Oecologia (2007) 154:247–258
DOI 10.1007/s00442-007-0832-x
ECOPHYSIOLOGY
Past climate changes and ecophysiological responses recorded
in the isotope ratios of saguaro cactus spines
Nathan B. English Æ David L. Dettman Æ
Darren R. Sandquist Æ David G. Williams
Received: 16 May 2007 / Accepted: 19 July 2007 / Published online: 28 August 2007
Springer-Verlag 2007
Abstract The stable isotope composition of spines produced serially from the apex of columnar cacti has the
potential to be used as a record of changes in climate and
physiology. To investigate this potential, we measured the
d18O, d13C and F14C values of spines from a long-lived
columnar cactus, saguaro (Carnegiea gigantea). To determine plant age, we collected spines at 11 different heights
along one rib from the stem apex (3.77 m height) to the
base of a naturally occurring saguaro. Fractions of modern
carbon (F14C) ranged from 0.9679 to 1.5537, which is
consistent with ages between 1950 and 2004. We observed
a very strong positive correlation (r = 0.997) between the
F14C age of spines and the age of spines determined from
direct and repeated height measurements taken on this
individual over the past 37 years. A series of 96 spines
collected from this individual had d18O values ranging
from 38% to 50% [Vienna standard mean ocean water
(VSMOW)] and d13C values from 11.5% to 8.5%
[Vienna Peedee belemnite (VPDB)]. The d18O and d13C
values of spines were positively correlated (r = 0.45,
P \ 0.0001) and showed near-annual oscillations over the
Communicated by Frederick C. Meinzer.
N. B. English (&) D. L. Dettman
Department of Geosciences,
University of Arizona, 4810 E 4th Street,
Bldg #77, Tucson, AZ 85721, USA
e-mail: nenglish@email.arizona.edu
D. R. Sandquist
Department of Biological Science,
California State University, Fullerton, CA, USA
D. G. Williams
Departments of Renewable Resources and Botany,
University of Wyoming, Laramie, WY, USA
15-year record. This pattern suggests that seasonal periods of reduced evaporative demand or greater precipitation
input may correspond to increased daytime CO2 uptake.
The lowest d18O and d13C values of spines observed
occurred during the 1983 and 1993 El Niño years, suggesting that the stable isotope composition recorded in
spine tissue may serve as a proxy for these climate events.
We compared empirical models and data from potted
experimental cacti to validate these observations and test
our hypotheses. The isotopic records presented here are the
first ever reported from a chronosequence of cactus spines
and demonstrate that tissues of columnar cacti, and
potentially other long-lived succulents, may contain a
record of past physiological and climatic variation.
Keywords Stable isotopes Oxygen-18 Carbon-13 Growth rate Carnegiea gigantea Cactus Radiocarbon El Niño southern oscillation (ENSO)
Introduction
Variation in stable isotope ratios of oxygen (d18O),
hydrogen (d2H) and carbon (d13C) in tissues that are
incrementally produced and preserved in plants, such as
tree-rings, is commonly exploited to reconstruct past
environmental changes and investigate associated plant
metabolic and physiological responses (e.g., Roberts et al.
1997; Roden et al. 2000; Dawson et al. 2002; McCarroll
and Loader 2004; Cernusak et al. 2005; Wright and Leavitt
2006; West et al. 2006). There are few studies documenting
isotopic variation in stem succulents, and none that we are
aware of that show isotopic variation in tissues that are
produced incrementally. Isotope measurements on tissues
that are sequentially added and preserved on stem
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248
succulents, such as spines, could be very useful proxies for
reconstructing past climatic events and documenting
responses to environmental change, especially in desert
regions lacking other suitable proxies for recent climate
changes.
The massive, long-lived (125–175 years) saguaro cactus
[Carnegiea gigantea (Engelmann) Britton & Rose] occurs
throughout the Sonoran Desert in southwestern Arizona
and western Sonora, Mexico (Turner et al. 1995). In this
region, monsoon rains that occur between July and September may provide up to 50% of the mean annual
precipitation (Eastoe et al. 2004), with the remainder falling mostly during the winter and spring. The monsoon is an
important source of water for saguaro growth in some
instances (Drezner 2005). However, stronger correlations
have been found between measures of saguaro success (i.e.,
branching, stem diameter and seedling recruitment) and
winter/spring rainfall (Drezner 2003a, b; Drezner and
Balling 2002), mediated by the uptake and storage of
winter/spring rainfall in the stem or through the prolonged
presence of soil moisture in the hot and dry pre-monsoon
months. Such precipitation is greatly enhanced during the
El Niño phase of the El Niño southern oscillation (ENSO)
(Gutzler et al. 2002), but it is unclear how this climatic
anomaly has affected, or will affect, saguaro water balance,
photosynthetic metabolism, growth and fruit production.
Given the relationships with winter/spring precipitation, El
Niño years are likely to have a pronounced influence on
saguaro growth, reproduction and demography, as well as
on the consumers that rely on resources provided by this
dominant stem succulent.
As in other cacti, saguaro spines develop on areoles near
the shoot apical meristem (Mauseth 2006). Areoles and
spines are displaced laterally on the large dome-shaped
apex of the cactus stem as new areoles are produced
(Gibson and Nobel 1986; Mauseth 2006). Spines closer to
the apex are therefore younger than spines lower on the
stem. Between four and eight areoles, each having about 15
spines, form on each elongate set of fused tubercles (the
‘rib’ of the stem) each year (N. English, personal observation), with the majority of growth occurring during warm
periods, i.e., April–October (Steenbergh and Lowe 1983).
Spines are highly lignified organs with no secondary
growth, as the cells die within days after they are formed
(Gibson and Nobel 1986; Mauseth 2006). The lignified
spines are very durable and are retained on the plant for
decades; thus, isotopic ratios of spines may provide a
useful record of environmental and physiological information in a manner similar to that of tree rings.
In this paper we: (1) present a theoretical framework
that relates the isotopic variation of cactus water and spines
to temporal and physical changes in the environment; (2)
describe the methods used to collect and prepare cactus
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Oecologia (2007) 154:247–258
stem-water and spine samples for isotopic analysis; (3)
develop and test a model for the isotopic enrichment of
cactus stem-water, using experimental potted saguaro
plants; (4) demonstrate the accuracy and utility of fractions
of modern carbon (F14C) (radiocarbon) dating in establishing growth models and spine formation dates for
naturally grown saguaro plants; and (5) evaluate a dated,
multi-year record of d18O and d13C values from spines of a
naturally occurring cactus and compare these values to
local precipitation records.
Theory
Oxygen and hydrogen isotope variation
in cactus water and tissue
Large stem succulents in the Sonoran Desert, like saguaro,
take up water during very discrete intervals (days) after
precipitation events, and then lose water slowly over
lengthy dry periods between precipitation events (Gibson
and Nobel 1986). Isotopic enrichment of stem water due to
evaporation during intervening dry periods in saguaro and
other stem succulents can be described by Rayleigh fractionation, expressed as:
dsw ¼ ðdi þ 1000Þfeða1v 1Þ 1000
ð1Þ
where dsw is the d18O or d2H value of stem water after
evaporation, di is the initial d18O or d2H value of water in
the stem, fe is the fraction of water lost from the stem due to
evaporation, and a1v is the fractionation during evaporation, which is the sum of an equilibrium fractionation
related to mean minimum temperature, and a kinetic fractionation related to mean maximum relative humidity (for a
lucid demonstration of how to calculate these values, see
Clark and Fritz 1997). We use mean minimum temperature
and mean maximum relative humidity because these most
likely represent night-time values, when stomates are open
and the majority of gas exchange occurs for plants with a
crassulacean acid metabolism (CAM). This simple model
can be used to examine variation in d18O and d2H values of
water at the stem apex, where spine development occurs.
When new water is added to the stem (recharged) and
well mixed, the water isotope value (dsw*) of the new stem
is determined by a two-component mixing model:
dsw ¼ dsw ð1 fr Þ þ dr ðfr Þ
18
ð2Þ
2
where dsw is the d O or d H value of stem water before
recharge (Eq. 1), fr is the fraction of new water added to the
stem and dr is the d18O or d2H value of this recharge water
(e.g., rainfall). fr can be estimated from changes in stem
diameter, since the majority of water in columnar cacti is
Oecologia (2007) 154:247–258
249
stored in the cortex and the stem will expand or contract in
direct proportion to the amount of water taken up or lost,
respectively, by the cortical tissues (McAuliffe and Janzen
1986). The fraction of water taken up (fr), or lost (fe), can,
therefore, be calculated from changes in plant diameter,
assuming the cactus shape approximates that of a cylinder
(Mauseth 2000) or by weighing the plant.
The oxygen or hydrogen isotope ratio of spine tissue
(d18Ospine or d2Hspine) can be expressed as:
dspine ¼ ½f ðdswapex þ 1000Þ abio þ ð1 f Þ ðdswchlorenchyma
þ 1000Þ abio 1000
ð3Þ
where dsw-apex is the oxygen or hydrogen isotope value of
water at the stem apex (dsw or dsw* from the above
equations) where spine tissue is synthesized, dsw-chlorenchyma
is the isotope value of water at the source of photosynthetic
carbon dioxide assimilation in chlorenchyma, abio is the
fractionation factor for oxygen (eO) or hydrogen (eH)
associated with the biosynthesis of plant tissue, and f is
the fraction of carbon-bound oxygen or hydrogen in
photosynthetic sugars that undergoes exchange with
medium water during spine tissue synthesis (for a
thorough discussion of the variables in this model, see
Roden and Ehleringer 1999; Roden et al. 2000; McCarroll
and Loader 2004). Although f may vary among taxa, for
saguaro we apply values reported in the literature for
cellulose synthesis in other dicotyledonous plants (i.e.,
trees, Roden et al. 2000). Note that, if the source of
photosynthates for spine formation is near the apex (i.e.,
dsw-chlorenchyma & dsw-apex), then Eq. 3 simplifies to:
dspine ¼ ½ðdswapex þ 1000Þ abio 1000:
ð4Þ
Carbon isotope variation in cactus tissue
Over short-term intervals (i.e., seasons to years), the isotopic variation of carbon in mature photosynthetic organs is
most greatly influenced by physiological processes affecting carbon isotope fractionation during CO2 assimilation
and compound synthesis (O’Leary 1988) and, to a lesser
degree, by seasonal variations in the d13C of atmospheric
CO2 (0.2%, Keeling et al. 1979). Crassulacean acid
metabolism (CAM) photosynthesis involves the initial
fixation of atmospheric CO2 by phosphoenolpyruvate-carboxylase (PEPc) at night, when stomates are open and
photosynthate is stored as malate (referred to as CAM
phase I; Dodd et al. 2002; Winter and Holtum 2002). At
dawn, while the stomates are still open, ribulose-1,5-bisphosphate carboxylase (Rubisco) activity in the chloroplast
increases as malate begins to be converted back to CO2 and
atmospheric CO2 is also available for assimilation
(phase II). This short phase is followed by a prolonged
period of malate decarboxylation during the daytime, when
stomates are closed, and only malate-released CO2 is fixed
by Rubisco in the Calvin cycle (phase III). Near the end of
the day, when all the malate has been consumed and
internal pCO2 has declined, stomates may open again and
allow direct assimilation of atmospheric CO2 by Rubisco
(phase IV). Each phase of CAM photosynthesis affects
isotopic discrimination of carbon (D13C) to varying degrees
and thus influences the isotopic ratio of the plant relative to
air (d13Cplant & d13Cair D13C). At night (phase I), D13C
is partially determined by changes in the balance of stomatal conductance (CO2 ‘‘supply’’) and PEPc activity (CO2
‘‘demand’’) during CO2 uptake. During the day, when the
stomates are closed (phase III), D13C is moderated by the
degree of CO2 leakage out of tissues. These fractionation
processes are diffusion-regulated, but enzymatically driven
fractionation also affects D13C in CAM plants (Winter and
Holtum 2002). When the stomates are open and the sun is
up (phases II and IV), atmospheric CO2 taken up by Rubisco (D13C = 27%) modifies D13C as it would in a C3
plant. Enzymatic uptake of CO2 by PEPc (D13C = 2%)
when the stomates are open at night (phase I) also modifies
D13C (O’Leary 1988; Griffiths 1992).
CAM plants grown in mesic environments tend to have
more negative values of tissue d13C than do those grown in
dry conditions (Schulze et al. 1976; Osmond 1978; Winter
and Holtum 2002). Two factors likely account for this
pattern: (1) substantial daytime CO2 assimilation and
associated expression of Rubisco fractionation with either
early morning or late afternoon CO2 uptake during wet
periods (CAM phases II and IV), or (2) enhanced leakage of
13
C-enriched CO2 when stomates are closed (phase III;
Griffiths et al. 1990; Haslam et al. 2003). A simple model
for d13C variation in obligate CAM species (Despain et al.
1970) discounts the impact of daytime CO2 assimilation—a
valid assumption for saguaro during extremely dry periods
(Lajtha et al. 1997). However, under favorable conditions
(moderate temperatures and moist soil), a large stemmed
cactus also common to the Sonoran desert [Ferocactus
ancanthodes (Lem.) Britt. & Rose] was shown to acquire
between 9% and 13% of its CO2 in the early morning and
late afternoon (phases II and IV; Gibson and Nobel 1986).
Given the large difference in D13C between Rubisco- and
PEPc-mediated CO2 uptake, small amounts of CO2 acquired
at dawn and in the late afternoon can have a disproportionate impact on the final d13C values of cactus tissues. We
predict that the d13C values of spines of saguaro should
increase during drought periods on an annual and interannual basis (decreased phase II and IV photosynthesis) and
should decline with more favorable conditions (increased
phase II and IV photosynthesis), especially in years with
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above-average rainfall, such as during a strong monsoon
year or after substantial winter rains (e.g., El Niño years).
Oecologia (2007) 154:247–258
vacuum distillation to extract stem water (Ehleringer et al.
2000) for isotope analysis. Boreholes in the stems were
plugged with 6-cm-long wooden dowels (10 mm diameter)
immediately after sample collection.
Methods
Experiment with potted saguaro
Spine sampling from a naturally occurring saguaro
Four 0.8 m tall saguaro plants, purchased from a local
nursery in June 2004, were grown in 10-gal (38 l) pots
outdoors in full sunlight at the University of Arizona Desert
Laboratory, Tucson, AZ, USA (32.22 N, 111.00 W,
800 m elevation). These plants were used to investigate the
influence of evaporation and recharge on the d18O and d2H
values of water at the stem apex. The plants were allowed to
acclimate for 8 months, being frequently watered prior to
experimentation (at least once every 1 or 2 weeks, as needed) using Tucson municipal water: d18O = 8.4%;
d2H = 61%. In order to induce drought we withheld all
irrigation from the cacti between 28 April and 26 July 2005.
We excluded meteoric water inputs from the potted soil for
the drought cycle by covering the pots around the base of
each plant with heavy plastic. Precipitation (recorded daily
at Tumamoc Hill by J. Bowers, personal communication)
may have reached the soil through gaps in the plastic or by
running down the stem, but very little of the 23.4 mm of
rainfall (d18O = 1%; d2H = 7%) recorded during the
drought cycle reached the soil. After the plastic had been
removed (27 July 2005), the cacti took up water from irrigation (provided at the same frequency as before) and
natural precipitation through October 2005.
We measured stem diameter at 15 cm below the stem
apex and total plant mass changes for each plant to calculate water recharge and evaporative losses. We
determined plant mass by weighing each plant, plus its pot
and soil (altogether 46 kg), on a lysimeter. We used the
monthly mass of each plant during the experiment, minus
the dry weight of the pot and soil, to determine fe or fr. We
subtracted 4 kg from the first and last months of the
experiment (April and October, respectively) to account for
the mass of water in saturated potting soils (4 l holding
capacity in the 10-gal pots). The potting soils were dry
during the other months of the experiment when the plants
were weighed. We took tissue samples from the stem
epidermis and cortex monthly, using a 9-mm-diameter cork
borer inserted between ribs slightly below the apex and
perpendicular to the plant surface on the north side. The 6cm long cores were divided into two subsamples, representing sections from the surface to 3 cm (chlorenchyma
and parenchyma) depth and from 3 to 6 cm depth (parenchyma only, but no wood tissue). The samples were sealed
in glass vials and stored in a freezer, and the surface to
3 cm samples were later processed using cryogenic
We sampled spines for isotopic analysis from the northernmost rib of Saguaro 162, a 3.7-m-tall, single-stemmed,
saguaro cactus whose height had been measured repeatedly
over 38 years as part of an effort to establish growth models
for saguaro (Pierson and Turner 1998). Saguaro 162 is
located at the University of Arizona Desert Laboratory at
Tumamoc Hill, Tucson, AZ, USA. We used a 4-m-tall
orchard ladder (Stokes Ladders, Kelseyville, CA, USA) and a
flexible meter tape to reach and measure the height above
ground level of the saguaro apex (Table 1) and of each
sampled spine. We used needle-nose pliers and sprue cutters
(The Testor Corporation, Rockford, IL, USA) to clip one
spine from each areole along the rib (we chose the longest
central spine that was most distal from the areolar meristem).
This site is on the eastern edge of the Sonoran Desert
and receives almost 50% of its mean annual precipitation
(284 mm) during the monsoon months of July–September.
At least monthly precipitation measurements have been
collected 200 m from Saguaro 162 for the last 25 years
at Tumamoc Hill (J. Bowers, personal communication).
Pierson and Turner (1998) first recorded the height of
Saguaro 162 in 1964 and subsequently in the spring of
1970 and 1993 (Table 1). Based on the height growth
model established for the saguaro population on Tumamoc
Hill (Pierson and Turner 1998), we estimate Saguaro 162
most likely germinated in the 1940s.
To serve as a control for potential contamination effects
of urban CO2 on F14C values, we sampled a single spine
from the apex of another 4-m-tall cacti in Saguaro
National Park East, in 2004 (32.22 N, 110.71 W, 843 m
elevation; permit #SAGU-2004-SCI-0012), 23 km from
downtown Tucson. We compared the measured F14C and
the resulting age of this control spine with a similarly
sampled spine from Saguaro 162 to determine the impact
of urban pollution on radiocarbon measurements yielded
by saguaro spines. This control sample was also used to
assess the use of stored carbon in spine growth.
123
Stable isotope analyses
We performed stable isotope measurements at the Laboratory of Isotope Geochemistry, Department of
Geosciences, University of Arizona. We analyzed waters
for d18O using a dual-inlet isotope ratio mass spectrometer
Oecologia (2007) 154:247–258
251
rate calculated from actual measured heights and years [i.e., between
1964 and 1970, the cactus took 0.2 years to grow 1 cm, thus 77 cm
(or 27 cm above the 1964 height) represents 1969.4]
Table 1 Height of sampled spine, measured heights recorded by
Pierson and Turner (1998), F14C content, and F14C year from spines
of Saguaro 162. Italicized values are interpolated from the growth
Height
(cm)
Year at
measured
height
F14Ca
b
F14C year
Corrected
F14C year
Corrected 2r
Corrected + 2r
377
2002.8
1.0698
0.0092
2004.7
2002.8
2000.7
2003.6
325
1993.9
1.1015
0.0039
1996.7
1994.8
1994.0
1995.6
320
1993
–
–
287.5
1989.9
1.1363
0.0039
1992.3
1990.4
1989.0
1991.9
255
1986.8
1.1695
0.0041
1989.0
1987.1
1985.2
1988.3
1982.6
1.2051
0.0026
1985.4
1983.5
1982.2
1984.4
1.2105
0.0037
1984.9
1983.0
1982.0
1983.9
Tip
211
211Base
–
–
–
–
–
151
1976.8
1.3028
0.0038
1979.4
1977.5
1977.0
1977.9
98
1971.7
1.4261
0.0060
1973.9
1972.0
1971.1
1972.9
80
1970
–
–
77
50
1969.4
1964
1.5537
–
0.0105
–
1969.5
–
1967.6
–
1966.3
–
1969.6
–
–
–
–
–
46
–
1.1991
0.0062
1958.7
1956.8
1956.4
1957.3
40
–
1.1174
0.0060
1957.8
1955.9
1955.6
1956.1
17c
–
0.9679
0.0042
1950.0
–
–
a
F14C is corrected to account for Desert Laboratory graphite line blank
b
Includes 0.1% uncertainty that represents long-term errors on the accelerator mass spectrometer at the University of Arizona
This is the most recent possible (2r) calibrated age of a pre-bomb radiocarbon age
c
(Delta-S, Thermo Finnegan, Bremen, Germany) attached to
an automated CO2–H2O equilibration unit. We measured
water d2H values on the same mass spectrometer equipped
with an automated chromium reduction device (H-Device,
Thermo Finnegan) for the generation of hydrogen gas using
metallic chromium at 750C. Standardization was based on
internal standards calibrated with Vienna standard mean
ocean water (VSMOW) and Vienna standard light Antarctic precipitation (VSLAP). Reported values are per mil
(%) relative to VSMOW. Precision on repeated analyses of
laboratory standard waters was less than 0.08% for d18O
and 1% for d2H.
A time-ordered series of isotope measurements was
created from a vertical series of 96 spines spanning 1.77 m
near the apex of Saguaro 162 (hereafter referred to as a
spine-series). For each spine, we analyzed the bulk tissue
of the top 2 mm (the tip) for d18O and the next 1 mm
section below the tip for d13C. d2H of spines was not
measured. Spines were dried overnight at 70C and chopped into fine pieces before d18O and d13C analyses. We
measured spine tissue d18O and d13C using a thermal
combustion elemental analyzer (Thermo Electron Corp.,
Waltham, MA, USA) and a CHN elemental analyzer
(Costech Analytical Technologies, CA, USA), each
attached to a continuous flow isotope ratio mass spectrometer (Delta Plus, Thermo Electron Corp.). Reported
values are per mil (%) relative to VSMOW for d18O
–
analyses and ViennaPeedee belemnite (VPDB) for d13C
analyses. The precision for our method based on repeated
analysis of working standards was 0.2% for d18O and
0.1% for d13C.
We measured the effect of tissue processing on d18O
values of spines from a saguaro nearby and similar to
Saguaro 162. We used ground (40 mesh) spine tissue from
3.7 m, 2.5 m and 1 m above ground level. The d18O values
of spine tissue holo- and a-cellulose (Brendel et al. 2000)
were 1.1–1.8% more positive than that of bulk spine tissues (95% confidence intervals from 0.4 to 2.9%; three
separate two-sample t tests, t8 and 18 [ 3.13, P \ 0.0057).
Given the inert nature of dead spine tissue and the relatively small and consistent offset in d18O values, we
analyzed raw spine tissue without further processing.
At selected heights on Saguaro 162, we used a segment
of the remaining raw spine tissue from just below the
location of the d18O and d13C sampling on the same spine
for F14C analyses. These segments were dried overnight at
70C and bathed in weak HCl acid (0.1 M) in an ultrasonic
bath for 30 min. Each of three acid baths was followed by a
30-min soak and then rinse in Milli-Q water (18 Mohm).
Spines were dried a second time and then reduced to
graphite and analyzed for F14C and d13C (the latter from a
gas split of the same graphite sample; Slota et al. 1987) at
the University of Arizona Accelerator Mass Spectrometry
Laboratory. We used the software program Calibomb
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252
(Reimer et al. 2004) to calculate possible spine ages from
measured F14C values corrected for d13C and line blank.
For the age calculations of pre-1999.5 ages, we used the
Northern Hemisphere Zone 2 data set (Hua and Barbetti
2004), a 0.2-year sample smoothing term and a resolution
of 0.2 years. For one sample with a post-1999.5 age, we
used an unpublished update of the same dataset provided
by Q. Hua (personal communication). For each F14C value
from a spine, Calibomb estimates a number of possible
ages, the 95% confidence interval for each possible age,
and a probability that each possible age is the correct age
(Reimer et al. 2004). To assign a finite date for a sampled
spine, rather than a range of dates, we used the average of
all the possible ages weighted by the probability of their
being correct. We conservatively determined the error of
that value to be the youngest and oldest ages from the 95%
confidence interval of all the possible ages for each sample
(2r age range). The time series was anchored by the 1964–
1965 atmospheric radiocarbon peak and the known height
of Saguaro 162 measured in 1964. Thus, for any spines
collected from above the 1964 height, we excluded any
possible ages that predated the 1964–1965 atmospheric
radiocarbon peak and, conversely, for samples taken below
the 1964 height. The same was true of our error determinations. This anchor also allowed us to exclude possible
dates that did not conform to a unidirectional time series
along the spine-series axis.
We used JMP IN 5.1.2 (SAS Institute, Cary, NC, USA)
to perform statistical analyses and the SSA-MTM Toolkit
(singular spectrum analysis/multi-taper method; Ghil et al.
2002; Dettinger et al. 1995) to analyze the power spectra of
isotopes in the dated spine-series from Saguaro 162. Singular spectrum analysis (SSA) is a smoothing function that
empirically determines stable cycles in time-series data and
is useful for short, noisy time series. The multi-taper
method (MTM) is used to estimate singular or continuous
components (e.g., frequencies or trends) within a time
series. We used P = 2 and three data tapers, which has
been shown to be suitable for climate time series (Mann
and Park 1994).
Oecologia (2007) 154:247–258
decreased rapidly thereafter to 11.7% in August. The sharp
increase in d18O preceded the artificial drought initiated in
late April, beginning when plants were being watered
frequently and when plant water content was high. This
period also corresponded to the dates when vapor pressure
deficit (VPD) increased greatly (Fig. 1). We suspect that an
increased rate of evaporation caused by higher VPD began
the upward trend of d18O, with desiccation after the cessation of irrigation contributing to even greater d18O
values. As expected, d18O decreased in late July and early
August after VPD had decreased, heavy rainfall had
occurred and irrigation had resumed. Although the effects
of climate and treatment were confounded in this experiment, the changes in d18O of stem water appeared to be
strongly associated with changes in VPD and the availability of soil water.
We used the measured plant mass, night-time temperature and relative humidity to model stem water d18O during
periods of evaporation (Eq. 1) and recharge (Eq. 2). We
took the measured stem water d18O values from each plant
in April and July as initial points for the evaporative and
recharge models, respectively (Fig. 2). During the artificial
drought (April–July 2005), the cacti lost 40% of their
mass, and both modeled and measured d18O values of
water at the stem apex increased (Fig. 2a–d). The Rayleigh
evaporative model, however, overestimated the final
Results and discussion
Recharge, evaporation and isotopic composition
of potted saguaro
The mean d18O value of cortex water near the apex of the
four potted saguaro plants varied by 11% over the course
of the year (Fig. 1). In general, changes in the d18O values
of apex water were small during the cooler months of
October through March. However, these values increased
rapidly from 11.8% in March to 22.3% in July and
123
Fig. 1 Mean d18O values and 95% confidence intervals of water from
stem tissue near the apex of four 0.8-m tall saguaro cacti (top panel).
Mean minimum vapor pressure deficit derived from monthly mean
minimum temperatures and monthly mean maximum relative humidity at the Tucson International Airport (bottom panel)
Oecologia (2007) 154:247–258
253
measured d18O values by 2%. Upon further examination,
we found strong vertical gradients (12% for d18O) within
the plant stem that may change from month to month and
dynamically influence the final isotopic value of water at
the apex. The isotopic gradients in these cacti resemble an
evaporative chain-of-lakes (Craig and Gordon 1965) in that
water becomes more enriched with 18O as it travels upward
from the plant base (Fig. 3). For the evaporative model, an
increased water flux from the base to the apex may have
brought water relatively unenriched in 18O to the apex
directly through the pith, thus reducing the d18O value
below the modeled value. Alternatively, an error in the
mass loss measurement of 7% (3 kg) would also yield a
difference in modeled d18O values of 2%.
Fig. 3 Local meteoric water line for Tucson, AZ (line, d2H = 5.27
· d18O 11.1) and potted cactus stem-water evaporation line (grey
arrow). Mean stem water isotope values and 95% confidence intervals
from potted 0.8 m tall cacti (circles, n = 4) at 25 cm, 50 cm and
75 cm height (respectively, from lower left to upper right) moving
away from mean irrigation–precipitation water isotope values
(square)
There was also a strong association between modeled and
measured d18O values of water at the apex during recharge
from July to October (Fig. 2e–h). For recharge, the twocomponent model (Eq. 2) underestimated the measured d18O
value of stem waters by 2.5%. Underestimation of d18O by
the recharge model may be a result of continued evaporation
after July while recharge occurred.
It is clear that, even with these discrepancies, evaporation and recharge have the overall effect of raising and
lowering, respectively, the d18O values of stem water at the
apex. The waters in a cactus stem, however, are clearly not
well mixed, and a more sophisticated spatio-temporal
model is needed to describe their isotopic value within the
stem and through time, with particular attention to the flux
of water through the cactus.
F14C derived growth model in a naturally
occurring saguaro
Fig. 2 Variation over time of measured (filled circles) and evaporative model (open circles) stem water d18O from stem tissue near the
apex of four 0.8 m tall saguaro cacti between April and July 2005
(panels a–d). Measured and recharge model d18O between July and
October 2005 (panels e–h). Fraction original mass is the fraction of
the cactus’ mass compared to the same cactus’ mass in April 2005, for
all cases (panels a–h). Time moves from left to right. Top and bottom
panels are paired to show data from one cactus each (i.e., the cactus in
panel a is the same cactus as in panel e)
An individual saguaro spine emerges quickly (within
months) from the areole, lengthening up to 0.7 mm each
day (N. English, personal observation). F14C ages, measured separately from the tip and base of a mid-1980s
spine, further support this observation (Table 1). As in
other plants (Reimer et al. 2004), spines incorporate
ambient carbon from the immediate atmosphere and appear
to use little storage carbon (Table 1). To confirm these
observations we measured a newly grown spine collected
in 2004 from the top of a plant growing 23 km from
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254
Fig. 4 F14C age of spine tips (triangles) from Saguaro 162 compared
to the age of spines at the same height interpolated from measured
heights in 1964, 1970, 1993 and 2002 (Table 1). Line is the one-toone correlation line. Error bars represent 2r age ranges as discussed
in the text
downtown Tucson, a relatively unpolluted environment.
This spine’s F14C age corresponded to 2004 (F14C =
1.0709 0.0016), indicating that, at the apex of this
plant, minimal carbon is allocated from previous years’
storage for synthesis of spine tissue. Thus, unlike the
needles of pine trees (Wright and Leavitt 2006), the apical
spines of saguaro plants do not appear to be constructed
from storage carbohydrates that have been assimilated in
previous years. In general, production of spines occurs only
at the stem apex (Mauseth 2006); however, areoles damaged after their formation will sometimes regrow spines
from an axillary bud that has not been used for flowering or
arm formation. Fortunately, these are easily identified by a
second areole growing either on top of another areole or
over an areole scar (N. English, personal observation).
For Saguaro 162 there was a one-to-one relationship
(95% confidence interval from 0.96 to 1.10) between the
age of spines derived from heights measured by Pierson
and Turner (1998) and the F14C age of spine tips from
heights spanning 77–377 cm (Fig. 4, r = 0.997, P
0.0001). For all the spines that were compared (n = 8),
however, the F14C ages were 2.1 years (95% confidence
interval from 1.2 to 3.2) more modern than the age interpolated from measured heights. This offset is not due to
stored carbon assimilated in previous years (with relatively
high F14C) being used to grow new spines, since the spines’
F14C ages would appear to be older not more modern (see
also discussion above). Thus, we attribute this offset to
either: (1) a discrepancy between our choice of a base for
height measurements and that used by Pierson and Turner
(1998), or (2) the incorporation of 14C-depleted CO2 from
urban fossil fuel emissions (Levin et al. 2003; Eastoe et al.
2004). The former is unlikely, given that a spine grown
during the summer of 2002 and collected from the apex of
123
Oecologia (2007) 154:247–258
Saguaro 162 (377 cm) yielded a F14C age of 2004.7,
1.9 years more modern than when sampled and consistent
with the offset of samples lower on the plant. However, the
incorporation of F14C depleted CO2 from fossil fuels is
quite probable, since the field site at Tumamoc Hill is
located fewer than 2 km from downtown Tucson and a
major interstate freeway. We used the offset measured in
2004 of 1.9 years as a correction factor for earlier F14C
ages to account for the input of fossil fuel carbon; however,
we also note that using the mean discrepancy of 2.1 years
yields similar results. We conclude, therefore, that, with
careful calibration, F14C measurements from spines are a
promising tool for measuring rates of plant growth and
estimating the age of a spine or plant between 1955 and
today.
Temporal d13C and d18O variations in a spine-series
from a naturally occurring saguaro
To compare the time series of d18O and d13C of spines
from Saguaro 162 to precipitation records on Tumamoc
Hill, we used date predictions based on observed heights of
Saguaro 162 measured by E. Pierson and R. Turner (personal communication) over the past 38 years (Table 1).
This is the more direct time-series measurement, but the
results would have been the same if the corrected F14C
ages of spines had been used. For dates that precede Pierson and Turner’s measurements, we used the corrected
F14C-derived ages.
Strong cyclical variations in the d13C and d18O can be
seen visually in the spine-series from Saguaro 162, and
multiple taper method (MTM, Ghil et al. 2002) and singular spectrum analysis (SSA, Dettinger et al. 1995)
confirmed these patterns (Table 2). Periods of low d13C
separate each year in the 15-year d13C spine-series record
(Fig. 5). Using MTM with F14C-corrected ages from spine
heights of 211 cm and 287.5 cm as boundaries, we found
statistically significant variance (99% confidence level) in
d13C on an annual frequency of 1.08 cycles/year (0.72–
1.52 years/cycle; Table 2). Visually, there appears to be a
strong annual cycle in the d18O record of spines over the
15-year record, but based on the MTM analysis the primary
spectral peak in d18O occurs above the annual frequency, at
1.63 years/cycle (1.08–2.29 years/cycle; Table 2). These
analyses suggest that the d13C variations in the spine-series
from Saguaro 162 may reasonably be used as an isotopic
chronometer representing annual periodicity, but that the
use of d18O for this purpose is less reliable.
Spines on saguaro in Tucson generally emerge between
April and September (Steenbergh and Lowe 1983)
although they are presented and analyzed here as a continuous time series. Periods during which spines do not
Oecologia (2007) 154:247–258
255
Table 2 Variables and spectral analysis results using the multiple
taper method (MTM) for d13C and d18O in the Saguaro 162 spineseries
Time-series variables
F14C
yearsa
Maximum
F14C years
Minimum
F14C years
Begins
1980.7
1978.3
1982.5
Ends
1992.4
1996.3
2000.2
Years
15.6
21.9
10.4
Data points
96
96
96
Unit time
0.16
0.23
0.11
Spines per year
6.15
4.38
9.23
13
d C
Years/cycle (1st component)
1.08
1.52
0.72
Years/cycle (2nd component)b
1.35
1.90
0.90
1.63
2.29
1.08
d18O spine-series
Years/cycle (1st component)
a
Based on unit-time interpolated and extrapolated from corrected
F14C ages at 211 cm and 287.5 cm and assuming year-round spine
growth
b
1st and 2nd components are significant (a = 0.95) periodicities in a
time series in order of greatest significance
grow (November–February; N. English, personal observation) will, therefore, not record changes in d13C or d18O
due to stem-water recharge or evaporative losses. Given the
variable nature of spine growth, we recognize several
potential sources of error in our spine-series analyses.
Firstly, changes in the number of spines added to the stem
each year due to climate or age may change the significance or add or subtract spectral components at decadal
scales by altering the resolution of the spine-series. For
example, when growing rapidly, a saguaro may produce
eight spines per year, thereby providing resolution at a subseasonal scale, but when it is growing slowly, there may be
only three spines per year, which can only provide information at the annual scale. Secondly, years with many
spines but low isotope variance due to climate factors (i.e.,
prolonged drought) may be difficult to detect as an annual
cycle, thereby altering the spectral character of a time
series. This would create the appearance of fewer cycles in
a given time period and decrease the strength of an
otherwise significant spectral component.
We see several potential scenarios of dampened amplitude in our d18O and d13C spine-series. For example,
between 290 cm and 310 cm, two dry winters separated by
a weak monsoon period yielded a less distinct trough in
d18O, so that 2 years appeared to represent only one
(Fig. 5). Likewise 2 years appeared as only one between
195 cm and 210 cm, when soil moisture and the premonsoon climate were very wet (El Niño winter of 1982–
1983), resulting in lower d18O and d13C values in spine
tissue (Fig. 5). As wet soil conditions persisted until the
start of the monsoons, we hypothesize that cacti would
continue greater expression of the C3 signal (CAM phases II and IV) through the normally dry period of the year,
resulting in the absence of a peak in d13C for that year.
The length of the spine isotope record based on the SSA
of d13C yields one year fewer than expected based on ages
interpolated from measured heights taken in 1970 and 1993
(Table 1; 15 vs 16 years). This discrepancy suggests that
either: (1) the SSA of d13C underestimates the number of
cycles present in the record, or (2) the rate of growth
interpolated from measured heights was an underestimate,
and, thus, the age over the spine-series period was overestimated. Saguaro has been observed to grow and
reproduce under the harshest of conditions (Steenbergh and
Lowe 1977), and SSA results closely match clear peaks and
troughs in the isotope record (Fig. 5). For these reasons, we
believe the discrepancy results from imprecision of height
measurements, giving an underestimation of growth rates.
In the context of Pierson and Turner’s (1998) demographic
study, measurement errors of 10 cm or 20 cm would have
had little effect on the outcome of their studies, due to their
large sample sizes and the use of saguaro height classes
rather than continuous numeric height data (R. Turner,
personal communication). For our purposes, however, the
cyclical variations seen in the SSA of d13C was used to
assign years (shaded bars in Fig. 5) to spines—using the
observed height in 1993 as an anchor for our chronology.
Environmental control of d13C and d18O variations
in a spine-series from a naturally occurring saguaro
The amplitudes of d18O and d13C variation in the spineseries of Saguaro 162 (13% and 3%, respectively) are
similar in magnitude and timing to variations seen in the
apical stem waters of much smaller potted saguaro cacti
and other obligate CAM plants (Roberts et al. 1997). Spine
tissue d13C values from Saguaro 162 were positively correlated with d18O (r = 0.45, P \ 0.0001). If stomatal
conductance and leakiness were driving d13C values, we
would expect them to be negatively correlated to d18O
values from the same spine. However, if we assume that
variation in d13C in spine tissues is caused only by the
photosynthetic pathway used to fix CO2 from the atmosphere, then the 3% variation in spines represents the
presence of 10% carbon derived from daytime (C3)
photosynthesis, an untested although reasonable conjecture
when we consider saguaro analogs like F. acanthodes.
Oxygen and carbon isotope values appear to be influenced
by anomalous climate conditions through enzymatically
driven processes. Two very low d18O excursions occurred in
1983 and 1993. These low values were seen after wet winters
of the previous year strongly influenced by ENSO, when the
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Oecologia (2007) 154:247–258
CO2 by Rubisco in the early morning or late afternoon
(CAM phases II and IV) and reduces the d13C value of
spines grown during these periods. During the dry premonsoon period, saguaro stomates are closed in the
morning and late afternoon, increasing the relative contribution of CO2 fixed by PEPc (phase I) and thus increasing
the d13C values of spine tissue grown during these periods
of drought.
Conclusion
Fig. 5 A record of isotopic variation in spine tips spanning 1.77 m of
Saguaro 162 on Tumamoc Hill, Tucson, AZ. Bars at top (a) are
interpolated years based on measured heights in 1970 and 1993
(Pierson and Turner 1998) and filled triangles with lines are corrected
F14C ages with 2r age ranges (i.e., F14C age minus 1.9 years; see
text). Spine tip d18O values (b) and d13C values (c), plotted by height
from the base of the plant, are shown with a singular spectrum
analysis (SSA) of d13C for comparison (d). Monthly precipitation
values at Tumamoc Hill (e) are shown for October through March
(grey bars) and April–September (black bars). The year 1993 of the
timescale at the top (a) and on the bottom axis (e) of this figure are
anchored to (i.e., in line with) the 320 cm height of Saguaro 162 (c
and Table 1, see text for more detail). Increased precipitation in the
spring of 1983 and winter of 1992–1993 coincided with El Niño in
those years. Shaded bars from top to bottom denote correlated years
based on the SSA
majority of precipitation ([200 mm) fell between January
and March. However, while the d18O of precipitation clearly
influences the bulk average d18O of water in the cactus over
time, the impact of any single rainfall event on the spine
tissue d18O is diminished by admixture with the large
reservoir of water in the stem. The unseasonably wet summer
of 1982 and ENSO-influenced winter of 1982–1983
also produced the most negative d13C values found in our
spine-series.
Given the presence of the strong ENSO signal in our
record, we suggest that the isotopic variability in this
record is due mostly to increased water availability and
cooler temperatures at the beginning and end of each
growing season that favor direct fixation of atmospheric
123
By efficiently collecting and storing precipitation between
long periods of drought, Saguaro, columnar cacti and other
succulents in deserts (e.g., Euphorbiaceae in Africa;
Cowling et al. 1994) contribute significant amounts of
water, nutrients and energy to consumers via flowers,
fruits, seeds and stems over the entire year (Markow et al.
2000; Wolf and Martinez del Rio 2003). Climate changes
affecting precipitation (NAST 2000) may greatly impact
the viability and distribution of saguaro and other species
of succulents, as well as their dependants (see, e.g.,
Houghton et al. 2001). As such, being able to determine
how these keystone species have responded to climate
variation in the past provides us with a valuable tool for
predicting their success in the future.
The data from Saguaro 162 and our potted cacti
experiments suggest that columnar cacti record changes in
and responses to rainfall and VPD in the stable isotopes of
their spine tissue. We have yet to quantify fully the interaction of precipitation, humidity, temperature, stem-water
flux and other variables, but we have shown that there is
good reason to suspect that the variation in d13C and d18O
in the spines of cacti are a result of distinct climate properties that include the interaction of these processes.
Additionally, we have put forward a new method for
establishing the age of columnar cactus, saguaro in this
case, using F14C in spines and, consequently, for calculating the stem growth rate. The isotopic chronometers
(F14C and d13C), and isotopic signals (d13C and d18O),
recorded in spines are just the beginning of many studies
that can improve our understanding of climate variation in
arid deserts and of the response of these organisms to a
changing environment.
Acknowledgments This work was funded by an Environmental
Protection Agency STAR Fellowship, a William G. McGinnies
Scholarship and a Geological Society of America student grant. Jeff
Pigati and Christa Placzek processed 14C samples to graphite, and
Warren Beck at the NSF-Arizona Accelerator Mass Spectrometry
Laboratory provided 14C analyses. Valuable discussions, data and
laboratory space were provided by K. Anchukitus, T. Ault, J. Bower,
J. Cole, T. Drezner, C. Eastoe, M. Fan, K. Hultine, S. Leavitt, J.
Mauseth, J. Overpeck, B. Peachy, E. Pierson, D. Potts, J. Quade and
R. Turner. We are also grateful for additional comments from F. C.
Oecologia (2007) 154:247–258
Meinzer and two anonymous reviewers. All experiments complied
with the current laws of the USA and the State of Arizona.
References
Brendel O, Iannetta PPM, Stewart D (2000) A rapid and simple
method to isolate pure alpha-cellulose. Phytochem Anal 11:7–10
Cernusak LA, Farquhar GD, Pate JS (2005) Environmental and
physiological controls over oxygen and carbon isotope composition of Tasmanian blue gum, Eucalyptus globulus. Tree Physiol
25:129–146
Clark I, Fritz P (1997) Environmental isotopes in hydrology. CRC
Press LLC, Boca Raton
Cowling RM, Esler KJ, Midgely GF, Honig MA (1994) Plant
functional diversity, species-diversity and climate in arid and
semiarid southern Africa. J Arid Environ 27:141–158
Craig H, Gordon LI (1965) Deuterium and oxygen-18 variations in
the ocean and the marine atmosphere. In: Tongiorgi E (ed)
Proceedings of a conference on stable isotopes in oceanographic
studies and paleotemperatures. Spoleto, Italy, pp 9–130
Dawson TE, Mambelli S, Plamboeck AH, Templer PH, Tu KP (2002)
Stable isotopes in plant ecology. Annu Rev Ecol Syst 33:507–559
Despain DG, Bliss LC, Boyer JC (1970) Carbon dioxide exchange in
saguaro seedlings. Ecology 51:912–914
Dettinger MD, Ghil M, Strong CM, Weibel W, Yiou P (1995) Software
expedites singular-spectrum analysis of noisy time series, Eos,
Trans. American Geophysical Union, 76, pp 12, 14, 21
Dodd AN, Borland AM, Haslam RP, Griffiths H, Maxwell K (2002)
Crassulacean acid metabolism: plastic, fantastic. J Exp Bot
53:569–580
Drezner TD (2003a) Saguaro (Carnegiea gigantea, Cactaceae) age–
height relationships and growth: the development of a general
growth curve. Am J Bot 90:911–914
Drezner TD (2003b) A test of the relationship between seasonal rainfall
and saguaro cacti branching patterns. Ecography 26:393–404
Drezner TD (2005) Saguaro (Carnegiea gigantea, Cactaceae) growth
rate over its American range and the link to summer precipitation. Southwest Nat 50:65–68
Drezner TD, Balling RC (2002) Climatic controls of saguaro
(Carnegiea gigantea) regeneration: a potential link with El
Niño. Phys Geogr 23:465–475
Eastoe C, Gu A, Long A (2004) The origins, ages and flow paths of
groundwater in Tucson Basin: results of a study of multiple
isotope systems. In: Hogan JF, Phillips FM, Scanlon BR (eds)
Groundwater recharge in a desert environment: the southwestern
United States. American Geophysical Union, Washington DC,
pp 217–234
Ehleringer JR, Roden J, Dawson TE (2000) Assessing ecosystem
level water relations through stable isotope ratio analysis. In:
Sala OE, Jackson RB, Mooney HA, Howarth RW (eds) Methods
in ecosystem science. Springer, New York, pp 181–198
Ghil M, Allen RM, Dettinger MD, Ide K, Kondrashov D, Mann ME,
Robertson A, Saunders A, Tian Y, Varadi F, Yiou P (2002)
Advanced spectral methods for climatic time series. Rev
Geophys 40:1003
Gibson AC, Nobel PS (1986) The cactus primer. Harvard University
Press, Cambridge
Griffiths H (1992) Carbon isotope discrimination and the integration
of carbon assimilation pathways in terrestrial CAM plants. Plant
Cell Environ 15:1051–1062
Griffiths H, Broadmeadow MSJ, Borland AM, Hetherington CS
(1990) Short-term changes in carbon-isotope discrimination
identify transitions between C3 and C4 carboxylation during
Crassulacean acid metabolism. Planta 181:604–610
257
Gutzler DS, Kann DM, Thornbrugh C (2002) Modulation of ENSObased long-lead outlooks of southwestern US winter precipitation by the Pacific decadal oscillation. Weather Forecast
17:1163–1172
Haslam R, Borland A, Maxwell K, Griffiths H (2003) Physiological
responses of the CAM epiphyte Tillandsia usneoides L. (Bromeliaceae) to variations in light and water supply. J Plant
Physiol 160:627–634
Houghton JT, Ding Y, Griggs DJ, Noguer M, van der Linden PJ, Dai
X, Maskell K, Johnson CA (2001) Climate change 2001: the
scientific basis. Contribution of working group 1 to the third
assessment report of the intergovernmental panel on climate
change. Cambridge University Press, Cambridge
Hua Q, Barbetti M (2004) Review of tropospheric bomb 14C data for
carbon cycle modeling and age calibration purposes. Radiocarbon 46:1273–1298
Keeling CD, Mook WG, Tans PP (1979) Recent trends in the C-13/C12 ratio of atmospheric carbon dioxide. Nature 277:121–123
Lajtha K, Kolberg K, Getz J (1997) Ecophysiology of the saguaro
cactus (Carnegiea gigantea) in the Saguaro National Monument:
relationship to symptoms of decline. J Arid Environ 36:579–590
Levin I, Kromer B, Schmidt M, Sartorius H (2003) A novel approach
for independent budgeting of fossil fuel CO2 over Europe by
14
CO2 observations. Geophys Res Lett 30:2194
Mann ME, Park J (1994) Global-scale modes of surface-temperature
variability on interannual to century timescales. J Geophys Res
Atmos 99:25819–25833
Markow TA, Anwar S, Pfeiler E (2000) Stable isotope ratios of
carbon and nitrogen in natural populations of Drosophila species
and their hosts. Funct Ecol 14:261–266
Mauseth JD (2000) Theoretical aspects of surface to volume ratios
and water-storage capacities of succulent shoots. Am J Bot
87:1107–1115
Mauseth JD (2006) Structure–function relationships in highly modified shoots of Cactaceae. Ann Bot 98:901–926
McAuliffe JR, Janzen FJ (1986) Effects of intraspecific crowding on
water uptake, water storage, apical growth, and reproductive
potential in the sahuaro cactus, Carnegiea gigantea. Bot Gaz
147:334–341
McCarroll D, Loader NJ (2004) Stable isotopes in tree rings. Q Sci
Rev 23:771–801
National Assessment Synthesis Team (NAST) (2000) Climate change
impacts on the United States: the potential consequences of
climate variability and change. Overview. US Global Change
Research Program. Cambridge University Press, Cambridge
O’Leary MH (1988) Carbon isotopes in photosynthesis. Bioscience
38:328–336
Osmond CB (1978) Crassulacean acid metabolism: a curiosity in
context. Annu Rev Plant Physiol 29:379–414
Pierson EA, Turner RM (1998) An 85-year study of Saguaro
(Carnegiea gigantea) demography. Ecology 79:2676–2693
Reimer PJ, Brown TA, Reimer RW (2004) Discussion: reporting and
calibration of post-bomb 14C data. Radiocarbon 46:1299–1304
Roberts A, Borland AM, Griffiths H (1997) Discrimination processes
and shifts in carboxylation during the phases of Crassulacean
acid metabolism. Plant Physiol 113:1283–1292
Roden JS, Ehleringer JR (1999) Hydrogen and oxygen isotope ratios
of tree-ring cellulose for riparian trees grown long-term under
hydroponically controlled environments. Oecologia 121:467–477
Roden JS, Lin G, Ehleringer JR (2000) A mechanistic model for
interpretation of hydrogen and oxygen isotope ratios in tree-ring
cellulose. Geochim Cosmochim Acta 64:21–35
Schulze ED, Ziegler H, Stichler W (1976) Environmental control of
crassulacean acid metabolism in Welwitschia mirabilis in its
natural range of distribution in the Namib Desert. Oecologia
24:323–334
123
258
Slota PJ, Jull AJT, Linick TW, Toolin LJ (1987) Preparation of small
samples for 14C accelerator targets by catalytic reduction of CO.
Radiocarbon 29:303–306
Steenbergh WF, Lowe CH (1977) Ecology of the saguaro. II.
Reproduction, germination, establishment, growth, and survival
of the young plant. Scientific Monograph Series 8. National Park
Service, Washington DC
Steenbergh WF, Lowe CH (1983) Ecology of the saguaro. III. Growth
and demography. Scientific Monograph Series 17. National Park
Service, Washington
Turner RM, Bowers JE, Burgess TL (1995) Sonoran desert plants: an
ecological atlas. The University of Arizona Press, Tucson
123
Oecologia (2007) 154:247–258
West JB, Bowen GJ, Cerling TE, Ehleringer JR (2006) Stable
isotopes as one of nature’s ecological recorders. Trends Ecol
Evol 21:408–414
Winter K, Holtum JA (2002) How closely do the d13C values of
Crassulacean acid metabolism plants reflect the proportion of
CO2 fixed during day and night? Plant Physiol 129:1843–1851
Wolf BO, Martinez del Rio C (2003) How important are columnar
cacti as sources of water and nutrients for desert consumers? A
review. Isot Environ Health Stud 39:53–67
Wright WE, Leavitt SW (2006) Needle cell elongation and maturation timing derived from pine needle cellulose d18O. Plant Cell
Environ 29:1–14