Palaeogeography, Palaeoclimatology, Palaeoecology 293 (2010) 108–119
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Palaeogeography, Palaeoclimatology, Palaeoecology
j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / p a l a e o
A 26-year stable isotope record of humidity and El Niño-enhanced precipitation in
the spines of saguaro cactus, Carnegiea gigantea
Nathan B. English a,⁎, David L. Dettman b, David G. Williams c
a
b
c
Earth and Environmental Sciences, Los Alamos National Laboratory, Los Alamos, NM 87545, United States
Department of Geosciences, University of Arizona, Tucson, AZ 85721, United States
Departments of Renewable Resources and Botany, University of Wyoming, Laramie, WY 82071, United States
a r t i c l e
i n f o
Article history:
Received 24 September 2009
Received in revised form 26 April 2010
Accepted 8 May 2010
Available online 20 May 2010
Keywords:
Stable isotopes
Radiocarbon
Dendrochronology
Acanthochronology
Terrestrial climate proxies
El Niño
Cactus
Saguaro
Carnegiea gigantea
a b s t r a c t
Seasonal and annual variations of rainfall and humidity are recorded in the carbon and oxygen stable isotope
ratios of sequentially grown spines found on the columnar cactus, Carnegiea gigantea. A 26-year long
composite δ18O and δ13C isotope record from the spines of five saguaro cacti was created using bomb
radiocarbon and semi-annual variations in δ13C. Once dating errors in the composite record are corrected,
mean annual spine δ18O is negatively correlated (P b 0.001) with total annual precipitation (TAP) from
November through October and positively correlated (P b 0.01) with mean annual nighttime vapor pressure
deficit (VPD). Year-to-year decreases (N 2‰) in the maximum annual spine δ18O are positively correlated
(P b 0.01) with the Southern Oscillation Index (SOI). We attribute these decreases to enhanced winter rainfall
associated with the El Niño phase of the El Niño-Southern Oscillation. Minimum annual δ13C is negatively
correlated with TAP (P b 0.05) and mean nighttime VPD (P b 0.05). These results bolster proposed mechanistic
models of isotopic variation in the spines of columnar cactus and demonstrate how isotopic spine series may
be used as climate proxies in regions of the Americas where trees suitable for traditional or isotopic
dendrochonology are absent.
Published by Elsevier B.V.
1. Introduction
Many columnar cacti grow durable woody spines in sequential
order, and these spines are retained in series along the sides of cacti
for decades (Mauseth, 2006). Analogous to tree rings, these spines
contain isotopic information linked to past climate variation. Isotopic
measurements from spines of long-lived columnar cacti should yield
useful records of climate and physiological variation (English et al.,
2007, 2010). English et al. (2007, 2010) have developed mechanistic
models of isotopic variation in the columnar saguaro cactus
(Carnegiea gigantea, (Engelm) Britt and Rose) that show how
precipitation and nighttime vapor pressure deficit (VPD) can
determine the δ18O and δ13C of spines by altering the water storage
and photosynthetic fractionation processes of saguaro. English et al.
(2007) observed that spines grown in series along the stem of a
saguaro cactus (hereafter referred to as a spine series) exhibit
seasonal and annual variations in stable isotope ratios (δ13C and
δ18O). Lower isotopic values in spines grown in 1983 and 1993 were
associated with winter rains enhanced by the El Niño phase of the El
Niño-Southern Oscillation (ENSO) (Gutzler et al., 2002). However, it
⁎ Corresponding author. Los Alamos National Laboratory, Earth and Environmental
Sciences, EES-14, MS J495, Los Alamos, NM 87545, United States. Tel.: +505 667 6551;
fax: +505 665 3866.
E-mail address: nenglish@lanl.gov (N.B. English).
0031-0182/$ – see front matter. Published by Elsevier B.V.
doi:10.1016/j.palaeo.2010.05.005
has yet to be shown that isotopic spine series of δ18O and δ13C from
multiple saguaros respond in unison to common environmental
changes (English et al., 2007). Here we take the next step and develop
a composite isotope spine-series from saguaro cacti and compare this
composite record with local instrumental and reanalysis climate data
to measure its utility as a climate proxy.
The massive, long-lived (125–175 yr) saguaro cactus occurs
throughout the Sonoran Desert in southwestern Arizona and western
Sonora, Mexico (Turner et al., 1995). Saguaro and the other ∼140
columnar cactus species of the new world (D. Yetman, pers. comm.)
are often vital to the functioning of arid and semi-arid ecosystems.
Significant amounts of water, nutrients and energy are provided to
consumers from flowers, fruits, seeds and stems of these large
succulents (e.g. Markow et al., 2000; Wolf and McKechnie, 2003).
Drezner and Balling (2002) and Drezner (2003a,b) find positive
correlations between branching (a proxy for reproductive potential),
stem diameter (water storage) and seedling recruitment in saguaro
and winter–spring precipitation, but only limited correlation with
summer precipitation. Saguaro growth rate, however, is highly
dependent on summer precipitation (Drezner, 2005) provided by
the North American Monsoon (NAM) in July, August and September
(Wright et al., 2001). Climate variability and future climate change
may have significant effects on saguaro growth and reproduction. El
Niño (warm) conditions in the eastern Pacific are associated with
increased winter precipitation in this region, although the summer
N.B. English et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 293 (2010) 108–119
109
are accurately dating the spine series and teasing out the confounding
effects on isotopic variability of relative humidity and rainfall. Trees
that lack annual rings also share these challenges, however, combined
advances in dendrochronology and isotope ratio mass spectrometry
have led to advances in tree physiological research (McCarroll and
Loader, 2004; West et al., 2006) and to quantitative estimates of past
climate regimes (Anchukaitis et al., 2008). Likewise, we have begun to
develop and expand our understanding of cactus physiology and
isotopic variation and the relationship of isotopic variations in cactus
spines to climate (English et al., 2007, 2010). To this end, in addition to
the spine series presented in English et al. (2007), we have collected
four additional spine series from nearby saguaros. Using radiocarbon
(F14C) and in-series measurements of spine δ18O and δ13C spines from
these cacti, we apply the methodologies and techniques of dendrochronology to test the following hypotheses: 1) cactus populations
show a common isotopic response in spines to environmental change;
2) oxygen isotope variation in spine series are associated with total
annual precipitation (TAP); 3) carbon isotope variation in the spine
series are associated with annual variations in nighttime vapor
pressure deficit (VPD); and 4) enhanced winter precipitation is
associated with anomalous δ18O and δ13C values in spine series.
2. Methods
2.1. Spine series and climate data collection
Fig. 1. Spine height and corrected F14C age (open circles) compared to observed age and
apical height of the cactus (filled squares). Observed apical heights are from E. Pierson
(Pers. communication). Numbers in upper left of each panel indicate the individual
cactus the spines were collected from (Table 1).
monsoon is unaffected. Decreases in humidity and rainfall associated
with anthropogenic induced climate change are predicted for the
American Southwest by a majority of climate models (Seager et al.,
2007) and may already be underway (Stahl et al., 2009). This
increased aridity is predicted to occur through decreased precipitation
and unchanged or moderately increased evaporation in the winter,
and reductions to precipitation that outpace reduced evaporation in
the summer (Seager et al., 2007).
We use the isotopic variation in spine-series from five cacti to
examine the relative importance of seasonal and annual rainfall, VPD
and isotopic variation in spines. The greatest challenges to this work
Between December 2006 and April 2007 we collected a heightordered series of spines for isotope measurement (spine series) from
five N3.7 m tall, saguaro cacti (including the spines presented in
English et al., 2007 and grown since on Saguaro 162). These cacti, all
within 100 m of each other, have grown naturally at the University of
Arizona Desert Laboratory at Tumamoc Hill, Tucson, Arizona. Their
heights have been measured repeatedly over 38 years as part of an
effort to establish growth models for this stand of saguaro (Pierson
and Turner, 1998). We used a 4-m tall orchard ladder (Stokes Ladders
Inc., Kelseyville CA) and a flexible meter tape to reach and measure
the height above ground level of the saguaro apex and of each
sampled spine. We used needle-nose pliers and sprue cutters (The
Testor Corporation, Rockford IL) to clip one spine from each areole
(we chose the longest central spine that was most distal from the
areolar meristem) along a single north-facing rib.
Precipitation measurements have been collected ∼200 m from the
saguaros used in this study at least monthly for the 28 years prior to
2007 (J. Bowers, personal communication). We use these data to
calculate total annual precipitation (TAP) between November and
October, total precipitation in January through April (JFMAP) and total
precipitation during the NAM in July through September (JASP).
Generally, spines grow only between March and October (pers.
observation; Steenbergh and Lowe, 1983), so we use November as the
beginning of the cactus water year (TAP). In Tucson, precipitation is
equally distributed between the winter and NAM.
We calculated monthly mean nighttime and daytime VPD for
Tumamoc Hill using reconstructed monthly mean minimum and
maximum temperatures, respectively, and the mean dew point
temperature from the PRISM online database (PRISM Group, 2008).
We use monthly values of the Southern Oscillation Index (SOI; NOAA,
2008) as a measure of ENSO strength (negative SOI is associated with El
Niño like conditions). For precipitation, nighttime and daytime VPD, and
SOI we calculated the mean, maximum and minimum of each variable
for each year. We evaluated the distribution of these parameters using
JMP IN 5.1.2 (SAS Institute, Cary, NC, USA) and those that were not
normally distributed (coefficient of variance N 10) were log transformed
before simple linear regressions with spine series parameters were
performed. We use the Pearson product–moment correlation with
α = 0.05 to quantify the association of annual climate parameters to
each other and to annual isotopic parameters in the composite record.
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Table 1
Saguaro cactus spine series attributes.
Series 162
Series 163
Series 168
Series 182
Series 184
Composite
a
Apex
(cm)
Base
(cm)
Spines
in series
F14C
dates
Start
datea
End
datea
Yearsa
415
414
410
372
413
–
98
115.5
110
96.5
87.5
–
189
176
168
153
167
–
11
4
3
4
4
–
1974.0
1982.6
1979.4
1982.8
1980.9
1980.9
2006.9
2006.9
2006.9
2007.4
2007.4
2006.9
32.9
24.3
27.5
24.6
26.5
26.5
Datum
in seriesa
198
147
166
149
160
157
Mean δ13Ca
Mean δ18O
(‰)
(‰)
− 10.98
−11.39
−11.21
− 10.91
− 12.12
− 11.32
45.71
42.90
41.84
40.75
40.85
42.41
Refers to attributes of the age modeled spine series corrected for atmospheric changes in δ13C.
2.2. Stable isotope and statistical analyses
We performed stable isotope measurements at the Environmental
Isotope Laboratory, Department of Geosciences, University of Arizona.
For each of the 853 spines collected, we analyzed the bulk tissue of the
top ∼2 mm (the tip) for δ18O, and the next ∼ 1 mm section below the
tip for δ13C (1706 total analyses). Spines were dried overnight at 70 °
C before δ18O and δ13C analyses. We measured spine tissue δ18O and
δ13C using a Thermal Combustion Elemental Analyzer (Thermo
Electron Corp, Waltham, MA) and a CHN elemental analyzer (Costech
Analytical Technologies, CA), each attached to a continuous flow
isotope ratio mass spectrometer (Delta Plus, Thermo Electron Corp,
Waltham, MA). Reported values are in per mil (‰) relative to VSMOW for δ18O analyses and PDB for δ13C analyses. The precision for
our method based on repeated analysis of working standards was
0.2‰ for δ18O and 0.1‰ for δ13C. English et al. (2007) measured the
effect of tissue processing on δ18O values of spines from these saguaro
and found that the δ18O values of spine tissue holo- and α-cellulose
(Brendel et al., 2000) were, respectively, 1.1‰ to 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 N 3.13, P b 0.0057).
When we weighed the relatively small and consistent offset in δ18O
values against the labor involved in processing spines to cellulose we
chose to analyze raw spine tissue without further processing.
2.3. Spine age determination
Spines growing from the apex of columnar cacti, such as saguaro,
do not yield readily apparent chronological markers like tree rings.
Fig. 2. Raw spine height and δ13C isotope spine series. Cactus sample #s are to the right of each spine series. Triangles are locations of radiocarbon dates shown in Figs. 1, 3 and 4. Each
δ13C tick mark is 1‰.
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111
Fig. 3. Raw spine height and δ18O isotope spine series. Top panel is cactus 162, the next lower panels are cactus 163, 168, 182 and 184, respectively. Triangles are locations of
radiocarbon dates shown in Figs. 1, 3 and 4. Each δ18O tick mark is 5‰.
Instead, at selected heights we measured the F14C of the segment of
raw spine tissue remaining after δ18O and δ13C analyses. These were
dried overnight at 70 °C and bathed three times in weak HCl acid
(0.1 M) in an ultrasonic bath for 30 min. Each acid bath was followed
by a 30-minute soak and then rinse in Milli-Q water (18 MΩ, Milli-Q,
Massachusetts). Spines were dried a second time and then reduced to
graphite and analyzed for F14C and δ13C (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 (Reimer et al., 2004) to calculate possible
spine ages from measured F14C values corrected for δ13C and line
blank. For the age calculations of pre-1999.5 dates, we used the
Northern Hemisphere Zone 2 data set (Hua and Barbetti, 2004), a 0.2year sample smoothing term and a resolution of 0.2 years. For samples
with a post 1999.5 date we used an unpublished update of the same
dataset provided by Q. Hua (pers. communication) and extrapolated
to 2007. For each F14C value from a spine, Calibomb estimates a
number of possible dates, the 95% confidence interval for each
possible date, and a probability that each possible date is the correct
date (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 possible dates
for that spine weighted by the probability of their being correct. We
conservatively determined the error of that value to be the youngest
and oldest date from the 95% confidence interval of all the possible
ages for each sample (2σ age range). The time series are anchored by
the 1964–1965 atmospheric radiocarbon peak and the heights of
these saguaros measured by Pierson and Turner (1998) in 1964, 1970,
1987, 1993 and by us in late 2006 and early 2007. Thus, for any spines
collected from above the 1964 height, we excluded from the average
of all possible dates any dates that predated the 1964–1965
atmospheric radiocarbon peak. The same is true of our error
determinations. The observed heights allowed us to exclude possible
dates that did not conform to a unidirectional time series along the
spine series axis. Furthermore, to correct for the incorporation of 14Cdepleted CO2 from fossil fuels (English et al., 2007), we subtract the
difference between the F14C age of a modern spine and the date it was
collected from all other F14C derived dates (this offset is less than
2.1 years for all cacti). The association between the observed height of
cacti in a given year and the F14C date of spines from those heights
(Fig. 1) provides a reasonable assurance that F14C spine dates are
within a couple of years of their formation and are consistent with
growth curves for cactus in this region calculated by Drezner (2003c).
2.4. Age-modeling and compositing of isotopic spine series
Tree-ring records from one location are commonly averaged
together to create an annually resolved composite record that can be
used as a proxy for one or more climate variables (McCarroll and
Loader, 2004). The purpose of creating composite records is to: 1)
reduce the signal “noise” associated with individual plant variability
caused by genetic, microclimatic or other effects unique to each plant;
and 2) to create a record that more accurately represents the mean
population response of a selected variable (e.g. δ13C and δ18O) to a
local climate variable (e.g. precipitation). We use δ13C and δ18O spine
series from five cacti (Table 1, Figs. 2 and 3) to demonstrate and
evaluate the utility of composited isotopic spine-series. Unlike trees
with rings, however, cacti and their spine series' lack indicators of
annual growth and we must first determine and apply an age model to
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Fig. 4. Age-modeled δ13C isotope spine series. Each series was interpolated from the raw δ13C isotope spine series (Fig. 2) at two-month intervals and was corrected for the long-term
decrease in atmospheric δ13C (13C Suess effect) and offset to match the mean of all series combined (− 11.32‰). Top panel is Cactus 162, the next lower panels are Cactus 163, 168,
182 and 184, respectively. Triangles are the locations and last two digits of the corrected radiocarbon dates shown in Fig. 1. Gray line with symbols is the raw δ13C isotope spine series
(i.e. identical to Fig. 2) for comparison. Each δ13C tick mark is 1‰.
each spine series so that the spine series are comparable to each other
and to climatic time series. Our methods deserve a detailed
explanation because this is the first time spine series have been
used in this manner, and the conversion from spine height to spine
age is vulnerable to error and subjectivity.
We use seasonal cycles in spine δ13C over a year (English et al.,
2007) in conjunction with F14C ages to guide the development of an
age model for each spine series (Fig. 2). Spine δ13C and δ18O values are
paired, so that the age model for the δ13C spine series can be applied
to the corresponding δ18O spine series. Each raw spine series contains
∼170 spines (Table 1, Figs. 2 and 3), but they are unevenly distributed
among years, with a higher number of spines per year occurring at
mid-height/age when apical growth rates were highest, and fewer
spines near the apex and base of the cactus where apical growth rates
are or were lower (Pierson and Turner, 1998; Drezner, 2003c). We use
Matlab (The MathWorks, Inc., Natick, MA) to develop and apply spine
series age models. The interpolation routine we use linearly interpolates the age of heights between each F14C-dated spine in the series
and then interpolates the spine δ13C values of that series at specified
time increments over the period of the spine series (every two
months, or six steps per year). This yields age-modeled δ13C spine
series with roughly the same number of data points as the raw spine
series (Table 1), although the data are now evenly distributed across
all years.
Next we assign (pin) each seasonal δ13C cycle to a unique year
based on the location and ages of the F14C-dated spines. We know
from sampling at different times of the year that the most negative
δ13C values occur at the beginning and end of the spine-growing
season and more positive δ13C values in the pre-monsoon months of
May and June. As such, we pin each year's beginning (e.g. 1986.0) and
middle (e.g. 1986.5) to the minimum and maximum carbon isotope
value, respectively. An effort is made to maintain the appropriate
number of annual δ13C cycles between F14C-dated spines and to do
this years are assigned with deference to, but not absolute adherence
to, the F14C-dated spines in that series. Additionally, we observed that
each age-modeled spine series exhibits minima in δ13C near 1984 and
1997. If possible within the constraints of annual δ13C cycles and the
F14C-dated spines, years were pinned to account for these benchmark
years. Once each carbon isotope cycle and the height of the spines
within it have been pinned to a unique year, we use this final age
model to interpolate the raw δ13C spine series to the new time scale,
yielding annually dated δ13C spine series. The final age model from
each δ13C spine series is applied to its paired δ18O spine series to yield
an annually dated δ18O spine series. No part of the age modeling is
derived from the δ18O spine series.
The individual isotopic spine series are now further processed to:
1) remove the carbon isotope effect of fossil-fuel pollution (the 13C
“Suess Effect”) (Francey et al., 1999): 2) adjust each spine series to a
common mean so that variation and confidence intervals are more
accurately reflected in the composite record. When fossil fuels are
burned, they release CO2 depleted in 13C. Over decades and centuries,
the accumulation of this isotopically negative CO2 in the atmosphere
can alter plant δ13C values. We accounted for this by detrending each
spine series from the date the most recently grown spine was
collected to 1980 (Francey et al., 1999). In 1980, this leads to ∼ 0.7‰
subtracted from the age modeled δ13C spine series. This is sufficient
N.B. English et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 293 (2010) 108–119
113
Fig. 5. Age modeled δ18O isotope spine series. Each series was interpolated from the raw δ18O isotope spine series (Fig. 3) at two-month intervals and was offset to match the mean of
all series combined (42.41‰). Top panel is Cactus 162, the next lower panel is Cactus 163, 168, 182 and 184, respectively. Triangles are the locations and last two digits of the
corrected radiocarbon dates shown in Fig. 1. Gray line with symbols is the raw δ18O isotope spine series (i.e. identical to Fig. 3) for comparison. Each δ18O tick mark is 5‰.
for a short time-series although more complicated correction schemes
exist (McCarroll et al., 2009). After this, we offset each age-modeled
δ13C spine series so that its mean is equal to a common mean (in this
case, a simple average of each δ13C spine series mean, or −11.3‰).
Likewise, for each δ18O spine series, we offset the series so that its
mean is equal to the common δ18O spine series mean (42.4‰). The
age modeled, corrected and adjusted spine series are shown in Figs. 4
and 5. Finally, the values from each unique time interval of the
adjusted and corrected δ13C and δ18O spine series are averaged to
create annually dated, composite records of spine δ13C and δ18O
variation (Figs. 6 and 7). The five averaged samples for each time
period are used to calculate the standard error of the mean.
Seasonal isotopic variations in the composite records are pinned to
the seasons (e.g. maximum δ13C to the pre-monsoon), so that a simple
linear regression of all 157 points in the composite record of δ13C or
δ18O with the climate record of interest will highlight the significance
of the seasonal variability while obscuring inter-annual isotopic
variability related to climate. For this reason we only compare the
relationship of annual parameters in the δ13C and δ18O composite
records, (e.g. mean, maximum and minimum values of any year) to
annual climate parameters (Figs. 6 and 7).
expressed population signal (EPS) (Briffa and Jones, 1990). The
number of cactus required to yield a record of isotopic variation
representative of the population depends on the degree to which the
isotopic spine series covary through time (Wigley et al., 1984;
McCarroll and Loader, 2004). The degree to which our composite
records represent this can be empirically and objectively measured by
comparing the mean inter-spine series correlation coefficient (r) with
a theoretical infinitely sampled (and hence fully representative)
composite where t is the number of spine series:
P
EPSðt Þ =
ðt × r Þ
P
ðt × r Þ + ð1− r Þ
P
ð1Þ
Although there is no strict demarcation, an EPS ≥ 0.85 is used in
dendrochronological studies to suggest that the composited record
accurately represents the mean variance of the population and
yields a signal relatively free of noise due to individual variation
(McCarroll and Loader, 2004). An EPS b 0.85 does not necessarily
indicate that the record is an inaccurate representation of the
population signal.
3. Results
2.5. Calculation of the expressed population signal (EPS)
3.1. EPS
When averaging isotopic time series, we expect that variance
unique to individual cactus will cancel out in proportion to the
number of cactus spine series used in the composite record. In our
composite records, we estimate the shared isotopic variance using the
Together, the five corrected and adjusted δ13C and δ18O spine
series have an EPS b 0.85 (0.68 and 0.66, respectively)(Table 2). We
have calculated the number of spine series required to reach an EPS of
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Fig. 6. Composite δ13C spine record and annual parameters. Bold black line in top panel is the composite δ13C record and is derived by averaging all five age modeled δ13C isotope
spine series (Fig. 4) at two-month intervals. 95% confidence intervals are in gray and account for the fewer spine series averaged before mid-1982. In the minimum annual δ13C,
* denote years that we associate with El Niño enhanced total annual precipitation (TAP, November through October) and very negative SOI (b − 4) in the composite δ18O record
(Fig. 7).
0.85 or greater using the r of the sampled cactus (Table 2). Visually,
there is a striking reduction in the amplitude of variability after ∼ 1997
that also coincides with a reduction in the correlation of paired δ13C
and δ18O (Fig. 4 and 5). When the period 1998 to 2006 is excluded,
EPS improves in the corrected and adjusted δ13C record, but is reduced
in the corrected and adjusted δ18O record (Table 2).
If we examine the EPS of only annual parameters derived from the
corrected and adjusted δ13C and δ18O records, the number of data
points available for regression decreases from 157 to 26. As expected,
the EPS of the annual parameters is less than that of the higher
resolution δ13C and δ18O records (Table 2) with two exceptions — the
EPS of mean annual and minimum annual δ18O is higher.
3.2. δ18O composite records
There is strong evidence that annual spine δ18O in the composite
record is correlated with same-year total annual precipitation (TAP),
January through April precipitation (JFMAP) and vapor pressure
deficit (VPD)(Fig. 7; Table 3). Mean nighttime VPD and same-year TAP
are positively and negatively correlated, respectively, with mean
annual spine δ18O in the composite record. Large reductions (N2‰)
from the previous year in annual maximum spine δ18O in the years
1984, 1992 and 1997 appear to approximately coincide with El Niño
enhanced precipitation in 1983, 1992 and 1998. There is no significant
association between minimum and mean annual δ18O with same year
TAP or JFMAP given the dating mismatch between 1984 and 1997 in
the composite record and 1983 and 1998, respectively, in the
precipitation record. However, even with the dating mismatch,
mean nighttime VPD is strongly associated with the same isotopic
parameters (P b 0.01) as is same- and preceding-year's JFMAP
(P b 0.01, Table 3). When we use the relationship from a simple linear
regression model (Fig. 8, uncorrected) to reconstruct TAP using δ18O,
it does a poor job of reconstructing TAP in 1984, 1997 and 1998
(r2 = 0.08, F24 = 1.98, P b 0.17) (Fig. 9, uncorrected).
We suspect that our age model is off by a year in 1984 and 1997
(i.e. 1984 should be 1983 and 1997 should be 1998). A combination or
any one of the following errors could account for this discrepancy: 1)
dating errors in the F14C dates; 2) extra or missing δ13C peaks; 3)
erroneous assignment of years to the δ13C spine series. To test if these
misplaced years in the composite record obscure the relationship
between minimum- and mean-annual spine δ18O and same-year TAP
and JFMAP, we replaced the 1983 and 1998 annual δ18O parameters
with the values from 1984 and 1997, removed 1984 and 1998, and left
all other values the same (Fig. 8, corrected). With this correction, the
significance of many associations between annual spine δ18O parameters, precipitation, nighttime VPD and SOI are greatly improved
(Table 4). The greatest change occurs in the relationship between
maximum and mean annual δ18O and TAP. Mean annual δ18O in 2003
is anomalously high (Fig. 8, corrected), and when it is also removed
from the regression, 73% of the variation in δ18O is explained by
changes in TAP (Fig. 8, corrected-2003). TAP and the minimum annual
SOI (this parameter captures the strongest El Niño years) are
associated with enhanced same-year JFMAP (F24 = 7.03, P b 0.014)
and decreased mean annual nighttime VPD (F24 = 8.11, P b 0.009) at
N.B. English et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 293 (2010) 108–119
115
Fig. 7. Composite δ18O spine series with annual parameters. Bold black line in top panel is the composite δ18O record and is derived by averaging all five age modeled δ18O isotope
spine series (Fig. 5) at two-month intervals. 95% confidence intervals are in gray and account for the fewer spine series averaged before mid-1982. In the year-to-year change in
maximum δ18O (Δ annual maximum δ18O), * denote years that we associate with El Niño enhanced total annual precipitation (TAP, November through October) and very negative
SOI (b −4). Note that Δ annual maximum δ18O derived from the composite series in 1984 and 1997 appear to be one year late and one year early, respectively.
Tumamoc Hill. Likewise, when the dating correction is made, the
difference between year-to-year maximum annual δ18O is positively
correlated with minimum annual SOI (P b 0.01). We get much better
estimates of TAP (r2 = 0.53, F22 = 24.9, P b 0.0001) when we use the
regression model from the chronologically adjusted annual isotope
data (Fig. 9, corrected).
3.3. δ13C composite records
Paired spine δ13C and δ18O are strongly correlated in individual
and composite spine series (F155 = 93, P b 0.0001). We find significant
associations between annual mean, maximum and minimum δ13C
with daytime and nighttime VPD and maximum annual SOI in the
uncorrected record (Table 3, Fig. 6). As in the δ18O composite record,
large reductions (N0.5‰) in the annual maximum δ13C and the
previous year's maximum δ13C in 1984 and 1997 occur near years
with El Niño enhanced JFMAP in 1983 and 1998. Spine δ13C is not
significantly associated with same-year TAP, same-year or same-andprevious-year's JFMAP. Minimum annual δ13C is positively correlated
with both daytime and nighttime vapor pressure deficit (P b 0.01).
Maximum and mean annual δ13C are negatively correlated with
maximum SOI (P b 0.01).
Table 2
Mean inter-cactus correlation coefficients (r) and expressed population signal (EPS) of age modeled, corrected and adjusted spine series.
1980 to 2006
1980 to 1997
r
EPS(t)
t needed to reach EPS ≥ 0.85
r
EPS(t)
t needed to reach EPS ≥ 0.85
0.30
0.28
0.68
0.66
13
15
0.39
0.22
0.76
0.59
9
20
Annual parameters of corrected and adjusted spine series
5
0.23
0.60
Maximum δ13C
5
0.20
0.55
Minimum δ13C
5
0.19
0.54
Mean δ13C
18
5
0.20
0.55
Maximum δ O
18
Minimum δ O
5
0.42
0.78
5
0.29
0.67
Mean δ18O
20
23
24
23
8
14
0.32
0.24
0.25
0.21
0.15
0.23
0.70
0.61
0.63
0.57
0.48
0.60
12
18
17
22
30
19
t
Corrected and adjusted spine series
δ13C
5
5
δ18O
t is the number of spine series used to calculate r, where each spine series is collected from a different cactus.
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Table 3
Uncorrected annual δ18O and δ13C correlations with annual precipitation, VPD and SOI.
Annual parameters from uncorrected δ18O composite record
Annual parameters from uncorrected δ13C composite record
Max δ18O
Min δ18O
Mean δ18O
Max δ18O difference
Max δ13C
− 0.28
−0.22
−0.13
− 0.27
− 0.32
− 0.11
− 0.27
− 0.56⁎⁎
−0.42
− 0.20
− 0.32
− 0.53⁎⁎
0.02
0.05
− 0.02
0.04
Nighttime vapor pressure deficit
Max nVPD
0.37†
Mean nVPD
0.37†
Log Min nVPD
0.27
0.36†
0.50⁎⁎
0.05
0.41⁎
0.56⁎⁎
0.24
0.02
0.06
0.21
Daytime vapor pressure deficit
Max dVPD
− 0.06
Mean dVPD
− 0.23
Log Min dVPD
− 0.01
0.03
0.29
0.59⁎⁎
Annual climate
parameters
Precipitation
Log TAP (N–O)
Log JASP
Log JFMAP
Log 2 × JFMAP
Southern Oscillation Index
Log Max SOI
− 0.25
Log Min SOI
0.08
Log Mean SOI
− 0.06
−0.08
0.04
−0.02
− 0.04
0.00
0.34†
− 0.10
0.21
0.05
Min δ13C
Mean δ13C
− 0.17
−0.24
− 0.12
−0.29
0.28
0.05
0.26
− 0.04
− 0.05
− 0.20
− 0.02
0.27
0.37⁎
−0.03
− 0.07
−0.12
− 0.12
0.00
− 0.12
0.14
0.14
−0.28
−0.11
0.05
− 0.21
− 0.35†
− 0.26
− 0.08
0.40⁎
− 0.05
− 0.28
− 0.12
0.10
− 0.02
−0.41⁎
0.14
0.04
0.16
−0.40⁎
− 0.18
−0.25
− 0.02
0.25
0.29
− 0.43⁎
−0.10
− 0.16
− 0.24
− 0.22
− 0.25
0.34
0.11
0.37†
0.16
Log Max δ13C difference
0.21
0.02
0.40⁎
0.27
TAP = Total annual precipitation measured from November to October; JASP = Total July to September precipitation; JFMAP = Total January to April precipitation; 2 × JFMAP =
same- and previous-year's JFMAP.
†
P b 0.10. * P b 0.05. ** P b 0.01.
When the record is corrected for dating errors, as it was for the
δ18O composite record, there is a significant association between
minimum annual δ13C and minimum annual SOI (El Niño phase of
ENSO), TAP and same-and-previous year's JFMAP (Table 4). The
associations of maximum and mean annual δ13C with maximum SOI
are slightly more significant. In both the corrected and uncorrected
δ13C composite record, mean annual nighttime VPD is more strongly
associated with spine δ13C than either TAP or same-year JFMAP. While
minimum annual SOI is significantly related to mean nighttime VPD
over this time period (F23 = 8.1, P b 0.009), the removal of one year
(1983) renders the relationship non-significant (F22 = 2.5, P b 0.13).
4. Discussion
4.1. Evaluation of EPS
While the EPS of our corrected and adjusted δ13C and δ18O records
does not exceed 0.85, the records still appear to express a population
response to the environment. Our EPS calculations suggest that at
least 8 or 9 cactus per site should be sampled to capture an EPS of
N0.85. It is not uncommon, however, for studies in isotope
dendrochronology to use 2 or fewer trees (Anchukaitis et al., 2008;
Anchukaitis and Evans, 2010) than in the dendrochronological
Table 4
Corrected annual δ18O and δ13C correlations with annual precipitation, VPD and SOI.
Annual climate
parameters
Annual parameters from corrected δ18O composite record
18
18
18
18
Max δ O
Min δ O
Mean δ O
Max δ O difference
− 0.69**
− 0.36†
− 0.38†
− 0.48*
−0.55*
−0.16
−0.46*
− 0.67**
− 0.70**
− 0.26
− 0.53**
− 0.69**
− 0.44*
− 0.11
− 0.37†
− 0.19
Nighttime vapor pressure deficit
Max nVPD
0.52**
Mean nVPD
0.53**
Log Min nVPD
0.36†
0.47*
0.60**
0.11
0.50**
0.63**
0.28
0.32
0.32
0.45*
Precipitation
Log TAP (N–O)
Log JASP
Log JFMAP
Log 2 × JFMA
Daytime vapor pressure deficit
Max dVPD
− 0.14
Mean dVPD
− 0.20
Log Min dVPD
0.06
−0.07
0.31
0.63**
− 0.13
0.03
0.37†
Southern Oscillation Index
Log Max SOI
−0.25
Log Min SOI
0.47*
Log Mean SOI
− 0.02
− 0.08
0.04
−0.02
− 0.09
0.44*
0.06
− 0.09
− 0.28
− 0.09
0.08
0.55**
0.21
Annual parameters from corrected δ13C composite record
Max δ13C
Min δ13C
Mean δ13C
0.15
0.06
0.23
0.06
−0.42*
−0.34†
−0.24
−0.42*
− 0.03
− 0.06
0.06
− 0.21
0.03
− 0.12
0.01
0.35†
0.47*
0.02
0.08
0.04
− 0.02
−0.05
− 0.15
0.05
0.01
− 0.20
− 0.30
− 0.30
0.00
0.47*
−0.14
− 0.25
− 0.05
0.14
− 0.03
− 0.36†
−0.46*
0.30
− 0.11
− 0.22
0.07
− 0.11
− 0.41*
0.18
− 0.17
0.00
0.41*
0.30
Log Max δ13C difference
0.20
0.06
0.38†
0.30
TAP = Total annual precipitation measured from November to October; JASP = Total July to September precipitation; JFMAP = Total January to April precipitation; 2 × JFMAP =
same- and previous-year's JFMAP. †P b 0.10, *P b 0.05, **P b 0.01, Bold type = P b 0.001.
N.B. English et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 293 (2010) 108–119
117
that track the amplitude of isotopic variation of stem waters and
carbon in large and small cactus and quantify the impact of spine
morphology on isotope fractionation should help in identifying the
cause of reduced variability as the plant ages. Ideally, as in tree ring
studies, plants from many different age classes should be sampled in
future studies to reduce age/height-related noise in the composite
record. Cactus are relatively short-lived compared to trees, however,
and with composite records of isotopic variation in spines compromises must be made between record length and noise to accommodate the question being examined. For this study, we sampled cacti in
the middle of their life cycle. Even though these cacti provide a shorter
record (26-years) than what we believe is possible (∼ 100 years), we
sampled these because: 1) middle-aged saguaro are more likely to
exhibit higher growth rates and therefore spine series with more
spines per year; 2) our sampling strategy was limited by the height of
our ladder and safety considerations; 3) we were unsure of how
resolvable years before 1980 would be given the slow growth rates of
cacti below 1 m tall (Pierson and Turner, 1998).
4.2. δ18O and climate
Fig. 8. A comparison of the mean annual δ18O of spines and total annual precipitation
(Log TAP, mm) for November through October for each year of the composite record.
Top panel shows the simple linear regression (solid line) of the temporally uncorrected
δ18O composite record against TAP. Circles and Xs show data points that are moved or
eliminated, respectively, when we place the mean annual δ18O composite spine values
of 1984 and 1997 in the years 1983 and 1998 while eliminating the uncorrected mean
annual δ18O composite spine values in 1983 and 1998. This yields an improved
regression (solid line, bottom panel) between TAP and mean annual δ18O of spines. The
explanatory power of TAP is improved when 2003 is eliminated from the regression
(dotted line, bottom panel) as well, although it alters the relationship between TAP and
mean annual δ18O very little. Equations represent the relationship of TAP to mean
annual δ18O and are used to reconstruct TAP (Fig. 9).
community from which EPS evolved. Regardless, we use EPS to
evaluate our records and to assess their utility in representing a local
response of cactus isotopes to climate.
For our spine series, the changes in variability and EPS between
1997 and 2006 could be associated with reduced variability in rainfall
or VPD. Alternatively, age- or height-related effects on isotope
fractionation might be responsible for reduced variability. The stem
volume of a saguaro increases over 700% when it grows from 1 to 4 m
tall (Mauseth, 2000 and 2006; N. English, unpublished data). Despite
this growth, there is no large long-term trend in δ18O in the spine
series over the period of time this growth represents (∼30 years)
(Pierson and Turner, 1998). However, reduced variability may be
related to this growth in two ways: 1) a general reduction of the apical
growth rate at ∼ 3 m (Drezner, 2003c) resulting in fewer spines per
year being grown and leading to a reduced probability that seasonal
extremes in climate will be recorded in isotope measurements of
spines; 2) the alteration of physical, physiological or post-photosynthetic fractionation processes associated with the onset of flowering
and fruit production (Steenbergh and Lowe, 1983), changes in the
timing of gas exchange, the changing morphology of spines or stem
growth. Drezner (2008) found that 10 km away from our site, the
average height of saguaro when they first flower is 2.44 m, very close
to ∼2.7 m where EPS degrades in our sampled cactus. Experiments
The variability in the composite δ18O record strongly suggests that
annual variability in precipitation and VPD is recorded in the δ18O of
cactus spines. We hypothesize that increased winter precipitation and
lower nighttime VPD act together in three ways to lower spine δ18O
values. First, weighted δ18O values of Tucson JFMAP (− 9‰) are ∼3‰
more negative than 18O values of precipitation in May through August
(−6‰) (C. Eastoe, unpublished data). Stem waters in cacti are a
mixture of winter and summer rainfall (McAuliffe and Janzen, 1986)
and cacti that take up proportionally more winter than summer
precipitation in that year will have reduced mean annual stem water
δ18O and consequently lower mean annual spine δ18O values for that
year. Second, the strength of Rayleigh fractionation, the mechanism
that has been proposed to increase stem water and spine δ18O values
(English et al., 2007) is determined by the water remaining in the
cactus after evaporation, measured as a percentage of the cactus'
initial water reservoir. Achieving a maximum water volume in the
spring, in conjunction with lower nighttime VPD, translates into lower
pre-monsoon water losses measured in percent of the initial reservoir,
a lower Rayleigh fractionation effect, and thus relatively lower
maximum stem water and spine δ18O values throughout the growing
season than in drier years. Third, there is an isotopic gradient in stem
water (i.e. evaporated water at the apex is enriched in 18O, whereas
relatively fresh water at the base is less so) (English et al., 2007).
Although difficult to model accurately, this gradient is due to
evaporative water loss in the plant (English et al., 2007). Lower VPD
and less evaporation of plant water as it moves upward would lessen
the gradient and consequently reduce the δ18O values of stem water at
the apex.
For these cacti, a reduction from the previous year in maximum
annual spine δ18O greater than 2‰ indicates a strong El Niño year
(SOI b −4, Fig. 7). Conversely, the most positive δ18O values in the
composite record occur between 2001 and 2003, a period of
drastically reduced winter and spring rainfall and increased nighttime
vapor pressure deficits. Overall, the reconstructed values reflect
changes in TAP quite well given the low EPS exhibited between spine
series. We expect that composite records of δ18O derived from more
and longer spine series (with an EPS ≥ 0.85) will yield records more
amenable to the application of statistical transfer functions and skills
testing and will be better able to reconstruct past climates.
4.3. δ13C and climate
The relationship between δ13C in spines and climate is less direct
than that of δ18O in spines. Current theoretical isotope models and
experimental evidence suggest that VPD alters the percentage of carbon
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N.B. English et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 293 (2010) 108–119
Fig. 9. Modeled total annual precipitation (TAP) for 1981 to 2006 using mean annual δ18O from the composite spine record. We model TAP using all three relationships shown in
Fig. 8. Missing years in the model reflect the missing data points in 1984 and 1997 that resulted from moving data from those years into 1983 and 1998, years with El Niño-enhanced
winter rains.
in plant tissues derived from the C3 photosynthetic pathway and the
Crassulacean acid metabolism photosynthetic pathway (CAM) with
consequences for the δ13C value of spines. Increases in VPD (drier) act in
such a way as to make δ13C in spines less negative, while decreases in
VPD (more humid) lead to more negative δ13C in spines. Changes in
mesophyll conductance related to changes in assimilation rates or
nighttime temperatures could also contribute to variation of spine δ13C
values (Griffiths et al., 2007), although the magnitude of this effect is
unknown. Like δ18O, relating δ13C in spines to either precipitation or
vapor pressure deficit is confounded by the strong negative correlation
between mean annual nighttime VPD and TAP (F24 = 22.2, P b 0.0001)
and same-year JFMAP (F24 = 11.8, P b 0.002). Over short periods of days
to weeks, English et al. (2010) suggest that spine δ13C responds to
changes in VPD and not water uptake, however, the short duration of
their daily-resolution stable isotope spine record cannot rule out that
over monthly and annual time scales cactus water status influences the
δ13C of spines. Like spine δ18O in composite records, a strong statistical
relationship suitable for the development of transfer functions awaits
the development of longer and better dated composite records with
expressed population signals ≥0.85.
5. Conclusions
There is strong evidence for a relationship between the annual
parameters of δ18O and δ13C of spines and total annual precipitation
between November and October and nighttime VPD. We cannot infer
from this study that δ18O, δ13C, TAP, and VPD are causally linked,
however, the relationships presented here are consistent with
saguaro demographic studies (Drezner and Balling, 2002; Drezner,
2003a) and theoretical and mechanistic models of isotopic fractionation that link climate variation to isotope variation in cactus spines
(English et al., 2007, 2010). We conclude that annual parameters of
precipitation and nighttime VPD are recorded in the spines of saguaro
cactus and we hypothesize that spines from other species of columnar
cactus record climate as well. Our data show that: 1) both annual
parameters of precipitation and nighttime VPD are linked in a
meaningful way with annual parameters of δ18O and δ13C of a
composite spine record; 2) that strong El Niño-enhanced winter
rainfall is recorded in the year-to-year difference in maximum annual
δ18O of composite records of spine δ18O; and 3) using the corrected
relationship between TAP and mean annual δ18O, reconstructions of
TAP were accurate in some years but overestimated in El Niño years.
We are optimistic that more empirical experiments combined with
more refined mechanistic models of carbon and oxygen in saguaro
and other columnar cactus will enhance the utility of spine series as
climate proxies.
The timing of each spine series is clearly critical in developing
accurate composite records of isotopic variation, and great care should
be taken in future studies to establish and confirm if possible the spine
age/height model. Either actual measurements of plant height or local
instrumental or historic records of extreme climate conditions can be
used to anchor salient cycles in the isotopic record to known years or
to confirm the accuracy of the age/height model, respectively. Even
with a record that is off by one or two years, over decades a composite
isotope record from columnar cactus that records climatic information
in arid and semi-arid regions can yield useful information regarding
the variability of extreme events such as ENSO-enhanced rainfall or to
calibrate regional climate models. For example, the columnar cactus
Trichocereus atacamensis (pasacana) is commonly found between
1900 and 4000 m asl along 11° of latitude in treeless northern Chile/
Argentina to just south of Lake Titicaca in Bolivia. This region is
affected by two climate modes (Placzek et al., 2009), but possesses
only sporadic instrumental records and annual climate proxy
records ∼ 30 years old (Vuille and Keimig, 2004). Trichocereus
atacamensis may live to be over 300 years old (Yetman, 2008) and
have large, robust spines (N10 cm) with distinct diurnal-like banding
(2010, N. English, pers. observation) and may contain useful records
of climate variation beyond what is available in the instrument or
current climate proxy record. While we doubt isotopic spine-series
would ever rival tree-ring records, in carefully calibrated studies they
N.B. English et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 293 (2010) 108–119
may provide useful records of climate and ecophysiology in regions
devoid of other proxies.
Acknowledgements
The research presented in this paper was funded by the United States
Environmental Protection Agency (EPA) under the Science to Achieve
Results (STAR) Graduate Fellowship Program, a William G. McGinnies
Scholarship, and a Geological Society of America student grant to N.B.
English. This work was also supported by funding from the National
Science Foundation to the authors (Grant #IOS 0717395 and #IOS
0717403). We are thankful to K. Anchukaitis, J. Betancourt, W. Beck, G.
Bowen, J. Bower, J. Cole, T. Drezner, C. Eastoe, Q. Hua, S. Leavitt, J.
Mauseth, J. Pigati, B. Osmond, J. Overpeck, E. Pierson, D. Potts, J. Quade, T.
Shanahan, and R. Turner. All experiments comply with the current laws
of the United States and Arizona.
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