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: dbronson@upenn.edu
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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Oecologia
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
123
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: <1.5 m (n = 3), 1.5–2.5 m
(n = 3), and >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-
123
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.
Oecologia
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.
123
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
123
Oecologia
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
123
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
Oecologia
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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