation (Anet; mol m¡2 s¡1), transpiration (E; mmol m¡2 s¡1) and stomatal conductance (gs; mol m¡2 s¡1) are the three parameters reported. Diurnals are reported by the month and year of measurement. Standard errors are listed in parentheses
Controlled environment study
Discussion
Gas exchange parameters were measured on the four potted saguaros in a single chamber, which held temperature constant and manipulated humidity to alter Da. Values of E and gs were similar between the Weld and controlledchamber study, but Anet was much lower for the controlledchamber study compared to the Weld measures (Fig. 6). The growth-chamber manipulation produced a range of daytime and nighttime Da comparable to that experienced by plants during Weld measurements (Fig. 7). Values for gs measured on potted plants in the growth chambers declined signiWcantly when Ds values were greater than 2 kPa and exponentially increased with decreasing Ds below 2 kPa. Importantly, the daytime and nighttime values of gs appeared to follow a common response function to changes in Ds, regardless of whether the plants were acclimated to high or low Da.
It is generally assumed that constitutive CAM plants, speciWcally columnar cacti, maintain low stomtal conductances during daytime, preventing signiWcant losses of water and CO2. Our hypothesis was that daytime stomatal closure in saguaro would suYciently limit midday CO2 and water vapor losses such that variation in WUE would be determined only by variation in CO2 uptake and transpiration at night. SigniWcant daytime CO2 losses associated with high internal CO2 partial pressure that develops during malate decarboxylation would substantially reduce WUEday, and if large enough could result in daily net losses of carbon, as some of our saguaro individuals displayed during both the February and August 2009 periods. Midday CO2 release in cacti has been observed in numerous other studies (Despain et al. 1970; Nobel 1977; Lajtha et al. 1997; PimientaBarrios et al. 2000, 2002; Nobel and De la Barrera 2002,
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Fig. 5 Response of stomatal conductance (gs) to stem to air vapor pressure deWcit (Ds) for saguaros located on Tumamoc Hill in Tucson, AZ
2004). Similar to our results, Pimienta-Barrios et al. (2000) observed daily net losses of carbon in Opuntia Wcus-indica and the columnar cactus Stenocereus queretaroensis due to large midday CO2 release. WUEday varied across measurement periods, but mean diVerences were not signiWcantly diVerent. The large variance in WUEday illustrates how gas exchange of saguaro individuals within a natural population can vary greatly during the same time period. Lajtha et al. (1997) reported instantaneous WUE values ranging from ¡4 to +5 mol CO2/mmol H2O over a 24-h diurnal measurement period. While our reported WUE values are a daily net value, when calculated as an instantaneous value, WUE ranged from ¡12 and +13 mol CO2/mmol H2O. WUE reported on an annual basis for barrel cacti had a transpiration ratio (mass of water transpired/mass of CO2 Wxed) of 70 (Nobel 1977). Saguaro in our study had a daily-integrated transpiration ratio of 85 during the February 2009 measurement; however, our daily-integrated transpiration ratio reached as high as 1,261 during the August 2008 measurement. Contrary to our prediction, saguaro during humid, summer monsoon periods, such as during August 2008, had lower WUEday than during dryer growing season periods.
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Over the Wve measurement periods in this study, we observed the lowest WUEday in saguaro during August 2008 and 2009. However, the causes for these low WUEday values diVered. Saguaro in August 2008, the measurement period characterized by the lowest atmospheric vapor pressure deWcits (Da) and stem-to-air vapor pressure diVerence (Ds), had very high stomatal conductance and transpiration rates as well as substantial daytime CO2 release, but nighttime carbon gain was similar to that measured during other periods. In contrast, transpiration rates observed during August 2009, a period with very high Da and Ds, were similar to those observed during other periods, but nighttime CO2 uptake rates were relatively depressed, resulting from low stomatal conductance and potentially reduced carboxylation capacity. Reduced nighttime CO2 uptake has been shown for Ferocactus acanthodes (barrel cactus; now referred to as Ferocactus cylindraceus), where a series of day/night temperature regimes were tested to investigate the eVect on gas exchange. The highest rate of CO2 uptake was for the moderate day/night temperatures of 23–24°C, compared to day/night temperatures of 32–23 or 11–5°C (Nobel 1986). Similarly, Pimienta-Barrios et al. (2000) showed that, for Stenocereus quertaroensis and Opuntia Wcus-indica, the highest rates of CO2 uptake occurred during moderate temperature periods compared to the hotter/ drier portions of the year. The highest WUEday was observed during February 2009 when daytime Da was high enough to induce low daytime stomatal conductance, yet evaporative demand at night was relatively low. Taken together, these results illustrate the importance of atmospheric humidity in determining WUE in saguaro cactus, and suggest that rapid shifts in climate over the Sonoran desert involving changes in air temperature and humidity would have important consequences for carbon gain and water loss in this ecologically important species. We also hypothesized that, with decreased nighttime Ds, gs would increase and nighttime CO2 uptake would increase as a result. Our hypothesis was based on previously reported observations of gas exchange in Opuntia robusta, a constitutive Sonoran desert CAM plant showing increased CO2 uptake with increasing humidity, with highest uptake rates observed during the summer monsoon months (Pimienta-Barrios et al. 2002). Carbon uptake in saguaro was restricted to nighttime and the Wrst hour of light. Many CAM plants have the capacity to assimilate CO2 from the atmosphere in the early morning or late afternoon (CAM Phases II and IV; Osmond 1976) using the enzyme Ribulose-1,5-bisphosphate carboxylase oxygenase (rubisco). While we did measure some CO2 uptake in the early morning, this ceased shortly after sunrise. Without additional information, such as that acquired with CO2 response relationships or isotopic analyses, it is diYcult to
Oecologia Fig. 6 Diurnal gas exchange for a controlled environment experiment using potted saguaros. Gas exchange parameters are net assimilation (Anet), transpiration (E), and stomatal conductance (gs). Shaded portions represent night-time periods. Data are averages of the four cacti used in the experiment, bars represent standard error
determine whether the early morning CO2 uptake was driven by PEPc or rubisco activities, or both. No CO2 uptake was observed in the late afternoon corresponding to CAM Phase IV (Osmond 1976). While instantaneous rates of Anet did not vary signiWcantly across the diVerent measurement periods, instantaneous rates of E did. Surprisingly, E was highest during periods of low Da. The highest observed E occurred during the August 2008 measurements, a period of high monsoonal activity. Though having the highest rates of E during periods of high humidity may seem paradoxical, the high water loss rates are explained by large increases in gs during periods of extremely low Da. Large increases in E during humid monsoon periods is expected for non-succulent desert plants due to associated increases in gs and soil water availability (Smith and Nobel 1977; Lange and Medina 1979). But since few data have been published for saguaro transpiration, comparisons were made with Ferocactus cylindraceus, a large globular cactus that shares a common geographical range with saguaro. Rates of transpiration in saguaro were very similar to those reported for barrel cactus (Nobel 1977).
Fig. 7 Stomatal conductance (gs) for potted saguaros in a growth chamber with increasing stem to air vapor pressure deWcit (Ds). Circles represent growth chamber conditions under elevated Da and triangles represent low Da conditions. Open symbols represent light periods, closed symbols dark periods
Instantaneous gs was also signiWcantly diVerent between measurement periods; the unusually high gs during August 2008 mostly accounted for these diVerences. Changes in Ds
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explained variation in gs over the diurnal cycle of measurements and across measurement dates. Over the Wve measurement periods, gs exponentially decreased with increasing Ds. A common relationship between gs and Da was observed in Weld and growth-chamber studies. When Da was reduced in the growth chamber from high values to values similar to those observed during the August 2008 measurement, gs responded similarly to Weld plants, increasing conductance to values approximating those observed in the Weld under similar humid conditions. To further evaluate the role of Da in driving diVerences in gs, we experimentally increased Da to original starting values and gs declined again to values approximating those observed under similarly dry conditions in the Weld. The eVect of Da on stomatal conductance in saguaro is not unexpected. Stomatal conductance in other cacti has been shown to respond signiWcantly to humidity. Conde and Kramer (1975) found that stomatal conductance in Opuntia compressa declined with increases in Da. And although Lange and Medina (1979) also observed a similar stomatal response in Tillandsia recurvata, increased stomatal conductance in this species under high humidity was associated with lower, not higher, transpiration rates as was observed in our study with saguaro. Apparently, the increased stomatal conductance in saguaro under conditions of high humidity overcompensates for the reduced water vapor partial pressure gradient between stem tissues and air. The increase in stomatal conductance caused transpiration to be higher, not lower, under these humid conditions, which reached as high as 88% relative humidity during our August 2008 measurement. The instantaneous Anet was signiWcantly greater on the south side compared to the north side of saguaro stems. We hypothesize that the stem tissues on the south side of saguaro stems are able to assimilate more carbon because they receive more total PAR than tissues on the north side of the stems. Although the light dependence of photosynthesis in saguaro is yet to be determined in detail, these Sonoran desert succulents likely require high PAR to reach light saturation. Similar to our results, Tinoco-Ojanguren and Molina-Freaner (2000) showed higher stem temperatures on the south sides of the columnar cactus Pachycereus pringleion compared to the north sides due to higher amounts of intercepted PAR on southern aspects compared to northern aspects. For this study, daytime PAR was high (»2,300 mol m¡2 s¡1) across all the measurement periods, and while all our measurement positions received light, it is reasonable to believe that the lower Anet and stem temperature on the north sides of our cacti was a product of reduced rates of intercepted PAR. Unlike our middle and small size classes, which had equal measures on both north and south sides, our tallest size class of cacti (>4 m) only had measurements on the south sides of the cacti, due to physical restraints. Had we measured the north sides of the
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tallest cacti, our reported mean Anet, which is an average of all cacti, may have been slightly lower. Our observed diVerences in Anet between north- and south-facing aspects are in contrast to patterns reported in one of the only other studies of saguaro photosynthesis. Lajtha et al. (1997) observed highest rates of CO2 uptake on northeast sides of saguaro stems, the side of the plant receiving the lowest PAR. However, the study of Lajtha et al. (1997) focused on stem browning and its eVect on CO2 exchange rates, so a portion of all tissues measured had some epidermal damage, which may account for the contrasting results from the two studies. Only visibly normal (non-damaged) tissue was measured in the current study. In any event, stem aspect and epidermal condition should be taken into account when selecting locations for gas exchange measurements in saguaro, and likely other columnar cacti. If the Sonoran desert receives higher rainfall and more humid conditions in the future as some predict (NAST 2000), then WUE in saguaro might decrease. Whether reductions in WUE would be detrimental to saguaro is not clear, as many other factors contribute to variation in saguaro Wtness and survival. However, high WUE is generally assumed to be one of the key adaptive features of desert CAM plants. If climate conditions no longer favor high WUE, then columnar cacti may suVer. Recently, English et al. (2007) found that 13C and 18O of spine tissue from saguaro cacti can be used as annual chronometers of growth and records of the water volume in the stem. These isotopes in spine tissue can be used as a proxy for total annual precipitation (English et al. 2010a) and evidence of changes in weekly, seasonal and annual patterns of physiology (English et al. 2010b), although the cause of the latter variation is still undetermined. Based on evidence presented here, we suggest that extensive daytime loss of CO2 can decrease 13C in spine tissue and increases in E may lead to greater 18O values. These variations should be considered in both 18O and 13C models of spine isotope variation.
Conclusions Saguaro instantaneous Anet was not signiWcantly diVerent across the Wve seasonal measurement periods, though the timing of carbon uptake and net daily carbon gain did vary. Unlike Anet, instantaneous E was signiWcantly diVerent over the Wve seasonal measurements, with the highest E during the monsoon (August 2008) measurement, which had the lowest Da. Instantaneous gs of saguaro was signiWcantly aVected by Ds, causing gs to decrease with increasing Ds. The eVect Ds had on gs was observed for both in the Weld study as well as the growth chamber study. The lowest
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WUEday was during August 2008 and August 2009, though the cause for low WUEday was diVerent between the two August time periods. Low WUEday in August 2008 was a product of low daytime Da and consequently higher daily transpiration losses. The low WUEday in August 2009 was due to high Da, and consequently less net daily carbon gain. Spring (February 2009) yielded the highest measurement of WUEday, likely due to moderate day and nighttime Da. Overall, these Wndings suggest that changes in climate, speciWcally daytime and nighttime Da, have a large impact on the gas exchange and WUE of saguaro cacti. Acknowledgments This research was supported by the National Science Foundation (NSF IOS-0717403). Nathan English was supported by the Los Alamos National Laboratory LDRD Director’s Fellowship. Also, we thank Samantha Stutz and Mark Trees for their invaluable contributions. Finally, thank you to the USDA-ARS Crops Research Laboratory in Fort Collins, CO.
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