Oecologia (2002) 130:165–172
DOI 10.1007/s004420100793
Park S. Nobel · Edward G. Bobich
Plant frequency, stem and root characteristics,
and CO2 uptake for Opuntia acanthocarpa: elevational correlates
in the northwestern Sonoran Desert
Received: 16 April 2001 / Accepted: 27 July 2001 / Published online: 28 September 2001
© Springer-Verlag 2001
Abstract A common cylindropuntia in the northwestern
Sonoran Desert, Opuntia acanthocarpa, was investigated
for the following hypotheses: its lower elevational limit
is set by high temperatures, so its seedlings require nurse
plants; its upper elevational limit is set by freezing; spine
shading is the least at intermediate elevations; and
changes in plant size and frequency with elevation reflect net CO2 uptake ability. For four elevations ranging
from 230 m to 1,050 m, the mean height of O. acanthocarpa approximately doubled and its frequency increased 14-fold. Nurse plants were associated with only
4% of O. acanthocarpa less than 20 cm tall at the two
lower elevations compared with 57% at 1,050 m, where
putative freezing damage was especially noticeable, suggesting that nurse plants protect from low temperature
damage. Spine shading of the stem doubled from the
lowest to the highest elevation. Net CO2 uptake, which
followed a Crassulacean acid metabolism pattern, was
maximal at day/night air temperatures of 25/15°C and
was halved by 4 weeks of drought and by reducing the
photosynthetic photon flux from 30 to 12 mol m–2 day–1.
The root system of O. acanthocarpa was shallow, with a
mean depth of only 9 cm for the largest plants. Root
growth was substantial and similar for plants at 25/15°C
and 35/25°C, decreasing over 70-fold at 15/5°C and
45/35°C. Based on cellular uptake of the vital stain neutral red, neither roots nor stems tolerated tissue temperatures below –5°C for 1 h while both showed substantial
high temperature acclimation, roots tolerating 1 h at
61°C and stems 1 h at 70°C for plants grown at 35/25°C.
The increase in height and frequency of O. acanthocarpa
with elevation apparently reflected both a greater ability
for net CO2 uptake and greater root growth and hence
water uptake. This species achieves its greatest ecological success at elevations where it becomes vulnerable to
low temperature damage.
P.S. Nobel (✉) · E.G. Bobich
Department of Organismic Biology, Ecology and Evolution,
University of California, Los Angeles, CA 90095-1606, USA
e-mail: [email protected]
Tel.: +1-310-2063903, Fax: +1-310-8259433
Keywords Elevation · Freezing damage · Nurse plant ·
Opuntia · Water relations
Introduction
The overriding importance of rainfall as a limiting factor
in deserts often causes interactions of water relations
with plant structure and CO2 uptake to be apparent
(Whittaker 1975; Huxman et al. 1998). For instance, the
sporadic and generally meager rainfall favors shallow
root distribution (Nobel 1988). Soil temperature, particularly during the rainy season, affects root growth and
may exert the primary influence on relative plant frequency in some desert ecosystems (Nobel and Linton
1997). The water-use efficiency of certain desert plants
can be enhanced by utilizing Crassulacean acid metabolism (CAM; Nobel 1999). The influence of topographical features, such as elevation, on the distribution of desert plants also can often be interpreted with respect to
plant water relations (Drennan and Nobel 1997).
The cylindropuntia Opuntia acanthocarpa is the most
common cactus at a well studied site at an elevation of
820 m in the northwestern Sonoran Desert within the
7,000-ha Philip L. Boyd Deep Canyon Desert Research
Center (Nobel 1988). It occurs from 150 m to 1,200 m,
one of the largest ranges among the 16 cactus species occurring at the Center (Zabriskie 1979) and has a lifespan
exceeding 100 years (Bowers et al. 1995). On horizontal
ground at 820 m, O. acanthocarpa represents about 17%
of the total ground cover, ranking third among the 33 perennials present (Drennan and Nobel 1997). Its main
roots have more lateral roots alongside and under rocks,
where accumulation of water leads to higher soil water
potentials than in rock-free regions (Nobel et al. 1992;
Matthes-Sears and Larson 1995). Yet, O. acanthocarpa
can survive for up to 3 years without water (Szarek and
Ting 1975a; Smith and Madhaven 1982). Competition
for both water and light has been proposed to influence
spacing between O. acanthocarpa and other species in
the Mojave Desert (Yeaton and Cody 1976). Of the 18
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species of cacti examined in the laboratory for high temperature responses, O. acanthocarpa is one of the most
sensitive, although it acclimates well as the day/night air
temperatures are increased (Smith et al. 1984; Nobel
1988). The effect of extreme temperatures on survival in
the field may be especially important during the seedling
stage, when cacti often use nurse plants (Nobel 1984;
Cody 1993; Leirana-Alcocer and Parra-Tabla 1999;
Valiente-Banuet and Godinez-Alvarez 2002).
O. acanthocarpa has long been known to have nocturnal net CO2 uptake and nocturnal increases in stem
tissue acidity, as is characteristic of CAM species (Patten
and Dinger 1969; Ting 1976). Its δC13 is characteristic of
CAM species (Sutton et al. 1976) and does not change
appreciably when the plants are droughted, suggesting
that O. acanthocarpa is an obligate CAM species (Smith
and Madhaven 1982). Its maximal net CO2 uptake
at night measured in the laboratory is 6 µmol m–2 s–1
(Nobel et al. 1991). Net CO2 uptake by O. acanthocarpa
has apparently not been measured in the field, nor have
the optimal environmental conditions for CO2 uptake
been established in the laboratory. In the present study,
the following hypotheses were tested for O. acanthocarpa: (1) its lower elevational limit in the field is
caused by excessively high temperatures for the seedling
stage, thus early survival requires nurse plants at such locations; (2) its upper elevational limit is caused by freezing damage; (3) spine shading of the stem is greater at
the lower and upper elevational limits than at intermediate elevations where temperatures are less extreme; and
(4) changes in its size and ground cover with elevation
reflect changes in shoot net CO2 uptake ability as environmental conditions change.
Materials and methods
Plant material and field sites
Opuntia acanthocarpa Engelmann and Bigelow var. ganderi (C.B.
Wolf) L. Benson (Cactaceae; Benson 1982), variously known as
deerhorn, buckhorn, and gander cholla, was studied at the University of California Philip L. Boyd Deep Canyon Desert Research
Center near Palm Desert, California. The main field site, known as
Agave Hill, was at 33°38′N latitude, 116°24′W longitude, and
820 m elevation. Mean daily maximum and minimum air temperatures, obtained from a hygrothermograph at a weather station at
1.5 m above the ground, ranged from 14/7°C for January to
34/25°C for July (Drennan and Nobel 1997). Rainfall at Agave
Hill averages 235 mm per year and tends to occur in late summer
and during the winter (Nobel 1988; Drennan and Nobel 1997).
Based on local weather records for Agave Hill, the average annual
minimum temperature over the last 14 years was –4°C and the average annual maximum temperature was 44°C.
Field measurements were made near the spring equinox in
2000 (4–5 March) and in 2001 (3–4 March). Effects of elevation
measured with a Thommen altimeter (Forestry Suppliers, St Louis,
Mo.) on plant height and frequency were determined at 230, 510,
820, and 1,050 ± 10 m using ten 10 m × 10 m quadrats randomly
chosen on horizontal ground (slopes <3°) at each elevation. The
soil particle size distribution is similar over the elevational range
of the four sites (e.g., 76±4% of the non-gravel fraction is sand,
particles from 0.05 to 2 mm) as are the levels of N, P, K, Ca, Mg,
Na, Fe, and Mn in the rooting zone of succulent plants (Nobel and
Hartsock 1986). At the four elevations chosen, the percentage
ground cover by O. acanthocarpa and other species was determined using line transects that were 30 m in length and oriented in
random directions. The possible association with nurse plants, defined as taller perennial plants under whose canopy O. acanthocarpa occurred, and the particular species involved were also investigated for O. acanthocarpa <20 cm in height at all four elevations.
Plants for laboratory studies
Plants approximately 35 cm tall with the main roots essentially intact were transplanted from the site at 820 m into a 1:1 mixture of
soil from Agave Hill and quartz sand. Some were maintained in a
glasshouse at the University of California, Los Angeles, with
mean day/night air temperatures of 25/14°C, day/night relative humidities of 35/70%, and 80% of the ambient radiation (measured
with an LI-190 S quantum sensor, LI-COR, Lincoln, Neb.). Others
were placed in Conviron E-15 environmental chambers (Controlled Environment, Asheville, N.C.) with day/night air temperatures of 15/5, 25/15, 35/25, or 45/35°C and a photoperiod of 13 h.
The photosynthetic photon flux (PPF, wavelengths of 400–
700 nm) incident on the top of the plants in the chambers was
460 µmol m–2 s–1 and averaged 320 µmol m–2 s–1 on the stem locations used for gas exchange measurements. Before placing plants
in the environmental chambers, root systems were dipped into
0.05% (w/w) neutral red (3-amino-7-dimethylamino-2-methylphenazine hydrochloride) for 10 min to stain the existing roots and
hence to facilitate identification of new root growth (Schumacher
et al. 1983), which was determined after excavating the root
systems 8 weeks later. All plants were watered weekly with
0.1-strength Hoagland’s solution (maintaining the soil water potential in the root zone > –0.1 MPa), except for those plants in the
glasshouse that were droughted for up to 9 weeks after growing
for 3 months under wet soil conditions.
Root and stem properties
Excavations to determine the distribution of root dry mass with
soil depth were done at Agave Hill for plants approximately 25 cm
in height at 5-cm increments of soil depth. The dry mass and surface areas of roots were also determined at 4-cm increments of
soil depth for plants of various heights at all four elevations. Root
dry mass was determined after drying the roots for 72 h at 80°C in
a forced-draft oven. Root surface area was determined using mean
diameter (d) and total length (l; area = πdl) for all main and lateral
roots. To determine soil water content, soil samples were removed
at depths of 10 and 20 cm within the root zone of O. acanthocarpa, weighed, and then dried at 80°C in a forced-draft oven until
no further weight change occurred. Soil water potential was determined using moisture release curves for soil from Agave Hill
(Young and Nobel 1986).
Stem water potential was determined for cores removed with a
cork borer that was 14 mm in diameter. After slicing off the cuticle and epidermis with a razor-blade, chlorenchyma disks approximately 4 mm thick were placed in a TruPsi SC10X thermocouple
psychrometer (Decagon Devices, Pullman, Wash.) to determine
the water potential after equilibrating for 3 h. Spine properties
(length, diameter, and number per areole) were determined for
plants at all four elevations; shading of the stem was estimated visually using charts prepared at 5% intervals of shading.
Gas exchange
Net CO2 uptake by O. acanthocarpa was determined with a
LI-COR LI-6200 portable photosynthesis system, and transpiration was determined with a LI-COR LI-1600 water-vapor steadystate porometer at both Agave Hill and also under controlled conditions in the laboratory. Measurements were made every 2 h over
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24-h periods. The cuvettes of both instruments were adapted to the
stems of O. acanthocarpa by replacing their lids with acrylic
plates having a 2-cm cylindrical extension, with an internal diameter of 1.5 cm for which the margin was covered with a foam rubber gasket to help form a tight seal with the stem surface from
which the spines had been removed locally.
Sensitivity to extreme temperatures
The sensitivity of stem chlorenchyma cells and root parenchyma
cells to low or high temperatures was determined for plants in environmental chambers at various day/night air temperatures using
the vacuolar uptake of neutral red following exposure for 1 h to a
particular extreme temperature (Onwueme 1979; Didden-Zopfy
and Nobel 1982; Nobel et al. 1995). Low temperatures were created at 1–2°C intervals decreasing from 0°C by an ULT-80 ultralow-temperature freezer (Rheem Manufacturing, West Columbia,
S.C.) and high temperatures in 5°C intervals increasing from 50°C
using a forced-draft oven. Approximately 1 g of roots or 10 g of
stems were removed with a scalpel and placed in contact with a
copper-constantan thermocouple 0.51 mm in diameter and
wrapped in aluminum foil to prevent desiccation; the samples
were then heated or cooled at 5°C h–1, similar to rates occurring in
the field (Nobel 1988; Nobel et al. 1995), to reach a particular
freezing or high temperature. After the tissue samples were exposed to a 1-h extreme temperature treatment, the samples were
sliced into sections approximately 700 µm thick using razor-blades
and then placed in 0.2% (w/w) neutral red in 0.25 M potassium
phosphate (pH 7.8) for 10 min for stain uptake, which occurs for
the vacuoles of living cells only and hence indicates membrane integrity (Onwueme 1979; Nobel et al. 1995). After the tissue samples had been placed for 10 min in 0.25 M potassium phosphate
(pH 7.8), approximately 130 intact cells per sample were examined at 100× using a BH-2 phase-contrast microscope (Olympus,
Lake Success, N.Y.) to check for stained (living) versus unstained
cells. The temperature that halved stain uptake (LT50), a reliable
test for eventual tissue necrosis (Didden-Zopfy and Nobel 1982;
Smith et al. 1984; Nobel et al. 1995), was determined under each
condition.
Data are presented as means ± SE (n=number of measurements).
Statistical comparisons were performed using Student’s t test or a
one-way ANOVA followed by a Tukey pairwise test. Data were
normally distributed and hence no transformations were necessary.
Fig. 1 Root biomass (%) versus depth (cm) in soil for 25±1-cmtall plants of Opuntia acanthocarpa at Agave Hill (820 m). Plants
were chosen whose canopy major and minor axes were similar to
their height and that had an average of eight branches. Root systems were excavated in 5-cm-thick soil layers. Data are means
± SE (n=10 plants)
Results
Root distribution
Roots of O. acanthocarpa were thin (most <1.5 mm in
diameter) and shallow (Fig. 1). Over half of the dry mass
of roots of 25 cm tall plants at Agave Hill (820 m) occurred in the upper 5 cm of the soil. The mean root depth
for these plants based on the distribution of dry mass in
each soil layer (Fig. 1) was only 6.3 cm. The roots had
greater mass (Fig. 2a) and greater surface area (Fig. 2b)
as plant height increased. Root mass increased faster
than did root surface area, consistent with larger diameters for roots on older plants. The surface area per dry
mass was 2.70 m2 kg–1 for the two shortest plants,
1.61 m2 kg–1 for two intermediate plants, and 1.37 m2
kg–1 for the two tallest plants (Fig. 2a, b). The mean
depth based on root surface area also increased with
plant height from 5.6 cm for the two shortest plants, to
8.6 cm for two intermediate plants, to 9.1 cm for the two
tallest plants (Fig. 2c). The mean depth based on the root
Fig. 2 Variations in root properties for Opuntia acanthocarpa of
various heights at Agave Hill: A root dry mass (g); B root surface
area (m2); and C mean rooting depth (cm) based on surface area,
calculated assuming uniform vertical distribution within each layer. Roots were excavated in 4-cm-thick soil layers. Canopy major
and minor axes were similar to plant heights
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Table 1 Effect of elevation on height, frequency, and ground cover for Opuntia acanthocarpa in the University of California Philip
L. Boyd Deep Canyon Desert Research Center. Height and frequency were obtained for plants in ten 10 m × 10 m quadrats. Percentage ground cover was measured using 18 non-overlapping line
transects that were 30 m in length. Data are presented as means
± SE; values in a column with different superscripts are significantly different at P<0.05 by a Tukey pairwise test following a
one-way ANOVA
Elevation
(m)
Height
(cm)
Plant frequency
(no. per 100 m2)
Ground cover by
O. acanthocarpa (%)
230
510
820
1,050
33±2a
40±2b
45±2b
62±4c
1.5±0.5a
8.9±0.8b
13.0±1.0c
20.3±1.6d
0.17±0.04a
1.18±0.12b
3.03±0.16c
5.14±0.21d
Table 2 Spine properties versus elevation for Opuntia acanthocarpa. Data are means ± SE for three replicates per plant (n=14
plants per elevation); numbers in a row with different superscripts
are different at P<0.05 as for Table 1
Property
Elevation (m)
230
Spine shading
17±2a
of stem (%)
Central spines
3.3±0.2a
(number per areole)
Radial spines
6.2±0.5a
(number per areole)
510
820
1,050
24±2b
27±3b
36±3c
4.3±0.3b
5.6±0.3c
6.9±0.3d
8.4±0.9b 11.2±1.0bc 13.1±0.9c
dry mass similarly increased, namely, 5.7 cm, 8.6 cm,
and 9.2 cm, respectively, for the three plant sizes. Similar shallow root distributions were observed at other elevations. Specifically, the mean root depth based on surface area for plants 25–40 cm tall averaged 7.8±0.3 cm
at 230 m, 7.4±0.2 cm at 510 m, and 7.9±0.4 cm at
1,050 m (n=5). Roots could extend laterally for long distances; e.g., for plants at least 48 cm tall, large lateral
roots often extended more than 2 m from the plant base,
maintaining a depth of 6–12 cm below the soil surface.
Elevational relationships
Plants of O. acanthocarpa steadily increased in height
from elevations of 230 to 1,050 m, where the average
height was nearly double that at the lowest elevation
(Table 1). Plant frequency increased 14-fold from the
lowest to the highest elevation (Table 1). The ground
cover by O. acanthocarpa also steadily increased from
230 to 510 to 820 to 1,050 m, where it was 30-fold
greater than at the lowest elevation (Table 1). Based on
seven transects that were 30 m in length, the total ground
cover of all species was 21.4±2.4% at 230 m, 23.4±4.6%
at 510 m, 26.2±2.1% at 820 m, and 29.9±2.2% at
1,050 m, with the site at 230 m differing from the one at
1,050 m and the other two being intermediate (one-way
ANOVA, P<0.05). At the highest elevation, many stems
Fig. 3 Association of Opuntia acanthocarpa in four height classes
with nurse plants: A 230 m elevation; B 510 m; C 820 m; and
D 1,050 m. Data are presented as percentage of total plants without nurse plants (open bars) or with nurse plants (hatched bars)
for 54 plants up to 20 cm in height at 230 m, 73 at 510 m, 57 at
820 m, and 62 at 1,050 m
of O. acanthocarpa were necrotic. Based on the examination of 40 m of stems from approximately 40 plants at
each of the upper two elevations, 9.2% of a total stem
length showed signs of necrosis at 1,050 m compared
with 1.4% at 820 m.
The shading of the stem surface by spines doubled
from 230 to 1,050 m (Table 2). For the four elevations,
central spines averaged 1.92 cm in length and 0.51 mm
in diameter, radial spines averaged 1.02 cm in length and
0.29 mm in diameter, and areole area averaged 1.02 cm2,
with no significant differences for any of these parameters among elevations. The increase in stem shading with
elevation resulted from both more central spines and
more radial spines per areole (Table 2).
The association of O. acanthocarpa in four 5 cm
height classes with possible nurse plants was examined
at all four elevations (Fig. 3). Nurse plant associations
169
were observed for 64% of the 11 plants that were up to
5 cm tall, 34% of the 44 plants from 5 to 10 cm tall, 20%
of the 76 plants from 10 to 15 cm tall, and 17% of the
115 plants from 15 to 20 cm tall. Nurse plants were associated with 4% of O. acanthocarpa at 230 and 510 m
compared with 28% at 820 m and 57% at 1,050 m
(Fig. 3). The most common nurse plant was Eriogonum
wrightii, which occurred only at 820 and 1,050 m and
accounted for one-third of the total associations; other
species as serving nurse plants more than once included
Adenostoma sparsifolium, Ambrosia dumosa, Encelia
farinosa, Ephedra aspera, Pleuraphis rigida, and Viguiera parishii.
Gas exchange in the field
Gas exchange was measured at Agave Hill on 4–5 March
2000 for O. acanthocarpa following light rainfalls in
February totaling 33 mm (no other rainfall had occurred
since September 1999). The soil water potential for horizontal ground was –0.88±0.04 MPa near the center of
the root zone of O. acanthocarpa at 10 cm below the soil
surface and –0.71±0.04 MPa at 20 cm (n=6 soil locations). The water potential for older stems close to
the base of plants on horizontal ground was –0.78±
0.02 MPa, and for young stems near the top of the plant
approximately 45 cm distal it was –0.86±0.02 MPa
(n=12 plants).
Transpiration on 4–5 March for medium-aged stems
facing sunward near noon for plants on horizontal
ground was 0.25±0.02 mmol m–2 s–1 near noon and
0.65±0.02 mmol m–2 s–1 near midnight (n=6 plants). The
mean gas-phase (stomatal) conductance increased from
10±1 mmol m–2 s–1 near noon to 120±4 mmol m–2 s–1
near midnight. Net CO2 uptake by O. acanthocarpa also
followed a CAM pattern, with uptake occurring primarily at night, and depended on the soil water potential
(Fig. 4), which differed among the three conditions
(P<0.05 for a one-way ANOVA followed by a Tukey
pairwise test, P<0.05). In particular, the maximal rate of
net CO2 uptake was 13.8 µmol m–2 s–1 for plants under
the wettest condition [soil water potential at a depth of
10 cm locally averaging –0.31±0.02 MPa (n=6) on
north-facing slopes]. The maximal rate of net CO2 uptake was 48% lower at an intermediate soil water potential (–0.51±0.03 MPa) and 67% lower under the driest
condition (–0.88±0.04 MPa; Fig. 4). In all three cases,
net CO2 uptake tended to increase during the night. The
total daily net CO2 uptake, obtained by integrating the
instantaneous values over 24 h, was 349 mmol m–2 day–1
for –0.31 MPa, 234 mmol m–2 day–1 for –0.51 MPa, and
161 mmol m–2 day–1 for –0.88 MPa (Fig. 4). Under similar temperatures and a soil water potential at a depth of
10 cm of –0.30 MPa on 3–4 March 2001, total daily net
CO2 uptake was 48% as great for north-facing stem surfaces receiving a total daily PPF averaging 12 mol m–2
day–1 compared with stem surfaces receiving 30 mol m–2
day–1 (P<0.01; n=4 plants).
Fig. 4 Net CO2 uptake rate (µmol m–2 s–1) over a 24-h period for
Opuntia acanthocarpa in soil of various water potentials at 820 m
for stem segments facing sunward at noon. The mean soil water
potential in MPa at a soil depth of 10 cm is indicated next to the
curves. Air temperature ranged from 22.8°C at 1400 hours to
6.4°C at 0300 hours; the total daily PPF on the stem surfaces averaged 36 mol m–2 day–1 on 4 March 2000. Data were obtained on
4–5 March 2000 and are means ± SE (n=5 stems on different
plants). The hatched bar indicates nighttime
Fig. 5 Influence of drought duration (weeks) on total daily net CO2
uptake (mmol m–2 day–1) for Opuntia acanthocarpa maintained in a
glasshouse. The total daily PPF at the stem locations used was
28±2 mol m–2 day–1 for plants droughted for the indicated periods
Gas exchange in the laboratory
Net CO2 uptake over a 24-h period was determined for
stem surfaces that received different incident PPF for plants
maintained in a glasshouse. Based on the stem orientation,
the total daily PPF levels were low (11±1 mol m–2 day–1),
medium (18±1 mol m–2 day–1), or high (28±2 mol m–2
day–1). The total daily net CO2 uptake averaged
119±8 mmol m–2 day–1 for the low PPF, 217±11 mmol m–2
day–1 for the medium PPF, and 286±12 mmol m–2 day–1 for
the high PPF (n=3 or 4 plants).
Total daily net CO2 uptake by O. acanthocarpa decreased as drought proceeded (Fig. 5). At 4 weeks of
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Table 3 New root dry mass versus growth temperatures for Opuntia acanthocarpa. Root systems were excavated 8 weeks after
35-cm-tall plants were placed under the indicated day/night air
temperature. Data are means ± SE (n=6 plants); numbers in a row
with different subscripts are different at P<0.05 as for Table 1
Property
Day/night air temperatures (°C)
15/5
25/15
35/25
45/35
Root dry 0.0003±0.0003a 3.71±0.27b 3.46±0.37b 0.051±0.014c
mass (g)
drought, the total daily net CO2 uptake was half of the
value for the well-watered condition. Total daily net CO2
uptake became 10% of the maximum value at about
7 weeks of drought and was negative at 9 weeks (Fig. 5).
Day/night air temperatures also affected net CO2 uptake for O. acanthocarpa maintained in environmental
chambers. The highest maximal rates of net CO2 uptake
near midnight averaged 5.8 µmol m–2 s–1 at 15/5°C,
6.9 µmol m–2 s–1 at 25/15°C, and 4.4 µmol m–2 s–1 at
35/25°C (n=4 or 5 plants). The total daily net CO2 uptake was 134±7 mmol m–2 day–1 at 15/5°C, 174±9 mmol
m–2 day–1 at 25/15°C, and 67±5 mmol m–2 day–1 at
35/25°C.
Stem and root properties in the laboratory
Both root and stem growth and also tolerances of extreme temperatures were affected by day/night air temperatures. For plants maintained at day/night air temperatures of 45/35°C, bleaching over the entire stem surface
area was evident at 3 weeks; the stems became pale
brownish-green at 5 weeks and beige at 8 weeks, at
which time they did not recover when placed at 25/15°C.
Only one out of six plants at 15/5°C had new root
growth in 8 weeks (Table 3). Substantial and similar new
root growth occurred for plants at 25/15°C and 35/25°C.
All plants at 45/35°C developed new roots in 8 weeks,
but the total dry mass was low (Table 3). The root surface area per dry mass was 11.6 m2 kg–1 for the 25/15°C
plants and 10.7 m2 kg–1 for the 35/25°C plants.
Tolerances to extreme temperatures maintained for
1 h were determined for both stems and roots of O.
acanthocarpa based on the temperature that halved the
uptake of neutral red (LT50; Table 4). Roots were more
sensitive to freezing temperatures than stems were, with
mean tolerances of –1.2°C and –3.5°C, respectively. The
low temperature acclimation for the LT50 of roots as
day/night air temperatures was reduced by 10°C was only 0.6°C compared with 2.8°C for stems (Table 4). Roots
and stems tolerated relatively high temperatures of
52–70°C. Roots were more sensitive to high temperatures than stems were and had an LT50 about 10°C lower
(Table 4). As day/night temperatures were raised by
10°C, roots showed a high temperature acclimation for
LT50 of 9.1°C compared with 6.1°C for stems.
Table 4 Sensitivity of Opuntia acanthocarpa to extreme temperatures. Plants were maintained under the indicated day/night air
temperatures for 8 weeks. Root parenchyma cells within the stele
or stem chlorenchyma cells were examined for various subzero or
high temperatures, each maintained for 1 h, and the LT50 (temperature at which the fraction of cells taking up neutral red declined by
50% from the control) was determined graphically. The fraction of
cells taking up the vital stain for the control at 25°C averaged 0.85
for the stems and 0.82 for the roots. Data are means ± SE (n=5–6
plants); numbers for low and high temperature tolerance within a
row or a column with different subscripts are different at P<0.05
by Student’s t test
Organ
LT50 for low temperatures (°C)
Day/night air temperatures (°C)
15/5
25/15
Root
–1.5±0.2a
–0.9±0.2a
Stem
–4.9±0.3b
–2.1±0.2c
Organ
LT50 for high temperatures (°C)
Day/night air temperatures (°C)
25/15
35/25
Root
51.7±1.4a
60.8±1.9b
Stem
63.4±0.6b
69.5±1.1c
Discussion
Opuntia acanthocarpa at 820 m for a location in the
northwestern Sonoran Desert had relatively shallow roots
– over half of the roots of short (25 cm tall) plants were in
the upper 5 cm of the soil. The mean depth of roots increased to only 9 cm for taller, and hence older, plants,
similar to the rooting depth for other desert succulents
(Nobel 1988), and did not vary with elevation. Thus this
species over the elevational range considered is expected
to respond rapidly to even light rainfall events. Net CO2
uptake for O. acanthocarpa in the field had a maximal instantaneous rate of 14 µmol m–2 s–1 and a total daily net
CO2 uptake of 349 mmol m–2 day–1. Both values are higher than observed for this species in the laboratory (Nobel
et al. 1991). Also, both values are higher than for most
other cacti under natural conditions (Nobel 1988), such as
the sympatric opuntias Opuntia basilaris (Szarek and Ting
1975b) and Opuntia bigelovii (Didden-Zopfy and Nobel
1982), helping to explain why O. acanthocarpa is so successful in the northwestern Sonoran Desert.
Net CO2 uptake by O. acanthocarpa depended on the
water availability in the soil, as for other cacti (Nobel
1988). The relatively light rainfalls in February 2000 following an extensive drought supported daily net CO2 uptake for O. acanthocarpa that was highly correlated with
the available soil moisture. Also, the rate of net CO2 uptake tended to increase during the night for plants under
relatively dry conditions in the field, as is typical for the
gas exchange pattern of CAM plants under such stress
(Nobel 1988). Daily net CO2 uptake decreased during
drought, becoming halved 4 weeks after the soil water
potential became less than the shoot water potential, similar to other cacti. For instance, total daily net CO2 up-
171
take decreases 50% from a well watered condition at
4 weeks for the sympatric barrel cactus Ferocactus
acanthodes and at 3 weeks for the platyopuntia Opuntia
ficus-indica (Nobel 1988).
The influences of temperature and PPF on total daily
net CO2 uptake by O. acanthocarpa are also similar to
those for other CAM succulents. In particular, the optimal
day/night air temperatures for daily net CO2 uptake were
near 25/15°C, as for other cacti (Nobel 1988). Compared
with daily net CO2 uptake at 25/15°C, uptake decreases
43% at 15/5°C and 69% at 35/25°C for F. acanthodes
(Nobel 1988) versus decreases of 23% and 61%, respectively, for O. acanthocarpa. The daily net CO2 uptake for
O. acanthocarpa increased with the daily PPF, becoming
maximal near a total daily PPF of 30 mol m–2 day–1. The
daily PPF leading to half-maximal total daily net CO2 uptake for O. acanthocarpa was about 12 mol m–2 day–1 in
both the field and the laboratory, which is similar to values found for other cacti (Nobel 1988).
Nurse plants provide protection from high temperatures for many cacti in desert ecosystems (Nobel 1984;
Cody 1993; Leirana-Alcocer and Parra-Tabla 1999;
Valiente-Banuet and Godinez-Alvarez 2002), although
proof of protection by a perennial plant is difficult in the
field, as observations tend only to show associations,
which could happen randomly. Putative nurse plants for
O. acanthocarpa, as for other cacti (Nobel 1988), were
more frequent for the shorter plants. At 230 m and 510 m,
perennial plants extensively shaded only 4% of O.
acanthocarpa up to 20 cm in height compared with 57%
at 1,050 m. Nurse plants could protect O. acanthocarpa
against freezing damage at the highest elevation, where
substantial stem necrosis was observed. Indeed, evidence
exists for nurse-plant protection of the columnar cactus
Carnegiea gigantea from freezing temperatures (Steenberg and Lowe 1977; Nobel 1980). Shading can also limit
photoinhibition, which can be more acute for seedlings
when their growth is limited by low temperatures (Egerton
et al. 1999). The increased shading of the stem by spines
as elevation increased could offer protection from low
temperature damage as well, as has been observed for C.
gigantea and other columnar cacti over latitudinal gradients in the Sonoran Desert (Nobel 1980, 1988).
Chlorenchyma cells in stems of O. acanthocarpa were
relatively sensitive to freezing temperatures and showed
little low-temperature hardening. Short-term (1 h) exposure to temperatures below about –5°C greatly inhibited
uptake of the vital stain neutral red, which is highly correlated with eventual tissue necrosis (Didden-Zopfy and
Nobel 1982; Smith et al. 1984; Nobel 1988; Nobel et al.
1995). Based on weather records from the site at 820 m
and the change in temperature over the elevations involved
(Nobel and Hartsock 1986), the average annual minimum
temperature at 1,050 m is predicted to be –5°C, which
could account for the considerable stem necrosis observed
at that elevation. On the other hand, stem cells could tolerate short-term exposure to 70°C, although not long-term
(8 weeks) exposure to 45°C (13 h per day). The remarkable tolerance of high temperatures by the stems reflected
a substantial high temperature hardening of 6°C as the
day/night air temperatures were raised by 10°C, consistent
with previous observations (Smith et al. 1984). Parenchyma cells in roots of O. acanthocarpa displayed similar responses, although they did not tolerate such extremes. In
particular, root cells were highly damaged by only –2°C,
and a high temperature hardening of 9°C per 10°C increase in air temperature led to half-inhibition of neutral
red uptake at 61°C for plants maintained at day/night air
temperatures of 35/25°C. Such high temperature tolerances help explain the lack of nurse plants for O. acanthocarpa at the lower elevations. In particular, the average annual maximum air temperature at 230 m is predicted to be
49°C, well below the lethal range for O. acanthocarpa.
The ground cover of O. acanthocarpa steadily increased 30-fold from 230 to 1,050 m concomitant with
improved environmental conditions for net CO2 uptake,
and hence plant productivity, as also occurs for the CAM
species Agave deserti over the same elevational range
(Nobel and Hartsock 1986). From 230 to 1,050 m, average annual rainfall more than doubles, air temperature
decreases approximately 6°C, and the total daily PPF is
similar (Nobel and Hartsock 1986). The resulting wetter
conditions at higher elevations greatly extend the annual
period for net CO2 uptake by O. acanthocarpa. In addition, the decrease in air temperature with increasing elevation leads to temperatures that are appreciably better
for net CO2 uptake during the usual wet period in late
summer; e.g., mean daily temperatures of 28/17°C at
1,050 m versus 34/23°C at 230 m in September (Nobel
1988; Drennan and Nobel 1997). The monotonic increase in plant height from 230 to 1,050 m, leading to a
doubling in average height, may also reflect the increasingly ideal average conditions for net CO2 uptake by
O. acanthocarpa with increasing elevation.
One key to the competitive success of desert perennials is the time of the year that favors root growth (Nobel
and Linton 1997; Dubrovsky et al. 1998). At Agave Hill
(820 m), the soil temperature in the middle of the root
zone when water is available helps to determine which
perennial species have an ecological advantage (Nobel
and Linton 1997; Drennan and Nobel 1998). In this regard, root growth by O. acanthocarpa was similar at
day/night air temperatures of 25/15°C and 35/25°C, suggesting that optimal day/night temperatures for root
growth would be approximately 30/20°C (essentially no
root growth occurred at 15/5°C or 45/35°C). Similarly,
the temperature range for root elongation by O. ficusindica is 12–43°C and its optimal temperature is 27–
30°C (Drennan and Nobel 1998). In the Deep Canyon
Desert Research Center, day/night air temperatures near
30/20°C occur during the relatively dry late spring and
late autumn at 230 m but occur during the relatively wet
late summer at 1,050 m (Nobel and Hartsock 1986;
Nobel 1988), which probably is a factor in the doubling
in the height of O. acanthocarpa and 30-fold increase in
its ground cover from the lowest to the highest elevation.
With regard to the four hypotheses considered, the
following conclusions can be drawn for O. acantho-
172
carpa: (1) nurse plants are not important at low elevations, as the plants are highly tolerant of high temperatures; (2) freezing temperatures most likely limit its upper elevational range in the Sonoran Desert, where nurse
plants are frequent; (3) the increasing spine shading of
the stem with elevation may protect the stem from freezing temperatures at higher elevations; and (4) increases
in size and frequency of O. acanthocarpa with elevation
correlate with annual net CO2 uptake ability. Environmental influences on net CO2 uptake and by extension
on productivity for O. acanthocarpa are similar to those
for other desert CAM succulents, suggesting that it has
no unique responses, although it has a high net CO2 uptake capacity compared to other cacti under natural conditions. Also, O. acanthocarpa has a shallow root
system, as for other desert succulents. In conclusion, the
increase in size and frequency of O. acanthocarpa from
230 to 1,050 m in the northwestern Sonoran Desert reflects better conditions for net CO2 uptake by the shoots
and water uptake by the roots. For the sites considered,
this species achieves its greatest ecological success at
high elevations where it becomes vulnerable to episodes
of freezing damage and resulting stem necrosis.
Acknowledgements The authors thank Erick De la Barrera for
assistance with the net CO2 uptake measurements and 24 undergraduate students for their participation in various aspects of this
research. Financial support from National Science Foundation
grant IBN-9975163 is also gratefully acknowledged.
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