STABLE ISOTOPES IN THE SPINES OF COLUMNAR CACTUS: A NEW
PROXY FOR CLIMATE AND ECOPHYSIOLOGICAL RESEARCH
by
Nathanael T. Brooks-English
______________________
Copyright © Nathanael T Brooks-English 2008
A Dissertation submitted to the Faculty of the
DEPARTMENT OF GEOSCIENCES
In Partial Fulfillment of the Requirements
For the Degree of
DOCTOR OF PHILOSPHY
In the Graduate College
THE UNIVERSITY OF ARIZONA
2008
2
As members of the Dissertation Committee, we certify that we have read the dissertation
prepared by Nathanael T. Brooks-English entitled:
“Stable Isotopes in the Stems and Spines of Columnar Cactus: a New Proxy for Climate
and Ecophysiological Research.”
and recommend that it be accepted as fulfilling the dissertation requirement for the
Degree of Doctor of Philosophy
_______________________________________________________________________
Date: 9/23/08
Julia E. Cole
_______________________________________________________________________
Date: 9/23/08
David L. Dettman
_______________________________________________________________________
Date: 9/23/08
David G. Williams
_______________________________________________________________________
Date: 9/23/08
Steven Leavitt
_______________________________________________________________________
Date: 9/23/08
Jonathan T. Overpeck
Final approval and acceptance of this dissertation is contingent upon the candidate’s
submission of the final copies of the dissertation to the Graduate College.
I hereby certify that I have read this dissertation prepared under my direction and
recommend that it be accepted as fulfilling the dissertation requirement.
________________________________________________ Date: 9/23/08
Dissertation Director: Julia E. Cole
3
STATEMENT BY THE AUTHOR
This dissertation has been submitted in partial fulfillment of requirements for an
advanced degree at The University of Arizona and is deposited in the University Library
to be made available to borrowers under rules of the Library.
Brief quotations from this dissertation are allowable without special permission,
provided that accurate acknowledgement of source is made. Requests for permission for
extended quotation from or reproduction of this manuscript in whole or in part may be
granted granted by the copyright holder.
SIGNED: Nathanael T. Brooks-English
ACKNOWLEDGEMENTS
The research presented in this dissertation 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. The ideas, support and countless hours of useful
discussion and laboratory work of many individuals constitutes the basis of this work.
The individuals responsible for this effort and whom I thank are K. Anchukaitis, T. Ault,
J. Betancourt, W. Beck, G. Bowen, J. Bower, J. Caulkins, M. Daniels ,T. Drezner, C.
Eastoe, M. Fan, C. Funnicelli, Q. Hua, K. Hultine, M. Mason, J. Mauseth, J. Pigati, B.
Osmond, W. Peachy, E. Pierson, D. Potts, , J. Quade, A. Reynolds, D. Sandquist, T.
Shanahan, R. Turner and M. Weesner.
The first mention of using cactus as a climate proxy was by Forrest Shreve and that
was almost 100 years ago. Dr. David Dettman and Dr. David Williams first proposed
using the isotopes of carbon and oxygen in spines as a climate and ecophysiological
proxy and it was they who encouraged me to pursue the idea. Dr. Julia Cole and Dr.
Jonathan Overpeck made it clear to me that developing a new climate proxy was not a
matter of just “lining up the squiggles”. Drs. Kevin Anchukaitis, Steven Leavitt, Julia
Cole and Mike Evans all provided me with invaluable assistance and ideas in
compositing and comparing the isotope spine series. Dr. Julio Betancourt told me at the
beginning of this work that “there are no new ideas” and when I think of any facet of this
work and the input from colleagues, I believe he is correct. The only thing I can rightly
lay claim to within this dissertation are any mistakes.
Dr. Dettman has single-handedly brought me up to speed on a great number of
isotopic techniques, entrusted me with the free-run of his laboratory and blasted through
the bureaucratic roadblocks graduate students sometimes face. Dr. Williams has with
great effort, skill and patience shown me what is wonderful and unique about
ecophysiology and the world of green things. Both Dettman and Williams have
encouraged me to exceed my own expectations, and I am deeply grateful for their
patience and mentorship. Dr. Jay Quade and Dr. Julio Betancourt both advised me on
previous isotopic research, and the work here in large part springs from their past
generosity and rigorous teaching. This dissertation is indebted to my wife, Dr. Christa
Placzek, who participated in the cactus research in the field, in the lab, in the office and at
home. Her ideas, her editing, her scientific skills and her patience — lots and lots of
patience — are present on every page of this document.
Finally, this dissertation is dedicated to my late friend Charles Burkhardt. Chuck was
technically savy and as handy with a hack-saw as he was with a hard-drive. He was
always ready and willing to help for nothing more than an opportunity to do something
new — it was his trailer and rope that transported the potted cactus from the nursery to
Tumamoc Hill; he helped to select and set-up the camera equipment used for the repeat
photography experiment; he helped collect the spine series from Saguaro 168 and 182
that are used in the composite record. Chuck never complained, always smiled and was
just a damned fine friend. Christa, the boys and I were blessed to be his neighbor and
consider him family for 9 years. He is sorely missed.
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TABLE OF CONTENTS
Page
LIST OF TABLES………………………………………………………………... 8
LIST OF FIGURES………………………………………………………….….... 9
ABSTRACT…………………………………………………………………...…...11
PREFACE………….……………………………………………………….……...13
STABLE ISOTOPES IN THE SPINES OF COLUMNAR CACTUS: A NEW
PROXY FOR CLIMATE AND ECOPHYSIOLOGICAL RESEARCH…….. 19
1. Introduction……………………………………………………………………... 20
2. Spine Growth and F14C Age…………………………………………………….. 24
3. Basic isotope Theory……………………………………………………………. 26
4. Mechanistic models of Carbon isotopes in cactus………………………………. 29
4.1 δ13C and Crassulacean Acid Metabolism …………………………………... 29
4.2 δ13C in cactus, two hypotheses of variation……………………………….…31
4.3 Observations from naturally grown cactus and spine series……………..….34
5. Mechanistic models of δ18O and δ2H in cactus and spines……………….……...37
5.1 Cactus anatomy and water……………………………………………..….…37
5.2 Oxygen Isotope model for stem waters and spine tissue in cactus………….. 39
5.3 Observations from experiments, naturally grown cactus and spine series…. 44
6. An isotopic framework for future cactus studies………………………………...47
Acknowledgements……………………………………………………….………...50
References…………………………………………………………………………..50
Figure Captions……………………………………………………………………..60
Figures……………………………………………………………………………... 63
APPENDIX A: PAST CLIMATE CHANGES AND ECOPHYSIOLOGICAL
RESPONSES RECORDED IN THE ISOTOPE RATIOS OF SAGUARO CACTUS
SPINES……………………………………………………………………………. 69
Abstract………………………………………………………………………….….70
1. Introduction………………………………………………………………………72
2. Theory……………………………………………………………………………74
2.1 Oxygen and Hydrogen Isotope Variation in Cactus Water and Tissue…….. 74
2.2 Carbon Isotope Variation in Cactus Tissue..……………………………….. 77
3. Methods…………………………………………………………………………. 79
3.1 Experiment with potted saguaro…………………………………………….. 79
3.2 Spine sampling from a naturally occurring saguaro…………………...……80
3.3 Stable isotope analysis…………………………………………………….…82
4. Results and Discussion………………………………………………………..… 85
4.1 Recharge, evaporation and isotopic composition of potted saguaro……..… 85
4.2 F14C derived growth model in a naturally occurring saguaro……………… 87
6
TABLE OF CONTENTS – Continued
Page
4.3 Temporal δ C and δ O variations in a spine-series from a naturally occurring
saguaro……………………………………………………………………..……… 89
4.4 Environmental control of δ13C and δ18O variations in a spine-series from a
naturally occurring saguaro……………………………………………………..… 91
5. Conclusion………………………………………………………………………. 93
Acknowledgements………………………………………………………..………..94
References…………………………………………………………………………..95
Figure Captions………………………………………………………………..……102
Tables……………………………………………………………………………….104
Figures………………………………………………………………………...…… 106
13
18
APPENDIX B: DAILY TO DECADAL PATTERNS OF PRECIPITATION,
HUMIDITY AND PHOTOSYNTHETIC PHYSIOLOGY RECORDED IN THE
SPINES OF COLUMNAR CACTUS, CARNEGIEA GIGANTEA……………. 112
Abstract……………………………………………………………………..……... 113
1. Introduction………………………………………………………………………114
1.1 Spine series and columnar cacti…………………………………………….. 114
1.2 Saguaro spines, F14C, δ13C and δ18O……………………………………….. 117
2. Sampling and Analytical methods………………………………………………. 121
2.1 Transverse Bands within single spines……………………………………… 121
2.2 Sub-daily, daily and annually resolved stable isotope records……………... 123
2.2.1 Sub-Daily records………………………………………………………. 123
2.2.2 Daily Records……………………………………………………………124
2.2.3 Annual records…………………………………………………………..125
3. Results……………………………………………………………………………126
3.1 Transverse bands within single spines……………………………………….126
3.2 Sub-daily, daily and annually resolved stable isotope records……………... 127
3.2.1 Sub-Daily records…………………………………………………….… 127
3.2.2 Daily Records…………………………………………………………....127
3.2.3 Annual records………………………………………..…………………128
4. Discussion……………………………………………………………………..… 129
4.1 Transverse bands within single spines……………………………….………129
4.2 Sub-daily, daily and annually resolved stable isotope records…………...… 130
4.2.1 Sub-Daily records…………………………………………………….… 130
4.2.2 Daily Records……………………………………………………………130
4.2.3 Annual records………………………………………………….……….133
5. Conclusions………………………………………………………………………135
Acknowledgements…………………………………………………………………137
References…………………………………………………………………………..137
Figure Captions……………………………………………………………………. 143
Figures…………………………………………………………………………..…. 146
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TABLE OF CONTENTS – Continued
APPENDIX C: A 26-YEAR STABLE ISOTOPE RECORD OF PRECIPITATION,
HUMIDITY AND EL NIÑO IN THE SPINES OF SAGUARO CACTUS,
CARNEGIEA GIGANTEA………………………………………………………. 153
Abstract……………………………………………………………………………. 154
1. Introduction……………………………………………………………………... 154
2. Methods………………………………………………………………………… 157
2.1 Spine series and climate data collection……………………………………..157
2.2 Stable isotope and statistical analyses……………………………………….159
2.3 Spine age determination…………………………………………………….. 160
3. Results and Discussion………………………………………………………….. 162
3.1 Compositing and analysis of isotopic spine series………………………….. 162
3.2 Calculation and evaluation of the expressed population signal (EPS) …… 165
3.3 δ18O composite records……………………………………………………... 167
3.4 δ13C composite records………………………………………………………170
4. Conclusions………………………………………………………………………172
Acknowledgements…………………………………………………………………174
References…………………………………………………………………………..175
Figure Captions……………………………………………………………………. 181
Tables……………………………………………………………………………….185
Figures……………………………………………………………………………... 189
APPENDIX D: MOVIE OF SPINE GROWTH OVER TWO DAYS IN MAY,
2007……………………………………………………………………………….. 199
Supplemental CD
APPENDIX E: DATA……………………………………………………………. 201
Stable isotope data from naturally occurring cactus ………………………………. 202
Stable isotope data of spine material from Cactus TH42 (Diurnal spine series)….. 209
F14C values and estimated dates for Tumamoc Hill and Saguaro National Park East
cactuses…………………………………………………………………………….. 212
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LIST OF TABLES
Page
Table A.1 Height of sampled spine, measured heights of Pierson and Turner (1998),
F14C content, and F14C year from spines of Saguaro 162…………………………..104
Table A.2 Variables and spectral analysis results using the multiple taper method
(MTM) for δ13C and δ18O in the Saguaro 162 spine series…………………...…… 105
Table C.1 Saguaro cactus raw and spine series attributes ………………………..185
Table C.2 Mean intercactus correlation coefficients (r) and expressed population signal
of age modeled, corrected and adjusted spine series……………………………..... 186
Table C.3 Uncorrected annual δ18O and δ13C correlations with annual precipitation,
VPD and SOI………………………………………………………………………. 187
Table C.4 Corrected annual δ18O and δ13C correlations with annual precipitation, VPD
and SOI……………………………………………………………………….……. 188
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LIST OF FIGURES
Page
INTRODUCTION FIGURES
Figure Captions……………………………………………………………………..60
Figure 1
Saguaro and spines….………………………………………………… 63
Figure 2
Inter- and intraspine δ13C variation over days, weeks and years…...… 64
Figure 3
The composite δ13C and δ18O record…………………………………. 65
Figure 4
δ18O and δ2H of cactus stem waters and Tucson precipitation………. 66
Figure 5
Modeled and actual δ18O values of water from cactus stem tissue…... 67
Figure 6
Spine δ18O and total annual precipitation…………………………….. 67
Figure 7
Modeled total annual precipitation using spine δ18O…………………. 67
APPENDIX A FIGURES
Figure captions……………………………….……………………………………..102
Figure A.1 Mean δ18O values of water from cactus stem tissue…………………. 106
Figure A.2 Measured and modeled stem water δ18O from stem tissue ………….. 107
Figure A.3 δ18O and δ2H of cactus stem waters and Tucson precipitation ……… 108
Figure A.4 Spine F14C age and measured heights ……..………………………..... 109
Figure A.5 δ18O and δ13C Isotope spine series from Saguaro 162………………... 110
APPENDIX B FIGURES
Figure captions……………………………….……………………………………..143
Figure B.1 Transverse bands in a spine……………………………………………146
Figure B.2 Linear saguaro spine growth and PAR over two days………………... 147
Figure B.3 High resolution δ13C record from a spine grown in late August……....148
Figure B.4 Daily resolution δ13C and δ18O record from three saguaro spines grown
between August and October 2006………………………………………………… 149
Figure B.5 δ13C record in spine tips spanning ~4 m of a natural saguaro…………150
Figure B.6 Stem and areole growth rates of a naturally occurring saguaro………. 151
APPENDIX C FIGURES
Figure captions……………………………….……………………………………..181
Figure C.1 Spine height and corrected F14C age compared to observed apical cactus
height and age……………………………………………………………………… 189
Figure C.2 Raw spine height and δ13C isotope spine series………………………. 190
Figure C.3 Raw spine height and δ18O isotope spine series……………………… 191
Figure C.4 Age modeled δ13C isotope spine series……………………………….. 192
Figure C.5 Age modeled δ18O isotope spine series……………………………….. 193
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LIST OF FIGURES — Continued
Page
Figure C.6 Composite δ18O spine series with annual parameters…………….…... 194
Figure C.7 Composite δ13C spine record and annual parameters………………….195
Figure C.8 δ18O of spines and total annual precipitation…………………………. 196
Figure C.9 Modeled total annual precipitation using mean annual δ18O from the
composite spine record…………………………………………………………….. 197
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ABSTRACT
There are relatively few annually resolved climate proxies in arid and semi-arid
regions. Columnar cactuses are common in these regions and the stable isotopes of
carbon and oxygen in durable spines record variations in rainfall, humidity and
ecophysiology as they grow in series along the sides of cactuses. Despite their spines,
columnar cactuses provide important ecosystem resources and services in drought prone
areas, however, the impact that long-term climate variability and infrequent storms (El
Niño or tropical storms) have on the ecology and ecophysiology of columnar cactus is
less clear. Stable isotopes in trees and corals serve as useful proxies of climate and
ecophysiological information, but for cactus we lack the most rudimentary information
about the isotopic systems and their links to the environment. Here, we present an
isotopic framework that begins with developing semi-empirical mechanistic models of
δ13C, δ18O and δ2H variation in saguaro cactuses that link physical and physiological
fractionation factors in stem water and spines to rainfall and humidity. We also review a
novel method for determining the age of spines, an important step in developing useful
chronologies of isotopic variation in spines. The mechanistic models combined with local
climate records enhance our understanding of isotopic variation in daily and annually
dated spine δ13C and δ18O records and explain the statistical association of δ13C and δ18O
in spines with rainfall, vapor pressure deficit, and El Niño enhanced winter rains.
While there are still some challenges to overcome, we expect that isotopic spine
series will be used as climate proxies to answer questions regarding regional climate
variability or to enhance current models of past and future climates. Likewise,
12
ecophysiologists can use the isotopic spine series in conjunction with gas exchange or
carbohydrate studies to look at reproductive or biological responses to changing
environments.
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PREFACE
The work that follows is a complex, interdisciplinary study of saguaro cactuses
(Carnegiea gigantea (Engelmann) Britton & Rose) and their isotopic responses to the
environment. The complexity of the research arises from the fact that we had two goals
for this work: 1) to understand the ecophysiology and isotope systematics of a long-lived
columnar cactus; and 2) to understand how the isotopes in spines, preserved for decades
in series on the side of the cactus, can be used as high-resolution records of past climate.
These goals are not independent, and we struggle still to understand either the
ecophysiology or isotopic variation while lacking key insights into either the underlying
isotopic variation or ecophysiology, respectively. Understanding the isotopic response of
a plant to its environment and climate is a difficult undertaking. Biochemical systems are
rife with complex, stochastic and age-related variation. What follows is our preliminary
attempt to see through this noise and develop an isotopic framework anyone can use to
study cactus ecophysiology or past climate change. We expect and welcome many of the
changes this framework will undergo as more is learned about the ecophysiology and
isotope systematics of cactus. There are still several challenges to be overcome before the
spines of columnar cactuses can be widely employed as climate proxies or used to
measure ecophysiological responses to the environment. We are confident, however, that
this dissertation represents a significant increase in our understanding of saguaros and
similar species that are widespread and important organisms in arid and semi-arid
ecosystems of the world.
Most cactuses, including columnar cactus, have spines along the length of their
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stems. Spines are only produced at the apex (top) of the cactus and are arranged in the
order they were produced. The spines grow rapidly, for a relatively short time and are
retained on the plant for decades after they stop growing. The spines are mostly
composed of carbon, oxygen and hydrogen, and the isotopic ratios of these elements are
preserved within the spine tissue. The result is a top-to-bottom line of spines along the
side of a cactus where the oldest spines are at the base of the cactus and the youngest,
most recent spines produced are at the apex of the cactus. The isotopic measurements of
carbon and oxygen from the tips of a single, time-ordered line of these spines is hereafter
referred to as an isotope spine series or spine series.
Our first paper (Appendix 1) lays out the foundation of our isotopic framework: 1)
evaporation and water uptake drive variation in the δ18O of stem water and spines, 2)
variations in photosynthetic chemistry and timing, related to humidity, drive variations in
the δ13C system of cactuses. We base these hypotheses on observations from both potted
and naturally-grown saguaro cactuses. Isotopes of δ18O and δ2H in stem water increased
during periods of water loss (measured by periodically weighing the cactus) and
decreased during periods of water uptake. A simple theoretical model of isotopic
variation in cactus water generally describes this change, however, the model does not
accurately replicate isotopic variation during periods with both water loss and uptake. We
also propose a theoretical model of δ13C that is based on the relative balance of
fractionation factors affecting CO2 assimilated by the plant at night and during the day.
This model is consistent with our observations in spine tissue but there is very little
positive evidence of such a balance. We use dates from bomb-spike radiocarbon to show
15
that the isotopic variation in δ13C is annual. Using the dated isotope spine series we
suggest a link between El Niño enhanced winter precipitation and decreased δ18O and
δ13C values.
Our second paper (Appendix 2) documents the range of temporal scales at which
isotopic variation can be observed in spines. We show that, at least on younger cactuses
with robust spines, the easily visible couplets of light and dark tissue represent diurnal
cycles. Spines in this study grew for roughly 30- 60 days before elongation and growth
ceased. There appears to be very little isotopic variation within diurnal bands, but
significant variation over many diurnal cycles and the length of a spine. We compare the
diurnal δ18O and δ13C record from several spines with climate data. We examine the
possibility that δ13C variation is determined solely by stomatal opening at night. Our
measurements of diurnal spine δ13C conflict with a model of carbon isotope variation
determined by stomatal opening, even when we consider a lag time between CO2
assimilation and spine tissue synthesis. We also confirm that bomb-spike radiocarbon
measurements can be used to infer the age of a saguaro cactus.
In our third paper (Appendix 3), we present the logical synthesis of our work,
namely the development of local climate records based on isotopic variation in spine
series collected from five individual cactus at Tumamoc Hill. We use bomb-spike
radiocarbon and δ13C variations to date each spine series independently and then average
the isotope spine series together. We observe a strong relationship in this composite
record between total annual precipitation (November to the next October) and the mean
δ18O of spines grown in that year. The relationship between δ13C and climate is less clear.
16
Most notable is the apparent influence of El Niño winter rains on the isotopic value of
spines grown in the following year. We still see strong annual variability in the δ13C of
spines. We use techniques borrowed from dendrochronology to evaluate the coherence of
the five spine series we collected. This evaluation suggests that by adding more spine
series to this data set we would likely improve our record so that it is comparable to treering records in accurately representing the isotopic response of a cactus population to
climate variation.
While we have presented a novel paleoclimate proxy for use in arid- and semi-arid
regions of the world with columnar cactuses, major challenges exist if we are to use
columnar cactuses as indicators of past climate change around the world. First and
foremost are the problems with dating isotopic variations in spine series to the year.
While bomb-spike radiocarbon can help us to establish the chronology of spines grown
after ~1950, we would be entirely dependant on annual δ13C variation for dating spines
grown before this 1950. No one has yet shown that this can be done accurately.
Additionally, as bomb-spike radiocarbon continues to decrease asymptotically in the
atmosphere, more recent dates will have increasingly larger confidence intervals
associated with them. Secondly, we must improve our understanding of the timing and
cause of carbon isotope variations in different tissues in the cactus. Work is underway
that will combine δ13C data from gas, sugar, spine and stem tissues to help us understand
the reservoirs, fluxes and fractionation factors associated with ecophysiological processes
in columnar cactuses. On top of the dating and carbon isotope challenges, isotopic
responses of cactuses may vary by species, and in order to establish a relationship
17
between climate and isotopic variation in spines we must first establish the isotopic
response to changing climate of each cactus species. This is a non-trivial task requiring
years of ecophysiological and high-resolution climate data. This work is underway now
for saguaro, but not for any other species of columnar cactus that we are aware of. We
doubt that columnar cactuses and spine series will surpass the utility of tree-ring records
in climate research. However, we do hope that with time, effort and resources columnar
cactuses will be able to contribute in a meaningful way to the ever-growing body of
climate and plant research.
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STABLE ISOTOPES IN THE SPINES OF COLUMNAR CACTUS: A NEW
PROXY FOR CLIMATE AND ECOPHYSIOLOGICAL RESEARCH
20
1. Introduction
Isotopic ratios in biologic and geologic materials are often used to quantify climate
and ecological processes in the past (West et al. 2006). In subtropical arid and semi-arid
ecosystems these materials, such as tree-rings (McCarroll and Loader, 2004), mineral
deposits in caves (Fairchild et al 2006) and pack-rat middens (Betancourt et al. 2000)
record ecological or climate changes over thousands of years in length. In these records
each datum only represents either a snapshot in time, decades or millennia and are useful
for looking at regional changes in climate and ecology over thousand of years. In arid
and semi-arid regions, climate proxies are often found in isolated mountain ranges,
riparian zones or springs — areas that are ecologically distinct from the surrounding
desert or representative of remote climatic shifts (Quade et al 2008, Bradley et al. 2006).
Modern instrumental (e.g. NCDC, 2008), reanalysis (e.g. Di Luzio et al., 2008) or
satellite data (e.g. Jobbagy et al. 2002, Vuille and Keimig 2004) provide climate and
ecological proxies with annual or sub-annual resolution in developing nations, but only
cover a small period of the most recent past and are sparsely or unevenly distributed
(Mann et al. 2007). In contrast, isotope records from the spines from columnar cactuses
are an example of relatively long-term climate and ecological proxies, have high
temporal resolution and are distributed throughout the arid and semi-arid Americas
(Yetman 2008).
Further development and broad application of spine time-series from cactuses would
be useful for documenting physiological responses to environmental change or
reconstructing past climate — especially where cactus populations are threatened with
21
extinction (Godinez-Alvarez et al. 2003). For example, the massive, long-lived (125-175
yrs) saguaro cactus occurs throughout the Sonoran Desert in southwestern Arizona and
western Sonora, Mexico (Fig. 1)(Turner et al. 1995). Saguaro and other columnar cacti
(cardón, Pachycereus pringlei; organ pipe cactus, Stenocereus thurberi) are vital to the
functioning of Sonoran Desert ecosystems — they provide water, nutrients and energy to
consumers from flowers, fruits, seeds and stems (e.g. Markow et al. 2000, Wolf and
McKechnie 2003). For this reason, ecosystem functioning and trophic structure in many
parts of the Sonoran Desert are shaped disproportionately by saguaro and associated
columnar cacti, establishing their critical role as a ‘foundation species’ (sensu Soulé and
Noss 1998). For saguaro, growth rate is highly dependent on summer precipitation
(Drezner 2005) provided by the North American Monsoon (NAM) in July, August and
September and it is an integral part of the Sonoran Desert climate (Wright et al. 2001).
Drezner (2003a, 2003b) and Drezner and Balling (2002) also found 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. In addition, the warm phase of the El Niño
Southern Oscillation (ENSO) is associated with greatly enhanced winter precipitation in
the Sonoran Desert (Gutzler et al. 2002). Occasionally large tropical storms and
hurricanes originating in the Pacific move onto land in Sonora and southern Arizona,
producing significant precipitation late in the growing season (A. Long and C. Eastoe,
unpublished data). A consensus is emerging that with increasing concentrations of
atmospheric CO2 and warming, Sonoran Desert summers will be hotter and drier
22
(Christensen et al., 2007). It is unclear whether the frequency and amplitude of ENSO in
the future will change (Meehl et al., 2007), although at least one study suggests ENSO
teleconnections over North America weaken in a warming world (Meehl et al., 2006).
Understanding the impact of these extreme events on ecological dynamics and change is
an important focus in ecology (e.g. Gutschick and BassiriRad 2003). However, we have
little information on how such rare, extreme events affect columnar cactuses or desert
ecosystems in the southwestern United States. Distributed isotopic records from saguaro
across the Sonoran Desert that record both climate and ecophysiology, in conjunction
with records of flowering and growth rates, would be a step forward in answering these
questions.
Alternatively, spine series from cactus could be used to address climate questions
where land-based climate proxies are sparse, such as the arid and semi-arid regions of
South America (Mann 2007). In southern Peru, Northern Chile and the Bolivian
Altiplano precipitation records are limited, forcing reliance on proxy data. An example of
the utility of modern proxy data in this region is the recent application of ~20 years of
cloud-cover data from satellite imagery to identify two geographically distinct modes of
modern precipitation variability in the central Andes (Vuille and Keimig 2004). One of
these modes (the North-northeast mode, Quade et al. 2008) is linked to ENSO variability
and is antiphased with precipitation anomalies on the Peruvian coast, the other (the
Southeast mode) is linked to lowland precipitation in the Chaco region of Argentina.
Since the available satellite record is short and only covers a few ENSO cycles it is
unable to link variability in the second mode to global climate events. Longer records
23
from widely distributed spine series in this region could address the causes of variability
in the second mode. Additionally, spine series from transects between the Peruvian coast
and the northern Altiplano, where the effects of ENSO are felt strongest and anti-phased
(Placzek et al. 2008), have the potential to quantify the strength of ENSO events from the
last century over this region of South America.
Cactuses respond to changes in rainfall, relative humidity or photosynthetically
active radiation (PAR) within hours or days (Nobel 1988). These responses are dictated
by three evolutionary features the ancestors of cactus have evolved since the Cretaceous
(Osmond et al. 2008) and that allow them to thrive in deserts with extreme,
spatiotemporal climatic variability (Noy-Meir 1973, MacMahon, 2000): 1) the ability to
rapidly acquire and store water (succulence) (Nobel 1988); 2) the use of the crassulacean
acid metabolism (CAM) photosynthetic pathway to reduce water loss over the diurnal
photosynthetic period (Osmond et al. 2008, Winter 1980); and 3) the leaves of most
cactus are greatly reduced or modified to become durable, woody spines radiating
outward from the succulent stem (Mauseth, 2006) and photosynthesis takes place in the
stem. On columnar cacti, these spines favorably alter the radiation budget of the plant
(Nobel, 1988) and are located in chronological order (in series) on vertical, accordionlike ribs (Box 1) that extend the length of the plant. Even during drought, growing spines
incorporate variations in the isotopic ratio of biologically active compounds (i.e. water,
CO2, sucrose, starch, etc.). The isotopic ratios of these compounds are themselves
determined by physiological and environmental parameters, such as stomatal opening or
vapor pressure deficit (VPD).
24
How then can we relate the isotopic variation in cactus spines to current and past
environmental and ecophysiological parameters? Here, we review isotope spine series
and our hypotheses and models of what environmental parameters determine the
variation in spine δ18O and δ13C. These models and observations provide a rudimentary
framework for using columnar cactus to address ecological and climate questions at
spatial and temporal resolutions that are relevant to contemporary climate change
science. In the course of this review we show how our proposed models of isotope
variation can be improved upon and further developed to create useful records of climate
and ecophysiology from columnar cactus. The exemplary saguaro cactus (Carnegiea
gigantea Brit & Rose) has been the focus of research for nearly 100 years (Shreve 1911)
and as such it is the source for much of our discussions and data on isotopes in columnar
cactuses.
2. Spine Growth and F14C Age
In general, the spines of columnar cactus grow from areoles at the stem apex
(Mauseth, 2006). In saguaro, rapid growth of spines (up to 0.7 mm/day) leads to
submillimeter alternating bands of light and dark tissue in spines that denote daily
increments (Fig. 2)(English et al. Submitted). Spines are highly lignified organs having
no secondary growth, as the cells die within days after they are formed (Mauseth 2006).
While newly generated spine tissue dies within days, the spine itself continues to grow
from the base and most spines on a saguaro grow for only 30-60 days. During this time,
areoles and spines move to the side as new areoles and spines are produced above and in
25
conjunction with continuing stem growth (Mauseth 2006). The lignified spines are very
durable, strongly attached to the stem by cork cambium, and are thus retained on the
plant in series for decades. Spines along the vertical axis of a cactus stem represent a
time series from top to bottom (youngest to oldest)(Fig. 1). Nobel (1986), Buskirk and
Otis (1994), and English et al. (Submitted) find that areole generation, and thus spine
generation, is strongly correlated with growth rate. Between 4 and 10 areoles form on
each elongate set of fused tubercles (the ‘rib’ of the stem) on a mature saguaro during a
growing season. A moderately branched columnar cactus in Costa Rica,
Lemaireoceraeruasg onii (Weber) can grow up to 12 areoles in one growing season
(Buskirk and Otis, 1994). In saguaro and other species of cactus, the morphology of
spines changes when the plant reaches a certain height, while in other species the spine
morphology is invariant with height and age (Trichocereus atacamensis (pasacana),
Yetman, 2008). In some cacti, spines are not grown at all after the stem is beyond the
height of potential grazers (Yetman 2008). Under some circumstances, older, dormant
areole meristems reactivate to produce new spines, but these are easily distinguished
from spines produced at the plant apex (N. English, pers. observation).
We simultaneously confirmed that spine regrowth below the apex is rare and
developed a technique to determine the age of a spine to within a few years by using
measurements of radiocarbon (F14C) from spines. F14C composition of the atmosphere is
unique for all years after 1955 due to dilution and removal of anthropogenic 14C in the
atmosphere produced by 20th century atmospheric nuclear testing (Reimer et al., 2004).
Spine tissue incorporates the 14C content of the atmosphere at the time of its initial
26
growth. The tips of spines from multiple heights of saguaro from across Arizona were
analyzed and then calibrated using CaliBomb (NH_zone2.14c dataset; Reimer et al.
2004, Hua and Barbetti 2004). The age of spines is positively correlated to its height on
the stem, with the highest spines yielding the most recent dates and the lowest spines
yielding the oldest dates. Small, dating offsets that make spines appear too modern are
found in spines growing from the apex of cactus and are most likely a result of cactus
taking up 14-carbon depleted carbon dioxide in the atmosphere, associated with fossil
fuel burning, being incorporated into plant tissue (Francey et al. 1999). We’re confident
this is the case because the use of stored carbohydrates from previous years with higher
atmospheric F14C would lead to spines with apparently older dates. Spines of saguaro
from outside urban areas, in Saguaro National Park and in the Kofa National Wildlife
refuge (English et al. Submitted, English et al. In prep) yielded F14C dates consistent
with the year of their simultaneous growth and collection. Buskirk and Otis (1994)
established an alternative dating method for columnar cactus stems using the annually
generated waxy bands on a Costa Rican cactus, and although similar waxy bands are
found on saguaro and other columnar cacti, the increment of time they represent is
uncertain. Fortunately, the seasonal oscillations of δ13C described below independently
verify the F14C work (Fig. 2)(English et al., 2007, English et al. submitted, English et al.
in prep). The utility of this method for determining more recent dates decreases every
year as the F14C content of the atmosphere asymptotically approaches pre-1955 levels.
3. Basic Isotope Theory
27
The spines and stems of cactus contain large amounts of water (hydrogen and
oxygen) and carbon. Each of these elements naturally possess more than one stable
isotope, and in carbon’s case an additional radioactive isotope (14C). The isotopes of 16O,
1
H and 12C are the most abundant, while the isotopes of 17O, 18O, 2H, 13C and 14C contain
extra neutrons (i.e. two more neutrons in 18O than in 16O) and are orders of magnitude
less abundant in natural materials. While isotopes of an element undergo the same
physical, chemical and biological processes, their mass differences lead them to do so at
different rates and so they are incorporated into the products of these processes at
different absolute ratios than in the original reactant. In a reservoir of water, water
molecules with 16O and 1H molecules will evaporate more readily than water enriched in
18
O and 2H. Evaporation yields a vapor whose molecules are relatively lighter (more
negative δ values) and a water reservoir whose molecules are relatively heavier (more
positive δ values) than the initial reservoir.
The alteration of isotopic ratios during a product-reactant conversion is referred to as
kinetic fractionation and it depends on the incomplete or inefficient consumption of the
reactants (it is reassuring to know that there are no processes, short of planetary
catastrophe, that can consume all of the oxygen or water in Earth’s atmosphere all at
once). Kinetic fractionation does not occur in processes that completely consume the
reactant in closed systems (the total evaporation of a lake) or are 100% efficient (the
movement of a discrete mass in it’s entirety, such as water flow into roots). Many natural
processes, however, do fractionate oxygen, hydrogen and carbon, and this has yielded a
28
remarkable tool with which scientists can quantitatively measure transfers of mass and
energy in the environment (West et al. 2006).
The absolute stable isotope composition of natural materials is difficult to measure
directly, and so by convention the isotope ratio of the sample material (Rs) is compared
to that of a standard (Rstd) in the following manner:
(1)
δ = (Rs / Rstd – 1000) * 1000
where δ (delta) is the relative deviation from the standard. For δ18O and δ2H the standard
is the Vienna-Standard Mean Ocean Water (VSMOW). For δ13C the standard is a
carbonate (CaCO3) material referred to as the Vienna-Pee Dee Belemnite (VPDB). The
differences in absolute ratios are very small so the permil (‰) annotation is used rather
than percent (%). Often, it is useful to describe the net fractionation a particular process
imparts to a product (δproduct) when using a reactant (δreactant), and this is called
discrimination (Δprocess). Discrimination is often described in terms of per mil:
(2)
Δprocess = (δreactant – δproduct)/(1 + δproduct /1000)
When the difference between the product and reactant isotope ratios is relatively
small, the discrimination of a process can be simplified. For instance, the photosynthetic
discrimination of 13C (Δ13C) in plant tissue growth using atmospheric CO2 could be
described as:
29
(3)
Δ13C ≈ δ13Catmosphere – δ13Cplant
Note that the discrimination term can be made from an infinite number of smaller
processes, each with its own distinct value of discrimination, and can be summed to
calculate the net discrimination.
4. Mechanistic models of carbon isotopes in cactus
4.1 δ13C and Crassulacean Acid Metabolism
Sutton et al. (1976) were the first to suggest that δ13C variation in cactus tissue might
record these variables. The variation in the isotope ratio of organic compounds in plants
is determined by the δ13C of atmospheric CO2 and isotopic fractionations that occur
during assimilation, compound synthesis and post-photosynthetic processes. Plant
discrimination of 13C is affected by photosynthetic pathway, plant moisture stress, light
availability and temperature (O’Leary 1988). Cactuses use the CAM photosynthetic
pathway to acquire atmospheric carbon for growth (Osmond et al., 2008) and this has
consequences for the δ13C of their tissue and spines. For carbon, the δ13C value of
atmospheric CO2 is currently –8‰, but has slowly declined from about –6.7‰ since the
beginning of the industrial revolution (~150 years) due to fossil fuel combustion
(Keeling et al. 1979). The δ13C value in turbulently mixed air is relatively constant over
short time periods (days, years or decades). Thus, CO2 assimilation, compound synthesis
30
and post-photosynthetic processes influence the fractionation of 12C and 13C in mature
photosynthetic organs of obligate CAM species.
The photosynthetic mechanics of CAM plants are commonly described in the context
of four distinct diurnal time periods (phases) based on changes in the concentration of
malic acid, for which the CAM pathway is partially named and is the primary CO2
storage compound of CAM plants (Osmond, 1978). Each CAM phase imparts a unique
isotopic effect on the δ13C value of organic compounds assimilated or synthesized during
that time, although it should be noted that CAM in nature is much more complicated than
the idealized description given here (Osmond 2008, Dodd et al. 2002). The CAM
photosynthetic pathway involves initial carboxylation of atmospheric CO2 by PEPcarboxylase and storage of photosynthate as malate during the nighttime when stomates
are open (Phase I). Decarboxylation of malate during the daytime when stomates are
closed releases CO2 that is carboxylated by Rubisco in the Calvin cycle (Phase III).
Transitional CAM phases (II and IV, respectively) occur in the morning when malate
begins to release stored CO2 and stomates close and in the afternoon when stomates may
open to admit CO2 after malate reserves are exhausted. Variation in 13C discrimination
during CAM photosynthesis is determined by changes in the balance of stomatal
conductance (CO2 ‘supply’) and PEP-carboxylase activity (CO2 ‘demand’) during CAM
phase I, the degree of CO2 leakage out of tissues during CAM phase III, and direct
carboxylation of atmospheric CO2 by Rubisco and PEP-carboxylase during the daytime
in CAM phases II and IV (O’Leary 1988, Griffiths 1992).
31
4.2 δ13C in cactus, two hypotheses of variation
Aside from changes in atmospheric δ13C and post-photosynthetic fractionations
(Boutton 1996, Badeck et al. 2005) there are two possible mechanisms that determine
Δ13C in CAM plant tissues. The first is that stomatal opening or closing in response to
decreased or increased VPD alters Δ13C in cactuses. If stomates are closed during the
morning and daylight hours (Phase II, III and IV), then only CO2 derived from decarboxylation of malate formed during the nighttime in Phase I is available for
photosynthate production and carbon allocation to spine tissue during growth and
consumption of all the released gas during Phase III. Assuming that Rubisco consumes
all of the stored CO2 during the subsequent Phase III with minimal leakage, δ13C of new
tissue will be closest to the endmember value of PEPC fixation in the dark (Phase I).
Carbon isotope discrimination (Δ13C) during Phase I would be equivalent to that in a C4
plant with no CO2 leakage, represented by the model (after Farquhar et al., 1989):
(4)
Δ13CCAM Phase I = a + (b4 – a) * pi/pa
where a is discrimination due to diffusion of CO2 through stomatal pores (4.4‰), b4 is
the net discrimination associated with carboxylation by PEPC (~ –5.7‰ at 25° C and is
temperature dependent), and pi/pa is the ratio of internal tissue to ambient partial pressure
of CO2. The balance of CO2 demand by PEPC reactions and atmospheric CO2 supply
through stomates is reflected in the pi/pa value. In Eq. 4, pi/pa and b4 are the only
parameters that vary significantly. Osmond et al. (1979a) showed that nighttime stomatal
32
opening in the cactus Opuntia stricta (Haworth) responded strongly and within hours to
vapor pressure deficit (VPD). If daytime CO2 exchange was negligible, then nighttime
changes in pi/pa would account for variation in δ13C of the photosynthate pool (Roberts et
al., 1997). Drought and high nighttime VPD reduce stomatal conductance, pi/pa and Δ13C
(increase in δ13C) in CAM plants (Osmond et al. 1979b; Roberts et al. 1997) and saguaro
(Lajtha et al. 1997). After assimilation of CO2 into plant carbohydrates, we expect the
carbon incorporated into lignin-rich spines to be additionally depleted in 13C by 1-3‰
with respect to atmospheric CO2 during post-photosynthetic fractionation processes
(Boutton 1996, Badeck et al. 2005).
The second possible determinant of Δ13C in cactus tissue is the time-of-day during
which the cactus fixes atmospheric CO2 (Osmond et al. 1979b; Dodd et al. 2002; Winter
and Holtum 2002; Griffiths et al. 2007). In saguaro, MacDougal and Working (1933)
observed that stomates remained open well into mid-morning in March, while Lajtha et
al. (1997) demonstrated that stomates are closed all day in the dry premonsoon months.
English et al. (2007, submitted, in prep) hypothesized that if stomates in saguaro are
open in the hours after sunrise (Phase II) or preceding sunset (Phase IV), then CO2 is also
fixed by Rubisco. Rubisco and PEPC carboxylation pathways have distinctive carbon
isotope fractionations, but Rubisco is only expressed isotopically if it operates in an
environment where respired CO2 can leave the plant (i.e. the stomates are open). If
stomates are open after dawn or before sunset then carbohydrates will be derived from
the incomplete fixation by Rubisco of atmospheric CO2 and PEPC released CO2 (leading
to tissues with δ13C > –27‰, the Rubisco endmember value; Winter and Holtum 2002).
33
These carbohydrates can be expected to mix later in the day and overnight with
carbohydrates derived from the nearly complete fixation by Rubisco of only CO2
released from malate fixed by PEPC during Phase I and possibly Phase II (leading to
tissue δ13C ≈ –10.9‰; Winter and Holtum, 2002; Griffiths et al., 2007). The net
fractionation of both nighttime and daytime fixation of CO2 can be expressed as:
(5) Δ13C CAM Phase II = {[a + (b4 – a)pi/pa] * f } + {[a + (es + b3 - a)pi/pa] * (1 – f)}
where es is the temperature-dependent discrimination of CO2 diffusing into water and b3
is the net discrimination associated with carboxylation by Rubisco (~ 27‰). In CAM
plants at dawn, it’s possible that CO2 released by PEPC may be mixed in proportion (f)
with atmospheric CO2, thus altering the net discrimination. Discrimination during direct
C3 photosynthesis during CAM Phase IV is simplified by the assumption that all CO2
stored in malate has been released and consumed, therefore the following equation
describes discrimination during CAM Phase IV:
(6)
Δ13CCAM Phase IV = a + ( es + b3 – a ) * pi/pa
As can be seen, CAM Phase I/III and Phase II/IV photosynthetic pathways are
associated with very different Δ13C. Only a small amount (~10%) of Rubisco fixed CO2
is required to shift δ13C in spine tissue by –1.8‰ (Winter and Holtum 2002), as can be
seen in the following equation:
34
(7)
Δ13CCAM = Δ13C CAM Phase I * f + Δ13C CAM Phase II/IV * (1 – f)
Osmond et al. (1979b) observed a rapid increase in expression of atmospheric CO2
fixation by Rubisco during Phase IV of CAM in Opuntia stricta (Haworth) following
rainfall inputs, accounting for up to 25% of the carbon fixed over the diurnal cycle. This
same study also found that irrigation not only induced Phase IV CO2 fixation, but a burst
of Phase II CO2 fixation as well. Interestingly, Osmond et al. (1979b) did not find these
changes altered the δ13C of whole stem tissues, probably as a result of the small
contribution to growth carbon assimilated during the day made to overall growth of the
stem during the year.
4.3 Observations from naturally grown cactus and spine series
This is probably the same reason that Sutton et al. (1976) did not find seasonal
variations in the stem tissue of cactus. However, spines show large daily, seasonal and
annual variations in δ13C (Fig. 2)(English et al. submitted), probably as a result of being
relatively near the foci of photosynthesis in chlorenchyma cells of the outer cortex. We
also hypothesize that the rapidly growing spines are permanently isolated within days
from the cactus’ carbohydrate reservoir. These hypotheses remain to be tested in future
experiments, although, the F14C data from spines presented in English et al. (2007,
submitted, in prep) consistently shows very little incorporation of carbon from older
35
carbohydrates in cactus spines. Indeed, variations as large as 3‰ are seen in over just a
week in newly grown spine tissue (Fig. 2)(English et al. submitted).
We investigated the possibility that changes in pi/pa associated with changes in
nighttime VPD determine Δ13C and might account for all the variation, without any
daytime CO2 uptake by Rubisco, using the model described in Equation 1. Over seventy
days in August and September, δ13C variations in spines are correlated with changes in
VPD, but spine δ13C was 6‰ lower and variations were the opposite of those predicted
solely by modeled VPD effects on nighttime stomatal conductance. The temperature
dependence of b4 accounts for ~0.2 to ~0.4‰ of the offset while post-photosynthetic
fractionation processes account for more (Boutton 1996, Badeck et al., 2005).
Continuous contributions of daytime CO2 fixation during this time may contribute the
remainder to the offset. Even a delayed response to VPD cannot explain the discrepancy
between modeled and actual spine δ13C after the first week in September. Evidence from
longer spine series in English et al. (2007, in prep) also show that spine δ13C and δ18O
are positively correlated (Fig. 3)(P < 0.001), inconsistent with spine δ13C variability
driven by changes in pi/pa.
So what explains the relationship between δ13C variation in spines and nighttime
VPD? We find that small rainstorms and higher VPD do not impact spine δ18O, but there
is a rapid return to more CAM-like δ13C values. This suggests that during the monsoon
daytime acquisition of CO2 (expression of Phase II or IV) is affected more by VPD than
plant water status (English et al. submitted). We hypothesize that stomates remain open
longer in the morning following lower nighttime and morning VPD and thus fix a greater
36
proportion of atmospheric CO2 with Rubisco than when VPD is high leading to lower
spine δ13C values. This hypothesis is consistent with the work of many other studies
(MacDougal and Working, 1933; Conde and Kramer, 1975; Osmond et al, 1979a;
Osmond et al. 1979b, Nobel, 1988; Lajtha et al. 1997). The evidence that VPD
determines CAM phase expression in saguaro, and thus δ13C values, is promising but
circumstantial and it remains to be confirmed by detailed gas exchange experiments.
Does pi/pa play a role in the δ13C variation in spines? We think so, but it appears the δ13C
variation in spines is either: 1) overwhelmed by δ13C variations due to CAM Phase
expression; 2) a lag time exists between CO2 fixation and carbohydrate synthesis; or 3)
stomates are either open or closed, with little variation of pi/pa in response to nighttime
VPD over the course of weeks. None of these possibilities can be ruled out, and it may
be that what is true during the monsoon is not true during other seasons.
The narrow tip of an emerging spine (the top 2 to 3 mm) represents just two or three
days of recorded isotopic variation in the cactus (English et al. submitted). Interpreting
this variation in a finitely sampled spine time-series that may record have grown over
many decades is analogous to interpreting temperature variability where only two or
three days every two months is represented in a 30 year long instrumental record. This
undersampling could lead to signal aliasing. However, when we use the F14C dates of
spines to age model δ13C spine series, we see that the dry/wet/dry monsoon cycle is fairly
represented by the δ13C record (Fig. 2 and 3) over the correct number of years. The
strong seasonal cycle in this δ13C time-series reflects high water–availability in March
and April (–13‰), a pre-monsoon drought in May and June (–10‰), and then the arrival
37
of the monsoon in July and August (–13‰) followed by a period of moderate rainfall,
low temperatures, and lower VPD until dormancy over the winter. Actively growing
spines from the apex of many cactus sampled at different times of the year confirm these
results. In composite records of δ13C variation, minimum annual δ13C is associated with
both mean annual nighttime VPD, but also with the Southern Oscillation Index, a
measure of El Niño strength (Fig. 3)(English et al. in prep). The link between nighttime
VPD is confounded with total annual precipitation (TAP) from November to October.
We hypothesize that enhanced winter rains or decreased VPD following El Niño years
increase the time and amount of CO2 fixed during the day and in the spring this is
reflected in very negative spine δ13C values. More experimental studies are needed to
attribute the impact VPD and water status each have on δ13C in spines.
5. Mechanistic models of δ18O and δ2H in cactus and spines
5.1 Cactus anatomy and water
The δ18O variations in spines form the basis of the cactus water isotope recorder. At
first glance (Fig. 4), stem waters appear to be similar to evaporating lakes (Craig and
Gordon, 1965). However, upon closer inspection there are large spatial and temporal
variations in stable isotope ratios of oxygen (δ18O) and hydrogen (δ2H) in stem waters
(English et al. 2007) that are not found in lakes. Succulent cactus can be up to 95% by
mass water and have large water storage capacities for their volume (mature saguaros can
store 1,700 L of water; McAuliffe and Janzen 1986). Water travels from the soil and
roots into the base of the cactus shoot and upwards to the apex through xylem in the
38
center of the cactus (for an excellent review of cactus anatomy see Mauseth 2006). All
along the axis of the cactus, cortical bundles transport water rapidly in bulk from the
xylem across the broad inner cortex to the base of chlorenchyma in the outermost cortex.
From the chlorenchyma phloem sap flows back to the central xylem. During drought,
vascular bundles also transport water from collapsible inner cortex cells (the cells are
easily rehydrated), to stiff chlorenchyma cells near the epidermis, thus assuring that the
photosynthetically active cells are always hydrated when water is available in the inner
cortex.
The water storage potential and anatomical structure of cactus combined with rapid,
periodic water uptake from the roots and continuous evapotranspiration along the stem
may account for the strong vertical and radial gradients in δ18O and δ2H of stem water
(Fig. 4). Alternatively, low stomatal density and activity at the plant base compared to
higher stomatal densities and activities at the apex of the plant could also cause the
gradients we see in stem waters. Regardless of the gradient’s cause, stem waters are
enriched in 18O and 2H with respect to rainwater at all times of the year (English et al.
2007, N. English unpublished data). Given this large reservoir of water, we believe that
any one storm has a small impact on the overall isotopic value of stem waters. However,
a significantly wet event or events after a long drought or a long-term shift in the isotopic
value of rainfall could significantly shift whole stem water values. Seasonal dynamics of
evapotranspiration during the arid premonsoon period followed by uptake of water
during the NAM and winter cause stem water δ18O and δ2H values of stem water to
increase and decrease, respectively (English et al. 2007). Spines continuously produced
39
during the growing season record variations in the δ18O and δ2H of stem water and
photosynthate, potentially allowing us to quantify a cactus’ past water status using spines
alone.
Over the course of a growing season and lifetime, cactuses undergo significant
changes both in the volume of stem water and the internal distribution of stable isotopes
in stem water (i.e., δ18O and δ2H)(English et al. 2007, Mauseth 2006). A model of δ18O
and δ2H in cactus should account for the isotopic gradient of stem waters, uptake of
water by the cactus after rainfall or irrigation, and evaporative enrichment of the stem
water during evapotranspiration. For spines and other biologically active compounds in
cactus the δ18O and δ2H values also reflect: 1) fractionations during biosynthesis; 2) the
δ18O and δ2H values of water where primary photosynthates are formed (chlorenchyma
in cactus stems) and where compounds are synthesized (the stem apex for saguaro
spines)(Roden et al. 2000).
5.2 Oxygen Isotope model for stem waters and spine tissue in cactus
We developed the following empirical model of water and spine isotope variation
using observations and data from four 1-m tall potted cactuses (English et al. 2007). It is
based on the model presented by English et al. (2007), but differs by including the stem
water gradient as an important variable in determining Δ18O. The previous model relied
upon prior knowledge of the isotope value of apical stem waters at the beginning of the
year or period of interest. The model presented here uses empirical relationships of VPD
and the measured isotopic gradient in experimental cactuses (English et al. 2007) to
40
estimate the beginning isotopic value of water at the apex, the isotopic gradient, and the
mean value of stem water. It then estimates the isotopic change caused by
evapotranspiration (Rayleigh fractionation model), water uptake (two-component mixing
model) and VPD determined changes in the gradient throughout the year. Although it is
clear that there are some months when there is very little water gain for saguaro (May
and June), in most other months (notably August) both evaporation or water uptake occur
simultaneously. We do not attempt to model this complexity — instead we apply the
Rayleigh model in months when the cactus is most likely to lose water (premonsoon,
postmonsoon) and the two-component mixing model in the months when it is most likely
to gain water (NAM).
At the cellular level, isotopic enrichment of stem water in chlorenchyma cells near
the surface of the cactus (Δ18Ochlorenchyma) is determined by:
(8)
Δ18Ochlorenchyma = ε+ + εk + (Δ18Ov – εk) * ea/ei
where ε+is the proportional depression of water vapor pressure by heavier species of
water (1H218O, 2H218O or 2H216O), εk is the fractionation of water as it diffuses through
the stomates of the chlorenchyma cells on the surface of the stem, and Δ18Ov is the
relative isotopic composition of water vapor in the atmosphere, and ea and ei are the
atmospheric and intercellular water vapor mole fraction (Barbour 2007). ε+varies slightly
with temperature (Bottinga and Craig 1969), while the total kinetic fractionation factor
through the boundary layer, εk, is 21‰ (Cernusak et al. 2003). In well-mixed conditions,
41
Δ18Ovapor approaches –ε+ so that Δ18Ochlorenchyma is proportional to 1 – ea/ei. This leads to
more positive δ18O values in stem waters when VPD is higher. However, the flux of
water with more negative δ18O values from the base and pith toward the apex and
chlorenchyma cells is opposed by the backward diffusion of evaporated water and
phloem sap from those same chlorenchyma cells at the apex and near the cactus’ surface.
This ‘Peclet effect’ creates both longitudinal and radial gradients in leaf water δ18O and
acts in a way that Eq. 8 overestimates the net effect of enrichment due to
evapotranspiration. Here, we consider the cactus stem as one large, very thick leaf, and
only the vertical gradient is considered (a simple but effective substitute for the complex
models presented in Barbour 2007).
The isotopic gradients in stem waters and the isotopic variation of stem water due to
evaporation and water uptake are the strongest controls on the δ18O and δ2H of water at
the apex of a cactus where spines grow (Fig. 4). English et al. (2007) determined that the
enrichment gradient is easily described for four potted ~1-m-tall saguaro by the linear
equation:
(9)
Δδsw = (4.42 * VPD + 16.61) * h + Δδp
where Δδsw is the isotopic enrichment of stem water δ18O or δ2H above source water at
stem height h (h = height of the sample/height of the apex), VPD (in kPa) is calculated
using the daily minimum temperature and the daily maximum relative humidity (we
assume these represent nighttime values). The fixed values are derived from mean
42
growing season slope and intercept for saguaro at one site in southern Arizona. The
gradient shown in Eq. 6 shares a weakness with the Peclet Effect in that it must be
known or fitted to the cactuses under consideration and cannot be determined through
simple anatomical measurements. The term Δδp accounts for the evaporation of soil
water before it is taken up by cactus roots (Allison et al. 1983). In practice, Δδp can be
considered the y-intercept of the isotopic gradient in the stem of the cactus, as at the base
of the plant (0 cm) very little evaporation will have occurred.
The isotopic enrichment of stem water 18O or 2H due to evaporation (Δδe) can be
described by Rayleigh fractionation for a cactus with measured changes in water storage
over time (fe or fr, whether determined by changes in mass or volume), and is expressed
as:
(10)
Δδe = [(1000 + δ0.5h) fe(α-1) – 1000] – δ0.5h
where Δδe is the change in δ18O or δ2H values of stem water after evaporation, δ0.5 is the
δ18O or δ2H value of water at 50% the height of the cactus in the previous time period, fe
is the fraction of water lost from the stem, and α is the fractionation during evaporation
determined by local nighttime temperature and relative humidity (Clark and Fritz 1997).
When water recharge occurs, after rainfall or irrigation, the change in average stem water
isotope value (Δδr) is determined by a two-component mixing model:
(11)
Δδr = [δ0.5h (fr) + δg (1 – fr)] – δ0.5h
43
where fr is the fraction of stem water taken up (again, determined empirically) and δg is
the δ18O or δ2H value of water taken up (soil water) during that time. To determine the
overall isotopic enrichment of water from the source water at any height over time (δsw*)
we use:
(12)
Δδsw* = Δδsw + Δδe or Δδr
Spines are likely to record these seasonal variations in stem water isotope variation.
However, we propose that the oxygen or hydrogen isotope ratio of spine tissue (δ18Ospine
or δ2Hspine) can be expressed as:
(10)
δspine = [ f (δsw* + 1000) α + (1 – f) (δh + 1000) α ] – 1000
where δsw-apex is the oxygen or hydrogen isotope value of water at the site of spine
tissue synthesis (i.e. the stem apex), δh is the isotope value of water at the source of
photosynthetic carbon dioxide assimilation in chlorenchyma (this can be estimated using
Eq. 9), α is the fractionation factor for oxygen (αO) or hydrogen (αH) associated with
photosynthetic sugar formation, and f is the fraction of carbon-bound oxygen or
hydrogen in photosynthetic sugars that undergoes exchange with medium water during
transport to the site of spine formation. We do know that compounds used in spine tissue
are synthesized at the base of a spine in an area known as the basal meristematic zone
44
(Mauseth, 2006). Although f may be variable, for now we use values reported in the
literature for trees (Roden et al. 1999). For δ2H in spines, we initially assume αH =
1.1580 (Roden et al. 1999). Initial data from English et al. (2007) yields an αO = 1.0227
± 0.0019. This value is less than the 1.0270 generally agreed upon for other plants and
suggests that sugars used in spine growth may be imported from lower on the stem. In
contrast to leafy trees, in cactuses the durable heterotrophic tissues (i.e. spines) are
located on top of and in contact with the autotrophic tissue (i.e. stem chlorenchyma
cells). Because of this anatomical arrangement, and the relatively small amount of
material spine growth requires, we hypothesize that sugars created in the apex of a cactus
are synthesized relatively quickly in situ with very little post-photosynthetic modification
by exchange with oxygen and hydrogen in phloem sap from lower on the stem. This
leads to a situation where 1 – f = 0 and the first term within the brackets in Eq. 10 is all
that is needed to estimate spine δ18O or δ2H value at anytime of year given relatively
accurate VPD, a height–VPD relationship and soil water δ18O or δ2H values. This is in
marked contrast to studies of the isotope value of tree-rings (Barbour 2007, McCarroll
and Loader 2004), where a great deal of effort is given to determining fractionation
factors due to the exchange of oxygen and hydrogen with water and other carbohydrates
as they are transported from the leaf to the trunk of the tree.
5.3 Observations from experiments, naturally grown cactus and spine series
These semi-empirical mechanistic models nicely match the observed temporal and
spatial dynamics of mean stem water δ18O in the actual experimental cactus (Fig. 5). The
45
same amplitude of variation (~15‰) found in the experimental cactus is found in the
stem waters of taller, naturally occurring saguaro (≤ 4 m-tall)(English et al. 2007,
submitted). In the potted plants, greater Δ18Ο is associated with drought and increased
VPD (Eq. 10) and lesser Δ18Ο is associated with water uptake and decreased VPD (Eq.
11)(English et al. 2007). Except in July and August, modeled changes in stem water δ18O
accurately reflected real changes in stem water δ18O. The discrepancy in July and August
between actual and modeled isotope values in stem water is probably the result of
stomatal closure in July when ~35% of the original water was lost, followed rapidly in
August by the simultaneous evapotranspiration (Eq. 10) and uptake of water (Eq. 11),
respectively. Measured vertical gradients in the experimental saguaro stem water δ18O
are linear, while those in taller cactus exhibit gradients better described by trinomial
relationships (Bronson and Aguilera, unpublished data). However, even a linear
relationship describes ~85% of the variation in stem water δ18O of tall cactuses. The
slope of the height-δ18O relationship, the y-intercept and apical δ18O value are very
similar for short and tall (young and old) saguaro cactus, suggesting that the flux of water
up the stem is evenly balanced with evaporation over the lifetime of the cactus. This
greatly simplifies isotopic modeling of water and spine isotopes in cactus of all ages.
Variation in cactus and spine δ18O and δ13C occurs over a range of temporal scales,
from hours to decades (Fig. 2 and 3). For spines, the temporal scale of isotope variation
is dependent on the speed of the process and the size of the reservoir involved. For
instance, atmospheric F14C ratios change over months and years, but δ13C in spines can
vary significantly over a day (Fig.2)(English et al., submitted). Likewise, spine δ18O
46
records changes in cactus water balance over days, while variations in δ13C of spines is
determined by hourly variations in VPD (English et al., submitted). The mass of water in
a cactus is orders of magnitude greater than the mass of gaseous and carbohydrate
reservoirs in cactus combined, and so it is not surprising that the diurnal δ18O record is
less variable over days compared to the variability in the δ13C record (English et al.
submitted). This makes sense given the large volume of water buffering the δ18O values
of stem water and primary photosynthates used to make spine tissue. Although δ18O and
δ13C do not co-vary on the scale of days, over weeks and seasons the two isotopes covary
positively (English et al. 2007, in prep.). Even within the two reservoirs, carbohydrates in
the cortex and pith appear to be decoupled even though they are structurally connected
(Sutton et al. 1981).
The high-resolution recording of isotopic variation in cactus stem water by spines
allows the construction of high-resolution composite records in a manner similar to that
applied to wood in tropical trees, which also lacks annual rings (Poussert et al. 2004;
Evans and Schragg 2004). When we construct composite records of spine δ18O variation
over decades, we find that mean annual δ18O in spines is negatively correlated with TAP
(P < 0.001)(Fig. 6) and positively correlated with mean annual nighttime VPD (Fig. 3)(P
< 0.01)(English et al., in prep.). Especially noticeable are large (>2‰) changes in the
maximum δ18O reached in the years after El Niño enhanced rains in 1983 and 1998 (Fig.
3). In addition to the changes modeled above, large inputs of rainfall with more negative
δ18O suppress δ18O in stem waters throughout the year, leading to lower spine δ18O.
Using the simple relationship between spine δ18O and TAP, we are able to reconstruct
47
TAP over the period of record with some accuracy including the years of El Niño
enhanced precipitation (Fig. 7).
6. An isotopic framework for future cactus studies
Carbon and oxygen isotopic systems in cactus are complex. Although the work
undertaken thus far suggests that vapor pressure deficit and water status are the primary
determinants of isotopic variation in spines, these variables are confounded and careful
experimental work must be done to improve the empirical models of isotopic variation in
cactus water and spines. For carbon, we need a better understanding of carbon reservoirs
and fluxes in carbohydrates with respect to the generation of spine tissue in the basal
meristematic zone. Previous studies (Osmond 1979a, Sutton et al. 1976) found that
cactus stem tissue did not yield seasonal variations in δ13C. Clearly, the spine series
records we’ve studied thus far do, and understanding the disconnect between cactus
tissue and spine tissue δ13C is critical to interpreting the physiological information spines
record. In conjunction with those studies, experimental evidence is needed that δ13C in
spine tissues is determined by either or some combination of: 1) the balance of carbon
assimilated via CAM/C3 photosynthetic pathways; 2) stomatal conductance at nighttime;
or 3) another undetermined mechanism. A better understanding of the carbon travel path
from the atmosphere to the spine will also help us to better understand the photosynthetic
and post-photosynthetic fractionations involved when spine tissue grows. Once these
mechanisms have been identified, it should be easier to discover which climate variable
or variables (VPD, PAR, cactus water storage, etc.) determine the δ13C of a spine. For
48
oxygen, we need a better understanding of what determines the stem water isotope
gradient throughout the year, especially in July and August, and what impact large
precipitation events can have on the overall isotopic value of cactus stem water.
Presently, our mechanistic model of water isotope variation requires a great deal of
apriori knowledge about the cactus and climate state (i.e. temperature, relative humidity,
water volume, etc.). Isotope spiking and gas exchange experiments can begin to address
many of these issues.While this is a good start, what is needed is a mechanistic model
that can be inverted so that variations in oxygen isotopes of spines can be used to
quantify past changes in precipitation, temperature or relative humidity (McCarroll and
Loader 2004, Barbour 2007).
For saguaro in particular, research is going forward that combines micrometeorological data, seasonal gas exchange data, isotope spine series and records of
flowering and growth from three climatically diverse sites in Arizona. We hope to reveal
annual and seasonal patterns and records of saguaro ecophysiology, population
demography, stem branching and flower production in a broad geographic and temporal
context so that the influence of local-scale processes and disturbances (competition, lowintensity fires, influence of exotic species, grazing by domestic livestock, etc.) can be
distinguished from larger-scale climatic anomalies affecting saguaro growth and
reproduction. Short-term observations of plant gas exchange, growth, water storage and
flowering are of insufficient duration or scope to capture important climatic events.
Development of a method to probe the dynamics of resource capture and response to
49
environmental change over the lifetime of individual saguaro plants will reveal how
climate anomalies are likely to affect ecosystem functioning in the Sonoran Desert.
In South America, the ubiquitous columnar cactus Trichocereus atacamensis
(pasacana) occupies 11° of latitude on the Altiplano between Lake Titicaca and northern
Chile and Argentina. F14C dating and isotope analysis of spines from this region suggest
that spine series in these cactuses record isotope variation from at least 1955 (N. English,
unpublished data). Some may live as long as 300 years (Yetman, 2008). A single rainy
season may yield a very simple relationship between spine isotope values and TAP
(>80% of precipitation falls between December and March). It may also be easier to
build mechanistic models of oxygen isotope variation for species like T. atacamensis in
regions with a single rainy season. If this is the case, precipitation proxy records from
cactus spine series would represent a two-fold improvement in temporal length over the
satellite cloud cover records now used as a precipitation proxy in this region. Longer
records of precipitation variability would go a long way toward proving or disproving a
link between the Southeast mode of precipitation variability on the Altiplano and
lowland precipitation in the Chaco region of Argentina (Quade et al. 2008). In addition to
this, transects of composite isotope spine series from east to west and north to south in
the central Andean region might provide a spatially distributed, decades-long record of
terrestrial ENSO impacts.
There are ~140 species of columnar cactus (D. Yetman, pers. comm.) and many other
possible applications using isotopic variation in cactus spines, including quantifying the
impact invasive grasses have on cactus water balance (Mack et al., 2000; Williams and
50
Baruch, 2000), examining ancient patterns of seasonality in spines from packrat middens
(Betancourt et al. 2000), or investigating the response of succulent cactus to changing
climate (Osmond et al. 2008). We expect that the framework we have presented here will
change as more is learned about the isotopic responses of cactus to their environments.
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. English. We are thankful to K. Anchukaitis, J. Betancourt,
W. Beck, G. Bowen, J. Bower, J. Caulkins, J. Cole, M. Evans, S. Leavitt, J. Mauseth, J.
Pigati, B. Osmond, J. Overpeck for useful discussions and data.
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Figure Captions
Figure 1. Young and old saguaro (left panel), a common columnar cactus in the Sonoran
Desert. The spines along the side of the plant (right panel) grow from areoles on ribs
(white circles at base of spines) and in series (younger spines at the top, oldest spines
toward the bottom). Photographs taken by N. English.
Figure 2. Inter- and intraspine δ13C variation over days (A), weeks (B) and years (C).
The paired picture to the right shows graphically what part of the spine or cactus
represents that time scale. In A and B, the diurnal bands are clearly visible within the
spines (English et al. submitted). In (C), the isotopic spine series shown derived from the
tips of spines taken from the entire length of one rib on the cactus shown, a fast growing
saguaro in Saguaro National Park East. The age model for this cactus was developed
using F14C and methods described in English et al. (in prep.).
Figure 3. The composite δ13C and δ18O record derived from the spine series of five tall
saguaro cactuses on Tumamoc Hill near Tucson, Arizona and contemporaneous climate
records. Bold black line in top two panels is the composite δ13C and δ18O and is derived
by averaging the age modeled δ13C and δ18O isotope spine series (Fig. 5) at two-month
intervals. 95% confidence intervals are in gray. In the year-to-year change in annual
mean δ18O (Δ annual mean δ18O) * denote years in the composite record that are
associated with El Niño enhanced total annual precipitation on Tumamoc Hill
61
(November through October) and very negative SOI (* next to SOI associated with
strong El Niños, > 4). Note that Δ annual mean δ18O derived from the composite series in
1984 and 1997 appear to be one year late and one year early, with respect to years with
El Niño enhanced precipitation. Also, in many of our analyses, TAP and minimum (i.e.
nighttime) VPD are confounded due to their close association with each other (English et
al. in prep.).
Figure 4. Local meteoric water line for Tucson, AZ (left panel)(line, δ2H = 5.27*δ18O –
11.1) and experimental 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, 50 and 75 cm height (respectively from lower left to upper right) moving
away from mean irrigation-precipitation water isotope values (square). Contour plot of
δ18O (1‰ contours) in stem waters of a dissected experimental saguaro (right panel).
Black circles are sample locations. Note the strong vertical and radial gradients in stem
water δ18O.
Figure 5. Mean δ18O values and 95% confidence intervals of water from stem tissue near
the apex of four 0.8 m tall saguaro cacti (filled circles) and modeled values of stem water
δ18O at the same height (open circles). The model used to model δ18O of water at the
apex takes into consideration the δ18O of soil water, the base-to-apex gradient of δ18O in
stem waters, evaporation and water uptake.
62
Figure 6. A simple linear regression (solid line, r2 = 0.49, P < 0.001) of mean annual
δ18O in a time corrected composite spine record (Fig 3) against log transformed total
annual precipitation (TAP). The equation describing the relationship of TAP (mm) to
mean annual δ18O is used in Fig. 7 to reconstruct TAP.
Figure 7. Modeled total annual precipitation (TAP) for 1981 to 2006 using mean annual
δ18O from the corrected composite spine record. We model TAP using the relationship
shown in Fig. 6. 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 (English et al. in prep.).
63
Figures
Figure 1
64
Figure 2
65
Figure 3
66
Figure 4
67
Figure 5
Figure 6
Figure 7
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69
APPENDIX A:
PAST CLIMATE CHANGES AND ECOPHYSIOLOGICAL RESPONSES
RECORDED IN THE ISOTOPE RATIOS OF SAGUARO CACTUS SPINES
Nathan B. English1, David L. Dettman1, Darren R. Sandquist2, David G. Williams3
1
Department of Geosciences, University of Arizona, Tucson AZ 85721
2
3
Department of Biological Science, California State University, Fullerton CA 92834
Departments of Renewable Resources and Botany, University of Wyoming, Laramie
WY 82071
70
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 δ18O, δ13C 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 last 37 years. A series of 96 spines collected from this
individual had δ18O values ranging from 38‰ to 50‰ (VSMOW) and δ13C values from
–11.5‰ to –8.5‰ (VPDB). The δ18O and δ13C values of spines were positively
correlated (r = 0.45, P < 0.0001) and showed near-annual oscillations over the ~15-yr
record. This pattern suggests that seasonal periods of reduced evaporative demand or
greater precipitation input may correspond to increased daytime CO2 uptake. The lowest
δ18O and δ13C 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
71
and demonstrate that tissues of columnar cacti, and potentially other long-lived
succulents, may contain a record of past physiological and climatic variation.
72
1. Introduction
Variation in stable isotope ratios of oxygen (δ18O), hydrogen (δ2H) and carbon (δ13C)
in tissues that are incrementally produced and preserved on 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 showing isotopic variation in
tissues that are produced incrementally. Isotope measurements on tissues that are
sequentially added and preserved on stem 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 yrs) 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; Drezner 2003b; Drezner and Balling 2002)
73
mediated by the uptake and storage of winter/spring rainfall in the stem or through the
prolonged presence of soil moisture into the hot and dry premonsoon 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 4 and 8 areoles, each having about 15 spines, form on each elongate set of fused
tubercles (the ‘rib’ of the stem) each year (N English, pers. obs.), with the majority of
growth occurring during warm periods, i.e., April through 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.
74
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 stem-water and spine samples for
isotopic analysis; 3) develop and test a model for the isotopic enrichment of cactus stemwater using experimental potted saguaro plants; 4) demonstrate the accuracy and utility
of 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 δ18O and
δ13C values from spines of a naturally occurring cactus and compare these values to local
precipitation records.
2. Theory
2.1 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:
(1) δsw = (δi + 1000) fe(αl-v-1) – 1000
where δsw is the δ18O or δ2H value of stem water after evaporation, δi is the initial
δ18O or δ2H value of water in the stem, fe is the fraction of water lost from the stem due
75
to evaporation, and αl-v 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 δ18O and δ2H values of water at the stem apex where spine
development occurs.
When new water is added to the stem (recharged) and well mixed, the new stem
water isotope value (δsw*) is determined by a two-component mixing model:
(2) δsw* = δsw(1 – fr) + δr ( fr)
where δsw is the δ18O or δ2H value of stem water before recharge (Equation 1), fr is
the fraction of new water added to the stem and δr is the δ18O or δ2H value of this
recharge water (e.g., rainfall). fr can be estimated from stem diameter changes since the
majority of water in columnar cacti is 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.
76
The oxygen or hydrogen isotope ratio of spine tissue (δ18Ospine or δ2Hspine) can be
expressed as:
(3) δspine = [f (δsw-apex + 1000) αbio + (1 – f) (δsw-chlorenchyma + 1000) αbio] – 1000
where δsw-apex is the oxygen or hydrogen isotope value of water at the stem apex (δsw
or δsw* from the above equations) where spine tissue is synthesized , δsw-chlorenchyma is the
isotope value of water at the source of photosynthetic carbon dioxide assimilation in
chlorenchyma, αbio is the fractionation factor for oxygen (εO) or hydrogen (εH) 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 dicot plants (i.e., trees, Roden et al. 2000). Note that if the source of
photosynthates for spine formation is near the apex (i.e., δsw-chlorenchyma ≈ δsw-apex),
equation 3 simplifies to:
(4) δspine = [(δsw-apex + 1000) αbio] − 1000
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2.2 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 δ13C of atmospheric
CO2 (~0.2‰, Keeling et al. 1979). CAM photosynthesis involves the initial fixation of
atmospheric CO2 by PEP-carboxylase (PEPc) at night when stomates are open and the
storage of photosynthate as malate (referred to as CAM phase I; Dodd et al. 2002; Winter
and Holtum 2002). At dawn while the stomates are still open, 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 of the malate is consumed and internal pCO2 declines, 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 (Δ13C ) to
varying degrees and thus influences the isotopic ratio of the plant relative to air
(δ13Cplant ≈ δ13Cair – Δ13C). At night (phase I), Δ13C is partially determined by changes in
the balance of stomatal conductance (CO2 ‘supply’) and PEP-carboxylase activity (CO2
‘demand’) during CO2 uptake. During the day when stomates are closed (phase III), Δ13C
is moderated by the degree of CO2 leakage out of tissues. These fractionation processes
are diffusion–regulated, but enzymatically driven fractionations also affect Δ13C in CAM
78
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 (Δ13C = 27‰) modifies Δ13C as it
would in a C3 plant. Enzymatic uptake of CO2 by PEPc (Δ13C = 2‰) when the stomates
are open at night (phase I) also modifies Δ13C (O’Leary 1988; Griffiths 1992).
CAM plants grown in mesic environments tend to have more negative tissue δ13C
values 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 13C-enriched CO2 when stomates are closed (phase III; Griffiths et
al. 1990; Haslam et al. 2003). A simple model for δ13C 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 conditions), a large
stemmed cactus also common to the Sonoran desert (Ferrocactus 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 Δ13C 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
δ13C values of cactus tissues. We predict that the δ13C 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
79
phase II and IV photosynthesis), especially in years with above average rainfall, such as
during a strong monsoon year or after substantial winter rains (e.g., El Niño years).
3. Methods
3.1 Experiment with potted saguaro
Four ~0.8 m tall saguaro plants, purchased from a local nursery in June, 2004, were
grown in ten-gallon (38 L) pots outdoors in full sunlight at the University of Arizona
Desert Laboratory, Tucson, AZ (32.22° N, 111.00° W, 800 m elevation). These plants
were used to investigate the influence of evaporation and recharge on the δ18O and δ2H
values of water at the stem apex. Plants were allowed to acclimate for 8 months with
frequent watering prior to experimentation (at least once every one or two weeks, as
needed) using Tucson municipal water: δ18O = –8.4 ‰; δ2H = –61‰. In order to induce
drought all irrigation was withheld from the cacti between April 28 and July 26, 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, pers. comm.) 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 (δ18O = –1 ‰; δ2H = –7‰) recorded during the drought cycle reached the soil.
After the plastic was removed (July 27, 2005), cacti took up water from irrigation
(provided at the same frequency as before) and natural precipitation through October,
2005.
80
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
month of the experiment (April and October, respectively) to account for the mass of
water in saturated potting soils (~4 L holding capacity in the ten-gallon 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 6-cm 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, stored in a freezer and the surface to 3 cm
samples were later processed using cryogenic vacuum distillation to extract stem water
(Ehleringer et al. 2000) for isotope analysis. Boreholes in stems were plugged with 6 cm
long wooden dowels (10 mm diameter) immediately after sample collection.
3.2 Spine sampling from a naturally occurring saguaro
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
81
Turner 1998). Saguaro 162 is located at the University of Arizona Desert Laboratory at
Tumamoc Hill, Tucson, Arizona. 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 (Table 1) and of each sampled spine. We used
needlenose pliers and sprue cutters (The Testor Corporation, Rockford IL) 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 through
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 comm.).
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 1940’s.
To serve as a control for potential urban CO2 contamination effects 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-SCI0012), 23 km from downtown Tucson. We compared the measured F14C and the
resulting age of this control spine to a similarly sampled spine from Saguaro 162 to
determine the impact of urban pollution on radiocarbon measurements yielded by
82
saguaro spines. This control sample was also used to assess the use of stored carbon in
spine growth.
3.3 Stable isotope analyses
We performed stable isotope measurements at the Laboratory of Isotope
Geochemistry, Department of Geosciences, University of Arizona. We analyzed waters
for δ18O using a dual-inlet isotope ratio mass spectrometer (Delta-S, Thermo Finnegan,
Bremen, Germany) attached to an automated CO2-H2O equilibration unit. We measured
water δ2H 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 750°C. Standardization was based on internal standards calibrated
with V-SMOW and V-SLAP. Reported values are in per mil (‰) relative to V-SMOW.
Precision on repeated analyses of lab standard waters was less than ± 0.08‰ for δ18O
and ±1‰ for δ2H.
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 spineseries). For each spine 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. δ2H of spines was not measured.
Spines were dried overnight at 70° C and chopped into fine pieces 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
83
isotope ratio mass spectrometer (Delta Plus, Thermo Electron Corp, Waltham, MA).
Reported values are in per mil (‰) relative to V-SMOW for δ18O analyses and V-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.
We measured the effect of tissue processing on δ18O values of spines from a saguaro
nearby and similar to Saguaro 162. We used ground (40 mesh) spine tissue from 3.7, 2.5
and 1 m above ground level. The δ18O values of spine tissue holo- and α-cellulose
(Brendel et al. 2000) were 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 >
3.13, P < 0.0057). Given the inert nature of dead spine tissue and the relatively small and
consistent offset in δ18O 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 δ18O and δ13C sampling on the same spine for F14C
analyses. These segments were dried overnight at 70° C and bathed in weak HCl acid
(0.1 M) in an ultrasonic bath for 30 minutes. Each of three acid baths was followed by a
30-minute 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 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 ages, we used
the Northern Hemisphere Zone 2 data set (Hua and Barbetti 2004), a 0.2–year sample
84
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 (pers.
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 age from the 95% confidence interval of
all the possible ages for each sample (2σ 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 is true of our error
determinations. This anchor also allowed exclusion of 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 Inc., Cary, NC) 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. MTM is used to estimate singular or continuous components (e.g. frequencies or
85
trends) within a time series. We used p = 2 and 3 data tapers, which has been shown to
be suitable for climate time series (Mann and Park 1994).
4. Results and Discussion
4.1 Recharge, evaporation and isotopic composition of potted saguaro
The mean δ18O 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 δ18O 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 decreased
rapidly thereafter to 11.7‰ in August. The sharp increase in δ18O 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 δ18O, with desiccation
after the cessation of irrigation contributing to even greater δ18O values. As expected,
δ18O 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 are
confounded in this experiment, the changes in δ18O of stem water appeared to be strongly
associated with changes in VPD and the availability of soil water.
We used the measured plant mass, nighttime temperature and relative humidity to
model stem water δ18O during periods of evaporation (Equation 1) and recharge
(Equation 2). We took the measured stem water δ18O values from each plant in April and
86
July as initial points for the evaporative and recharge models, respectively (Fig. 2).
During the artificial drought (April to July, 2005), the cacti lost ~40% of their mass and
both modeled and measured δ18O values of water at the stem apex increased (Fig 2A–D).
The Rayleigh evaporative model, however, overestimated the final measured δ18O values
by ~2‰. Upon further examination, we found strong vertical gradients (~12‰ for δ18O)
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
δ18O value below the modeled value. Alternatively, an error in the mass loss
measurement of 7% (~3 kg) would also yield a difference in modeled δ18O values of
~2‰.
There was also a strong association between modeled and measured δ18O values of
water at the apex during recharge from July to October (Fig. 2E–H). For recharge, the
two-component model (Equation 2) underestimated the measured δ18O value of stem
waters by ~2.5‰. Underestimation of δ18O by the recharge model may be a result of
continued evaporation after July while recharge occurs.
It is clear that even with these discrepancies evaporation and recharge have the
overall effect of raising and lowering, respectively, the δ18O values of stem water at the
apex. The waters in a cactus stem, however, are clearly not well mixed and a more
87
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.
4.2 F14C derived growth model in a naturally occurring saguaro
An individual saguaro spine emerges quickly (within months) from the areole,
lengthening up to 0.7 mm each day (N English, pers. obs.). F14C ages measured
separately from the tip and base of a mid-1980s spine further support this observation
(Table 1). Like 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 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 in pine trees (Wright and Leavitt 2006), saguaro
plants do not appear to construct apical spines from storage carbohydrates that were
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 either a second areole growing on
top of another areole or over an areole scar (N English, pers. obs.).
For Saguaro 162 there was a 1-to-1 relationship (95% confidence interval from 0.96
to 1.10) between the age of spines derived from heights measured by Pierson and Turner
88
(1998) and the F14C age of spine tips from heights spanning 77 to 377 cm (Fig. 4, r =
0.997, P < 0.0001). For all the compared spines (n = 8), however, the F14C ages are 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
14
C-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 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 less than 2 km from downtown Tucson
and a major interstate freeway. We use 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.
89
4.3 Temporal δ13C and δ18O variations in a spine series from a naturally occurring
saguaro
To compare the time series of δ18O and δ13C 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 (pers. comm.) over the
past 38 years (Table 1). This is the more direct time-series measurement, but the results
would have been the same using the corrected F14C ages of spines. For dates that precede
Pierson and Turner’s measurements, we used the corrected F14C-derived ages.
Strong cyclical variations in the δ13C and δ18O 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 δ13C separate each year in the 15-year δ13C spine series record (Fig. 5).
Using MTM with F14C-corrected ages from spine heights of 211 and 287.5 cm as
boundaries, we found statistically significant variance (99% confidence level) in δ13C on
an annual frequency of 1.08 cycles/year (0.72 to 1.52 years/cycle; Table 2). Visually,
there appears to be a strong annual cycle in the δ18O record of spines over the 15–year
record, but based on the MTM analysis the primary spectral peak in δ18O occurs above
the annual frequency, at 1.63 years/cycle (1.08 to 2.29 years/cycle; Table 2). These
analyses suggest that the δ13C variations in the spine series from Saguaro 162 may
reasonably be used as an isotopic chronometer representing annual periodicity, but that
use of δ18O for this purpose is less reliable.
90
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 grow (November through
February; N. English, personal obs.) will therefore not record changes in δ13C or δ18O
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 8 spines per year, thereby providing resolution at a subseasonal
scale, but when growing slowly, there may be only 3 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 δ18O and δ13C 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 δ18O so that two years appeared to
represent only one (Fig. 5). Likewise two 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 1982-83) resulting in lower δ18O and δ13C values in spine tissue (Fig. 5). With
91
wet soil conditions persisting until the start of the monsoons, we hypothesize that cacti
would continue greater expression of the C3 signal (CAM phase II and IV) through the
normally dry period of the year resulting in the absence of a peak in δ13C for that year.
The length of the spine isotope record based on the SSA of δ13C yields one year less
than expected based on ages interpolated from measured heights taken in 1970 and 1993
(Table 1; 15 years vs. 16 years). This discrepancy suggests that either: 1) the SSA of
δ13C 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 have 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 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, pers. comm.). For our
purposes, however, the cyclical variations seen in the SSA of δ13C was used to assign
years (grey bars in Fig. 5) to spines – using the observed height in 1993 as an anchor for
our chronology.
4.4 Environmental control of δ13C and δ18O variations in a spine series from a naturally
occurring saguaro
92
The amplitudes of δ18O and δ13C variation in the spine series 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 δ13C values from Saguaro 162 are positively correlated
with δ18O (r = 0.45, P < 0.0001). If stomatal conductance and leakiness were driving
δ13C values we would expect them to be negatively correlated to δ18O values from the
same spine. However, if we assume that variation in δ13C 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 δ18O excursions
occured in 1983 and 1993. These low values were seen after wet winters of the previous
year strongly influenced by ENSO, when the majority of precipitation (>200 mm) fell
between January and March. However, while the δ18O of precipitation clearly influences
the bulk average δ18O of water in the cactus over time, the impact of any single rainfall
event on the spine tissue δ18O is diminished by admixture with the large reservoir of
water in the stem. The unseasonably wet summer of 1982 and ENSO-influenced winter
of 1982-83 also produced the most negative δ13C values found in our spine series.
Given the presence of the strong ENSO signal in our record, we suggest that the
isotopic variablity in this record is due mostly to increased water availability and cooler
93
temperatures at the beginning and end of each growing season that favor direct fixation
of atmospheric CO2 by Rubisco in the early morning or late afternoon (CAM phases II
and IV), and reduces the δ13C value of spines grown during these periods. During the dry
pre-monsoon, 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 δ13C
values of spine tissue grown during these periods of drought.
5. Conclusion
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 may greatly
impact the viability and distribution of saguaro and other species of succulents as well as
their dependants (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 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 fully quantify 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 δ13C and δ18O in the spines of cactus are a result of
94
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 δ13C) and isotopic signals (δ13C and δ18O) 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.
Acknowledgements
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. Anchukaitis, 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. Meinzer and two anonymous reviewers.
All experiments comply with the current laws of the United States and the State of
Arizona.
95
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Figure Captions
Figure 1. Mean δ18O 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).
Figure 2. Variation over time of measured (filled circles) and evaporative model (open
circles) stem water δ18O 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 δ18O
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. cactus in Panel A is the same cactus as in panel E).
Figure 3. Local meteoric water line for Tucson, AZ (line, δ2H = 5.27*δ18O – 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, 50 and 75
cm height (respectively from lower left to upper right) moving away from mean
irrigation-precipitation water isotope values (square).
103
Figure 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–to–one correlation line. Error bars represent 2σ age
ranges as discussed in the text.
Figure 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 2σ age ranges (i.e. F14C age minus 1.9 years; see text). Spine
tip δ18O values (B) and δ13C values (C) plotted by height from the base of the plant are
shown with a singular spectrum analysis (SSA) of δ13C for comparison (D). Monthly
precipitation values at Tumamoc Hill (E) are shown for October through March (grey
bars) and April through 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 1992–93 coincided with El Niño in those years. Shaded
bars from top to bottom denote correlated years based on the SSA.
104
Table 1. Height of sampled spine, measured heights of Pierson and Turner (1998), F14C
content, and F14C year from spines of Saguaro 162.
Height
(cm)
377
325
320
287.5
255
211Tip
211Base
151
98
80
77
50
46
40
17§
Year at
Measured
Height *
2002.8
1993.9
1993
1989.9
1986.8
1982.6
–
1976.8
1971.7
1970
1969.4
1964
–
–
–
14
†
F C
1.0698
1.1015
–
1.1363
1.1695
1.2051
1.2105
1.3028
1.4261
–
1.5537
–
1.1991
1.1174
0.9679
‡
+/–
0.0092
0.0039
–
0.0039
0.0041
0.0026
0.0037
0.0038
0.0060
–
0.0105
–
0.0062
0.0060
0.0042
F14C
year
2004.7
1996.7
–
1992.3
1989.0
1985.4
1984.9
1979.4
1973.9
–
1969.5
–
1958.7
1957.8
1950.0
Corrected Corrected Corrected
– 2σ
+ 2σ
F14C year
2002.8
2000.7
2003.6
1994.8
1994.0
1995.6
–
–
–
1990.4
1989.0
1991.9
1987.1
1985.2
1988.3
1983.5
1982.2
1984.4
1983.0
1982.0
1983.9
1977.5
1977.0
1977.9
1972.0
1971.1
1972.9
–
–
–
1967.6
1966.3
1969.6
–
–
–
1956.8
1956.4
1957.3
1955.9
1955.6
1956.1
–
–
–
* Italicized values are interpolated from the growth rate calculated using 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)
† 14
F C is corrected to account for Desert Laboratory graphite line blank.
‡
Includes 0.1 per mil uncertainty that represents long term errors on the accelerator mass
spectrometer at the University of Arizona.
§
This is the most recent possible (2σ) calibrated age of a pre–bomb radiocarbon age.
105
Table 2. Variables and spectral analysis results using the multiple
taper method (MTM) for δ13C and δ18O in the Saguaro 162 spine
series.
Time Series
F14C
Maximum
Minimum
14
Variables
Years*
F C Years
F14C Years
Begins
1980.7
1978.3
1982.5
Ends
1996.3
2000.2
1992.4
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
δ C
Years/Cycle
1.08
1.52
0.72
(1st component)
Years/Cycle
1.35
1.90
0.90
(2nd component)†
δ18O Spine series
Years/cycle
1.63
2.29
1.08
(1st component)
*Based on unit–time interpolated and extrapolated from corrected
F14C ages at 211 and 287.5 cm and assuming year–round spine
growth.
† st
1 and 2nd components are significant (α = 0.95) periodicities in a
time series in order of greatest significance.
106
Figure 1
107
Figure 2
108
Figure 3
109
Figure 4
110
Figure 5
111
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112
APPENDIX B:
DAILY TO DECADAL PATTERNS OF PRECIPITATION,
HUMIDITY AND PHOTOSYNTHETIC PHYSIOLOGY RECORDED
IN THE SPINES OF COLUMNAR CACTUS, CARNEGIEA
GIGANTEA.
Nathan B. English1, David L. Dettman1, Darren R. Sandquist2, David G. Williams3
1
Department of Geosciences, University of Arizona, Tucson AZ 85721
2
Department of Biological Science, California State University, Fullerton CA 92834
3
Departments of Renewable Resources and Botany, University of Wyoming, Laramie
WY 82071
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Abstract
We measured spine growth in saguaro cactus over days, months and years with timelapse photography, periodic marking and δ13C, δ18O and F14C isotopic analyses of spine
bulk organic material. Transverse bands of light and dark tissue corresponded to daily
increments of growth in this long-lived columnar cactus. A diurnally resolved δ13C and
δ18O record from three spines grown in series over a 70-day period was developed using
the transverse color bands as chronometers of diurnal growth. We also constructed a 22year record of δ13C variations from spine tips arranged in series along the side of a 4-m
tall, single stem saguaro. Temporally constrained isotope spine series from cactus could
be useful in both ecological and climate studies.
However, we first use these two temporally constrained records to evaluate two
mechanisms, both related to vapor pressure deficit (VPD) and cactus water status, that
are likely to determine the daily and annual variability of δ13C and δ18O in spines: 1) the
ratio of carbon assimilated during the nighttime by phosphenolpyruvate carboxylase
(PEPC) to that from the daytime period by Ribulose–bisphosphate carboxylase (Rubisco)
during the CAM diurnal cycle; and 2) variation in 13C discrimination during nighttime
associated with VPD-determined changes in nighttime stomatal conductance. Our data
suggest that VPD and post-photosynthetic fractionations are the most likely determinant
of δ13C in spines. In the daily record, δ18O variability in spines appears to be driven by
water uptake following strong storms (>10 mm).
Second, we demonstrate the utility of temporally constrained isotope spine series by
estimating the annual growth rate of a saguaro and relate growth rate, areole generation
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and plant productivity to local precipitation in March, May and June, and suggest that
winter rainfall may not be as important to plant productivity in less water stressed
saguaro.
1. Introduction
1.1 Spine series and columnar cacti
In saguaro cactus (Carnegiea gigantea (Engelmann) Britton & Rose) climatic
variation and physiological response are integrated and recorded in the stable isotope
ratio values of carbon (δ13C) and oxygen (δ18O) in serially-produced spines (English et
al., 2007). Further development and broad application of spine time-series in cactus
would be useful for documenting physiological responses to environmental change or
reconstructing past climatic events — especially where cactus populations are threatened
with extinction (Godinez-Alvarez et al. 2003) or other land-based climate proxies are
sparse (e.g. treeless deserts). For example, saguaro fruit is a vital food source for birds,
bats and insects of the Sonoran desert (Wolf and McKechnie, 2003) but little is known
about the impacts of hurricanes or El Niño enhanced winter rains on fruit production. An
isotopic record that quantitatively links precipitation and cactus physiology and
productivity to these climate phenomena, in conjunction with regional climate models,
could help forecast future ecological responses or management strategies for these
species. An example of the utility of modern proxy data in this region is the recent
application of ~20 years of cloud-cover data from satellite imagery to identify two
geographically distinct modes of modern precipitation variability in the central Andes
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(Vuille and Keimig, 2004). One of these modes (the northern Altiplano mode) is linked
to ENSO variability that is antiphased with precipitation anomalies on the Peruvian
coast, whereas, the other is linked to lowland precipitation in the Chaco region of
Argentina. Since the available satellite record is short, it only covers a few ENSO cycles
and is unable to link variability in the second mode to global climate events. Longer
records from cactus spine series in this region could address the causes of variability in
the second mode. Additionally, spine series from transects between the Peruvian coast
and the northern Altiplano, where the effects of ENSO are felt strongest and anti-phased,
have the potential to quantify the strength of ENSO events from the last century over this
region of South America.
A barrier to developing and understanding spine time-series is a lack of knowledge
concerning: 1) the chronology of spine growth and accurate methods for determining
when individual spines on a saguaro grew (their “age”); and 2) the environmental
parameters recorded in the isotopic variability of cactus spines. Here, we describe the
growth of the spines over a day, part of a growing season, and throughout the life of a
columnar cactus and discuss probable physiological and climatic drivers of isotopic
variability in spines. The anatomy and growth of cactus stems over daily and annual
cycles have been well studied (e.g. Robinson, 1974; Gibson and Nobel 1986; Mauseth,
2006), but not with a focus on the chronology of spine growth or anatomical patterns
over multiple time-scales. Gouws et al. (2005) measured maximal tissue growth at night
on cladodes of Opuntia engelmannii (Salm-Dyck) and Opuntia phaeacantha (Engelm.).
Buskirk and Otis (1994) noted waxy, annual bands on the columnar cactus
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Lemaireocereus aragonii (Webb) and used these to accurately infer stem growth rates.
Nobel (1986) and Buskirk and Otis (1994) both found strong correlations between the
growth rate of a cactus stem (i.e. height) and the number of new areoles and spines added
at the cactus’ apex. Water status, temperature, and photosynthetically active radiation
(PAR) affect the overall productivity of cactus (Nobel, 1988), and the relationship
between climate and growth rate is observed in many studies linking climate variability
over the last century, such as the El Niño/Southern Oscillation, to physiological and
demographic changes in saguaro (Pierson and Turner, 1998; Drezner and Balling, 2002;
Drezner, 2003, 2005).
Our purpose here is to present a chronology of saguaro spine growth and explain the
isotopic variations within spines and along spine series. Here we provide a temporal
context for spine series that together with a better understanding of isotopic variability
can be used to link climate to plant or ecosystem productivity or to validate climate
models in regions with relatively sparse historical climate data. In English et al. (2007)
we discussed the annual dating of saguaro spines using δ13C, δ18O and F14C. Here we
will expand our observations over a larger range of time-scales — sub-daily to decadal
—to show that: 1) the regularly spaced light and dark bands of tissue within and
transverse to the axis of spines (Fig. 1, hereafter referred to as “transverse bands”) grow
rapidly and represent days of growth; 2) there is a strong temporal relationship between
climate and isotopic variability over days, weeks and years; 3) δ13C is most likely, but
not certainly, driven by CAM phase expression; and, 4) demonstrate that F14C and δ13C
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in spines can be used to determine the growth rates of cactus without repeated annual
measurements.
1.2 Saguaro spines, F14C, δ13C and δ18O
The massive, long-lived (~125–175 yrs) saguaro cactus occurs throughout the
Sonoran Desert of southwestern Arizona and western Sonora, Mexico (Turner et al.,
1995). This range roughly coincides with the region affected by the North American
Monsoon — a season of strong convective storms between July and September. As in
other cactuses, spine tissue in saguaro grows from areoles near the shoot (stem) apical
meristem (Fig. 1; Mauseth, 2006). Carbon and oxygen isotope ratios are incorporated in
the molecular structure of the lignin-rich spine tissue (Mauseth, 1977) as it emerges from
the areole (English et al., 2007). Like isotopes in tree rings (McCarrol and Loader, 2004),
once fixed in spine tissue the carbon and oxygen isotope ratios are retained in-series on
the plant for decades. Areoles form on each elongate set of fused tubercles (the ‘rib’ of
the stem) and are displaced laterally on the large dome-shaped apex of the cactus stem as
new areoles are produced on the upward extending apex (Mauseth, 2006). Over the
growing season when spines are added (April through October; Steenbergh and Lowe,
1983), changing environmental conditions, plant physiology or the arrival of the summer
rainy season (North American Monsoon) alter the δ13C and δ18O values of carbohydrates
and stem water, respectively, and these changes are recorded in spines (English et al.,
2007). Unlike tree-rings, however, no easily observable anatomic patterns of cactus spine
growth have been documented.
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The F14C and δ13C variability in spine time-series is helpful in quantifying the age of
spines and the growth of saguaro stems (English et al., 2007). While the F14C is based on
the dilution and removal of anthropogenic 14C in the atmosphere produced by
atmospheric nuclear testing (Reimer et al., 2004), the δ13C chronometer is based on interspine δ13C variations. Saguaro, like other cactuses, employ the crassulacean acid
metabolism (CAM) photosynthetic pathway to acquire atmospheric carbon for growth
(Osmond et al., 2008) and this has consequences for the δ13C of cactus tissue and spines.
In CAM plants, it is common for stomates to open at night (Phase I of the diurnal CAM
cycle) while CO2 is fixed by phosphenolpyruvate carboxylase (PEPC). Stomates close
during the day as stored organic acids are de-carboxylated (Phase III) to prevent water
loss and maintain high CO2concentrations within photosynthetic tissues, leading to more
efficient carboxylation by Ribulose–bisphosphate carboxylase (Rubisco).
Aside from changes in atmospheric δ13C (Francey et al. 1999) and postphotosynthetic fractionation processes (Badeck et al., 2005), there are two possible
mechanisms that may influence δ13C values in CAM plant biomass. Variation in
nighttime stomatal conductance associated with changes in vapor pressure deficit (VPD)
is one possible determinant of δ13C variation in CAM plants. If stomates are closed
during the morning and daylight hours (Phase II, III and IV), then only CO2 derived from
de-carboxylation of malate formed during the nighttime in Phase I is available for
photosynthate production and carbon allocation to spine tissue growth. Consequently,
δ13C is closest to the endmember value of PEPC fixation in the dark (Phase I). Carbon
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isotope discrimination (Δ13C) during Phase I would be equivalent to that in a C4 plant
with no CO2 leakage, represented by the model (after Farquhar et al., 1989):
(1)
Δ13C = a + (b4 – a)pi/pa
where a is discrimination due to diffusion of CO2 through stomatal pores (4.4‰), b4 is
the net discrimination associated with carboxylation by PEPC (~ –5.7‰ at 25° C), and
pi/pa is the ratio of internal tissue to ambient partial pressure of CO2. The balance of
atmospheric CO2 supply through stomates and CO2 demand by PEPC reactions is
reflected in the pi/pa value. This and the temperature dependence of b4 are the only
parameters that vary significantly in the above model. Osmond et al. (1979a) showed that
nighttime stomatal opening in the cactus Opuntia stricta (Haworth) responded strongly
and within hours to VPD. If daytime CO2 exchange was negligible, then nighttime
changes in pi/pa would account for variation in δ13C of the photosynthate pool (Roberts et
al., 1997). Drought and high nighttime atmospheric VPD reduce stomatal conductance,
pi/pa and Δ13C (increase in δ13C) in most CAM plants (Osmond et al. 1979b; Roberts et
al. 1997) and saguaro (Lajtha et al., 1997). After assimilation of CO2 into plant
carbohydrates, we expect the carbon incorporated into lignin-rich spines to be depleted in
13
C by 1-3‰ compared to other tissues in the plant (Boutton, 1996, Badeck et al., 2005).
Another possible determinant of the δ13C of biomass in some CAM plants is the time
of day during which the cactus fixes atmospheric CO2 (Osmond et al., 1979b; Dodd et
al., 2002; Winter and Holtum, 2002; Griffiths et al., 2007). In saguaro, MacDougal and
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Working (1933) observed that stomates remained open well into mid-morning in March,
while Lajtha et al. (1997) demonstrate that stomates are closed all day in the dry
premonsoon months. English et al. (2007) hypothesized that if stomates in saguaro are
open in the hours after sunrise (Phase II) or preceding sunset (Phase IV), then
atmospheric CO2 is also fixed directly by Rubisco. Rubisco and PEPC carboxylation
pathways have distinctive carbon isotope fractionations, but the fractionations associated
with these enzymes are only expressed if there is incomplete CO2 fixation. If stomates
are open after dawn or before sunset then carbohydrates will be derived from the
incomplete fixation of atmospheric CO2 (leading to tissues with δ13C > –27‰; Winter
and Holtum, 2002) and CO2 derived from malate decarboxylation by Rubisco. These
carbohydrates can be expected to mix later in the day and overnight with carbohydrates
derived from the nearly complete fixation by Rubisco of only CO2 released from malate
fixed by PEPC during Phase I and possibly Phase II (leading to tissue δ13C ≈ –10.9‰;
Winter and Holtum, 2002; Griffiths et al., 2007). Only a small amount (~10%) of CO2
fixed during Phase II or IV would be required to shift δ13C in photosynthate by –1.8‰
(Winter and Holtum, 2002).
Osmond et al. (1979b) observed a rapid increase in expression of atmospheric CO2
fixation by Rubisco during Phase IV of CAM in Opuntia stricta (Haworth) following
rainfall inputs, accounting for up to 25% of the carbon fixed over the diurnal cycle. This
same study also found that irrigation not only induced Phase IV CO2 fixation, but a burst
of Phase II CO2 fixation as well. Interestingly, Osmond et al. (1979b) did not observe a
concurrent shift in δ13C of whole stem tissues. We suggest this is probably a result of the
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small contribution carbon assimilated during the day made to overall growth of the stem
during the year. Spine tissue differs from the whole stem tissue in that the carbon and
oxygen used to make spines is isolated from any further carbohydrate reservoir changes
once the spine is grown, so we hypothesize that small changes in δ13C are most likely
recorded permanently and not overwritten by later stem tissue δ13C variability.
Variability in the δ18O value of spines is strongly influenced by isotopic changes of
water in the body of the cactus associated with evaporation and plant uptake of rainfall
(English et al., 2007). Evaporative water losses in cactus have been observed to increase
δ18O values of stem water, and presumably spine tissue as well, while water uptake by
cactus after rainfall or lower VPD has been observed to decrease the δ18O value of stem
waters (English et al., 2007). There are strong vertical and radial gradients in the δ18O
and δ2H of water in the stem. These gradients develop in the stem as either: 1) water
undergoes increasing evaporative enrichment as it travels from the base of the stem to the
apex; or, 2) evaporative enrichment of water along the stem reflects the relative density
or activity of stomates and consequently opportunities for evaporative enrichment.
2. Sampling and analytical methods
2.1 Transverse Bands
To determine what time of day and how fast a saguaro spine may grow, we measured
the incremental growth of a single spine growing on a naturally established ~30 cm-tall
saguaro cactus at the University of Arizona Desert Laboratory in Tucson, AZ (32.22° N,
111.00° W, 800 m elevation). We marked a single spine with white fabric paint at the
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position where the spine emerges from the areole (Fig. 2A). We affixed a small scale bar
to an adjacent, parallel spine and, to clear the field of view, removed two spines that were
not growing on the same areole by cutting to just near the base. We photographed the
growing spine every hour over a two-day period (May 16 to May 17, 2007) with a
tripod-mounted, 10-megapixel camera with an automatic-flash (Canon Powershot A640,
Canon Inc., Tokyo, Japan) connected to a remote computer running RemoteCapture Task
software (version 1.7.0.4, Canon Inc.). For each hourly image, we measured the pixellength of the scale bar and the pixel-length between the cut spine base and the white
paint on the spine. To account for the angle of the camera to the spine and for changes in
the focal length of the lens over the 24-hour cycle, we used the scale bar to determine the
pixel-to-millimeter conversion factor in each image. We used iMovie (Apple Corp.,
Cupertino, CA) to build a time-lapse film of the growth from the images (Appendix D).
A Hobo Microstation Datalogger (Onset Computer Corp., Pocasset, MA) approximately
10 m from the cactus and mounted on a ~8 m high roof collected average hourly
measurements of photosynthetically active radiation (PAR) and total rainfall over the
same two-day period. The cactus was shaded after 3 pm during the 48-h observation
period by one of the buildings of the laboratory.
Additionally, to verify that transverse bands represent increments of daily spine
growth, we used fabric paint to periodically mark the apical spines of 12 randomly
selected saguaro 0.4 to 1.8 m tall within ~1 km of the University of Arizona Desert
Laboratory. We marked the bases of growing and newly emerging spines (Fig. 1A;
indicated by a soft, yellow to red tissue at the base of the spine) with different colored
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fabric paint six times between August 13 and October 8, 2006. On November 2, 2006 we
collected 10 spines from each plant by clipping them at the base with sprue cutters.
Under a reflected–light microscope we bisected the spines longitudinally from each plant
with a razor and counted the number of transverse bands (one light/dark couplet)
between each marked period, using the most recent mark (closest to the base) as the
starting reference point for counting bands (Fig. 1B). Counting errors on the marked
spines resulted from: 1) the difficulty in marking the base of a spine surrounded by other
spines and ~1 mm–tall trichomes that obscure the area of cell generation on the spine
base; and 2) the paint occasionally sticking to the trichomes and then stretching while the
spine grew, leaving a paint “flap” and obscuring where the actual bottom of the mark
should have been on the spine. From this pool of 120 counted spines, we selected at
random one spine from each plant and analyzed the resulting band counts (n = 12 spines)
with the statistical software package JMP 5.1.2 (SAS Institute, Cary, NC). We also
cryostatically thin-sectioned one spine and examined the section with both epiflourescent
and normal transmitted–light microscopes to determine the anatomical cause of the
banding.
2.2 Sub-daily, diurnally and annually resolved stable isotope records
2.2.1. Sub-Daily records
We investigated whether differential expression of CAM phases II and IV would
produce sub-daily δ13C variability in spines. To do this we selected one spine from the
group of 12 spines described above and subsampled daily growth increments with a razor
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blade over six transverse bands (six days growth) for δ13C analysis (n = 29). Each sample
represented approximately 1/4 to 1/6 of that day’s growth (Fig. 3A). Sample preparation
and stable isotope analyses were identical to those described in English et al. (2007).
Reported values are in per mil (‰) relative to V-SMOW for δ18O analyses and V-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.
2.2.2. Daily Records
To examine the temporal relationship of spine δ13C and δ18O to rainfall, VPD and
modeled pi/pa we separately collected three marked spines in series that grew between
August 13 and October 8, 2006 from the apex of a 1.12 m tall saguaro, one of the 12
marked cactuses. These spines were bisected and digitally photographed using a reflected
light microscope. Using Image J 1.37v (Abramoff et al., 2004; Rasband, 2007), we
acquired a surface brightness profile of both the spine and the white background it was
on. We corrected the surface brightness profile of the spine with the plane background
brightness profile to account for vignetting near the edges of the image. We spectrally
analyzed the corrected surface brightness profile and used the peaks of the 2nd and 3rd
components of the reconstructed singular spectrum analysis (RCSSA, K-Spectra
1.0.15A, Ghil et al., 2000) to demarcate individual bands (days) along the spine. We laid
the spine atop an exact scale printout of the RCSSA and using this as a guide, each band
(day) was cut from the spine in series. The sample was then crushed or cut lengthwise
(parallel to the axis of the spine) to provide whole-band subsamples for δ13C and δ18O
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analysis. Stable isotope analytical methods were identical to English et al. (2007). Daily
minimum temperature and maximum relative humidity data from the Tucson
International Airport (KOLD weather station) were used to calculate nightime VPD
(Wang et al., 2004). Daily precipitation records were from an accumulating rain gage on
Tumamoc Hill ~150 m from the saguaro population.
2.2.3. Annual records
We also collected a spine time-series from a 4 m–tall saguaro (hereafter referred to as
SNPE A) in Saguaro National Park on June 27, 2004 (Permit #SAGU-2004-SCI-0012,
32.21° N, 110.73° W, 870 m elevation). For δ13C analysis, we sampled and recorded the
height of one spine from every areole along the length of one rib over the entire height of
the cactus using the methods described in English et al. (2007). After cleaning the spines
(as in English et al., 2007), their F14C content was measured at the Keck-Carbon Cycle
Accelerator Mass Spectrometry facility at the University of California, Irvine. For each
F14C value from a spine, we used the software program Calibomb (Reimer et al. 2004) to
estimate a number of possible ages, the 95% confidence interval for each possible age,
and a probability that each possible age is the correct age (English et al., 2007). 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 age from
the 95% confidence interval of all the possible post-1960’s ages for each sample (2σ age
range, English et al. 2007). Years in the δ13C record were demarcated using minima of
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the 2nd and 3rd components of the reconstructed singular spectrum analysis of the δ13C
record (RCSSA, K-Spectra 1.0.15A, Ghil et al., 2000). A composite record of total
monthly precipitation was constructed for 1980 through 2004 using data from the
National Climate Data Center. Precipitation data for January 1980 through January 1992
are from the Tucson Magnetic Observatory (NCDC Coop ID 028800) and February 1992
to 2004 are from the Vail 7 North station (NCDC Coop ID 28998), both stations are
several kilometers from the cactus. VPD was calculated using reconstructed monthly
mean minimum temperature and mean dew point temperature from PRISM for this
location (PRISM Group, 2008)
3. Results
3.1. Transverse bands within single spines
The majority of spine growth over two days in early May occurred in the hours just
after sunrise (Fig. 2B, Appendix D). Maximum spine growth rates (up to 0.16 mm hr-1)
and the majority of growth occurred from dawn until noon. This burst of morning growth
was followed by a short period of negative growth (retraction) and then a recovery to the
length achieved at noon by early evening. Continued growth occurred until pre-dawn and
added 16% (Day 1) and 33% (Day 2) to the total daily growth of 0.44 mm and 0.52 mm,
respectively. A late–morning thunderstorm on Day 1 of measurements reduced total
daily PAR, while Day 2 was cloudless (Fig. 2C).
For each day of growth, a saguaro spine produces a single transverse band, a couplet
of dark and light spine tissue in cross section (Fig. 1B, 0.3 to 0.7 mm wide). Using one
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spine selected at random from each of the marked cactuses (n = 12), we observed that
one day produces a mean of 1.00 bands (95% confidence intervals of 1.04 to 0.96 bands
day-1). We note that using similar methods on a spine of Ferocactus wislizeni (Engelm.)
Britt. & Rose, we find a 1:1 relationship between the number of growing days and the
number of transverse bands produced (results not shown). Saguaro spines in thin-section
contain distinct areas of long and short fibers that create the distinctive banding visible to
the naked eye. The cross-sectional density of the spine is less (lighter) in areas with
longer fibers.
3.2. Sub-daily, Daily and annually resolved stable isotope records
3.2.1. Sub-daily records
The high-resolution subsamples taken from one of the periodically marked cacti
failed to reveal significant sub-daily cycles in δ13C (Fig. 3B). However, we did observe a
negative trend from –12.2‰ to –13.8‰, a change of 1.6‰ over the length of the spine
corresponding to 6 days of growth. Darker areas of the daily banding also tended to have
more negative δ13C values than the lighter portion, potentially because of differences in
the degree of tissue lignification.
3.2.2. Daily records
Inter-daily changes in δ13C and δ18O values are seen in consecutively grown spines
(Fig. 4). The composite record spans ~70 days of spine growth. The δ13C and δ18O
values over this record range from, respectively, –11.0‰ to –13.6‰ and 33.1‰ to
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38.6‰. In each isotopic record, there is good coherence between spines when their
growth overlaps. Spine δ13C variations are correlated with changes in VPD, but
variations were the opposite of those predicted solely by modeled VPD effects on
nighttime stomatal conductance (Fig. 4, note modeled δ13C variations are inverted).
Spine δ18O decreases rapidly after periods of heavy rain (>10 mm), and increases during
periods with little or no rainfall. There is a notable positive δ18O spike in early
September that coincides with a decrease in δ13C, a reduction in VPD, and a large storm
on September 7.
3.2.3. Annual records
The spine series collected from SNPE A shows high annual variation in carbon
isotope ratios (from –9.8‰ to –13.4‰), but low inter-annual variation (Fig. 5). The F14C
measurements reveal that the cactus is at least 22 years old, consistent with the number
of peaks in the δ13C record. The period of the δ13C cycle is short in the early part of the
record while the cycles gradually lengthen as the cactus grows taller. While presented as
continuous records, the records are censored between the months of November and
March when spines are not growing (English et al., 2007).
Growth and areole generation rates derived from the dated spine time-series (Fig. 6)
show increased rates of stem growth with plant growth, with three significant minima
centered around 1990, 1996 and 2002. The last two minima correspond to precipitation
minima in the annual sum of March through June rainfall in 1996 and 2002.
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4. Discussion
4.1. Transverse bands
The repeat photography, microscope and marked spine data all suggest that the
repeated initiation and cessation of growth over the diurnal cycle is the cause of the
transverse banding and that each transverse band (one dark/light couplet) represents one
day. Spines grow rapidly during daylight hours, however, it is still unclear whether they
can grow all day or how much PAR is a factor in their growth rate (Nobel, 1988). A
thunderstorm on the morning (~10 am) of the first day appears to coincide with lower
total spine growth and lower spine growth rates compared to the second, cloudless day.
Spine growth at night may be a result of increased turgor pressure of the cactus and
hydration of living cells near the spine base rather than from addition of new tissue. We
attribute post-growth retraction (5% of the daily linear growth) to desiccation of the soft
spine tissue during the driest part of the day when osmotic pressure also declines due to
consumption of stored malate by decarboxylation in CAM Phase III. This precedes an
additional ~38% reduction in spine diameter at the base between first emergence from
the areole and total desiccation several weeks later.
In relatively young saguaro cactuses (<3 m tall), transverse bands on spines record
the number of days a spine grew. We suspect that the relationship between banding and
diurnal growth holds true in other species of cactuses with transverse banding in their
spines. Transverse bands are present on the spines of many other species of cacti near the
Desert Laboratory, including F. wislizeni, Stenocereus thurberi (Engelm.) Buxbaum, and
O. engelmannii (ex. Engelm.) Salm-Dyck.
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4.2 Sub-daily, daily and annually resolved stable isotope record
4.2.1. Sub-daily records
The sampling resolution we chose in the 5-day high-resolution δ13C record (Fig. 3)
did not resolve any regular δ13C variation, except a decline in δ13C over several days.
Most likely, use of stored carbohydrates (generated during the previous Phase II, III or
IV) to regenerate PEP during Phase I overprints any short-term variability in δ13C in
sucrose. Sutton et al. (1981) also noted that younger cortex tissue exhibits more rapid
responses to changes in malic acid concentrations and that the carbohydrate reservoirs of
the cortex (where spines emerge) and pith and younger and older tissue in cactus are
decoupled.
4.2.2. Daily records
Diurnally resolved spine δ13C and δ18O records can be composited to create long,
high-resolution spine isotope records (Fig. 4). Over just one week (September 5 to 12),
the spine δ13C values spanned ~2/3 and δ18O values spanned ~1/2 of the range observed
in a ~15 year spine time-series reported by English et al. (2007). Counting errors may
account for the 1-2 day offsets between spine isotopic minima, maxima and precipitation.
We investigated the possibility that changes in pi/pa associated with changes in
nighttime VPD determines δ13C values and might account for all the variation, without
any daytime CO2 uptake by Rubisco, using the model described in Equation 1. There is
no published relationship between VPD and pi/pa for any cactus but there is for two
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species of Clusia (pi/pa = -0.1858 x VPD + 0.7835), a CAM plant (Roberts et al. 1997).
Clusia are not ideal cactus analogs and we accept that the intercept and slope of the
relationship is probably different for saguaro than Clusia, however, we assume the sign
of the slope is the same and so in our model we use the Clusia derived linear relationship
of VPD and pi/pa measured by Roberts et al. (1997). Using Eq.1, we modeled δ13C in
spines using VPD from the 70-day period and accounting for temperature-related
changes in the net discrimination associated with carboxylation by PEPC (b4 in Eq. 1).
The predicted spine δ13C is 6‰ more positive and antiphased with the δ13C in spines
grown over the same 70 days (Fig. 4). The temperature dependence of b4 could account
for ~0.2 to ~0.4‰ of this offset while the remainder is probably due to postphotosynthetic discrimination as sucrose from autotrophic stem tissues is used in the
heterotrophic spines (Boutton, 1996, Badeck et al., 2005). Continuous contributions of
daytime CO2 fixation throughout the 70-day record may contribute the remaining ~3‰
to the offset. English et al. (2007) also found a positive correlation between spine δ13C
and δ18O that is inconsistent with spine δ13C variability driven by changes in pi/pa. Even
if there were evidence of a time lag between CO2 fixation and synthesis in tissue, this lag
cannot explain the discrepancy between modeled and actual spine δ13C after the first
week in September.
However, δ13C variation in spines is correlated and in phase with nighttime VPD and
opposite of what is expected if δ13C variation was driven by nightttime VPD as modeled
above. After small storms occur (<10 mm, i.e. Aug. 21) that do not impact spine δ18O,
the rapid return to more CAM-like δ13C values as high VPD returns suggests that, at least
132
during the monsoon, daytime acquisition of CO2 (expression of Phase II or IV) is
affected more by VPD than plant water status. Our hypothesis is that lower nighttime
VPD, and consequently lower morning VPD, allows stomates to remain open longer in
the morning and thus fix a greater proportion of atmospheric CO2 with Rubisco than
when VPD is high, lowering spine δ13C values. This hypothesis is consistent with the
work of many other studies (MacDougal and Working, 1933; Conde and Kramer, 1975;
Osmond et al, 1979a; Osmond et al. 1979b, Nobel, 1988; Lajtha et al. 1997). The
evidence that VPD drives CAM phase expression in saguaro, and thus δ13C values, is
promising but circumstantial and it remains to be confirmed by detailed gas exchange
experiments. Does pi/pa play a role in the δ13C variation in spines? We think so, but it
appears the δ13C variation in spines is either: 1) overwhelmed by δ13C variations due to
CAM Phase expression; 2) a lag time exists between CO2 fixation and carbohydrate
synthesis; or 3) stomates are either open or closed, with little variation of pi/pa in
response to nightime VPD over the course of weeks. None of these possibilities can be
ruled out, and it may be that conditions during the monsoon are not the same as during
other seasons.
The mass of water in a cactus is orders of magnitude greater than the mass of gaseous
and carbohydrate reservoirs in cactus combined, and so it is not surprising that the
diurnal δ18O record is less variable over theses short temporal scales compared to the
variability in the δ13C record (Fig. 4). The oxygen isotope ratio of internal plant water is
also affected by evaporation-driven vertical and radial isotope gradients in which more
positive δ18O values occur closest to the evaporating surface and at greater stem heights
133
(English et al., 2007). We hypothesize that the uptake of rainwater (with δ18O values of ~
–5 to –10‰ in Tucson) through the root system increases the gradient by the addition of
fresh water depleted in 18O to the saguaro’s lower core. The spike in δ18O in early
September may represent a spurious signal or extraordinarily high evapotranspiration on
that day. We do not expect a rapid response to daily or weekly variation in VPD or other
climate parameters due to the large volume of plant water buffering the water status of
the plant and the δ18O values of primary photosynthates used to make spine tissue.
Although δ18O and δ13C do not co-vary on the scale of days, over weeks and years the
two isotopes co-vary positively (English et al., 2007).
4.2.3. Annual records
The narrow tip of an emerging spine (the top 2 to 3 mm) represents just two or three
days of recorded isotopic variability in the cactus. Interpreting isotopic variation in an
under-sampled spine time-series is analogous to interpreting decades of temperature
variability where only one day every two months is represented in the record, and could
lead to signal aliasing. However, when we use F14C dated spines to establish the spine
series chronology for SNPE A, we see that the dry/wet/dry monsoon cycle is accurately
recorded by the δ13C record (Fig. 5) over the correct number of years. The strong
seasonal cycle in this δ13C time-series reflects high water–availability in March and April
(–13‰), a pre-monsoon drought in May and June (–10‰), and then the arrival of the
monsoon in July and August (–13‰) followed by a period of moderate rainfall, low
temperatures, and lower VPD until dormancy over the winter. Growing spines from
134
SNPE A were sampled from the apex in June and confirm that the most CAM-like δ13C
values (–10.3‰) are present in spines formed in the pre-monsoon season. We find very
little relationship, however, between year-to-year variation in this δ13C spine time-series
and that of local precipitation (Fig. 5).
Analogous to observations in dendrochronological studies (McCarrol and Loader,
2004), the position of this cactus in a shallow wash may make it much less sensitive to
annual or decadal variation in precipitation. Even so, just like a tree ring series, a spine
time-series from an insensitive saguaro is still annually resolvable. We hypothesize that
cacti located on hill slopes and away from water drainages will show greater sensitivity
to annual and decadal variation in rainfall because they are unable to reach their full
water–holding capacity in March and April preceding the pre-monsoon drought. The
range of spine δ13C values from the SNPE A saguaro is more negative than that from an
equally tall cactus located on a hillside at Tumamoc Hill (–8.5‰ to –11.5‰, English et
al., 2007) suggesting that the SNPE A cactus may fix relatively more carbon with
Rubisco during CAM Phase II or IV.
Using F14C and δ13C in spines we can derive very accurate annual growth rates of the
stem (Fig. 6). SNPE A has a growth rate 1.8 times faster than that predicted by the local
population growth model (calculated as in Drezner, 2003; Steenbergh and Lowe, 1977).
This magnitude of variation is not uncommon across the saguaro’s range (Drezner,
2005), but we are surprised to find it within a single population. Several lines of evidence
suggest that the growth rate we have derived for this cactus is correct: 1) the independent
agreement between the F14C and δ13C record; 2) the cactus lies within a small plot where
135
all saguaro cacti were surveyed and permanently tagged by Steenbergh and Lowe in
1977, however, SNPE A has neither a tag nor is noted on the 1977 survey map (Plot
41A, C. Funecelli, pers. comm.) suggesting that it was either not present or not visible in
1977; and 3) the shape of the growth curve (Fig. 6) described by the F14C and δ13C
record over the life of this cactus is similar to that of other saguaro (Drezner, 2003). We
hypothesize that the position of this cactus in a shallow wash, and therefore its ability to
recharge its stem water to full capacity before the onset of drought each year has
contributed to its rapid growth. While this example demonstrates the utility of F14C and
δ13C dating of spine time–series, it is also a caution against using population derived
growth models (Drezner, 2003) to infer the age of an individual cactus.
Using these F14C- and δ13C-derived growth records, we confirm that areole
generation in saguaro is positively correlated (t21 = 9.96, p < 0.0001) to apical growth
(Nobel, 1986; Buskirk and Otis, 1994). Additionally, it appears that for this cactus
productivity is best associated with March, May and June. March, May and June are on
average, respectively, the first month of growth and the two driest months of the year.
Rainfall in these months would be expected to augment stem growth and plant
productivity (Nobel, 1986) by providing water at the start of the growing season and
during the height of the premonsoon drought.
5. Conclusions
Stable isotope time-series from saguaro spines, and possibly other cactuses and stem
succulents with sequentially added and durable tissues, can be resolved with daily to
136
annual temporal resolution for climatic and ecophysiological studies. The transverse
bands present in saguaro spines are accurate chronometers of daily growth — other
species of cacti with transverse bands in their spines likely share this characteristic.
Spines can grow rapidly in the morning hours and also exhibit more negative δ13C
coincident with lower VPD and wetter water status in the early spring and during the
monsoon. We find circumstantial evidence suggesting that in cactus, as has been found
in other CAM plants (Griffiths et al. 2007), the balance of CO2 fixed by Rubisco or
PEPC photosynthesis, and not just Phase I stomatal conductance, also determines δ13C
variability in spines. It is possible that changes in pi/pa altered by nighttime VPD
influence δ13C, but this cannot be reconciled with the seasonal changes in spine δ13C
seen in longer annual records. Intra-spine δ13C and δ18O variability along the five-day
high-resolution spine transect and along the composite spine time-series however, show
that daily changes of physiological (the balance of PEPC/Rubisco CO2 fixation, pi/pa,
plant water status) and environmental parameters (VPD, precipitation) are recorded in
spines at diurnal time scales. Once the determinants of diurnal and annual spine δ13C and
δ18O variability and the temporal dynamics of cortical carbohydrate reservoirs are
reasonably well understood, inter-spine δ13C time-series along with F14C can be
combined to create exceptionally detailed isotopic records of cactus growth and
environmental change.
137
Acknowledgements
The research described in this paper has been funded in part by the United States
Environmental Protection Agency (EPA) under the Science to Achieve Results (STAR)
Graduate Fellowship Program. All experiments comply with the current laws of the
United States and Arizona. We are thankful to C. Funnicelli, M. Weesner, M. Daniels
and Saguaro National Park for providing access to Steenbergh and Lowes’ original notes
and allowing us to sample within the park. G. Bowen and J. Quade generously provided
lab space and supplies. Valuable discussions, data and field assistance were provided by
K. Anchukaitis, J. Betancourt, J. Cole, T. Drezner, C. Eastoe, M. Fan, Q. Hua, S. Leavitt,
M. Mason, J. Mauseth, J. Overpeck, W. Peachy, D. Potts, T. Shanahan and R. Turner.
This paper is dedicated to the late C. Burkhardt, who was a dear friend and provided
invaluable technical assistance during this study.
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Figure Captions
Figure 1. A) Transverse bands visible in situ on actively growing spines atop a ~1m tall
saguaro cactus. Actively growing spines at the apex have orange fleshy bases. Colored
paint was applied periodically. B) Transverse bands visible within a single bisected
spine. The left and right half of the bisected spine are aligned and the blue, purple orange
and white paint were applied, respectively, on August 30, September 9, 16 and 21. The
tip of the spine is towards the top of the figure.
Figure 2. Linear saguaro spine growth and PAR over two days (May 16 and 17, 2007).
A) Photograph of the spine, the fixed scale and the reference marks as they appeared on
May 17 at 8 am, the time of the maximum linear growth rate (*). B) The relative and
actual linear distance between reference marks over time (i.e. spine growth). C) The
spine’s linear growth rate (black) compared to hourly PAR measurements (grey).
Figure 3. High-resolution δ13C record from a saguaro spine grown in late August. A)
Reflected light micrograph of the sampled spine with sample divisions. B) δ13C of
sampled spine tissue (horizontal scale is the same as in A). Closed circles are from dark
144
banded tissue with short fiber lengths, open circles are from light banded tissue with long
fiber lengths. September 2 was divided into one more sample than shown in A.
Figure 4. Daily resolution δ13C and δ18O record from three saguaro spines grown
between August and October 2006. A) δ18O of spine tissue. Open circles, closed circles
and squares are the spines taken from the closest areole, the second closest areole, and
third closest areole to the apex, respectively. B) δ13C of spine tissue, symbols same as
above. Grey line is high resolution δ13C record from Fig. 3. C) Three day running
average of nighttime vapor pressure deficit (bold black line) and precipitation at the
Tucson International Airport (grey bars). The bold black line in (C) also represents
modeled spine δ13C (see text) over the whole 70 days by the floating scale bar (*). Note
that the scale bar on the modeled data is inverted and a correction of –6‰ has been
added to the modeled data.
Figure 5. δ13C record in spine tips (open circles) spanning ~4 m of a naturally occurring
saguaro (SNPE A) in Saguaro National Park, AZ. In A) filled triangles with horizontal
lines are corrected F14C ages. B) Monthly nighttime VPD (bold grey line) is shown
above monthly precipitation values from nearby climate stations: October through March
(grey bars); and April through September (black bars, see text for data sources). In all
panels, light grey bands denote correlated years.
145
Figure 6. Stem and areole growth rates of a naturally occurring saguaro in Saguaro
National Park East (SNPE A). A) Estimated annual growth rate of SNPE A cactus
(closed circles) and the number of areoles produced each year (open circles), axis on left.
Also shown is the total estimated height of the cactus (bold black line, axis on right). B)
Estimated annual growth rate of SNPE A cactus (closed circles) and total March through
June precipitation for each year over the same time period (open circles).
146
Figure 1
147
Figure 2
148
Figure 3
149
Figure 4
150
Figure 5
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Figure 6
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APPENDIX C:
A 26-YEAR STABLE ISOTOPE RECORD OF PRECIPITATION, HUMIDITY
AND EL NIÑO IN THE SPINES OF SAGUARO CACTUS, CARNEGIEA
GIGANTEA
Nathan B. English1, David L. Dettman1, David G. Williams2
1
Department of Geosciences, University of Arizona, Tucson AZ 85721
2
Departments of Renewable Resources and Botany, University of Wyoming, Laramie
WY 82071
154
Abstract
Seasonal cycles of rainfall and humidity are recorded in stable isotope ratios in the
spines of columnar cactuses and we explore the possibility that year-to-year variations in
rainfall and humidity are also recorded. Multi-decadal δ18O and δ13C records from the
spines of saguaro cactus, dated using bomb radiocarbon and semi-annual variations in
δ13C, demonstrate the reproducibility of the signal between five spine series. Composite
δ18O and δ13C records constructed from five spine series show significant relationships to
external climate forcing. Once dating errors are corrected, mean annual spine δ18O is
negatively correlated with total annual precipitation (TAP) from November through
October and positively correlated with mean annual nighttime vapor pressure deficit
(VPD). Year-to-year decreases (>2‰) in the maximum annual spine δ18O are positively
correlated with the Southern Oscillation Index. We hypothesize these decreases are
caused by enhanced winter rainfall following strong El Niño years. While less
significant, minimum annual δ13C is negatively correlated with TAP and mean nighttime
VPD. These results bolster proposed mechanistic models of isotopic variation in the
spines of columnar cactus and demonstrate the potential of isotopic spine series as
climate proxies.
1. Introduction
Many columnar cactuses grow durable woody spines in sequential order that are
retained in series along the side of the cactus for decades as it grows taller (Mauseth
2006). Analogous to tree rings, these spines contain isotopic information linked to past
155
climate variation. In long-lived columnar cactuses isotopic measurements from spine
series could yield useful records of climate and physiological variation (English et al.
2007; in prep). English et al. (2007; in prep) have proposed empirical mechanistic
models of isotopic variation in the columnar saguaro cactus (Carnegiea gigantea,
(Engelm) Britt and Rose). These models show how precipitation and nighttime vapor
pressure deficit (VPD) can determine the δ18O and δ13C of spines by altering water
storage and photosynthetic fractionation processes of a cactus. English et al. (2007) also
observed that spines grown in series along the stem a saguaro cactus (hereafter referred
to as spine series) record seasonal stable isotope (δ13C and δ18O) variations. Lower
isotopic values in 1983 and 1993 were associated with growing seasons when winter
rains were enhanced by the warm phase of the El Niño/Southern Oscillation
(ENSO)(Gutzler et al. 2002). However, it has yet to be shown that isotopic spine series
from multiple columnar cactuses respond in unison to common climatic or
environmental changes or that δ18O and δ13C variations in spines are associated with
precipitation or nighttime vapor pressure deficit (English et al. 2007). To this end, we
have expanded the spine series presented in English et al. (2007) and collected four
additional spine series from nearby cactuses. Using radiocarbon (F14C) and in-series
measurements of spine δ18O and δ13C spines from these cactuses, 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
156
variations in nighttime vapor pressure deficit (VPD); and 4) enhanced winter
precipitation is associated with anomalous δ18O and δ13C values in spine series.
The massive, long-lived (125-175 yrs) 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 (2003a, 2003b) and Drezner and Balling (2002) 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). Stronger winter,
but not monsoon, rainfall is linked with El Niño conditions in the eastern Pacific.
Conflicting predictions exist for summer precipitation in this region, either increasing or
decreasing by 50% under global warming conditions (Giorgi et al. 1998, NAST 2000,
respectively, Christensen et al. 2007). It is unclear whether the frequency and amplitude
of ENSO in the future will change (Meehl et al., 2007), although at least one study
suggests ENSO teleconnections over North America weaken in a warming world (Meehl
et al., 2006). Given that summer and winter rainfall both provide roughly half of the
annual total of precipitation in Tucson, it is unknown whether or not spine δ18O and δ13C
157
reflect water uptake or VPD during the NAM, the winter months or the winter months
following a strong El Niño.
We use the isotopic variation in several cactuses’ spine-series to address the relative
importance of seasonal and diurnal VPD and rainfall. The greatest challenges to this
work are accurately dating the spine series and teasing out the confounding effects on
isotopic variability of relative humidity and rainfall. With a century of research,
combined advances in dendrochronology and isotope ratio mass spectrometry have
allowed isotopic studies of tree rings to become an important tool in climate and tree
physiological research (McCarroll and Loader 2004, West et al. 2006). Stable isotope
analyses of tree rings combined with mechanistic models of stable isotope variation in
trees are used to quantitatively estimate past climate regimes (Anchukaitus et al. 2008).
Stable isotope analyses of tree rings will be used in the future to validate climate models
and for agricultural and water resource planning in a manner similar to how tree-wing
widths are used today (e.g. Foster 2001, Bradley et al. 2006). Likewise, we have begun
to develop and expand our understanding of cactus growth and isotopic variation and
their relationship to climate (English et al. 2007, in preparation). Here we take the next
step and develop a composite isotope spine series from saguaro cactuses and compare
this composite record with local instrumental and reanalysis climate data to measure its
utility as a climate proxy.
2. Methods
2.1 Spine series and climate data collection
158
We sampled spines for isotopic analysis from the northernmost rib of five >3.7 m
tall, single-stemmed saguaro cactuses. A height-ordered series of isotope measurements
was created from the spine series of each cactus sampled. The heights of these five
cactus had been measured repeatedly over 38 years as part of an effort to establish
growth models for saguaro (Pierson and Turner 1998). These cactuses, all within 100 m
of each other, have grown naturally at the University of Arizona Desert Laboratory at
Tumamoc Hill, Tucson, Arizona. 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 along the rib (we chose the longest central spine that was most distal from the
areolar meristem). Precipitation measurements have been collected #at least monthly ~200
m from the saguaros used in this study for the last 28 years at this site (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). In Tucson,
precipitation is equally distributed between the winter and NAM. Generally, spines grow
only between March and October, so we use months in the calculation of TAP that
coincide with the spine growing season. Nighttime and daytime VPD for Tumamoc Hill
was calculated using reconstructed monthly mean minimum and mean 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
159
Index (NOAA, 2008) as a measure of ENSO strength (negative SOI indicates El Niño
like conditions). For precipitation, night 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 > 10) were log
transformed before simple linear regressions were performed. We use the Pearson
product-moment correlation with α = 0.95 to quantify the association of annual climate
parameters to each other and to annual isotopic parameters in the composite record.
2.2 Stable isotope and statistical analyses
We performed stable isotope measurements at the Laboratory of Isotope
Geochemistry, 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 (1,706 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 V-SMOW
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
160
saguaro and found that the δ18O values of spine tissue holo- and α-cellulose (Brendel et
al. 2000) were 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 > 3.13,
P < 0.0057). Given the relatively small and consistent offset in δ18O values, we analyzed
raw spine tissue without further processing.
2.3 Spine age determination
Spines growing from the apex of columnar cactus, such as saguaro, do not yield
readily apparent chronological markers like tree rings. Instead, at selected heights on
each saguaro, we used a segment of the remaining raw spine tissue from just below the
δ18O and δ13C sampling site on the same spine for F14C analyses. These segments were
dried overnight at 70° C and bathed in weak HCl acid (0.1 M) in an ultrasonic bath for
30 minutes. Each of three acid baths was followed by a 30-minute 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 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 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 samples with a post 1999.5 age we used an unpublished update of the same
dataset provided by Q. Hua (pers. communication) and extrapolated to 2007. For each
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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 age 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 any possible ages 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 14C-depleted 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 ages (this offset is less than 2.1 years for all
cactuses). The association between the observed height of cactuses in a given year and
the F14C age of spines from those heights (Fig. 1) provides a reasonable assurance that
F14C spine ages can be used to date spines to within a couple of years of their formation
and is consistent with growth curves for cactus in this region calculated by Drezner
(2003c).
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3. Results and Discussion
3.1 Compositing and analysis of isotopic spine series
Tree ring records from one location are commonly averaged (composited) together to
create annually resolved records that can be used as proxies for climate (McCarroll and
Loader 2004). The purpose of compositing records is to reduce the signal “noise”
associated with individual plant variability caused by genetic, microclimatic or other
effects unique to each plant and to create a record that more accurately represents the
mean population response of a selected variable (e.g. δ13C and δ18O) to local climate. To
more accurately represent the isotopic response of saguaro to local climate and reduce
the influence of individual variability, we average five δ13C and δ18O spine series from
five cactuses (Table 1, Fig. 2 and 3) to create a composite record that more accurately
represents the mean δ13C and δ18O responses of these cactuses (hereafter referred to as
the composite record) to precipitation or vapor pressure deficit. Unlike tree rings,
however, cactus spine series lack annual banding and we must first apply an age model
to each spine series so that: 1) they are comparable to each other; and 2) comparable to
climatic time series. English et al. (2007) showed that δ13C varies seasonally and, in
combination with F14C ages, we use these variations in δ13C to guide the development of
an age model for each spine series. Spine δ13C and δ18O values are paired, so that the age
model for the δ13C spine series can be used for the corresponding δ18O spine series. The
conversion from spine height to spine age is the step most vulnerable to error and
subjectivity and as such we explain it in detail.
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We create unique age models for each spine series based on simple linear
interpretation between F14C-dated spines and then modified using cyclical variations in
δ13C (Fig. 2). Each raw spine series contains ~170 spines (Table 1, Fig. 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 when apical growth rates are 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 distributed evenly 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 (generally March through October, respectively) and maximum δ13C values in the
premonsoon months of May and June. As such, we pin each years 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
164
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 “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 present day to 1980 (Francey et al., 1999).
In 1980, this adds up to ~0.7‰ subtracted from the age modeled δ13C spine series. After
this, we adjust each age modeled δ13C spine series to a common mean (in this case, a
simple average of each δ13C spine series mean, or –11.3‰). For each δ18O spine series,
we adjust the mean so that it is equal to the common δ18O spine series mean (42.4‰).
The age modeled, corrected and adjusted spine series are shown in Figures 4 and 5.
Finally, the values from each unique time interval of the adjusted and corrected δ13C and
165
δ18O spine series are averaged to create annually dated, composite records of spine δ13C
and δ18O variation (Fig. 6 and 7).
3.2 Calculation and evaluation of the expressed population signal (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. We estimate the shared isotopic variance in our composite records by
calculating the 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 interspine series correlation coefficient (r) with a theoretical infinitely sampled (and hence
fully representative) composite where t is the number of spine series:
2) EPS(t) =
€
(t × r)
(t × r) + (1− r)
Although there is no strict demarcation, an EPS ≥ 0.85 suggests that the composited
record will accurately represent the mean variance of the population and yield a signal
relatively free of noise due to individual variation (McCarroll and Loader, 2004).
Together, the five age modeled δ13C and five δ18O spine series presented here have an
166
EPS < 0.85 (0.68 and 0.66, respectively)(Table 2). Using r for the cactus we have
sampled and assuming that r will change little with more sampled individuals, we can
calculate the number of spine series required to reach an EPS of 0.85 or greater (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. 2 and 3).
When 1998 to 2006 is excluded, EPS improves in the δ13C composite record, but is
reduced in the δ18O composite record (Table 2). The changes in variability and EPS
between 1997 and 2006 could be associated with changes 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, 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 (~60 years)(Pearson 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 postphotosynthetic fractionation processes associated with the onset of flowering and fruit
production, changes in the timing of gas exchange, the changing morphology of spines or
stem growth. Drezner (2008) found that 10 km away, 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 that track the amplitude of isotopic variation of stem waters and
167
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, however,
cactus are relatively short-lived compared to trees and so compromises between record
length and noise must be made to accommodate the question being examined with
composite records of isotopic variation in spines.
Seasonal isotopic variations in the composite records are pinned to the seasons (e.g.
maximum δ13C to the premonsoon), 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 compare the relationship of annual parameters in
the δ13C and δ18O composite records such as the mean, maximum and minimum values
of any year and compare these to annual climate parameters (Fig. 6 and 7). As expected
(the number of data points available for regression decreases from 157 to 26), the EPS of
these parameters generally decreases (Table 2), however, the EPS of mean annual and
minimum annual δ18O is higher than in the adjusted δ18O spine series.
3.3 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. 6 and 7; Table 3). Mean nighttime VPD
168
and same-year TAP are positively and negatively correlated, respectively, with mean
annual spine δ18O in the composite record. Large reductions (>2‰) 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 < 0.01) as is
same- and preceding-years’ JFMAP (P < 0.01, Table 3).
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). 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). 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 TAP and mean annual δ18O (Fig.
8). Mean annual δ18O in 2003 is anomalously high, and when it is also removed from the
regression, 73% of the variation in δ18O is explained by changes in TAP. 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 < 0.014) and decreased mean annual
nighttime VPD (F24 = 8.11, P < 0.009) at Tumamoc Hill. Likewise, when the dating
169
correction is made, the difference between year-to-year maximum annual δ18O is
positively correlated with minimum annual SOI (P < 0.01). For these cactuses, a
reduction in mean annual spine δ18O greater than 2‰ indicates a strong El Niño year
(SOI < –4, Fig. 6). 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. JAS precipitation is not significantly
associated with any annual δ18O parameter (Table 3 and 4) in either the corrected or
uncorrected records.
For δ18O in spines grown mostly between April and October (Steenbergh and Lowe,
1983), we hypothesize that increased winter precipitation and lower nighttime VPD act
together in three ways to lower δ18O values. First, weighted δ18O values of JFMAP
(–9‰) are ~3‰ more negative than δ18O values of precipitation in May through August
(–6‰)(C. Eastoe, unpublished data). Stem waters in cactuses are a mixture of winter and
summer rainfall (McAuliffe and Janzen, 1986) and cactuses 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
170
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). The cause of this gradient is still uncertain but decreased VPD and
evaporation of water could lessen the gradient and consequently reduce the δ18O values
of stem water at the apex.
When we use the relationship from a simple linear regression model (Fig. 8) to
reconstruct TAP using δ18O, we find that reconstructed values of TAP are similar to
actual TAP values (Fig. 9). The uncorrected regression model does a poor job of
reconstructing TAP in 1984, 1997 and 1998 (r2 = 0.08, F24 = 1.98, P < 0.17). However,
we get much better estimates of TAP (r2 = 0.53, F22 = 24.9, P < 0.0001) when we use the
relationship from the chronologically adjusted annual isotope data as described above
(Fig. 9, middle panel). 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 will yield records more
amenable to the application of statistical transfer functions and skills testing and better
able to reconstruct past climates.
3.4 δ13C composite records
Paired spine δ18O and δ13C are strongly correlated in individual and composite spine
series (F155 = 93, P < 0.0001). We find significant associations between annual mean,
maximum and minimum δ13C with daytime and nighttime VPD and maximum annual
171
SOI in the uncorrected record (Table 3, Fig. 7). As in the δ18O composite record, large
reductions (> 0.5 ‰) in the annual maximum δ13C and the previous years 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 either same-year TAP, same- or same-andprevious-years JFMAP. Minimum annual δ13C is positively correlated with both daytime
and nighttime vapor pressure deficit (P < 0.01). Maximum and mean annual δ13C are
negatively correlated with maximum SOI (P < 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), TAP and same-and-previous years JFMAP (Table 4). The
association 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, suggesting that over monthly and annual time scales nighttime VPD is the
strongest determinant of δ13C value in spines. The link from SOI through mean nighttime
VPD to minimum annual δ13C in spines is tenuous at best. While minimum annual SOI is
significantly related to mean nighttime VPD over this time period (F23 = 8.1, P < 0.009),
the removal of one year (1983) renders the relationship non-significant (F22 = 2.5, P <
0.13). 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 greater than 0.85.
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The relationship between δ13C in spines and climate is less direct than that of δ18O in
spines. Current theoretical isotope models for saguaro suggest that VPD alters the
percentage of carbon in plant tissues derived from the C3 photosynthetic pathway and
the crassulacean acid metabolism photosynthetic pathway (CAM)(English et al., EPSL),
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. 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 < 0.0001) and same-year JFMAP (F24 =
11.8, P < 0.002). Over short periods of days to weeks, English et al. (EPSL) 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.
4. Conclusions
There is strong evidence for a relationship between the annual δ18O and δ13C
parameters 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
empirical mechanistic models of isotopic fractionation that link climatic variation to that
in cactus spines (English et al., 2007). We conclude that annual parameters of
173
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
associated 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 maximum annual
δ18O of composite records of spine δ18O; and 3) simple linear models based on the
relationship between TAP and δ18O and that account for dating errors are useful in
estimating TAP in some years but overestimated rainfall 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 1,900 to 4,000 masl along 11° of latitude in treeless
174
northern Chile/Argentina to just south of Lake Titicaca in Bolivia. This range spans a
region affected by two climate modes, but possesses only sporadic instrumental records
and annual climate proxy records 20 years old (Vuille et al. 2004). T. Atacamensis may
live to be over 300 years old (Yetman, 2008) and have large, robust spines (>10 cm) with
distinct diurnal-like banding (EPSL, N. English, pers. observation) and may contain
useful records of climate variation beyond what is available in the instrument record.
While we doubt isotopic spine-series would ever rival tree-ring records, in carefully
calibrated studies they may provide useful records of climate and ecophysiology.
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. English. We are thankful to K. Anchukaitis, T. Ault, J.
Betancourt, W. Beck, G. Bowen, J. Bower, C. Burkhardt, J. Caulkins, J. Cole, M.
Daniels ,T. Drezner, C. Eastoe, M. Evans, C. Funnicelli, Q. Hua, K. Hultine, S. Leavitt,
M. Mason, J. Mauseth, J. Pigati, B. Osmond, J. Overpeck, W. Peachy, E. Pierson, D.
Potts, , J. Quade, T. Shanahan R. Turner, and M. Weesner. All experiments comply with
the current laws of the United States and Arizona.
175
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181
Figure Captions
Figure 1. Spine height and corrected F14C age (open circles) compared to observed apical
cactus height and age (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).
Figure 2. Raw spine height and δ13C 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 ages shown in Figures 1, 3 and 4. Each δ13C tick mark is 1‰.
Figure 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 ages shown in Figures 1, 3 and 4. Each δ18O tick mark is 5‰.
Figure 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 is corrected for the
long-term decrease in atmospheric δ13C (13C Suess effect) and adjusted to the mean
series-mean (–11.3‰). 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 ages shown in Figure 1. Gray line with symbols is the raw δ13C
182
isotope spine series for comparison to the age modeled δ13C isotope spine series. Each
δ13C tick mark is 1‰.
Figure 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 is adjusted to the mean
of all series (42.4‰). 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 ages shown in Figure 1. Gray line with symbols is the raw δ18O isotope
spine series for comparison to the age modeled δ13C isotope spine series. Each δ18O tick
mark is 5‰.
Figure 6. Composite δ18O spine series with annual parameters. Bold black line in top
panel is the composite δ18O and is derived by averaging the 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 mean δ18O (Δ annual mean δ18O), * denote times in the composite record that we
associate with El Niño enhanced total annual precipitation (November through October)
and very negative SOI (< –4). Note that Δ annual mean δ18O derived from the composite
series in 1984 and 1997 appear to be one year late and one year early, respectively.
Figure 7. Composite δ13C spine record and annual parameters. Bold black line in top
panel is the composite δ13C and is derived by averaging the age modeled δ13C isotope
183
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 in the composite record that we associate with El Niño enhanced
total annual precipitation (November through October) and very negative SOI (< –4).
Note that the year-to-year change in maximum δ13C (Δ annual minimum δ13C) derived
from the composite series in 1984 and 1997 appear to be one year late and one year
early, respectively.
Figure 8. The effect of correcting misplaced years in the comparison of the mean annual
δ18O of spines and total annual precipitation (TAP) in November through October. Top
panel shows the simple linear regression (solid line) of the uncorrected δ18O composite
record against TAP. Circles and X’s 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)
between TAP and mean annual δ18O of spines. The explanatory power of TAP is
improved when 2003 is eliminated from the regression (dotted line) as well, although it
alters the relationship between TAP and mean annual δ18O very little. Equations
represent the relationship of TAP (mm) to mean annual δ18O and are used in Fig. 9 to
reconstruct TAP.
184
Figure 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.
Base
(cm)
98
115.5
110
96.5
87.5
-
Spines
in series
189
176
168
153
167
-
F14C
dates
11
4
3
4
4
Start
Date*
1974.0
1982.6
1979.4
1982.8
1980.9
1980.9
End
Date*
2006.9
2006.9
2006.9
2007.4
2007.4
2006.9
Years*
32.9
24.3
27.5
24.6
26.5
26.5
198
147
166
149
160
157
Datum in
series*
-10.98
–11.39
–11.21
–10.91
–12.12
–11.32
Mean
δ C(‰)*
13
Mean
δ O (‰)*
45.71
42.90
41.84
40.75
40.85
42.41
18
* Refers to attributes of the age modeled spine series corrected for atmospheric changes in δ13C and adjusted to a common
mean.
Series 162
Series 163
Series 168
Series 182
Series 184
Composite
Apex
(cm)
415
414
410
372
413
-
Table 1. Saguaro cactus raw and spine series attributes.
185
0.32
0.24
0.25
Annual Parameters of corrected and adjusted spine series
Maximum δ13C 5 0.23
0.60
20
Minimum δ13C 5 0.20
0.55
23
13
Mean δ C 5 0.19
0.54
24
0.70
0.61
0.63
0.76
0.59
12
18
17
9
20
1980 to 1997
t needed to
reach EPS ≥
EPS(t)
0.85
Maximum δ18O 5 0.20
0.55
23
0.21
0.57
22
18
Minimum δ O 5 0.42
0.78
8
0.15
0.48
30
Mean δ18O 5 0.29
0.67
14
0.23
0.60
19
t is the number of spine series used to calculate r, where each spine series is collected
from a different cactus.
0.39
0.22
r
1980 to 2006
t needed to
reach EPS
t
r
EPS(t)
≥ 0.85
Corrected and adjusted spine series
δ13C 5 0.30
0.68
13
18
δ O 5 0.28
0.66
15
Table 2. Mean intercactus correlation coefficients (r) and expressed population signal (EPS)
of age modeled, corrected and adjusted spine series.
186
Table 3. Uncorrected annual δ18O and δ13C correlations with annual precipitation, VPD and SOI.
Annual parameters from
Annual parameters from
18
uncorrected δ O composite record
uncorrected δ13C composite record
Annual climate
Max
Min
Mean
Max
Min
Mean Log Max δ13C
Max δ18O
18
18
18
13
13
parameters
δ O
δ O
δ O
δ C
δ C
δ13C
Difference
Difference
Precipitation
Log TAP (N-O) -0.28
-0.32
-0.42
0.02
0.34
-0.17
0.28
0.21
Log JASP -0.22
-0.11
-0.20
0.05
0.11
-0.24
0.05
0.02
Log JFMAP -0.13
-0.27
-0.32
-0.02
0.37†
-0.12
0.26
0.40*
Log 2 x JFMAP -0.27
-0.56** -0.53**
0.04
0.16
-0.29
-0.04
0.27
Nighttime vapor pressure deficit
Max nVPD 0.37†
0.36†
0.41*
0.02
-0.05
0.27
-0.07
0.00
Mean nVPD 0.37†
0.50** 0.56**
0.06
-0.20
0.37*
-0.12
-0.12
Log Min nVPD
0.27
0.05
0.24
0.21
-0.02
-0.03
-0.12
0.14
Daytime vapor pressure deficit
Max dVPD
-0.06
0.03
-0.04
0.14
0.05
-0.26
-0.05
0.10
Mean dVPD
-0.23
0.29
0.00
-0.28
-0.21
-0.08
-0.28
-0.02
Log Min dVPD
-0.01
0.59** 0.34†
-0.11
-0.35†
0.40*
-0.12
-0.41*
Southern Oscillation Index
Log Max SOI
-0.25
-0.08
-0.10
0.14
-0.40*
-0.02
-0.43*
-0.24
Log Min SOI
0.08
0.04
0.21
0.04
-0.18
0.25
-0.10
-0.22
Log Mean SOI
-0.06
-0.02
0.05
0.16
-0.25
0.29
-0.16
-0.25
TAP = Total annual precipitation measured from November to October; JASP = Total July to September
precipitation; JFMAP = Total January to April precipitation; 2 x JFMAP = same and previous year’s
JFMAP.
† P < 0.10, * P < 0.05, ** P < 0.01
187
Table 4. Corrected annual δ18O and δ13C correlations with annual precipitation, VPD and SOI.
Annual parameters from
Annual parameters from
18
corrected δ O composite record
corrected δ13C composite record
Annual climate
Max
Min
Mean
Max
Min
Mean Log Max δ13C
Max δ18O
18
18
18
13
13
parameters
δ O
δ O
δ O
δ C
δ C
δ13C
Difference
Difference
Precipitation
Log TAP (N-O) -0.69** -0.55* -0.70**
-0.44*
0.15
-0.42*
-0.03
0.20
Log JASP -0.36†
-0.16
-0.26
-0.11
0.06
-0.34†
-0.06
0.06
Log JFMAP -0.38†
-0.46* -0.53**
-0.37†
0.23
-0.24
0.06
0.38†
Log 2 x JFMA -0.48* -0.67** -0.69**
-0.19
0.06
-0.42*
-0.21
0.30
Nighttime vapor pressure deficit
Max nVPD 0.52**
0.47*
0.50**
0.32
0.03
0.35†
0.08
-0.05
Mean nVPD 0.53** 0.60** 0.63**
0.32
-0.12
0.47*
0.04
-0.15
Log Min nVPD 0.36†
0.11
0.28
0.45*
0.01
0.02
-0.02
0.05
Daytime vapor pressure deficit
Max dVPD -0.14
-0.07
-0.13
-0.09
0.01
-0.30
-0.14
0.14
Mean dVPD -0.20
0.31
0.03
-0.28
-0.20
0.00
-0.25
-0.03
Log Min dVPD
0.06
0.63**
0.37†
-0.09
-0.30
0.47*
-0.05
-0.36†
Southern Oscillation Index
Log Max SOI -0.25
-0.08
-0.09
0.08
-0.41*
0.00
-0.46*
-0.22
Log Min SOI 0.47*
0.04
0.44*
0.55**
0.18
0.41*
0.30
0.07
Log Mean SOI -0.02
-0.02
0.06
0.21
-0.17
0.30
-0.11
-0.11
TAP = Total annual precipitation measured from November to October; JASP = Total July to September
precipitation; JFMAP = Total January to April precipitation; 2 x JFMAP = same and previous year’s
JFMAP.
† P < 0.10, * P < 0.05, ** P < 0.01, Bold type = P < 0.001
188
189
Figure 1
190
Figure 2
191
Figure 3
192
Figure 4
193
Figure 5
194
Figure 6
195
Figure 7
196
Figure 8
197
Figure 9
198
This page is intentionally left blank.
199
APPENDIX D:
MOVIE OF SPINE GROWTH OVER TWO DAYS IN MAY, 2007
200
See supplemental video file.
201
APPENDIX E:
ISOTOPE DATA FROM TUMAMOC AND SAGUARO NATIONAL PARK EAST
CACTUSES
202
Carbon isotope values (VPDB) of spine tips from naturally occurring cactus near Tucson, Arizona.
Numbered cactus are from Tumamoc Hill in Tucson (32.22° N, 111.00° W, 800 m elevation) and SNPE A
is from Saguaro National Park East (Permit #SAGU-2004-SCI-0012, 32.21° N, 110.73° W, 870 m
elevation).
δ13C
162
415.0
413.0
410.0
408.0
406.0
404.5
403.0
401.5
400.0
398.0
396.5
395.0
394.0
392.0
390.5
389.0
387.5
386.0
384.0
383.0
381.5
380.0
379.0
377.0
375.5
373.0
372.0
370.0
368.5
367.0
365.7
364.0
362.7
361.0
359.5
357.5
356.0
354.8
353.5
352.0
350.5
349.0
348.0
346.5
345.0
343.0
341.0
339.5
338.0
336.5
335.0
-11.6
-11.9
-11.8
-11.5
-10.7
-10.8
-11.1
-11.3
-11.0
-10.9
-11.5
-10.6
-11.2
-10.8
-11.1
-11.3
-11.1
-11.0
-11.8
-11.6
-11.4
-11.3
-11.3
-10.9
-10.8
-11.1
-10.8
-10.9
-10.4
-11.0
-10.6
-10.5
-10.7
-10.4
-11.0
-10.7
-10.6
-10.7
-10.8
-10.6
-10.4
-11.0
-10.6
-10.1
-10.5
-10.4
-10.6
-10.7
-11.0
-10.5
-9.8
δ13C
163
414.0
412.5
411.0
410.0
409.0
407.5
405.0
403.5
402.0
400.5
399.0
397.5
396.0
394.5
393.0
391.5
390.0
388.0
387.0
385.5
384.0
382.5
381.0
379.0
377.5
376.0
374.0
372.5
371.0
369.5
368.0
366.0
364.5
363.5
362.0
360.0
358.0
356.5
354.5
353.0
351.5
350.0
348.5
347.0
345.5
344.0
342.0
341.0
339.0
338.0
336.5
-12.7
-12.3
-12.2
-12.0
-12.2
-12.1
-12.8
-12.4
-10.9
-11.0
-11.8
-11.8
-11.8
-11.5
-11.2
-11.2
-11.7
-10.4
-10.9
-10.7
-10.8
-11.5
-11.0
-11.4
-11.4
-10.9
-11.7
-12.3
-11.4
-11.6
-11.9
-11.5
-11.9
-11.8
-12.0
-11.4
-11.4
-11.2
-11.4
-11.0
-11.1
-10.8
-11.3
-11.7
-11.4
-10.5
-11.0
-11.3
-11.1
-10.9
-12.0
δ13C
168
410.0
408.5
407.0
404.0
402.0
400.0
399.0
397.0
395.0
393.0
391.5
390.0
388.0
386.5
385.0
383.0
381.0
379.0
377.0
375.0
373.5
372.0
370.0
368.5
367.0
365.0
363.5
362.0
360.0
358.0
356.0
354.5
353.0
351.0
349.5
348.0
346.0
344.0
342.5
341.0
339.5
338.0
336.0
334.0
332.0
330.0
328.0
326.5
325.0
323.0
321.5
-12.1
-11.9
-11.6
-11.3
-11.1
-11.2
-11.3
-11.5
-10.6
-10.6
-11.0
-10.8
-11.1
-10.3
-11.6
-10.7
-11.1
-11.1
-10.5
-10.4
-9.8
-10.4
-10.0
-10.5
-10.8
-10.6
-10.9
-10.8
-10.8
-10.9
-10.8
-10.7
-10.4
-10.4
-10.6
-10.9
-11.1
-10.9
-10.9
-10.6
-10.9
-11.3
-10.8
-10.7
-11.9
-11.1
-9.8
-10.4
-10.2
-10.1
-10.1
δ13C
182
372.0
370.0
368.5
367.0
365.0
363.5
361.0
359.0
357.0
355.0
353.0
351.0
349.0
347.0
345.0
343.0
341.5
339.0
337.0
335.0
333.5
331.5
330.0
328.0
326.0
324.0
323.0
321.0
319.5
318.0
316.5
315.0
313.0
311.5
310.0
308.0
306.0
304.0
302.0
300.5
299.0
297.0
295.0
294.0
292.0
290.5
289.0
287.0
285.5
284.0
282.5
-11.6
-11.3
-11.4
-10.9
-11.1
-11.0
-10.4
-10.3
-11.9
-11.0
-10.2
-9.9
-9.9
-10.4
-10.4
-10.1
-10.7
-10.6
-11.1
-11.0
-10.6
-10.3
-10.2
-11.3
-10.9
-10.9
-10.5
-10.7
-10.6
-10.8
-10.7
-11.2
-11.0
-11.7
-11.3
-11.3
-11.1
-11.5
-11.7
-11.0
-10.5
-10.5
-10.3
-11.7
-11.3
-12.1
-11.3
-10.8
-10.8
-10.7
-9.6
δ13C
184
413.0
412.0
410.0
408.0
406.0
404.0
402.0
400.0
398.0
396.0
395.0
393.0
391.0
389.0
387.5
386.0
384.0
382.0
380.0
378.0
376.0
374.0
372.0
370.0
368.0
366.0
364.0
362.0
360.0
358.0
356.5
355.0
353.0
351.0
350.0
348.0
346.0
344.0
342.0
338.0
336.0
335.0
332.5
330.0
328.5
327.0
325.0
323.5
322.0
320.0
318.5
-11.8
-11.6
-11.8
-12.2
-12.6
-12.8
-12.1
-11.5
-11.6
-11.6
-12.6
-12.4
-11.6
-11.4
-12.0
-11.6
-10.8
-11.0
-12.0
-12.4
-12.9
-12.2
-10.9
-11.6
-12.2
-12.3
-11.7
-12.2
-11.7
-12.3
-12.3
-12.0
-12.0
-12.1
-11.6
-12.6
-12.5
-12.4
-11.7
-12.4
-12.7
-12.3
-12.0
-11.7
-11.6
-11.6
-11.1
-10.7
-11.9
-11.5
-12.1
SNPE A
404.0
402.5
402.0
401.0
400.0
398.0
395.0
393.0
391.0
389.0
388.0
385.0
383.0
382.0
380.0
378.0
376.0
375.0
373.0
371.0
369.0
367.0
365.0
363.0
361.0
357.0
355.0
352.0
350.0
348.0
345.0
343.0
341.0
339.0
337.0
335.0
332.0
330.0
328.0
326.0
324.0
321.0
319.0
317.0
315.0
313.0
311.0
307.0
305.0
302.0
300.0
δ13C
-10.3
-10.3
-10.2
-10.5
-10.5
-10.7
-11.0
-11.7
-11.6
-11.8
-11.5
-11.5
-11.4
-10.7
-10.3
-10.5
-10.9
-10.3
-11.8
-12.8
-12.3
-11.4
-10.9
-10.6
-10.0
-11.7
-11.4
-11.7
-11.4
-10.9
-11.5
-10.7
-10.4
-10.5
-12.2
-12.2
-12.3
-12.3
-12.8
-12.4
-12.2
-11.5
-9.9
-11.0
-10.8
-10.5
-10.9
-10.5
-12.3
-12.3
-12.7
203
333.5
332.0
330.7
329.5
328.0
326.5
325.0
323.5
322.0
320.0
318.5
317.0
315.5
314.0
312.2
311.0
309.5
308.0
306.0
304.5
303.0
301.5
300.0
298.0
296.5
295.0
293.5
292.0
290.5
289.0
287.5
286.0
284.0
282.5
281.0
279.5
277.5
276.5
274.5
272.5
271.0
269.5
267.5
266.0
264.0
262.0
260.5
258.5
257.0
255.0
253.0
251.5
249.5
247.5
245.5
243.5
242.0
-9.8
-10.6
-10.2
-10.3
-10.6
-10.0
-10.3
-10.9
-11.1
-10.5
-10.3
-10.9
-10.7
-11.2
-11.3
-10.2
-10.5
-10.6
-9.5
-9.6
-9.6
-10.9
-10.5
-10.8
-9.5
-9.5
-9.8
-10.5
-10.0
-10.8
-10.5
-9.2
-9.3
-9.4
-10.3
-10.9
-9.9
-9.9
-9.8
-10.7
-10.4
-10.5
-10.6
-9.4
-9.5
-10.0
-10.7
-10.6
-10.6
-9.4
-10.0
-10.0
-10.2
-10.3
-9.9
-10.6
-9.7
334.5
333.0
331.5
330.0
328.0
326.5
325.0
323.0
321.5
320.0
318.5
316.5
314.5
313.0
311.0
309.0
307.5
306.0
304.0
302.5
300.5
299.0
297.0
295.5
294.0
292.0
290.5
289.0
287.0
285.5
283.5
282.0
280.0
278.5
277.0
275.5
274.0
272.0
270.5
268.5
267.0
265.0
263.0
261.5
260.0
258.0
256.0
254.0
251.5
250.0
248.0
246.0
244.0
242.5
240.5
238.5
236.0
-11.6
-11.3
-11.6
-11.2
-11.4
-11.6
-11.0
-11.7
-12.0
-11.9
-11.8
-12.2
-11.5
-11.2
-10.8
-10.6
-9.3
-9.7
-10.1
-10.1
-10.6
-11.0
-11.2
-10.9
-10.9
-10.6
-10.6
-11.8
-11.6
-11.4
-11.0
-10.9
-11.5
-11.2
-10.9
-10.9
-11.1
-11.6
-11.2
-11.3
-10.3
-9.5
-9.7
-10.4
-11.1
-11.0
-11.1
-11.1
-9.9
-10.3
-10.1
-10.4
-10.1
-10.3
-10.4
-10.9
-11.1
320.0
318.0
316.5
315.0
313.0
310.5
309.5
308.0
306.5
305.0
303.5
302.0
300.0
298.0
296.5
295.0
293.0
291.0
289.0
287.5
285.5
283.5
282.0
280.0
278.0
276.0
274.0
272.5
271.0
269.0
267.0
265.0
263.0
261.0
259.5
258.0
256.0
254.0
252.0
250.0
248.5
247.0
245.0
243.0
241.0
239.0
237.5
235.5
234.0
232.0
230.0
227.5
225.5
224.0
222.0
220.0
218.0
-10.8
-10.7
-10.7
-11.1
-11.2
-10.9
-11.4
-11.3
-11.0
-10.6
-10.9
-9.8
-11.0
-10.7
-10.6
-10.7
-11.1
-10.8
-10.8
-9.7
-10.5
-10.9
-11.8
-11.5
-10.3
-11.3
-10.5
-10.3
-10.6
-10.7
-11.8
-11.2
-10.5
-9.8
-10.8
-10.3
-9.9
-11.1
-11.7
-11.1
-11.4
-11.7
-10.7
-10.5
-10.5
-11.9
-11.3
-10.7
-10.4
-10.9
-10.6
-11.0
-11.3
-11.5
-10.9
-11.3
-10.6
280.5
278.5
277.0
275.0
273.0
271.0
269.0
267.0
265.0
263.5
262.0
260.0
258.0
256.5
255.0
253.0
251.0
249.0
247.0
245.0
243.5
242.0
240.0
238.5
237.0
235.0
233.0
231.0
229.0
227.0
225.0
223.5
221.5
220.0
218.0
216.0
214.0
212.0
210.0
208.0
206.0
204.0
202.0
200.0
198.0
196.0
194.0
192.0
190.0
188.0
186.5
185.0
182.0
181.0
179.0
177.0
175.0
-10.8
-11.4
-11.0
-11.0
-10.3
-10.8
-10.5
-10.3
-10.6
-10.6
-10.4
-10.7
-11.8
-11.0
-9.7
-9.8
-9.8
-10.4
-10.8
-11.1
-10.4
-9.5
-10.0
-9.7
-9.7
-10.3
-11.5
-10.8
-9.8
-10.1
-10.9
-11.5
-11.6
-10.5
-10.3
-10.1
-10.8
-11.1
-10.7
-10.6
-10.5
-10.7
-10.9
-10.4
-10.2
-10.2
-10.6
-10.6
-10.7
-10.5
-11.3
-10.7
-10.4
-10.9
-10.3
-9.7
-9.3
317.0
315.0
314.0
312.0
311.0
309.0
307.0
305.0
303.0
302.0
300.0
298.5
297.0
295.0
293.0
291.0
289.0
286.5
284.0
282.5
280.5
278.0
276.0
274.5
273.0
271.0
268.5
267.0
265.0
263.0
260.5
258.5
256.5
254.0
252.0
250.0
247.5
245.0
243.0
241.0
239.0
237.0
235.0
233.5
231.0
228.0
226.0
224.0
222.0
220.5
218.0
216.0
214.0
211.5
209.0
207.0
205.0
-13.1
-12.4
-11.3
-12.0
-11.5
-12.2
-12.1
-12.1
-11.6
-11.7
-11.1
-11.2
-11.3
-11.5
-11.7
-12.2
-12.3
-12.1
-12.4
-11.9
-12.2
-11.5
-11.3
-11.1
-11.3
-11.8
-13.0
-12.7
-11.8
-11.3
-11.3
-12.5
-12.3
-11.6
-11.9
-11.8
-12.8
-12.2
-11.9
-11.3
-10.9
-11.0
-10.9
-12.2
-13.0
-11.8
-11.5
-11.0
-11.6
-11.5
-13.0
-11.9
-12.5
-11.0
-10.6
-11.0
-12.6
298.0
295.0
293.0
291.0
289.0
286.0
284.0
282.0
280.0
277.0
275.0
272.0
270.0
268.0
265.0
262.0
260.0
255.0
253.0
250.0
248.0
245.0
243.0
241.0
238.0
235.0
232.0
230.0
227.0
225.0
222.0
220.0
218.0
215.0
213.0
208.0
206.0
203.0
201.0
198.0
196.0
193.0
191.0
189.0
186.0
184.0
181.0
179.0
177.0
174.0
172.0
169.0
167.0
165.0
162.0
157.0
155.0
-11.8
-11.6
-11.8
-11.1
-10.7
-11.5
-11.3
-11.1
-10.8
-11.2
-12.6
-13.3
-12.7
-12.7
-12.1
-13.4
-11.1
-10.2
-10.5
-11.3
-12.1
-12.0
-10.7
-11.4
-10.2
-10.3
-10.3
-10.5
-9.8
-11.9
-11.7
-12.1
-10.8
-12.5
-10.6
-12.9
-12.7
-11.8
-11.3
-10.3
-11.1
-10.3
-11.0
-12.7
-12.5
-12.7
-12.1
-11.3
-10.5
-10.3
-11.2
-11.3
-11.3
-12.5
-12.0
-11.1
-11.4
204
240.0
238.5
236.5
235.0
231.0
229.0
227.0
225.5
224.0
222.0
220.0
218.5
216.5
214.5
213.0
211.0
209.0
207.0
205.5
203.5
202.0
200.5
197.0
195.0
193.0
191.0
189.5
187.5
186.0
184.0
182.5
181.0
179.0
177.0
175.5
173.5
172.0
170.0
168.0
166.5
162.0
161.5
160.5
158.5
156.5
155.0
153.5
151.0
149.5
148.0
146.0
144.5
142.5
141.0
139.0
137.5
136.0
-9.2
-9.1
-9.2
-9.4
-10.7
-10.4
-10.0
-8.8
-9.8
-9.0
-10.5
-11.0
-10.5
-10.8
-10.6
-8.9
-9.6
-10.2
-10.6
-10.6
-10.7
-10.7
-11.0
-10.1
-11.0
-9.8
-9.7
-9.3
-10.8
-11.1
-10.8
-10.7
-9.4
-9.6
-11.1
-10.8
-10.8
-10.8
-10.8
-10.6
-10.6
-10.2
-11.7
-10.8
-10.4
-11.4
-11.3
-11.8
-10.8
-10.5
-10.6
-10.7
-10.1
-10.9
-10.9
-10.7
-10.5
234.0
232.5
231.0
229.0
227.5
226.0
224.0
222.0
220.0
218.5
217.0
215.5
214.0
212.0
210.0
208.0
206.0
204.0
202.5
201.0
199.0
197.0
195.0
193.0
191.0
189.5
188.0
186.0
184.0
182.0
180.0
179.0
177.0
175.0
173.0
171.0
169.0
167.0
165.0
163.0
161.5
160.0
158.0
157.0
155.0
153.0
151.5
150.0
148.0
146.0
145.0
142.0
140.5
139.0
137.5
136.0
134.0
-9.6
-10.6
-10.2
-9.5
-11.0
-11.1
-11.3
-11.3
-10.5
-10.3
-9.8
-9.0
-9.4
-11.0
-11.2
-10.6
-11.0
-10.8
-10.3
-10.5
-11.5
-11.0
-10.8
-11.2
-11.4
-10.6
-10.5
-10.0
-10.0
-11.3
-11.5
-10.9
-11.5
-10.5
-10.5
-11.1
-11.1
-11.8
-11.0
-11.0
-10.0
-10.1
-10.1
-11.8
-12.1
-10.5
-10.6
-9.5
-9.6
-10.8
-11.4
-11.0
-10.5
-11.0
-11.0
-10.2
-11.1
216.0
214.0
212.0
210.0
208.0
206.5
205.0
203.0
201.0
199.5
197.5
196.0
194.0
192.5
191.0
189.0
187.0
185.0
183.0
181.5
179.5
177.5
175.0
173.0
171.0
169.0
167.5
165.0
163.5
161.5
160.0
158.0
156.5
155.0
153.0
151.0
149.5
147.5
146.0
144.0
142.0
140.5
139.0
137.0
135.5
134.0
132.0
130.0
128.0
126.5
125.0
123.0
122.0
120.0
118.5
117.0
115.0
-10.6
-11.8
-12.2
-11.7
-10.5
-10.3
-10.4
-10.8
-11.5
-10.9
-10.5
-10.8
-10.6
-10.7
-11.9
-11.5
-10.4
-10.1
-9.9
-11.7
-11.5
-10.4
-10.6
-10.8
-10.8
-11.2
-11.0
-11.4
-11.0
-10.8
-11.0
-11.3
-11.7
-11.0
-11.2
-10.3
-10.1
-10.3
-11.4
-10.6
-10.1
-10.2
-9.6
-11.4
-11.5
-10.8
-10.5
-9.7
-11.4
-11.0
-11.1
-11.2
-10.8
-11.1
-10.5
-10.6
-10.9
173.5
171.5
169.0
167.5
165.5
164.0
162.0
160.0
158.0
156.5
155.0
153.0
151.0
149.0
147.0
145.0
143.5
142.0
140.0
138.5
137.0
135.5
134.0
132.5
131.0
129.0
127.0
125.5
124.0
122.0
120.5
118.5
117.0
115.0
114.0
112.0
110.5
109.0
107.0
105.5
103.5
102.0
100.5
98.0
96.5
-9.8
-11.3
-10.7
-10.2
-10.0
-10.4
-10.3
-10.4
-10.3
-10.2
-10.5
-10.4
-10.6
-10.2
-10.5
-10.4
-10.0
-10.0
-10.6
-11.2
-9.7
-9.9
-10.0
-11.1
-10.5
-9.7
-9.7
-10.3
-9.5
-9.9
-10.0
-10.4
-10.6
-10.4
-9.4
-9.9
-10.6
-9.4
-9.0
-9.1
-10.1
-10.0
-10.2
-9.2
-9.5
203.0
201.0
198.5
196.0
194.0
192.0
190.0
188.0
186.0
184.0
182.0
180.0
177.5
175.0
173.0
171.0
168.5
166.5
164.0
162.0
160.0
158.0
156.0
154.0
152.0
150.0
148.0
145.0
144.0
142.0
139.5
137.0
136.0
134.0
132.5
131.0
129.0
127.0
125.0
123.0
121.0
119.0
117.0
115.5
113.5
112.0
110.0
108.0
105.5
104.0
101.0
99.5
97.0
96.0
94.5
92.5
91.0
-12.9
-12.9
-11.6
-11.6
-11.8
-11.6
-11.8
-11.9
-12.0
-11.5
-11.5
-11.5
-12.0
-12.6
-12.0
-11.0
-11.0
-11.4
-11.6
-11.9
-11.4
-11.8
-10.8
-11.7
-11.8
-10.9
-11.7
-11.5
-12.0
-11.0
-10.4
-10.9
-11.6
-12.1
-11.1
-11.3
-11.7
-11.3
-10.9
-10.8
-11.8
-10.7
-11.5
-10.7
-11.6
-11.7
-10.8
-11.2
-12.3
-11.3
-10.5
-12.1
-11.8
-11.9
-11.7
-10.7
-11.6
152.0
150.0
147.0
145.0
143.0
140.0
138.0
135.0
133.0
130.0
128.0
126.0
124.0
123.0
121.0
118.0
116.0
114.0
112.0
108.0
105.0
103.0
100.0
98.0
95.0
93.0
90.0
88.0
86.0
84.0
81.0
80.0
77.0
75.0
72.0
70.0
68.0
65.0
63.0
61.0
57.0
55.0
53.0
51.0
49.0
47.0
44.0
42.0
40.0
39.0
36.0
34.0
33.0
31.0
29.0
27.0
25.0
-11.2
-11.9
-11.4
-12.6
-11.5
-12.0
-12.1
-11.2
-11.8
-11.3
-11.2
-12.2
-12.0
-11.7
-11.3
-10.7
-10.7
-10.8
-10.5
-12.8
-12.3
-10.5
-10.7
-12.8
-12.4
-12.1
-11.7
-10.9
-11.3
-12.6
-11.9
-11.3
-11.1
-11.0
-10.7
-11.5
-12.8
-11.2
-11.4
-11.4
-10.4
-12.5
-12.6
-10.8
-11.1
-11.5
-11.8
-11.9
-11.7
-11.5
-11.5
-9.9
-10.2
-11.2
-10.8
-9.8
-10.1
205
135.0
133.5
132.0
130.0
128.0
126.5
125.0
123.0
121.5
120.0
118.0
116.5
115.0
113.0
111.5
109.5
108.0
106.5
105.0
103.5
102.5
101.0
99.5
98.0
96.5
95.0
93.0
91.5
90.0
88.5
87.0
-10.5
-10.6
-11.7
-10.3
-11.2
-10.3
-9.9
-10.8
-10.9
-10.6
-10.1
-10.6
-10.3
-10.5
-10.6
-9.3
-9.7
-9.9
-9.6
-10.2
-9.7
-9.9
-9.9
-10.9
-10.1
-9.3
-9.6
-9.4
-10.1
-10.2
-9.9
132.0
130.5
129.0
127.0
125.5
123.5
122.0
120.0
118.5
117.0
115.5
-11.2
-11.2
-10.0
-10.4
-9.7
-9.8
-11.0
-10.6
-10.0
-11.2
-10.7
113.0
111.5
110.0
-10.5
-10.6
-10.6
89.0
87.5
-11.9
-10.5
23.0
21.0
20.0
18.0
16.0
14.0
12.0
-11.0
-11.8
-9.8
-10.3
-11.6
-12.2
-11.2
Oxygen isotope values (VSMOW) of spine tips from naturally occurring cactus near Tucson, Arizona.
Numbered cactus are from Tumamoc Hill in Tucson (32.22° N, 111.00° W, 800 m elevation) and SNPE A
is from Saguaro National Park East (Permit #SAGU-2004-SCI-0012, 32.21° N, 110.73° W, 870 m
elevation).
δ18O
162
415.0
413.0
410.0
408.0
406.0
404.5
403.0
401.5
400.0
398.0
396.5
395.0
394.0
392.0
390.5
389.0
387.5
386.0
384.0
383.0
45.3
45.8
46.3
41.3
42.1
42.4
42.6
41.4
49.9
50.0
48.9
50.6
49.1
46.7
46.5
45.5
46.0
46.2
46.1
46.7
δ18O
163
414.0
412.5
411.0
410.0
409.0
407.5
405.0
403.5
402.0
400.5
399.0
397.5
396.0
394.5
393.0
391.5
390.0
388.0
387.0
385.5
40.7
43.1
43.9
46.1
45.5
45.3
47.3
38.9
42.6
41.9
42.0
41.2
43.8
41.0
47.8
42.2
47.4
51.1
51.7
50.0
δ18O
168
410.0
408.5
407.0
404.0
402.0
400.0
399.0
397.0
395.0
393.0
391.5
390.0
388.0
386.5
385.0
383.0
381.0
379.0
377.0
375.0
38.0
38.3
45.2
43.1
44.5
42.3
39.4
39.7
41.4
39.5
44.7
41.1
41.4
41.3
43.2
45.9
44.9
46.6
49.6
49.0
δ18O
182
372.0
370.0
368.5
367.0
365.0
363.5
361.0
359.0
357.0
355.0
353.0
351.0
349.0
347.0
345.0
343.0
341.5
339.0
337.0
335.0
37.9
36.9
37.4
37.5
40.2
41.3
40.2
41.8
37.9
38.4
38.0
39.8
40.8
37.4
39.6
38.8
41.5
42.4
44.4
44.3
δ18O
184
413.0
412.0
410.0
408.0
406.0
404.0
402.0
400.0
398.0
396.0
395.0
393.0
391.0
389.0
387.5
386.0
384.0
382.0
380.0
378.0
41.4
42.7
41.6
36.7
36.7
36.8
40.0
42.8
40.9
44.5
48.1
37.9
39.0
41.3
39.0
41.4
39.8
40.4
38.9
46.9
SNPE A
404.0
402.5
402.0
401.0
400.0
398.0
395.0
393.0
391.0
389.0
388.0
385.0
383.0
382.0
380.0
378.0
376.0
375.0
373.0
371.0
δ18O
46.0
45.0
43.8
43.1
47.5
43.7
40.8
40.1
39.9
40.4
42.2
42.0
42.8
43.3
50.5
51.3
45.7
49.2
43.3
45.3
206
381.5
380.0
379.0
377.0
375.5
373.0
372.0
370.0
368.5
367.0
365.7
364.0
362.7
361.0
359.5
357.5
356.0
354.8
353.5
352.0
350.5
349.0
348.0
346.5
345.0
343.0
341.0
339.5
338.0
336.5
335.0
333.5
332.0
330.7
329.5
328.0
326.5
325.0
323.5
322.0
320.0
318.5
317.0
315.5
314.0
312.2
311.0
309.5
308.0
306.0
304.5
303.0
301.5
300.0
298.0
296.5
295.0
46.1
43.3
49.7
45.8
47.4
46.4
47.4
48.1
43.5
45.7
43.4
46.1
46.4
46.1
46.6
39.2
40.0
41.7
41.6
42.0
42.4
45.1
44.1
46.9
47.7
47.5
47.4
46.7
45.6
47.4
48.3
47.0
44.4
46.2
46.8
47.9
45.6
38.7
40.9
41.9
44.3
44.5
48.3
47.0
48.8
46.5
44.2
43.1
43.9
46.2
47.1
45.8
46.1
44.3
43.8
45.1
43.0
384.0
382.5
381.0
379.0
377.5
376.0
374.0
372.5
371.0
369.5
368.0
366.0
364.5
363.5
362.0
360.0
358.0
356.5
354.5
353.0
351.5
350.0
348.5
347.0
345.5
344.0
342.0
341.0
339.0
338.0
336.5
334.5
333.0
331.5
330.0
328.0
326.5
325.0
323.0
321.5
320.0
318.5
316.5
314.5
313.0
311.0
309.0
307.5
306.0
304.0
302.5
300.5
299.0
297.0
295.5
293.5
292.0
51.3
50.1
49.3
49.9
49.4
47.4
44.9
47.5
48.5
48.8
47.8
46.7
45.0
39.6
38.0
40.5
41.0
39.3
39.7
41.1
40.8
41.1
37.8
37.2
38.1
41.4
40.9
40.8
41.0
41.2
35.9
36.3
35.9
34.6
35.2
36.8
37.5
36.6
37.9
38.7
38.5
37.8
38.6
39.9
41.4
42.4
45.6
49.2
48.0
47.0
46.2
44.6
40.7
42.9
45.6
46.1
47.8
373.5
372.0
370.0
368.5
367.0
365.0
363.5
362.0
360.0
358.0
356.0
354.5
353.0
351.0
349.5
348.0
346.0
344.0
342.5
341.0
339.5
338.0
336.0
334.0
332.0
330.0
328.0
326.5
325.0
323.0
321.5
320.0
318.0
316.5
315.0
313.0
311.0
309.5
308.0
306.5
305.0
303.5
302.0
300.0
298.0
296.5
295.0
293.0
291.0
289.0
287.5
285.5
283.5
282.0
280.0
278.0
276.0
49.6
48.4
46.4
44.3
43.6
43.6
42.8
43.5
41.1
43.4
42.3
45.2
45.8
43.8
42.8
43.0
38.2
37.1
37.7
36.9
39.8
38.9
39.1
40.1
39.0
39.5
45.3
49.0
45.0
43.1
40.9
42.0
41.9
42.0
39.7
39.6
39.9
41.2
40.4
41.4
44.7
43.0
42.9
35.3
35.8
34.4
35.9
37.4
43.2
44.0
43.9
45.6
37.6
38.4
40.2
41.8
41.1
333.5
331.5
330.0
328.0
326.0
324.5
323.0
321.0
319.5
318.0
316.5
315.0
313.0
311.5
310.0
308.0
306.0
304.0
302.0
300.5
299.0
297.0
295.0
294.0
292.0
290.5
289.0
287.0
285.5
284.0
282.5
280.5
278.5
277.0
275.0
273.0
271.0
269.0
267.0
265.0
263.5
262.0
260.0
258.0
256.5
255.0
253.0
251.0
249.0
247.0
245.0
243.5
242.0
240.0
238.5
237.0
235.0
46.5
42.8
40.8
41.5
42.3
40.1
41.2
41.9
43.5
44.2
45.9
43.9
41.0
40.4
38.9
37.3
40.1
39.4
40.0
39.1
39.5
41.3
38.9
38.6
37.0
39.8
38.3
39.4
35.1
38.7
40.3
39.2
43.4
39.4
36.4
39.6
37.2
37.9
41.6
40.0
40.0
43.3
37.4
38.6
40.9
44.5
44.1
41.9
41.3
41.2
39.8
41.2
44.6
35.7
45.1
44.8
39.6
376.0
374.0
372.0
370.0
368.0
366.0
364.0
362.0
360.0
358.0
356.5
355.0
353.0
351.0
350.0
348.0
346.0
344.0
342.0
338.0
336.0
335.0
332.5
330.0
328.5
327.0
325.0
323.5
322.0
320.0
318.5
317.0
315.0
314.0
312.0
311.0
309.0
307.0
305.0
303.5
302.0
300.0
298.5
297.0
295.0
293.0
291.0
289.0
286.5
284.0
282.5
280.5
278.0
276.0
274.5
273.0
271.0
47.7
48.8
46.1
42.9
42.8
41.8
42.9
43.3
42.6
42.3
41.8
44.3
45.7
46.5
46.6
39.3
38.5
38.9
40.5
41.6
40.1
38.6
43.0
44.2
45.5
47.1
45.3
43.1
42.8
42.3
43.6
40.8
41.0
43.5
41.9
41.4
34.2
35.0
34.9
34.8
36.7
37.6
41.8
43.5
44.9
45.3
36.7
36.3
37.2
36.7
39.0
39.1
39.8
42.0
41.0
42.0
42.1
369.0
367.0
365.0
363.0
361.0
357.0
355.0
352.0
350.0
348.0
345.0
343.0
341.0
339.0
337.0
335.0
332.0
330.0
328.0
326.0
324.0
321.0
319.0
317.0
315.0
313.0
311.0
307.0
305.0
302.0
300.0
298.0
295.0
293.0
291.0
289.0
286.0
284.0
282.0
280.0
277.0
275.0
272.0
270.0
268.0
265.0
262.0
260.0
255.0
253.0
250.0
248.0
245.0
243.0
241.0
238.0
235.0
41.2
41.0
42.6
44.3
47.2
40.1
41.4
39.9
40.9
42.2
44.2
43.7
45.5
40.8
38.4
37.0
38.9
40.5
39.3
41.7
42.7
44.1
44.2
43.4
45.0
44.3
44.4
43.8
44.5
34.8
34.6
36.0
35.3
34.2
34.7
41.8
42.3
40.8
41.3
43.0
42.9
34.8
35.8
34.8
35.1
35.4
36.5
40.2
40.2
41.8
39.3
38.4
40.1
41.2
45.0
46.0
207
293.5
292.0
290.5
289.0
287.5
286.0
284.0
282.5
281.0
279.5
277.5
276.5
274.5
272.5
271.0
269.5
267.5
266.0
264.0
262.0
260.5
258.5
257.0
255.0
253.0
251.5
249.5
247.5
245.5
243.5
242.0
240.0
238.5
236.5
235.0
231.0
229.0
227.0
225.5
224.0
222.0
220.0
218.5
216.5
214.5
213.0
211.0
209.0
207.0
205.5
203.5
202.0
200.5
197.0
195.0
193.0
191.0
42.3
42.7
43.4
46.4
49.1
48.8
47.8
46.6
43.0
43.7
45.2
43.6
46.1
45.0
45.3
49.7
47.7
46.9
49.5
47.2
44.3
43.8
43.6
47.6
48.1
47.7
47.8
50.7
47.8
43.8
46.2
48.3
45.1
45.4
45.5
43.5
43.5
46.7
49.2
47.7
48.2
42.9
41.8
43.1
43.9
43.9
47.2
48.7
37.7
41.0
42.5
44.4
43.2
41.0
42.2
44.9
47.9
290.5
289.0
287.0
285.5
283.5
282.0
279.5
278.5
277.0
275.5
274.0
272.0
270.5
268.5
267.0
265.0
263.0
261.5
260.0
258.0
256.0
254.0
251.5
250.0
248.0
246.0
244.0
242.5
240.5
238.5
236.0
234.0
232.5
231.0
229.0
227.5
226.0
224.0
222.0
220.0
218.5
217.0
215.5
214.0
212.0
210.0
208.0
206.0
204.0
202.5
201.0
199.0
197.0
195.0
193.0
191.0
189.5
43.8
47.2
38.0
38.7
40.4
40.4
39.3
43.9
44.0
44.4
44.9
40.9
38.8
40.9
42.5
43.6
42.9
40.6
38.9
38.1
39.0
41.7
43.5
42.3
41.5
43.9
41.7
41.4
39.6
40.0
42.6
47.0
46.3
46.1
47.7
36.3
37.8
39.4
38.8
39.8
44.5
46.3
47.0
51.3
40.6
41.0
42.7
45.5
46.6
48.4
48.8
45.3
38.6
40.8
41.5
45.5
45.9
274.0
272.5
271.0
269.0
267.0
265.0
263.0
261.0
259.5
258.0
256.0
254.0
252.0
250.0
248.5
247.0
245.0
243.0
241.0
239.0
237.5
235.5
234.0
232.0
230.0
227.5
225.5
224.0
222.0
220.0
218.0
216.0
214.0
212.0
210.0
208.0
206.5
205.0
203.0
201.0
199.5
197.5
196.0
194.0
192.5
191.0
189.0
187.0
185.0
183.0
181.5
179.5
177.5
175.0
173.0
171.0
169.0
41.6
42.1
42.4
42.3
39.1
42.1
48.6
46.5
46.9
45.1
45.4
37.7
38.0
44.6
44.6
46.1
48.6
47.3
47.2
35.9
38.1
43.2
44.4
43.2
41.1
39.5
39.4
43.2
40.7
44.3
44.8
45.6
36.1
39.3
37.7
44.2
44.2
47.4
45.7
40.2
41.4
40.7
39.3
40.2
39.5
37.4
38.1
45.1
46.2
45.1
37.5
39.2
36.7
41.7
41.8
41.8
39.9
233.0
231.0
229.0
227.0
225.0
223.5
221.5
220.0
218.0
216.0
214.0
212.0
210.0
208.0
206.0
204.0
202.0
200.0
198.5
196.0
194.0
192.5
190.0
188.0
186.5
185.0
182.5
181.0
179.0
177.0
175.0
173.5
171.5
169.0
167.5
165.5
164.0
162.0
160.0
158.0
156.5
155.0
153.0
151.0
149.0
147.0
145.0
143.5
142.0
140.0
138.5
137.0
135.5
134.0
132.5
131.0
129.0
39.3
43.0
44.3
42.7
37.3
37.0
42.5
41.6
40.8
39.4
40.2
42.2
41.6
42.1
42.6
45.8
39.8
42.6
42.1
41.3
37.3
42.7
39.1
39.9
39.5
38.1
39.7
38.5
39.2
42.8
43.8
43.8
36.7
36.5
40.0
41.7
40.1
40.0
40.4
39.5
48.1
39.3
41.0
41.7
49.6
39.7
43.1
42.7
46.6
38.7
39.8
41.0
40.2
40.3
39.6
40.8
34.9
268.5
267.0
265.0
263.0
260.5
258.5
256.5
254.0
252.0
250.0
247.5
245.0
243.0
241.0
239.0
237.0
235.0
233.0
231.0
228.0
226.0
224.0
222.0
220.0
218.0
216.0
214.0
211.5
209.0
207.0
205.0
203.0
201.0
198.5
196.0
194.0
192.0
190.0
188.0
186.0
184.0
182.0
180.0
177.5
175.0
173.0
171.0
168.5
166.5
164.0
162.0
160.0
158.0
156.0
154.0
152.0
150.0
38.7
39.7
41.1
41.3
46.8
38.2
38.5
41.5
44.9
47.3
35.8
35.4
35.8
40.3
43.1
42.8
43.2
39.3
40.0
41.1
43.8
45.1
46.7
46.3
37.1
37.1
40.7
45.1
45.4
45.3
38.3
37.1
38.4
39.2
40.1
38.9
38.5
38.7
37.4
37.1
38.9
40.3
41.5
35.6
36.2
34.5
35.7
42.0
41.0
41.4
38.4
39.6
40.4
43.8
41.6
43.0
44.3
232.0
230.0
227.0
225.0
222.0
220.0
218.0
215.0
213.0
208.0
206.0
203.0
201.0
198.0
196.0
193.0
191.0
189.0
186.0
184.0
181.0
179.0
177.0
174.0
172.0
169.0
167.0
165.0
162.0
157.0
155.0
152.0
150.0
147.0
145.0
143.0
140.0
138.0
135.0
133.0
130.0
128.0
126.0
124.0
123.0
121.0
118.0
116.0
114.0
112.0
108.0
105.0
103.0
100.0
98.0
95.0
93.0
45.1
43.9
44.4
37.0
42.3
42.0
41.8
44.1
46.9
36.1
36.6
37.9
40.9
41.3
41.6
37.8
39.2
40.0
39.7
45.3
44.0
41.5
39.1
40.6
34.5
36.4
40.4
38.4
38.2
35.6
36.1
34.3
36.4
35.4
36.5
40.4
36.4
37.0
36.4
37.8
38.0
41.3
41.5
43.2
38.9
37.4
35.5
31.8
33.1
38.0
45.1
37.1
37.7
38.2
208
189.5
187.5
186.0
184.0
182.5
181.0
179.0
177.0
175.5
173.5
172.0
170.0
168.0
166.5
162.0
161.5
160.5
158.5
156.5
155.0
153.5
152.0
149.5
147.5
146.0
144.5
142.5
141.0
139.0
137.5
136.0
135.0
133.5
132.0
130.0
128.0
126.5
125.0
123.0
121.5
120.0
118.0
116.5
115.0
113.0
111.5
109.5
108.0
106.5
105.0
103.5
102.5
101.0
99.5
98.0
47.6
48.6
40.9
43.5
44.9
45.5
49.7
48.0
42.2
45.1
45.2
47.4
47.7
46.6
43.8
46.7
46.7
47.1
47.3
40.3
42.9
39.0
44.2
45.4
46.3
45.4
44.2
44.3
43.0
48.2
46.5
47.2
44.4
43.0
43.9
42.8
50.8
51.4
46.7
43.8
43.6
46.9
48.1
47.9
43.1
42.5
49.3
47.6
50.4
41.8
40.7
49.9
52.9
55.0
47.0
188.0
186.0
184.0
182.0
180.0
179.0
177.0
175.0
173.0
171.0
169.0
167.0
165.0
163.0
161.5
160.0
158.0
157.0
155.0
153.0
151.5
150.0
148.0
146.0
145.0
142.0
140.5
139.0
137.5
136.0
134.0
132.0
130.5
129.0
127.0
125.5
123.5
122.0
120.0
118.5
117.0
115.5
44.9
45.4
45.9
39.1
40.7
41.1
45.0
46.0
45.3
37.9
38.7
39.9
41.3
44.8
47.0
47.6
45.8
38.5
39.5
39.2
40.6
50.3
38.8
34.1
34.6
35.4
36.9
35.1
40.0
47.9
37.0
38.6
39.3
40.7
46.9
50.3
48.7
47.6
38.1
48.6
41.2
43.4
167.5
164.5
163.5
161.5
160.0
158.0
156.5
155.0
153.0
151.0
149.5
147.5
146.0
144.0
142.0
140.5
139.0
137.0
135.5
134.0
132.0
130.0
128.0
126.5
125.0
123.0
122.0
120.0
118.5
117.0
115.0
113.0
111.5
110.0
41.5
46.3
47.9
43.2
40.4
41.2
37.9
37.7
42.0
47.1
43.0
43.0
36.7
49.7
44.3
42.6
43.3
36.9
37.1
39.7
45.4
46.2
36.8
37.5
40.1
34.2
33.3
34.7
35.6
39.2
37.1
35.9
41.4
37.4
127.0
125.0
124.0
122.0
120.5
118.5
117.0
115.0
114.0
112.0
110.5
109.0
107.0
105.5
103.5
102.0
100.5
98.0
96.5
45.0
37.1
42.3
40.9
41.7
34.3
34.8
39.5
44.6
34.3
36.5
42.4
42.5
43.2
36.2
37.9
38.4
45.2
40.4
148.0
145.0
144.0
142.0
139.5
137.0
136.0
134.0
132.5
131.0
129.0
127.0
125.0
123.0
121.0
119.0
117.0
115.5
113.5
112.0
110.0
108.0
105.5
104.0
102.0
101.0
99.5
97.0
96.0
94.5
92.5
91.0
89.0
87.0
35.9
37.8
40.3
45.9
45.0
45.4
37.9
37.2
42.9
47.3
35.8
38.2
39.6
41.3
37.4
38.2
41.6
43.8
33.9
35.4
36.4
40.3
34.6
36.5
37.7
44.4
38.2
36.4
37.2
39.2
44.7
38.2
37.4
43.0
90.0
88.0
86.0
84.0
81.0
80.0
77.0
75.0
72.0
39.9
41.5
42.1
35.0
35.7
37.6
39.9
42.0
42.6
209
Estimated date of growth and isotope value of spine material from Cactus TH42
(Diurnal spine time series) in Tucson, Arizona (Tumamoc Hill 32.22° N, 111.00° W,
820 m elevation). Carbon and Oxygen isotope values are VPDB and VSMOW,
respectively.
Spine 1
1-1
1-2
1-3
1-4
1-5
1-6
1-7
1-8
1-9
1-10
1-11
1-12
1-13
1-14
1-15
1-16
1-17
1-18
1-19
1-20
1-21
1-22
1-23
1-24
1-25
1-26
Est. Date
8/1/06
8/2/06
8/3/06
8/4/06
8/5/06
8/6/06
8/7/06
8/8/06
8/9/06
8/10/06
8/11/06
8/12/06
8/13/06
8/14/06
8/15/06
8/16/06
8/17/06
8/18/06
8/19/06
8/20/06
8/21/06
8/22/06
8/23/06
8/24/06
8/25/06
8/26/06
δ13C
-12.9
-12.1
-11.6
-12.1
-11.9
-12.3
-12.1
-12.1
-11.8
-12.2
-12.3
-12.3
-12.5
-12.7
-12.6
-12.6
-12.4
-12.5
-11.9
-12.0
-11.6
-12.3
-12.6
-13.0
-13.0
-12.6
Spine 2
2-1
2-2
2-3
2-4
2-5
2-6
2-7
2-8
2-9
2-10
2-11
2-12
2-13
2-14
2-15
2-16
2-17
2-18
2-19
-2-20
-2-21
-2-22
-2-23
-2-24
-2-25
-2-26
-2-27
-2-28
-2-29
-2-30
-2-31
-2-32
-2-33
-2-34
-2-35
-2-36
-2-37
-2-38
-2-39
-2-40
Est. Date
7/27/06
7/28/06
7/29/06
7/30/06
7/31/06
8/1/06
8/2/06
8/3/06
8/4/06
8/5/06
8/6/06
8/7/06
8/8/06
8/9/06
8/10/06
8/11/06
8/12/06
8/13/06
8/14/06
8/15/06
8/16/06
8/17/06
8/18/06
8/19/06
8/20/06
8/21/06
8/22/06
8/23/06
8/24/06
8/25/06
8/26/06
8/27/06
8/28/06
8/29/06
8/30/06
8/31/06
9/1/06
9/2/06
9/3/06
9/4/06
δ13C
-12.7
-12.4
-11.9
-11.7
-11.9
-12.3
-12.3
-12.2
-12.0
-12.1
-12.4
-12.3
-12.4
-12.4
-12.5
-12.6
-12.7
-12.8
-12.9
-12.5
-12.3
-12.7
-13.0
-12.4
-12.1
-11.8
-12.4
-12.6
-13.0
-12.9
-12.8
-12.4
-11.9
-12.0
-12.1
-12.1
-12.1
-12.5
-12.6
-13.3
Spine 3
31
32
33
34
35
36
37
38
39
3 10
3 11
3 12
3 13
3 14
3 15
3 16
3 17
3 18
3 19
3 20
3 21
3 22
3 23
3 24
3 25
3 26
3 27
3 28
3 29
3 30
3 31
3 32
3 33
3 34
3 35
3 36
3 37
3 38
3 39
3 40
Est. Date
8/11/06
8/12/06
8/13/06
8/14/06
8/15/06
8/16/06
8/17/06
8/18/06
8/19/06
8/20/06
8/21/06
8/22/06
8/23/06
8/24/06
8/25/06
8/26/06
8/27/06
8/28/06
8/29/06
8/30/06
8/31/06
9/1/06
9/2/06
9/3/06
9/4/06
9/5/06
9/6/06
9/7/06
9/8/06
9/9/06
9/10/06
9/11/06
9/12/06
9/13/06
9/14/06
9/15/06
9/16/06
9/17/06
9/18/06
9/19/06
δ13C
-12.2
-12.2
-12.3
-12.7
-12.5
-12.4
-12.2
-11.9
-11.5
-11.7
-11.7
-12.2
-12.5
-12.6
-12.4
-12.5
-12.2
-11.8
-11.8
-11.7
-11.8
-11.9
-12.0
-12.0
-12.7
-13.1
-13.1
-12.3
-12.0
-12.1
-11.8
-11.4
-11.6
-11.7
-11.5
-11.5
-11.3
-11.3
-11.3
210
-2-41
-2-42
-2-43
-2-44
-2-45
-2-46
-2-47
-2-48
-2-49
-2-50
-2-51
-2-52
Spine 1
1-1
1-2
1-3
1-4
1-5
1-6
1-7
1-8
1-9
1-10
1-11
1-12
1-13
1-14
1-15
1-16
1-17
1-18
1-19
1-20
1-21
1-22
1-23
1-24
1-25
1-26
Est. Date
8/1/06
8/2/06
8/3/06
8/4/06
8/5/06
8/6/06
8/7/06
8/8/06
8/9/06
8/10/06
8/11/06
8/12/06
8/13/06
8/14/06
8/15/06
8/16/06
8/17/06
8/18/06
8/19/06
8/20/06
8/21/06
8/22/06
8/23/06
8/24/06
8/25/06
8/26/06
δ18O
37.5
36.9
35.4
35.3
35.2
34.6
34.6
35.3
35.2
33.4
33.6
33.5
33.5
34.1
34.0
34.2
34.4
33.1
34.1
33.8
33.9
34.6
34.8
34.5
Spine 2
2-1
2-2
2-3
2-4
2-5
2-6
2-7
2-8
2-9
2-10
2-11
2-12
2-13
2-14
2-15
2-16
2-17
2-18
2-19
2-20
2-21
2-22
2-23
2-24
2-25
2-26
2-27
2-28
2-29
2-30
9/5/06
9/6/06
9/7/06
9/8/06
9/9/06
9/10/06
9/11/06
9/12/06
9/13/06
9/14/06
9/15/06
9/16/06
Est. Date
7/27/06
7/28/06
7/29/06
7/30/06
7/31/06
8/1/06
8/2/06
8/3/06
8/4/06
8/5/06
8/6/06
8/7/06
8/8/06
8/9/06
8/10/06
8/11/06
8/12/06
8/13/06
8/14/06
8/15/06
8/16/06
8/17/06
8/18/06
8/19/06
8/20/06
8/21/06
8/22/06
8/23/06
8/24/06
8/25/06
-13.6
-12.7
-12.4
-12.2
-12.3
-12.0
-12.1
-11.8
-12.2
-12.1
-12.0
δ18O
37.0
37.2
36.4
36.5
34.9
34.9
35.1
34.9
34.0
35.3
34.5
33.9
33.4
34.0
33.8
33.4
34.4
34.3
34.1
34.0
34.0
34.0
34.3
35.0
34.9
35.1
35.2
3 41
3 42
3 43
3 44
3 45
3 46
3 47
3 48
3 49
3 50
3 51
3 52
3 53
3 54
3 55
Spine 3
3-1
3-2
3-3
3-4
3-5
3-6
3-7
3-8
3-9
3-10
3-11
3-12
3-13
3-14
3-15
3-16
3-17
3-18
3-19
3-20
3-21
3-22
3-23
3-24
3-25
3-26
3-27
3-28
3-29
3-30
9/20/06
9/21/06
9/22/06
9/23/06
9/24/06
9/25/06
9/26/06
9/27/06
9/28/06
9/29/06
9/30/06
10/1/06
10/2/06
10/3/06
10/4/06
Est. Date
8/11/06
8/12/06
8/13/06
8/14/06
8/15/06
8/16/06
8/17/06
8/18/06
8/19/06
8/20/06
8/21/06
8/22/06
8/23/06
8/24/06
8/25/06
8/26/06
8/27/06
8/28/06
8/29/06
8/30/06
8/31/06
9/1/06
9/2/06
9/3/06
9/4/06
9/5/06
9/6/06
9/7/06
9/8/06
9/9/06
-11.1
-11.4
-11.8
-11.3
-11.4
-11.3
-11.1
-11.1
-11.1
-11.2
-11.3
-11.8
-11.5
-11.6
-11.4
δ18O
33.3
33.6
33.7
33.9
33.6
33.4
33.5
33.1
33.2
33.4
33.6
34.2
34.5
34.5
34.0
34.4
34.4
35.2
34.2
34.9
35.1
34.8
35.3
35.6
36.1
38.6
35.4
35.0
34.9
35.0
211
2-31
2-32
2-33
2-34
2-35
2-36
2-37
2-38
2-39
2-40
2-41
2-42
2-43
2-44
2-45
2-46
2-47
2-48
2-49
2-50
2-51
2-52
8/26/06
8/27/06
8/28/06
8/29/06
8/30/06
8/31/06
9/1/06
9/2/06
9/3/06
9/4/06
9/5/06
9/6/06
9/7/06
9/8/06
9/9/06
9/10/06
9/11/06
9/12/06
9/13/06
9/14/06
9/15/06
9/16/06
35.0
35.2
35.0
36.0
36.3
35.8
36.2
36.1
36.3
36.1
36.9
35.7
35.7
35.4
35.1
35.3
34.9
36.0
35.8
35.4
35.1
37.1
3-31
3-32
3-33
3-34
3-35
3-36
3-37
3-38
3-39
3-40
3-41
3-42
3-43
3-44
3-45
3-46
3-47
3-48
3-49
3-50
3-51
3-52
3-53
3-54
3-55
9/10/06
9/11/06
9/12/06
9/13/06
9/14/06
9/15/06
9/16/06
9/17/06
9/18/06
9/19/06
9/20/06
9/21/06
9/22/06
9/23/06
9/24/06
9/25/06
9/26/06
9/27/06
9/28/06
9/29/06
9/30/06
10/1/06
10/2/06
10/3/06
10/4/06
34.5
33.9
33.9
33.9
34.3
34.9
34.0
34.9
35.3
37.7
36.4
36.4
37.0
36.0
36.6
36.2
36.8
36.1
36.4
36.6
36.7
37.7
36.7
37.6
37.8
1
15
500
0
5
10
Temperature (C)
1000
1500
1500
1.0757
1.0774
1.1317
1.2341
1.0710
1.1177
1.1757
1.2639
1.0660
1.1181
1.1560
1.2680
1.0589
1.0941
1.1423
1.2313
20
1000
Temperature (C)
0.20
0.20
0.20
0.20
0.20
0.20
0.20
0.20
0.20
0
0.2
0.4
0.6
0.8
1
1.2
500
Samples processed at the University of California, Irvine AMS Lab
UCIT#
UCIT13322
13322
SNPE A 3cm
1.0709
0.0016
UCIT13323
13323
SNPE A 51cm
1.0862
0.0017
UCIT13324
13324
SNPE A 101cm
1.0934
0.0017
UCIT13325
13325
SNPE A 153cm
1.1044
0.0018
UCIT13326
13326
SNPE A 200cm
1.1140
0.0020
UCIT13327
13327
SNPE A 250cm
1.1384
0.0018
UCIT13343
13343
SNPE A 300cm
1.1547
0.0027
UCIT13329
13329
SNPE A 351cm
1.1933
0.0019
UCIT13330
13330
SNPE A 400cm
1.2506
0.0020
168A-0cm-Apex
168A-82cm
168A-203.5cm
168A-300cm
163A-0cm-Apex
163A--106.5cm
163A-198.5cm
163A-298.5cm
182A-372.0cm-Apex
182A-282.5cm
182A-190cm
182A-96.5cm
184B-413cm-Apex
184B-320cm
184B-220cm
184B-112cm
1
0
5
10
15
20
0.20
0.20
0.20
0.20
0.20
0.20
0.20
0.20
0.20
0.20
0.20
0.20
0.20
0.20
0.20
0.20
79568
79569
79570
79571
79572
79573
79574
79575
79579
79578
79577
79576
79580
79581
79582
79583
0
0.2
0.4
Cnt +/- RME (%)
0.0037
-0.80
0.0033
0.20
0.0033
0.20
0.0035
0.20
0.0010
0.20
0.0028
0.20
0.0029
0.20
0.0054
0.20
0.0060
0.20
0.0038
0.20
0.0103
0.20
0.0058
0.20
0.0057
0.20
0.0038
0.20
0.0055
0.0036
0.0040
0.0040
0.0044
0.0047
0.0039
0.0049
0.0027
0.0038
0.0053
0.0059
0.0044
0.0042
0.0045
0.0058
X10152A
X10153A
X10154A
X10155B
X10156A
X10157A
X10158A
X10159A
X10163
X10162B
X10161A
X10160A
X10164
X10165
X10166A
X10167
1
0.8
0.6
CO2 (ug)
CO2 (ug)
1.2
Samples processed at the University of Arizona AMS Lab
Graphite line #
AA #
Sample #
Fm
DL-13A
70228
Sag-162b-0.0
1.0864
DL-6
68553
Sag-162b-52.0
1.1183
DL-7
68554
Sag-162b-89.5
1.1530
DL-8
68555
Sag-162b-122.0
1.1882
DL-9
68556
Sag-162b-166.0-A
1.2250
DL-10
68557
Sag-162b-166.0-B
1.2304
RCTH-1082
63556
Sag-162b-226.0 cm
1.3196
RCTH-1083
63557
Sag-162b-279.0 cm
1.4455
RCTH-1085
63558
Sag-162b-47 cm
0.9937
RCTH-700
55891
Sag-162b-27 cm
1.1192
RCTH-701
55892
Sag-162b-300 cm
1.5728
RCTH-702
55893
Sag-162b-331 cm
1.2154
RCTH-703
55894
Sag-162b-337 cm
1.1337
RCTH-704
55895
Sag-162b-17 cm
0.9826
0.0027
0.0028
0.0028
0.0028
0.0030
0.0029
0.0035
0.0030
0.0032
0.0059
0.0042
0.0046
0.0047
0.0049
0.0052
0.0046
0.0055
0.0034
0.0044
0.0058
0.0064
0.0049
0.0047
0.0050
0.0063
Eq. 25
Tot +/0.0094
0.0040
0.0040
0.0042
0.0026
0.0037
0.0039
0.0061
0.0063
0.0044
0.0108
0.0063
0.0061
0.0043
F14C values and estimated dates for Tumamoc Hill and Saguaro National Park East cactuses
0.15
0.15
0.15
0.15
0.15
0.15
0.15
0.15
-9.4
-9.6
-8.9
-11.7
-11.3
-10.7
-9.8
0.1
0.1
0.1
0.1
0.1
0.1
0.1
0.1
0.1
0.1
0.1
0.1
0.1
0.1
0.1
0.1
-9.5
-12.06
-9.79
-10.20
-10.63
-12.72
-9.29
-9.01
-10.72
-11.59
-9.61
-10.74
-9.48
-11.83
-11.46
-11.47
-11.68
+/0.1
0.1
0.1
0.1
0.1
0.1
0.1
0.1
0.1
0.1
0.1
0.1
0.1
0.1
1.0709
1.0862
1.0934
1.1044
1.1140
1.1384
1.1547
1.1933
1.2506
1.0616
1.0609
1.1148
1.2162
1.0577
1.1000
1.1567
1.2457
1.0515
1.1007
1.1393
1.2481
1.0448
1.0791
1.1267
1.2147
F14C
1.0698
1.1012
1.1360
1.1691
1.2046
1.2099
1.3020
1.4249
0.9796
1.1035
1.5521
1.1986
1.1171
0.9679
fractionation correction
d13C
-9.86
-9.86
-10.38
-9.03
-8.47
-8.47
-11.79
-10.89
-10.98
-11.09
-12.01
-11.3
-10.51
-10.24
0.0016
0.0017
0.0017
0.0018
0.0020
0.0018
0.0027
0.0019
0.0020
0.0058
0.0041
0.0045
0.0046
0.0048
0.0051
0.0044
0.0054
0.0034
0.0043
0.0056
0.0063
0.0048
0.0046
0.0049
0.0061
+/0.0092
0.0039
0.0039
0.0041
0.0026
0.0036
0.0038
0.0060
0.0062
0.0043
0.0105
0.0061
0.0060
0.0042
1.0709
1.0862
1.0934
1.1044
1.1140
1.1384
1.1547
1.1933
1.2506
0.0000
0.0016
0.0017
0.0017
0.0018
0.0020
0.0018
0.0027
0.0019
0.0020
0.0001
0.0058
0.0041
0.0045
0.0046
0.0048
0.0051
0.0045
0.0054
0.0034
0.0043
0.0057
0.0063
0.0048
0.0046
0.0049
0.0062
0.0039
0.0039
0.0041
0.0026
0.0037
0.0038
0.0060
0.0062
0.0043
0.0105
0.0062
0.0060
0.0042
1.1015
1.1363
1.1695
1.2051
1.2105
1.3028
1.4261
0.9796
1.1037
1.5537
1.1991
1.1174
0.9679
1.0618
1.0610
1.1151
1.2168
1.0578
1.1003
1.1572
1.2463
1.0517
1.1010
1.1397
1.2488
1.0449
1.0793
1.1270
1.2153
0.0001
+/-
blank correction
0.0028
F14C corrected
212
1995.9
1989.2
1980.9
1995.9
1990.4
1980.8
2001.9
1992.0
1983.6
2004.50
2002.00
2001.00
1999.80
1996.09
1993.69
1990.99
1987.07
1982.79
1997.5
1993.8
1983.7
2002.8
1995.8
1985.8
Samples processed at the University of California, Irvine AMS Lab
UCIT#
UCIT13322
13322
SNPE A 3cm
2003.2 2001.80
UCIT13323
13323
SNPE A 51cm
2001.5 2001.00
UCIT13324
13324
SNPE A 101cm
2000.0 1999.00
UCIT13325
13325
SNPE A 153cm
1998.5 1997.20
UCIT13326
13326
SNPE A 200cm
1995.9 1994.87
UCIT13327
13327
SNPE A 250cm
1991.9 1990.20
UCIT13343
13343
SNPE A 300cm
1990.4 1989.82
UCIT13329
13329
SNPE A 351cm
1986.8 1985.75
UCIT13330
13330
SNPE A 400cm
1981.9 1980.94
2005.5
2005.5
1995.5
1984.8
2006.1
1996.7
1990.2
1982.3
2007.2
1996.7
1992.3
1982.0
2008.2
2002.5
1994.2
1984.7
1997.5
1991.9
1983.7
168A-0cm-Apex
168A-82cm
168A-203.5cm
168A-300cm
163A-0cm-Apex
163A--106.5cm
163A-198.5cm
163A-298.5cm
182A-372.0cm-Apex
182A-282.5cm
182A-190cm
182A-96.5cm
184B-413cm-Apex
184B-320cm
184B-220cm
184B-112cm
1993.8
1983.8
79568
79569
79570
79571
79572
79573
79574
79575
79579
79578
79577
79576
79580
79581
79582
79583
1997.1
1985.7
X10152A
X10153A
X10154A
X10155B
X10156A
X10157A
X10158A
X10159A
X10163
X10162B
X10161A
X10160A
X10164
X10165
X10166A
X10167
1991.48 1991.80
1987.30 1987.80
1983.52 1983.55
1996.32 1997.01
2002.4 2002.8
1992.00 1992.34
1983.63 1985.82
1995.89 1997.5
1990.37 1990.47
1980.79 1982.99
1995.87 1997.50
1989.18 1991.02
1980.92 1983.73
1993.79 1997.13
1983.79 1985.74
1993.84
2001.9
1992.84
1990.73
1983.27
1991.45
1994.07
2002.1
1995.81
1993.79
1983.70
1991.87
1
1
1
1
0.469724
0.986987
0.869664
0.60537
0.828525
0.9
0.068905
0.676008
0.877146
0.004879
0.756847
0.863522
0.886813
0.751943
0.974653
0.689075
0.067363
0.299079
0.003519
0.439884
0.1
0.898085
0.94911
0.036416
0.056948
For Post-bomb age determination using CALIBomb (http://calib.qub.ac.uk/CALIBomb/frameset.html)
Samples processed at the University of Arizona AMS Lab
First peak
Second Peak
P1
P2
Graphite line #
AA #
Sample # 14C age
Max
Min
Oldest
Most
2sigma
recent 2 sigma
Oldest
Most
2sigma
recent 2 sigma
DL-13A
70228
Sag-162b-0.0
DL-6
68553
Sag-162b-52.0 1996.71 1995.92 1997.50
1995.92 1997.50
0.016424
DL-7
68554
Sag-162b-89.5 1992.35 1990.92 1993.77
1990.92 1993.77
0.945191
DL-8
68555
Sag-162b-122.0 1988.99 1987.09 1990.17
1987.09 1987.25 1987.94
1990.17 0.032512
0.95527
DL-9
68556
Sag-162b-166.0-A 1985.37 1984.05 1986.32
1984.05 1984.33 1984.59
1986.32 0.055224
0.749405
DL-10
68557
Sag-162b-166.0-B 1984.87 1983.94 1985.80
1983.94 1985.80
0.867759
RCTH-1082
63556
Sag-162b-226.0 cm 1979.37 1978.94 1979.79
1978.94 1979.79
0.92743
RCTH-1083
63557
Sag-162b-279.0 cm 1973.92 1972.99 1974.84
1972.99 1974.84
0.991357
RCTH-1085
63558
Sag-162b-47 cm
165.92
RCTH-700
55891
Sag-162b-27 cm 1957.59 1957.50 1957.68
1957.50 1957.68
0.02014
RCTH-701
55892
Sag-162b-300 cm 1969.47 1968.17 1971.45
1968.17 1970.76 1971.43
1971.45 0.944366
0.001691
RCTH-702
55893
Sag-162b-331 cm 1958.74 1958.30 1959.18
1958.30 1959.18
0.145621
RCTH-703
55894
Sag-162b-337 cm 1957.76 1957.50 1958.01
1957.50 1958.01
0.050248
RCTH-704
55895
Sag-162b-17 cm
262.44
0.059266
P3
0.2
0.2
0.2
0.2
0.2
0.2
0.2
0.2
0.2
0.2
0.2
0.2
0.2
0.2
0.2
0.2
0.2
0.2
0.2
0.2
0.2
0.2
0.2
0.2
0.2
0.2
0.2
0.2
0.2
0.2
0.2
0.2
0.2
0.2
0.2
0.2
0.2
0.2
0.2
0.2
0.2
0.2
0.2
0.2
0.2
0.2
0.2
0.2
0.2
0.2
0.2
0.2
0.2
0.2
0.2
0.2
0.2
0.2
0.2
0.2
0.2
0.2
0.2
0.2
0.2
0.2
0.2
0.2
0.2
0.2
0.2
0.2
0.2
0.2
Resolution
Smoothing
213