Plant Physiology and Competition in a Mojave Desert Riparian Ecosystem: Proximate Solutions to Ultimate Questions

UNLV Retrospective Theses & Dissertations

1-1-1999

Plant physiology and competition in a Mojave Desert riparian ecosystem: Proximate solutions to ultimate questions

James Ray Cleverly University of Nevada, Las Vegas

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Repository Citation Cleverly, James Ray, "Plant physiology and competition in a Mojave Desert riparian ecosystem: Proximate solutions to ultimate questions" (1999). UNLV Retrospective Theses & Dissertations. 3076. http://dx.doi.org/10.25669/3lb8-t2l8

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Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Pl a n t Ph y sio l o g y AND C o m p e t it io n in a M o ja / e

D e se r t R ipa r ia n Ec o s y s t e m : P r o x im a te

S o l u t io n s to U ltim a t e Q u e s t io n s

James R. Cleverly Bachelor of Science University of Utah 1993

A dissertation submitted in partial fulfillment of the requirements for the degree of

Doctor of Philosophy

Biological Sciences

Department of Biological Sciences University of Nevada, Las Vegas July 1999

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B B B a The Graduate College University of Nevada, Las Vegas

^ 19.

The Dissertation prepared by James R Cleverly

Entitled Plant Physiology and Competition in a hbjave Desert Riparian Ecosystem: Proximate Solutions to Ultimate Questions______

is approved in partial fulfillment of the requirements for the degree of

______Doctor of Philosophy ______

Examination Committee Ciiair

Dean o f the Graduate College

ExaminatioiiQommitteeMem&er I

Examuiation Comr littee-i^ m b er

/ y

Graduate College Faculty Representative 1

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. ABSTRACT

Plant Physiology and Competition in a Mojave Desert Riparian Ecosystem: Proximate Solutions to Ultimate Questions

James R. Cleverly

Dr. Stanley D. Smith, Examination Committee Chair Professor of Biological Sciences University of Nevada, Las Vegas

The distribution and abundance patterns of species are of primary interest in

ecology, and the interactions between an organism and its abiotic and biotic environment

provide a basis for a better understanding of the mechanisms by which distribution and

abundance patterns are governed. Physiological ecology provides an ideal platform for

integrating the effects of both biotic and abiotic influences upon species performance,

thus conferring a process-oriented insight into ecological patterns. This dissertation

considers the physiological characteristics that may be related to Mojave Desert

floodplain domination by Tamarix ramosissima, an exotic invasive riparian plant.

Four woody riparian species - Tamarix ramosissima, Salix exigua, Prosopis

pubescens and Pluchea sericea — were studied along the Virgin River in southern

Nevada. Through field observation and manipulative experiments in the field and iii

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. glasshouse, the relationships between plant water relations, competition, facilitation, and

abiotic stress and environment were investigated at both proximate (i.e., process) and

ultimate (i.e., pattern) levels.

Tamarix dominated the Virgin River floodplain at a previously bumed site(Half-

Way Wash) within 50 years following fire. Physiological mechanisms for the success of

Tamarix include its water use (on both leaf- and whole branch-levels), starch storage,

early investment in additional ramets, and slow radial growth. Pluchea, a native,

summer-active halophyte, dominates early seres through tolerance to extreme abiotic

stresses, as indicated by the general unresponsiveness of physiological characteristics to

the imposition of stress. Salix, which is also native, demonstrated radial growth patterns

consistent with sensitivity to drought stress, demonstrated sensitivity to heat and drought

stresses in many key physiological traits, and was relatively insensitive to the presence of

other species.

Studies of plant responses to stress yield a great deal o f information concerning

the relationships, both inhibitive and facilitative, between species. Furthermore, the

relationships between abiotic stress, inhibition, facilitation, and chance environmental

events (e.g., aseasonal flooding) contributes to further understanding the short- and long

term mechanisms involved in the successful invasion of the Virgin River floodplain by

Tamarix ramosissima.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. TABLE OF CONTENTS

ABSTRACT...... iii

LIST OF FIGURES...... viii

LIST OF TABLES...... x

LIST OF SYMBOLS AND ABBREVIATIONS...... xi

ACKNOWLEDGEMENTS...... xiv

PREFACE...... xvii

CHAPTER 1 INTRODUCTION...... 1 Desert Floodplain Ecosystems ...... 1 Tamarix ramosissima Ledeb. (saltcedar) ...... 4 Salix exigua Nutt, (coyote willow) ...... 6 Pluchea sericea (Nutt.) Cov. (arrowweed)...... 6 Prosopis pubescens Benth. (screwbean mesquite) ...... 7 Stress Physiology ...... 7 Community Ecology ...... 10 The Functional Basis of Competition, Inhibition and Facilitation ...... 10 The Functional Basis of Succession...... 11 Questions and Hypotheses ...... 13

CHAPTER 2 INVASIVE CAPACITY OF Tamarix ramosissima IN A MOJAVE DESERT FLOODPLAIN: THE ROLE OF DROUGHT...... 19 Abstract...... 21 Introduction...... 22 Materials and Methods ...... 25 Study Site and Climate ...... 25 Gas Exchange ...... 27 Canopy Transpiration ...... 28 Tissue Analysis...... 29

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Tree Ring Analysis and Successional Trajectories ...... 30 Data Analysis ...... 30 Results...... 32 Discussion...... 39 Acknowledgements ...... 44

CHAPTER 3 A FLUID-DYNAMIC MODEL OF ADVECTIVE ENERGY EXCHANGE BETWEEN ADJACENT ARIDLAND SHRUB AND RIPARIAN ECOSYSTEMS...... 45 Abstract...... 46 Introduction...... 47 Fluid-dynamic Model ...... 52 Materials and Methods ...... 54 Results...... 57 Discussion...... 61 Acknowledgements ...... 68

CHAPTER 4 WATER, GROWTH AND CARBON RELATIONS FOLLOWING COMPETITIVE RELEASE IN SEEDLING POPULATIONS OF THREE WOODY FLOODPLAIN SPECIES OF THE MOJAVE DESERT...... 69 Abstract...... 70 Introduction...... 71 Materials and Methods ...... 74 Study Site and Plant Removal ...... 74 Water Relations...... 77 Growth and Carbon Relations ...... 79 Data Analysis ...... 81 Results...... 82 Water relations...... 82 Growth and Carbon Relations ...... 86 Discussion...... 89 Acknowledgments ...... 97

CHAPTER 5 THE EFFECT OF INTERACTING HEAT AND DROUGHT STRESSES ON COMPETITION AMONG WOODY PHREATOPHYTES IN THE GLASSHOUSE...... 99 Abstract...... 100 Introduction...... 101 Materials and Methods ...... 103 Results...... 110

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Growth ...... 110 Stress Physiology ...... I l l Discussion...... 118 Acknowledgements ...... 121

CHAPTER 6 INFERENCE OF SUCCESSIONAL RELATIONSHIPS IN A SOUTHWESTERN FLOODPLAIN COMMUNITY THROUGH UTILIZATION OF CLIMATE AND ANNUAL TREE RING DATA. 123 Abstract...... 124 Introduction...... 125 Materials and Methods ...... 128 Results...... 130 Discussion...... 136 Acknowledgements ...... 138

CHAPTER? CONCLUSIONS...... 140

APPENDIX 1 DIGITAL IMAGE ANALYSIS OF ANNUAL TREE-RING SURFACE AREA IN MOJAVE DESERT FLOODPLAIN SPECIES.. 145 Abstract...... 146 Introduction...... 146 Materials and Methods ...... 148 Results...... 151 Discussion...... 152 Acknowledgements ...... 154

APPENDIX 2 PERMISSION TO USE COPYRIGHTED MATERIAL...... 155

BIBLIOGRAPHY...... 160

VITA...... 184

V ll

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. LIST OF HGURES

FIGURE 1-1: STRESS PHYSIOLOGY HYPOTHESES...... 15

FIGURE 2-1 DAILY MAXIMAL TEMPERATURE, 1994 ...... 26 FIGURE 2-2 STAND AGE VERSUS SPECIES COVER...... 34 FIGURE 2-3 SAP FLOW...... 35 FIGURE 2-4 TKN, CHLOROPHYLL AND GAS EXCHANGE...... 36 FIGURE 2-5 FACTOR ANALYSIS...... 38

FIGURE 3-1 HEAT TRANSFER SCHEMATIC MODEL...... 52 FIGURE 3-2 WIND SPEED AND DIRECTION...... 58 FIGURE 3-3 DIURNAL TEMPERATURE GRADIENT...... 59 FIGURE 3-4 TEMPERATURE AND WIND SPECTRA...... 60 FIGURE 3-5 DIURNAL SENSIBLE HEAT ADVECTION...... 62 FIGURE 3-6 BOWEN RATIO AND SENSIBLE HEAT...... 63

FIGURE 4-1 LEAF WATER POTENTIAL...... 84 FIGURE 4-2 SEEDLING HEIGHT AND DENSITY...... 87 FIGURE 4-3 TAPROOT AND STEM STARCH STORAGE...... 88 FIGURE 4-4 COMPETITION INTENSITY...... 90 FIGURE 4-5 DROUGHT EFFECTS ON INTERSPECIFIC INTERACTIONS 98

FIGURE 5-1 TEMPERATURE AND MOISTURE TREATMENTS...... 108 FIGURE 5-2 GENET RELATIVE GROWTH RATE...... 112 FIGURE 5-3 RELATIVE BRANCHING RATE...... 113 FIGURE 5-4 TAPROOT GROWTH...... 114 FIGURE 5-5 WATER POTENTIAL...... 115 FIGURE 5-6 NET PHOTOSYNTHESIS AND STOMATAL CONDUCTANCE.. 116 FIGURE 5-7 FLUORESCENCE...... 117

FIGURE 6-1 STAND SAMPLING SCHEME...... 128 FIGURE 6-2 CLIMATE DATA RELIABILITY...... 131 FIGURE 6-3 AGE-XYLEM SURFACE AREA...... 132 FIGURE 6-4 STREAMFLOW HISTOGRAM...... 133 FIGURE 6-5 SPECTRAL AND COHERENCE ANALYSES...... 136 viii

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. FIGURE 7-1 ; SUMMARY - CHAPTER 2...... 144

FIGURE Al-1 ; SIMULATED TREE RINGS...... 150 FIGURE Al-2: ACCURACY ANALYSIS...... 152 FIGURE Al-3: SURFACE AREA GROWTH DEVIATION...... 153

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. LIST OF TABLES

TABLE 2-1 : STEM GROWTH RATE...... 33

TABLE 3-1: ENVIRONMENTAL CONDIHONS...... 64

TABLE 4-1 HYDROLOGICAL AND SOIL CHARACTERISTICS...... 77 TABLE 4-2 STOMATAL CONDUCTANCE...... 85 TABLE 4-3 APOPLASTIC ABA CONCENTRATION...... 86

TABLE 5-1; PERCENT MORTALITY...... I l l

TABLE 6-1 : MULTIPLE REGRESSION COEFFICIENTS...... 134 TABLE 6-2: MULTIPLE REGRESSION MODEL COEFFICIENTS...... 135

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. LIST OF SYMBOLS AND ABBREVIATIONS

Chapters a — Coefficient of competition 1 a — Probability of a Type I error 2,4, 5, 6, Apl a m^ s'^ Thermal diffusivity due to molecular 3 Conduction A, Anet pmol Net photosynthetic carbon fixation rate 2,4, 5 m'^ s‘‘ ABAap nmol cm'^ Apoplastic abscisic acid concentration 4 ANCOVA — Analysis of covariance 3 ANOVA — Analysis of variance 2,4,5 P — Bowen ratio 3 P — Model coefficient 6 BREB — Bowen ratio energy balance 3 CIrgr — Competition intensity (response): RGR 4 CIs — Competition response: starch 4 Cp J kg'* K'* Specific heat of air 3 AT ° C Leaf-air temperature gradient 4 df — Degrees of freedom 2,3,4,5 E mol m'^ s'* Leaf-level transpiration 2 ET — Evapotranspiration 7 ETo mm day'* Penman-Monteith potential 2,3 évapotranspiration ETa mm day'* Actual évapotranspiration 3 ECe dS m * Electrical conductivity, soil extract 1,4 Eh m^ s'* Thermal eddy diffusivity 3 Em m^ s'* Eddy viscosity 3 F — Ratio of means squares of treatment 2, 3, 4, 5 and error Fq mV Baseline (groundstate) fluorescence 5 XI

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Fm mV Maximal fluorescence 5 Fv mV Variable fluorescence 5 G Wm-^ Soil heat flux 3 gs mol m'^ s'* Stomatal conductance 2 ,4 ,5 H Wm'^ Sensible heat flux 3 h cm Plant height 4,5 hmax cm Maximal ramet height 5 Eh cm Total sum height of all ramets 5 ho cm Initial plant height 4,5 IFC — Initial floristic composition 6 Kw m^ s'* Turbulent exchange coefficient: water 3 Kh m^ s'* Turbulent exchange coefficient: heat 3 Ksh g m'^ s'* Zero flow value (sapflow) 2 i m Prandtl mixing length 3 XET Wm'^ Latent heat of evaporation flux 3

— ith Eigenvalue 2,4

LI-1600 — LiCor steady-state porometer 4

LI-6200 — LiCor gas exchange system 2,4

LI-6400 — LiCor gas exchange system 5

LSD — Least significant difference 2,4

MANCOVA — Multivariate analysis of covariance 4

MANOVA -- Multivariate analysis of variance 2

n, N — Sample size 4, 5, Apl NUE mol g'* Nitrogen use efficiency 2

P — P (x 1 Ho is true) 4

pdf — Probability distribution function 5 PPFD mol m'^ s'* Photosynthetic photon flux density 2

Prt — Turbulent Prandtl number 3

psn — Photosystem 11 5

PVC — Polyvinyl chloride 5 e cm^ cm'^ Volumetric soil water content 5 q" Wm'^ Sensible heat advected flux 3 g g ’^ Gravimetric water content of dry soil 4

qP — Photochemical quenching 5

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. p kgm'^ Mass density of air 3 — Regression coefficient 3, 6, Apl RBR week* Relative branching rate 5 RGR day'* Relative growth rate 4 RGRh day* Maximal ramet growth relative growth 5 rate RGRref day* Relative growth rate in reference plots 4 RGRrem day* Relative growth rate in removal plots 4 RGRt day'* Total genet relative growth rate 5 RH % Relative humidity 2 Rn W m '2 Net radiation 3 SAS — Statistical analysis software 2, 3, 4, 5, 6, A pl se, SE — Standard error of the mean 2 ,4 SWA — Sapwood Area 2 T °C Air temperature 3 Ta °C Air temperature 2,4 T, °c Leaf temperature 2,4 t — Student’s t statistic 4 TDR — Time domain reflectometry 5 TIFF — Tagged image file format Apl TKN gmol mg'* Total Kjeldahl nitrogen 2 u m s'* Horizontal wind speed 3 u' m s'* Horizontal eddy velocity deviation 3

Ut m s'* Transverse wind speed 3 m s' Superboundary wind speed (transverse) 3 V m s' Vertical wind speed 3 V m s' Vertical eddy velocity deviation 3 Vilk’s A — MANOVA test statistic 2 ,4 m, s, a — Degrees of fireedom (MANOVA) 2 ,4 WUE fimol Water use efficiency 2 mmol'* 'Fi MPa Leaf water potential 2,4, 5,7 z m Height above the canopy 3 Zi — ith eigenvector (i = 1 if none) of 2,4 xm

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. ACKNOWLEDGEMENTS

There are numerous people who have provided much support and assistance

throughout my time at UNLV. First among them is Stan Smith, my advisor; you have

been exceptionally patient with my unexpected ideas and strange research interests. I’m

certainly glad that we were able to make something o f this experience. Almost as

important in developing these concepts and connecting them properly to the evidence

available is Dale Devitt. Without fail your suggestions were sound and led to vast

improvement in the manuscripts. I would like to next thank my examination committee.

You have all assisted in my efforts to produce good quality work (and get it published).

I would also like to thank my co-authors and collaborators throughout my stay

here. Among you are: Anna Sala, Kent Sovocool, Dale Devitt, Stan Smith, Dawn

Neuman, Lynn Shaulis, Travis Huxman, Jeff Piorkowski and Jinmei Shen. Working

with you has enriched my experiences here more than you can imagine. I have learned a

great deal from all of you. To Dawn, I would like to offer my especial thanks. You have

been a compadre, looked out for me, and helped me when I couldn’t let anyone else in.

Thank you very much.

XIV

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. I wish to express my gratitude to Catherine Heyne. I cannot imagine how cold

my life would be without your warm presence. This dissertation, along with much, much

more, is dedicated to you.

There are many graduate students at UNLV that I must also show gratitude for

social and personal support. First among them are Paul Territo and John Bolling, with

whom I began this grand adventure. John, you were my closest friend in Las Vegas

those first couple years. Your friendship and help with statistics (don’t laugh, we

struggled through together) will last a lifetime. Paul, you have been one of my closest

friends, when you finally showed up. Remember that skeleton we found in our brand

new office at UNLV?? It’s hard to believe so much water can pass under the bridge,

even in the desert.

Later, after Paul and John had left, I had the fortune of getting to know Steve

Vrooman. It’s been a long, hard road for two misfits who are just tired of the rigmarole

and want to know a nice, quite peace in the wilds of New Mexico. Finally, there is Kent

Sovocool. From what I’ve heard, you are most responsible for bringing my reality

function closer to the mean. (What was it Paul? 6 sd’s?) Anyway, we have some very

interesting memories to take with us from UNLV. You were a boon, both scientifically

and personally. Hopefully, that added cynicism you have developed will wane with a

happy home and career. Take care.

Of course, there are many, many others who have contributed greatly to directing

me here. There isn’t the space (and I have to get back to revising the substance of this XV

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. monster), so I will list some of you. I extend my gratitude to everyone, those appearing

on this abbreviated list and off: Bill Hanly, Mom and Dad, Tracie, and Richard Teerlink

(ancient history, I know, but where would I be without history?).

Further thanks are tendered toward the institutions and agencies that supported

this research. Each chapter provides details on the support of The Biological Association

of Graduate Students (B.A.G.S.), the Las Vegas Valley Water District, the UNLV

Graduate Student Association (GSA), and the Society of Wetland Scientists. I would like

to also offer gratitude one last time to those who contributed their efforts to this research:

Simon Lei, Matt Ronshaugen, Kim Mace, Chris Schaan, Matthias Rillig and Stan

Hillyard. Your assistance and insight was invaluable.

XVI

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. PREFACE

“Heraclitîis somewhere says that all things are in process and nothing stays still, and likening existing things to the stream of a river he says that you would not step twice into the same river. ” Plato (Catylus) describing Heraclitus o fEphesus

This work began by investigating the competitive attributes of Tamarix

ramosissima that leads to its invasion and domination of southwestern U.S. riparian

ecosystems. As the research developed, however, competition became too narrow a term

to describe the phenomena observed, but there wasn’t much terminology to describe

interspecific interactions based upon conditions rather than resources. Rather than adopt

an entirely new lexicon, the underlying conceptual firamework for the interpretation of

data (i.e., the paradigm) in this study follows that of Osmond et al. (1987), in which

stress is loosely defined as a factor that lowers the potential growth or reproduction of an

organism. In this firamework, the presence of another species, if it causes a decline in

physiological traits, is a biogenic stress. This broad view takes into consideration both

resource competition and other forms of inhibition, regardless of their source.

Chapter 1 is the Introduction, and it develops the conceptual firamework relating

the roles of biotic and abiotic factors that may contribute to the success of Tamarix, as

well as presenting background information on the ecosystem and organisms studied, the

xvii

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. research questions, their related hypotheses, and the justification for those a priori

hypotheses. Chapter 2 describes an observational study that was carried out to

characterize the potential interactions between these plants with respect to their physical

environment in a young, successional stand. Chapter 3 further describes the physical

forces that shape the physiological arena within which these plants are interacting during

succession. Chapter 4 chronicles the field experimentation that relates plant water and

carbon relations to potential competition. Chapter 5 directly investigates the roles of

abiotic and biotic stress among seedlings in the glasshouse, where conditions could be

better controlled at the expense of understanding the actual, or realistic, conditions under

which these plants interact. Chapter 6 applies the concepts developed in the previous

short-term studies to long-term trends in environment, species abundance and growth

through an analysis of tree-ring chronologies. Chapters 2, 3, and 5 focus on individual

ramets and genets, as one would expect firom physiological-level investigations.

Chapters 4 and 6 focus on populations of plants, much like population-level studies.

Phenomena occurring at each level are not always the same, but they tend to provide

complementary views into the structuring of a community and ecosystem. Appendix 1 is

a supplement that does not address the primary or secondary hypotheses of this

dissertation. Rather, Appendix 1 chronicles the digital methods developed for collecting

tree ring data used in Chapter 6. As a whole, abiotic and biotic factors relevant to the

successful invasion of a Mojave Desert floodplain by Tamarix ramosissima are briefly

illustrated under various levels of realism (observation > field manipulation > glasshouse xviii

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. manipulation) and experimental control (glasshouse manipulation > field manipulation :

observation).

XIX

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. CHAPTER 1

INTRODUCTION

Desert Floodplain Ecosystems

Desert floodplain ecosystems are densely vegetated corridors that occur along

large rivers in arid regions. These regions are characterized by extreme water deficit,

making rivers and streams foci for high productivity riparian ecosystems in an otherwise

water-limited system (Malanson 1993). However, such high production in riparian

ecosystems can be limited by flooding, ephemeral drying (and associated drought), and

plant dormancy (Malanson 1993). The view that riparian corridors are an ecotone firom

an aquatic to a desert ecosystem has been proposed (Gregory et al. 1991). However,

riparian corridors are better understood as distinct edaphic and floristic assemblages that

form open ecosystems with the surrounding landscape (Malanson 1993).

Nutrient dynamics in floodplain soils are variable in both time and space.

Inorganic nitrogen is most concentrated in the upper 10 cm, as predominantly nitrate

(NO3) during the summer and spring and as ammonium (NH 4) during the winter

(Peterson and RoLfe 1985). Higher concentrations of inorganic nitrogen also exist

directly under the canopies of large nitrogen fixing trees (e.g., Prosopis', Virginia et al.

1982), and on depositional (as opposed to erosional) riverbanks (Pinay et al. 1992). In

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 2 fact, higher concentrations of inorganic nitrogen at the surface occur despite higher

surface denitrification potential (Virginia et al. 1982; Lowrance 1992). This indicates

that deposition of nutrients occurs at a faster rate than loss due to denitrification and plant

uptake, leaving patches rich in nitrogen seasonally (i.e., during the spring) as well as

spatially (i.e., under Prosopis).

Seasonal flooding disturbance during mid to late spring is a characteristic of arid

and semiarid floodplains. Spring flooding is largely responsible for soil water recharge

in riparian zones (Stromberg and Patten 1992), for creation of low-salinity, hydric

sandbars where seedling establishment occurs (Van Auken and Bush 1988), and for

pulses of nutrient availability (Pinay et al. 1992). Another hydrodynamic property of

seasonal flooding related to seedling establishment is the consequential drydown rate and

hydraulic transport characteristics of the sediments (Segelquist et al. 1993). Drydown

rate is influenced not only by flooding amount and duration, but also by evaporative

demand (e.g., air temperature).

In the southwestern U.S., native riparian genera have been subdivided into 2

groups based upon their floristic origin (Johnson et al. 1988). The genera Populus

(cottonwood and poplar), Salix (willow), Platanus (sycamore), Juglans (walnut) and

Fraxinus (ash) belong to the Arcto-Tertiary group, indicating their poleward (i.e., arcto)

origin during the Tertiary. These genera are rehcs of the wet and cool conditions in

Tertiary western North America, and they are currently obligate pbreatophytes (Johnson

et al. 1988), verified by Busch et al. (1992) for Populus fremontii and Salix gooddingii.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 3 The Madro-Tertiary group, which originated in the drier southern regions of western

North America during the Tertiary, consists of Prosopis (mesquite). Acacia, Olneya

(ironwood), Chilopsis (desert willow) and Cercidium (palo verde). These genera are

probably facultative phreatophytes and can persist on the margins and upper terraces of

riparian corridors and in washes with only ephemeral subsurface water. Of considerable

importance in floodpiains and canyons of the Southwest is Tamarix, which originated in

the Middle East, Africa and Asia. Tamarix can be grouped with the dry riparian species

because it, too, is a stress tolerant facultative phreatophyte (Busch et al. 1992; Busch and

Smith 1995; Devittetal. 1997).

Tamarix ramosissima has established large populations along most of the riparian

habitat in the arid Southwest, making its eradication a focus of conservation efforts

throughout the region. To understand the competitive displacement of native species by

Tamarix, the woody species that occupy and co-dominate the Virgin River floodplain

{Salix exigua, Prosopis pubescens, and Pluchea sericea) were studied in addition to

Tamarix. The Virgin River floodplain in southern Nevada was chosen as the focus of

this research because both mixed stands of phreatophytes and monospecific stands of

Tamarix can be found on different reaches of the river. The following descriptions of

these species are meant to provide a species- and genera-specific introduction to the

dominant plant species of the Virgin River floodplain ecosystem.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Tamarix ramosissima Ledeb. fsaltcedar’)

The Tamaricaceae is a family that is widespread throughout Africa, Asia and the

Middle East, although its members, such as Tamarix ramosissima, seldom dominate

communities to which they are native (Wyant and Ellis 1990). Nonetheless, some

members of this family have quite successfully invaded ecosystems in Australia (Griffin

et al. 1989) and the southwestern United States (Christensen 1962; Robinson 1965;

Brock 1994), where they are considered noxious weeds.

Tamarix affects invaded floodplain habitats by forming dense thickets that slow

the river’s velocity and causes greater sedimentation rates than before the introduction of

Tamarix (Blackburn et al. 1982). Moreover, stabilization of floodplain soil by densely

vegetated Tamarix stands leads to channelization during subsequent flooding, in which

terraces are formed in the floodplain. Those terraces are hydrologically isolated from the

river, potentially isolating phreatophytes from the water table. Desiccation throughout

the entire soil profile is further enhanced by Tamarix's long taproots (Gary 1963) that

extract water from the capillary fringe, as well as their ability to deplete soil v/ater in the

vadose zone (Busch et al. 1992). Tamarix physiognomy, sedimentation and terrace

formation contribute to the drying and salinization of floodplain soils, conditions which

favor Tamarix dominance. The Virgin River is relatively unregulated, where flooding

conditions cut channels and form terraces and where Tamarix augments soil drying and

sedimentation.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 5 Tamarix ramosissima’s high transpiration rate on a stem area basis and

maintenance of high leaf area (Busch and Smith 1995; Sala et al. 1996) contribute to high

water use rates at the stand level and subsequent floodplain desiccation in mature

Tamarix stands. Furthermore, Tamarix maintains productivity under high leaf

temperatures and relatively low leaf water potentials (Devitt et al. 1997), desiccating

floodpiains through drought seasons when the ecosystem is most susceptible to drying.

Fire is a factor that has recently become important with the invasion of Tamarix

in the southwestern U.S. (Busch and Smith 1993). Fire disturbance affects

predominantly later serai stands and has been extensively investigated on the Colorado

River by Busch and Smith (1993, 1995), who illustrated that post-fire soils were saline,

with significant increases in NH4, NO3, HCO3, SO4, Ca, K, Mg, Na, Cl and B. Such soils

(ECg = 4.6 ± 1.0 dS m'*) provide a growth medium ideal for Tamarix and Pluchea, both

of which are highly salt tolerant (Hagemeyer and Waisel 1989; Busch and Smith 1995).

Tamarix and Pluchea resprout from the base of burnt stems, increasing their tendency to

dominate fire-prone floodpiains (Busch 1995). This ability to resprout compensates for

inhibition of seedling germination by soil salinity (Shafroth et al. 1995) and makes fire

disturbance in arid floodpiains unique because fire disturbance further directs succession

toward a mature community dominated by Tamarix.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Salix exigua Nutt, (covote willow)

The Salicaceae is a large, diverse family with riparian and non-riparian members

distributed globally in Alaskan floodpiains (Walker et al. 1986), alpine riparian forests

(Dawson and Bliss 1989), and desert riparian corridors (Busch and Smith 1995). Desert-

adapted Salix range in their mesophytic character from the arborescent Salix gooddingii,

which is drought sensitive (Stromberg 1997), to the thicket-forming Salix exigua, which

is more drought tolerant (Busch and Smith 1995). Drought and salt sensitivity is

especially important for Salix abundance, as variations in floodplain desiccation and

salinity can affect distribution patterns in the genus (Busch and Smith 1995; van

Splunder et al. 1996). Both S. gooddingii and S. exigua are present along the Virgin

River, but the thicket forming habit of S. exigua allows it to reach much higher stem

density than the arborescent S. gooddingii.

Pluchea sericea fNutt.l Cov. farrowweedl

Pluchea sericea is a summer-active halophyte (Busch and Smith 1995) that is

geographically distributed on the floor of Death Valley (e.g., the Devil’s Cornfield), and

throughout the lower Colorado River drainage system, including the Virgin River.

Common to all of these habitats is the presence of a shallow water table. Pluchea tends

to have a spreading root system that is more shallow than that of co-occurring riparian

species (Gary 1963). Due to its shorter stature and shallower roots, it is an early-

successional species in desert floodpiains of the region. Therefore, depression of water

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 7 tables with time eliminates this species from late-successional communities. It has larger

leaves than sympatric floodplain species, so evaporative cooling is probably essential for

its survival in desert floodpiains. O f all of the woody floodplain species investigated in

this study, Pluchea is the only evergreen species; the other species are winter deciduous.

Prosopis pubescens Benth. fscrewbean mesquite!

Prosopis spp. are winter-deciduous phreatophytes (Nilsen et al. 1984) and are

abundant along some stretches of the Virgin River. As a member of the Fabaceae,

Prosopis forms root nodule associations with the nitrogen-fixing bacterium Rhizobium

(Shoushtari and Pepper 1985), potentially increasing soil nitrogen availability

(Klemmedson and Tiedemann 1986).

Prosopis is moderately salt tolerant, showing leaf area decline at 5 dS m*^ soil

electroconductivity (ECg). Prosopis is also moderately drought tolerant, as illustrated by

its tendency to occupy the upper terraces of many desert floodpiains. While it responds

to drought by producing epicuticular wax (Pacoby et al. 1990) and by seasonal leaf

dimorphism (Nilsen et al. 1986), very long taproots (e.g., up to 60 m; Phillips 1963;

Nilsen et al. 1981) contribute to drought avoidance by Prosopis (Stromberg et al. 1992).

Stress Physiology

“In plant physiological ecology, as in many other subdisciplines of biology, the term stress has general connotations rather than a precise definition. By defining stress as any factor that decreases plant growth and reproduction below the genotype’s potential, we make the term measurable and thus meaningful to ecology and agriculture. " (Osmond et al. 1987)

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. The term stress refers to the environmental conditions that may cause an organism

to experience decreased physiological performance. When a species responds to the

potentially stressful environmental conditions, it is stress sensitive; a stress tolerant

species does not respond to the same conditions that cause a response in another species.

Physiological response includes, but is not limited to, changes in allocation patterns that

are associated with growth, survival or reproduction, decline in the ability to transpire

water, or decline in water potential — these characteristics also reflect a plant’s

physiological performance. A potentially stressful environmental condition can be biotic

or abiotic in origin.

Riparian corridors are traditionally assumed to be free from abiotic stress, and

riparian species are considered to be examples of drought escapers (Shantz 1927); i.e.,

they are plants that use shallow water table sources to stay well hydrated throughout the

dry season. Both of these views are misleading, as it has been shown that flooding, heat,

drought, and salinity affect the physiology and interspecific interactions in desert riparian

species (Kleinkopf and Wallace 1974; Kelliher et al. 1980; Hanson 1982; Braatne et al.

1992; Stromberg et al. 1992; Busch and Smith 1993; Shafroth et al. 1995). In fact,

drought stress due to stream diversion has been postulated to be largely responsible for

the decline of native species in many riparian corridors (Rood and Mahoney 1990; Smith

et al. 1991; Rood et al. 1995).

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 9 O f these three stresses (heat, drought and salinity), the impact that salinity has on

woody riparian species has been well characterized (Busch and Smith 1993, 1995).

Therefore, the foci of this study are primarily heat and drought effects on the physiology

of riparian vegetation.

Acute heat stress can affect membrane integrity and photosynthesis (Berry and

Bjorkman 1980; Thebud and Santarius 1982). Nonetheless, thermal acclimation in some

species can cover the range of extreme temperatures (> 45° C) experienced in warm

desert ecosystems (Downton et al. 1984), and it is assumed that riparian species behave

similarly.

The effect of high temperature on plants is known to interact closely with water

availability (Ehrler et al. 1978), coupling heat stress to drought stress (Henckel 1964).

Some typical responses of drought sensitive species are carbon allocation shifts and

declining stomatal conductance and photosynthesis (Henckel 1964; Hsiao and Acevedo

1974; Schulze 1986; Chaves 1991). The interaction between heat and drought stress is

factorial, and heat and drought can be uncoupled under certain conditions. For example,

integration of hydraulic and chemical control of stomatal conductance and

photosynthesis (Tardieu and Davies 1993) can somewhat decouple declines in stomatal

conductance from declines in photosynthetic rate (Boyer 1971; Bunce 1977; Briggs et al.

1986; Bunce 1988; Ni and Pallardy 1992), which permits heat and drought to affect plant

performance to different degrees.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 10 Community Ecology

The Functional Bases of Competition

Competition was originally defined at the population level, in which the presence

of another species was associated with a decline in population growth rate, generally in

proportion to the population densities of the competing species. These population growth

relationships did not address the reasons for such declines; the Lotka-Volterra equations

(Lotka 1932) estimate the coefficient of competition, a, from measured population

growth decline with density rather than building toward an understanding of the factors

controlling a.

Competition later became viewed as an interaction, at a single trophic level,

between two or more species in which the competitors ( 1) deplete a common resource,

causing the inferior species to do with less or to alter resource use patterns, or ( 2) directly

interfere with each other (e.g., through allelopathy or space occupation), restricting the

losing species to lower quality habitats. Competition studies often incorporate the

resources specifically relating to the objects of competition (Tilman 1980), which may be

water (Eissenstat and Caldwell 1988), light (sensu Kohyama 1987), soil nutrients

(Caldwell et al. 1987; Tilman 1989), or space (McConnaughay and Bazzaz 1992a, b).

The supply rates of plant resources are strongly dependent upon abiotic environmental

conditions. While competition at this level can be consistent with the original definition

of competition (i.e., a depletion of resources by one species leading to declined

population growth in another), explicit consideration of abiotic conditions serves to

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 11 expand the focus of competition studies to include resource dynamics and the abiotic

environment.

Physiological studies further expand the scope of competition by explaining the

manner in which species respond to their abiotic and biotic environments. One species

may outperform another under one set of environmental conditions, regardless of the

resources available to the species interacting. More often, plants physiologically respond

to variations in the abiotic environment, resource availability, competition, and other

interspecific interactions (Osmond et al. 1987); therefore, physiological interpretations of

ecological phenomena relate to the primary causes of species interactions. In some cases,

physiological studies of competition (e.g., Fonteyn and Mahall 1981) reflect the original

concept of interspecific competition, investigating the interactions between two or more

species in which plant performance suffers in the presence of another species (Keddy

1989). The term inhibition (Cormell and Slatyer 1977) is synonymous with this wider

definition of competition.

The Functional Basis of Succession

The model of Connell and Slatyer (1977), as revised in Connell et al. (1987) and

expanded upon in Walker and Chapin (1987), has been extensively used as a conceptual

framework for the potential mechanisms of succession. In this model of succession, life

history characteristics, physiology, environment, disturbance, and evolutionary ecology

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 12 contribute to an explanation of the net inhibitive and facilitative interactions between two

or more species, projected over the long-term.

One especially useful application of the Connell and Slatyer (1977) model is the

investigation of successional mechanisms within a sere as a net balance of inhibition and

facilitation (Franco and Nobel 1988; Callaway 1994; Callaway and King 1996; Callaway

et al. 1996). In contrast to inhibition, facilitation is an interaction between plants in

which one plant (the target plant) benefits physiologically or ecologically by the presence

of a neighbor. For example, a physiological benefit may be a greater photosynthetic rate,

better water use efficiency, or enhanced growth. The impact of a neighboring plant can

be quantified by the relative competition intensity (Cl), where net inhibition occurs when

Cl is positive, and net facilitation occurs when performance is enhance by a putative

competitor (i.e.. Cl < 0; Twolan-Stmtt and Keddy 1996). When competition intensity is

0, inhibition and facilitation are balanced; in that case, the target plant is neither inhibited

nor facilitated by the presence of neighbors. Physiological interpretation of plant

performance, with respect to the presence of neighbors, includes facilitation (Osmond et

al. 1987) and refines our understanding of successional mechanisms beyond models that

do not include facilitation (e.g.. Grime 1977; Tilman 1987b).

Questions and Hypotheses

There is one overall, general question that this dissertation has set out to answer.

That question, and the hypothesized answers and their justification, is presented first.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 13 The general question is followed by three subordinate questions. The hypotheses to these

three subordinate questions form specific solutions to the primary, general question.

While they do not capture the objective of the whole dissertation, they represent a

methodical attempt to split up the investigation of the general question.

fVhat are the physiological bases q/’Tamarix invasion o f a shallow floodplain ecosystem

along the Virgin River, NY?

Hypothesis: Growth, water relations and carbon budgets in Tamarix are expected to be

either (1) insensitive or (2) improved when Tamarix is exposed to salinity,

drought or heat (i.e., conditions that promote abiotic stress; Busch and

Smith 1995). Therefore, Tamarix will be at an advantage in an

environment that impairs the function of native species. The effect of

abiotic stress on the native species is greater favors Tamarix more greatly

than Tamarix' expected physiological sensitivity to biotic stress (e.g.,

shading by neighbors).

Tamarix is expected to demonstrate inhibited growth, water relations and carbon

budgets in the presence of healthy neighboring species because natives like Salix,

Prosopis and Pluchea because they have a longer association with the local environment.

Therefore, they should have more optimal photosynthesis, growth, and transpiration rates

for this environment.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 14 The balance between abiotic and biotic factors in the invasion o f the southwestern

U.S. by Tamarix is affected by environmental variability. Water table depth and ambient

temperature vary both spatially (across sites) and temporally (within and between seasons

and years), there is no single solution to the relationship between interspecific

interactions and physiological responses to the environment. Because different

functional types respond (or fail to respond) to various stresses (Fig. 1-1 A), each could

successfully persist in a variable environment by developing a specialized response to

various temperature and water availability regimes in both time and space (Brown 1988;

Tilman 1994).

The broad question concerning Tamarix establishment, and related species

abundance and distribution patterns, in the Virgin River floodplain community can be

dissected into more specific questions concerning environment, physiology and

community interactions. The following questions depend upon fundamental assumptions

about the hierarchical relationships between ecological scales.

First, abiotic environmental conditions are assumed to influence the species-

specific physiological response space (i.e., physiological space = /(abiotic enviromnent);

Fig. 1-lA). Second, inhibitive and facilitative relationships are assumed to be based

upon species-specific physiological responses to the abiotic environment (i.e.,

competitive space = /(physiological space)). The third assumption indicates that short-

and long-term abundance patterns are functions of the abiotic environment and species-

specific physiological responses to that abiotic environment, as well as other factors (e.g..

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 15 life history, sedimentation, grazing, fire and salinity). Thus, the succession of species in

a community is responsive to the net effect of the abiotic and biotic environments

(successional space = /(abiotic environment, competitive space); Fig. 1-1B), even though

succession is frequently viewed as a purely biological phenomenon.

sensitive tolerant oCD c 8 CO E o I o < CL extremely sensitive tolerant

Stress Stress

Figure 1-1. Stress physiology assumptions and their relationship to species abundance. Physiological responses to abiotic and biotic stress depend upon the species’ sensitivity to that stress (A), and the species that are tolerant of a stress are expected to increase in relative abundance following application of that stress (B). Responses are illustrated as linear functions but may often exist in nonlinear or complex relationships for specific functions. ______To answer the next question, a simplifying assumption was proposed that a

relationship between streamflow and water availability exists. The validity of this

assumption depends upon the spatial and temporal scale that is being investigated.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 16 How will the dominant woody species respond physiologically to a range o f realistic

environmental conditions?

Hypotheses:

(a) Tamarix ramosissima will not respond to drought (i.e., low

streamflow).

(b) Salix exigua is best suited for high streamflow and will show

decreased performance (e.g., lower transpiration) under drought.

conditions of high water table, responding negatively to drought.

(d) Prosopis pubescens is best suited for conditions of low

streamflow.

The justification for the choice of preferred habitat quality is based on leaf-level

physiological and morphological characteristics that are known a priori, based upon

previous research and personal observation. Salix and Pluchea are generally observed in

areas with a shallow water table (Busch and Smith 1995). Salix is not found growing in

soils with high salinity, but Pluchea is not sensitive to salinity (Busch and Smith 1995).

Tamarix and Prosopis are more xeric species than Salix and Pluchea, and Tamarix and

Pluchea are highly tolerant of salinity, while Prosopis is only moderately salt tolerant.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 17 What is the pattern o f relative short-term performance under various environmental

conditions?

Hypotheses: (a) On wet sites, Salix > Pluchea > Tamarix > Prosopis.

(b) On dry sites, Tamarix > Prosopis > Pluchea > Salix.

Tamarix > Pluchea > Salix.

Species to the left of > are expected to outperform the species on the right, as well

as serve as predictions of the slope of the lines in figure 1-lB. These changes in relative

cover can be caused not only by direct inhibition, but due to differential mortality or

senescence caused by abiotic factors that affect only sensitive species. Predictions at this

level describe instantaneous trajectories, effective over short time scales, as with the

balance between inhibition and facihtation (Franco and Nobel 1988; Callaway 1994;

Callaway et al. 1996; Callaway and King 1996). The hypothesis (c) reflects the tendency

of Prosopis to occupy dry washes and upper terraces, whereas Tamarix is more

frequently found in riparian zones.

Will short-term relationships between environment, physiology, and

inhibition/facilitation patterns be reflected over the long-term (i.e., > 2 season)?

Hypothesis: Growth over multiple seasons will reflect the predominate climate (e.g.,

long-term median streamflow), as well as maintain the interspecific

relationships observed in the short-term.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 18 Over the long-term, physiological and competitive effects are tempered or

exaggerated by demographics. A long-term analysis of environment and growth will

incorporate physiology with population growth trajectories, integrating the successional

trajectory and fluctuations of the abiotic environment.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. CHAPTER 2

INVASIVE CAPACITY OF Tamarix ramosissima IN A MOJAVE DESERT FLOODPLAIN: THE ROLE OF DROUGHT

This chapter has been published in Oecologia and is presented in the style of that journal. Permission from Springer-Verlag has been granted to include this chapter. The complete citation is:

Cleverly, J.R., S.D. Smith, A. Sala and D.A. Devitt. 1997. Invasive capacity of Tamarix ramosissima in a Mojave Desert floodplain: the role of drought. Oecologia. Ill: 12-18

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 20

1997 Springer-Verlag

INVASIVE CAPACITY OF Tamarix ramosissima IN A MOJAVE DESERT FLOODPLAIN: THE ROLE OF DROUGHT

Cleverly, James R .\ Stanley D. Smith*, Anna Sala^ and Dale A. Devitt^ *

* *Department of Biological Sciences University of Nevada, Las Vegas Las Vegas, NV 89154-4004

^Division of Biological Sciences University of Montana Missoula, MT 59812

^Department o f Environmental and Resource Sciences University of Nevada, Reno Reno, NV 89557

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 21

Abstract

Tamarix ramosissima (Tamaricaceae) is a woody phreatophyte that has invaded

thousands of hectares of floodplain habitat in the southwestern U.S. In this study, we

examined the response of gas exchange and stem sap flow of Tamarix and three co

occurring native phreatophytes {Pluchea sericea (Asteraceae), Prosopis pubescens

(Fabaceae) and Salix exigua (Salicaceae)) to drought conditions in an early successional

floodplain community in the Mojave Desert of southern Nevada. In an analysis of a

size/age series of each species across the whole floodplain (both mature and successional

stands), stem growth rate was lowest for Tamarix. However, along the same

successional chronosequence, Tamarix came to dominate the 50+ year old stands with

dense thickets of high stem density. Xylem sap flow, when expressed on a sapwood area

basis, was highest in Tamarix under early drought conditions, but comparable between

the four species toward the end of the summer dry season. Multivariate analysis of the

gas exchange data indicated that the four species differentiated based on water use under

early drought conditions and separated based on plant water potential and leaf

temperature (indices of drought effects) at the end of the summer dry season. This

analysis suggests that the invasive Tamarix is the most drought tolerant of the four

species, whereas Salix transpires the most water per unit leaf surface area and is the least

tolerant of seasonal water stress. Therefore, Salix appears to be well adapted to early

successional communities. However, as floodpiains in this arid region become more

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 22 desiccated with age, Tamarix assumes greater dominance due to its superior drought

tolerance relative to native phreatophytes and its ability to produce high density stands

and high leaf area.

Keywords: succession, riparian, Mojave Desert, Tamarix , drought stress

Introduction

Tamarix ramosissima Ledeb. (saltcedar) is an exotic phreatophyte that has

invaded many thousand hectares of floodplain habitat in the southwestern U.S.

(Christensen 1962; Robinson 1965; Brock 1994). It often forms monospecific thickets in

which most of the native riparian plants have been eliminated (Busch and Smith 1995).

Tamarix also occurs with a mixture of native riparian species in early successional

habitats, such as recently scoured sandbars or in post-bum floodplain communities.

Variability of environmental attributes may have a great impact on the

mechanisms controlling populational and ecological relationships between floodplain

species. For instance, annual stream discharge in the Lower Virgin River of Southern

Nevada shows up to a 7-fold difference between wet and dry years (USGS stream

discharge data over a 60-year period). Furthermore, this great annual variability is quite

random, making the set of successful physiological strategies complex and the number of

species that can coexist potentially numerous. Different functional types could

successfully persist in such an environment by specializing to varying levels in this

episodic environment and secure temporal réfugia, similar to species in spatially

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 23 heterogeneous environments (Brown 1988; Tilman 1994). Alternatively, species that are

most successful in variable environments may have to combine the ability to grow

rapidly in wet years with the ability to tolerate or avoid potential extreme water and heat

stress in drought years, effectively generalizing their response over the entire range of

environmental fluctuation.

In variable floodplain environments of arid regions, it is important to understand

the physiological attributes of plants under both ideal, mesic conditions and following

prolonged drought, which is characterized by depressed water tables and high air

temperatures. Under ideal moisture conditions, plants that are best able to use water,

rather than being efficient with their water use, may be expected to have a competitive

advantage (Cohen 1970; Midgley and Moll 1993). Thus, an analysis of physiological

characteristics preceding a prolonged drought should indicate which species that may be

most successful based upon water use and other related phenomena. On the other hand,

an analysis of physiological characteristics following a long-term drought may indicate

the species that are most able to tolerate the drought, illustrating a potential competitive

advantage when the environment fluctuates toward its dry extremes. If the same species

is competitively superior under both extremes, that generahst species would be expected

to solely persist through successional time.

In this study, we compared the gas exchange and water use of Tamarix

ramosissima and three co-occurring native phreatophytes {Pluchea sericea (Nutt.) Cov.

(arrowweed), Prosopis pubescens Benth. (screwbean mesquite), and Salix exigua Nutt.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 24 (coyote willow)) in a low-runoff year characterized by water and heat stress. This was

done on a three-year-old successional terrace community along the lower Virgin River of

southern Nevada in a flat, wide floodplain environment. Tamarix is well known to be

tolerant of the desiccation of watercourses (Blackburn et al. 1982) and the salinization of

surface soils (Busch and Smith 1993), and is a facultative rather than obligate

phreatophyte (Busch et al. 1992). Prosopis is also a phreatophyte that is fairly tolerant of

drought stress (Nilsen et al. 1981; Johnson et al. 1988). Salix, on the other hand, is

restricted to mesic microhabitats with consistent water tables throughout much of the

year in the western U.S. (Johnson et al. 1988; Busch and Smith 1995). The fourth woody

species in the lower Virgin River floodplain, Pluchea sericea, is an evergreen ruderal

shrub that has an apparent ability to tolerate periodic water and high temperature stresses,

as surmised by its presence on the floor o f Death Valley, California. Since these four

coexisting species have very different habitat requirements and evolutionary histories, it

was our objective to determine the physiological basis for their success and whether they

are transient members of the community which may eventually be dominated by a single

species (such as Tamarix), or if each species has specific adaptations that would allow

them to persist as the community matures. As we have shown above, it is quite possible

that physiological relationships may change through succession and plant age. However,

we have based the following hypotheses upon previous work with mature riparian plants

as a set of null-based hypotheses. We hypothesized that Tamarix would exhibit greater

water use per unit sapwood area but not per unit leaf area (Sala et al. 1996), higher water-

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 25 use efficiency (Busch and Smith 1995) and more negative water potentials (Busch and

Smith 1995) than the co-occurring native species. This would lead to the prediction that

Tamarix fits the requirements of a successful species capable of growing in periodically

stressful environments. We also predicted that Salix experiences greater water use during

early drought conditions, suggesting that temporal réfugia can be occupied by Salix over

the course of environmental fluctuations with the final successional outcome in such a

variable environment being determined by the periodicity and pattern of environmental

conditions in the habitat.

Materials and Methods

Studv Site and Climate

The study was conducted on the lower Virgin River floodplain, located in the

Mojave Desert of southern Nevada. The vegetation consisted of remnant populations of

cottonwood {Populus fremontiî) and willow {Salix gooddingii) trees, but is now

dominated by extensive thickets of Tamarix ramosissima that often occur in

monospecific stands. This study was performed near the mouth of Half-Way Wash (36°

40"N, 114° 20'E, elev. 380 m) on a 3-yr-old sandbar that had been scoured by high flows

in the winter of 1993. This particular site had a high abundance of arrowweed {Pluchea

sericea), coyote willow {Salix exigua) and screwbean mesquite {Prosopis pubescens) in

addition to Tamarix. Thus, it made an ideal site for studying biotic interactions in an

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 2 6 ecosystem with a predicted successional trajectory toward monospecific Tamarix

dominance.

This study occurred under low streamflow drought conditions (USGS stream

discharge data) and was designed to circumscribe the intensely hot, dry conditions

characteristic of a Mojave Desert summer season. Gas exchange and tissue collections

were performed on June 50 9 and August 23, 1994 9 June 45 - 3£ (Fig. 2-1). Canopy o2 Q. 40 - transpiration and oE

CD weather variables were E 35 1 continuously measured 23 August 30 1 5 0 200 2 5 0 for one week inclusive Day of Year of the gas exchange Figure 2-1. Daily maximal temperature (° C) on cloudless days for the spring, summer and autumn of 1994 for the days. The first sampling Virgin River, Nevada. Measurements were taken at Half- Way Wash (36° 40' N, 114° 20' E, elev 380 m) and nearby date corresponded to Lake Mead National Recreation Area (36° 35' N, 114° 20' E, elev 380 m) as described in the text. The arrows early drought conditions indicate the gas exchange sampling days preceding and following the high-temperature summer season following peak

streamflow in the spring. The second sampling date corresponded to late drought

conditions and declining summer temperatures (Fig. 2-1).

A Campbell Scientific (Logan, UT) weather station was placed 1 m above the

canopy in a central location. Rainfall, wind speed, relative humidity (RH) and incident

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 27 photosynthetic photon flux density (PPFD) were measured every 10 min and recorded as

half-hourly mean values during each sampling week. Depth to the water table was

measured weekly with 5 piezometers placed at 100-200 m intervals into the floodplain

community, along a transect perpendicular to the river channel.

Gas Exchange

On June 9 and again on August 23, gas exchange measurements were made on

each of the four species using a LI-6200 gas exchange system (Li-Cor, Lincoln, ME).

Temperature of random terminal shoots or leaves were measured with a thermocouple

probe. Leaves were then immediately placed in the sample cuvette for two consecutive

gas exchange measurements on the same sample. Each of the four species was sampled

once (for a total of 4 species X 2 measurements = 8 measurements) before beginning the

next duplicate sampling upon a given species. Gas exchange was sampled from 0700h to

1300h on each day; 24 measurements were made on each species (i.e., 12 samples X 2

measurements per sample). Transpiration was calculated using measured stomatal

conductance (gj and independent measurements of leaf temperature and air vapor

pressure (see below). Instantaneous water use efficiency (WUE) was calculated as the

fractional molar quantity of carbon fixation (A) per unit transpiration (E) (i.e., —). E

After the two measurements of each sample were made, the sample tissue was

transferred to a plastic bag for immediate water potential measurements. Leaf water

potential (Y|) was measured using a Scholander-type pressure chamber (Soil Moisture

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 28 Stress, Corvallis, OR). After obtaining the Yi, the bagged leaves were transported back

to the laboratory in a cool, dry container for leaf area measurements using a Delta-T Leaf

Area Meter (Pullman, WA). Samples were stored at 5° C and leaf area measurements

were made within 24 hours of collection.

Within the canopy boundary layer, relative humidity was measured using RH and

temperature sensors attached to the cuvette of a LI-6200 gas exchange system (Li-Cor,

Lincoln, NE). This measurement was taken with the cuvette open (fan on) and exposed

to the air within the canopy’s shading. Leaf-level PPFD was measured using a LI-COR

190 SB quantum sensor concurrent to gas exchange measurements. Canopy air and leaf

temperatures (Ta and T|, respectively) were ascertained using a fine wire (0.02 mm)

copper-constantan thermocouple. Leaf temperature was determined on the specific

leaves measured in the gas exchange measurements immediately preceding placement in

the cuvette.

Canopv Transpiration

Transpirational water loss was estimated firom representative plants in the

fioodplain using the stem heat balance sapflow method (Baker and van Bavel 1987;

Devitt et al. 1993). The sap flow system consisted of a DNXIO data logger (Dynamax

Inc., Houston, TX) attached to three 8 -channel multiplexers. Two days preceding the gas

exchange sampling dates (June 7 and August 21), Dynamax stem-flow gauges were

placed on the basal stems of the plants to be monitored. The stem flow gauges

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 29 continuously averaged data every 1/2 hour for one week. Salix, Tamarix, and Prosopis

plants had stem diameters ranging from 10 mm to 25 mm, representing a random

sampling of the ages of these four species. Pluchea plants had stem diameters near 10

mm, representing the oldest Pluchea stems. The week of 7 June 1994, gauges were

placed on 12 Tamarix stems and 4 stems each of Pluchea, Prosopis and Salix. The week

of 23 August 1994, gauges were placed on 4 plants of each species. The gauges were

well wrapped with insulation and several layers of aluminum foü to prevent direct

insolation and naturally-induced temperature gradients from affecting the heat balance

measurements (Shackel et al. 1992).

At the end of each sampling week the entire canopy of each branch used for sap

flow and gas exchange measurements was collected. The stems with the gauges still

attached were taken into the laboratory to estimate the zero flow value, Ksh- Total leaf

area in each canopy was inferred using an empirical relationship between dry mass and

leaf area which was obtained using leaf subsamples taken during the gas exchange

analyses.

Tissue Analvsis

Chlorophyll analysis was done on a 1 cm^ subsample of leaf tissue which was

washed in distilled water to remove surface salts. The 1 cm^ subsamples were soaked

under darkness in 5 ml N,N-Dimethylformamide for 48 hours. Chi a and b

concentrations were determined following the methods of Moran (1982).

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 30 The remaining leaf fraction was dried for 48 hours at 60° C for subsequent leaf

nitrogen analysis. Total Kjeldahl Nitrogen (TKN) concentration was determined on 10 g

of tissue using a colorimetric method (Alpkem Co., Wilsonville, OR). A standard

sulfuric acid wash at 380° C was used to form ammonium sulfate, followed by reaction

with salicylate and hypochlorite in the presence of sodium nitroferricyanide, yielding an

absorbance of 660 mn light in proportion to the tissue nitrogen concentration and

compared to a 2% TKN apple leaf standard.

Tree Ring Analysis and Successional Trajectories

Basal stems of all four species were collected from different stands within the site

on two days during the winter of 1995 following leaf-loss in all except Pluchea, which is

evergreen. These stands were of varying ages from 5 to 54 years. Age of the stand was

assumed to be equal to the oldest living individual stem present in these clonal species.

Percent relative cover of each species was estimated, and stem sections were collected,

re-cut, sanded and varnished to bring out the grain of the wood to facihtate estimation of

age and diameter. Characteristic relationships between stem age and diameter were

compared between these stands and relationships previously determined for Tamarix

from other Mojave Desert locations.

Data Analvsis

Variables were separated into environmental (RH, PPFD, and Ta) and

physiological (T,, A, gs, E, TKN, 'F, and chlorophyll concentration) groups. Statistical

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 31 Analysis Software (SAS, SAS Institute, Cary, NC) was used to design full interaction

models of Multivariate Analysis of Variance (MANOVA) in which physiological

variables were modeled as responses to day and species factors.

Because ofa priori dependence between the variables within each group, full

interaction, two-factor (day and species) MANOVA and non-parametric MANOVA

models were designed and followed by applicable post-hoc comparisons (ANOVA and

greatest characteristic root (gcr) analysis (Harris 1985), followed by post-hoc Fisher’s

Protected LSD or Least Squares Means comparisons (SuperANOVA, Abacus Concepts,

Inc., Berkeley, CA)). The purpose of such tests (i.e., the MANOVA followed by post-

hoc characterization) was to infer statistically significant differences between the mean

values of two groups (e.g., early drought and late drought) for a specific variable (e.g.,

gs)-

As normality and homoscedasticity are important assumptions of linear ANOVA

and MANOVA modeling, normality was tested on model residuals using the Shapiro-

Wilk test (SAS) and homoscedasticity was tested using Hartley’s F^ax-test.

Transformations to near-normality were performed using the Box-Cox family of power

transformations and homogeneity of variances was achieved using the rank

transformation. The probability of a type I error was presumed to be a = 0.05 (p < 0.05)

in all hypothesis tests.

Factor analysis was used to analyze the internal structure of the gas-exchange data

and form post-hoc hypotheses. These post-hoc hypotheses are mostly useful as

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 32 predictive tools describing, in our case, possible physiological mechanisms for

population responses to the environment. Using the principal components approach,

SAS produced factor eigenvalues, standardized scoring coefficients (factor loadings) and

orthogonal data firom the correlation matrix. This method is preferred in such a data set

because the correlation matrix is not sensitive to units of different orders as is the

variance-covariance matrix.

Results

The long-term climate of the region is arid (mean annual rainfall of 10 cm) and

hot (summer maxima exceeding 45° C). Because of the dry nature of this region, nearly

all of the water available to this fioodplain ecosystem is provided firom the upper Virgin

River watershed in Utah. 1994 was a dry year with record-breaking summer

temperatures (Fig. 2-1); thus, runoff was low and water tables were depressed (> Im

below the surface in August, versus 0.1-0.2 m in late spring). Potential

évapotranspiration (ETq) was 7.6 ± 0.15 and 6.7 ± 0.18 mm d’* during the weeks of June

7-12 and August 11-17, respectively.

Table 2-1 illustrates that, in the Virgin River stands, the areal stem growth rate in

Salix, Prosopis and Pluchea were significantly higher (F = 13.8, df = 3, 126) than in

Tamarix. Analysis of species dominance of lower Virgin River fioodplain communities

(Fig. 2-2) showed equal dominance of the four species in young (< 50 yr) stands,

dominance by Tamarix (> 50 % relative cover) but with the other three species as

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 33 important subordinates (5 - 25 % relative cover) in medium-aged stands (15 - 40 yr) and

finally monospecific Tamarix dominance in the oldest (50 + yr) stands.

Xylem sap flow on a leaf area basis was found to be comparable on both days

between the four species (data not shown). However, when expressed on a sapwood area

Table 2-1. Stem growth rate [diameter (cm) per ring] for main stems of four Mojave riparian species firom various locations in the Southwest. Numbers with different superscript letters are significantly different (LSD, a = 0.05; Tamarix values fi*om locations other than the Virgin River were not available for analysis). Data for Tamarix firom Death Valley and the Amargosa River are firom S.D. Smith (unpublished observations)

Mean Width of Annual Growth Rings Species Location (cm/ring count)

Tamarix ramosissima Virgin River 0.26" (Nevada) Salix exigua Virgin River 0.40*’ (Nevada) Prosopis pubescens Virgin River 0.43 ” (Nevada) Pluchea sericea Virgin River 0.42^ (Nevada) Tamarix ramosissima Death Valley Sand Dunes 0.29 (California) Tamarix ramosissima Amargosa River 0.30 (California)

basis, Tamarix was found to have higher sap flow than the other three species in June

(Fig. 2-3). By August, all four species had comparable sap flow rates per unit sapwood

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 34 area (Fig. 2-3). Each o f the species exhibited its maximal sap flow rate near midday,

with the exceptions of Prosopis in June and Salix in August, when they exhibited highest

sap flow between 0600 and 0900 h (Fig. 2-3).

Leaf-level physiological variables (TKN, A, g^, E, WUE, and YJ exhibited a

significant day-by-species-interaction (Wilk’s A = 0.59, s = 3, m = 1.5, n = 88 ),

indicating that, for at 8 Tamarix Prosopis least one of these Pluchea Salix 6

observed. The linear 0 0 1 0 20 3 04 0 5 0 combination of these Stand Age (years)

physiological variables Figure 2-2. Relationship between stand age and mean relative cover class (7 < 5%, 2 5-15%, 3 15-35%, 4 that was significantly 35-65%, 5 65-85%, 6 85-95%, 7 > 95%) for Tamarix ramosissima, Prosopis pubescens, Pluchea sericea, and associated with the Salix exigua

greatest rejection in the MANOVA model was Z = T,-A + 3gs + 2 WUE - + TKN (Xi

= 0.42), indicating that nearly all of these variables contributed to a species-specific

physiological response to the imposition of a summer drought.

Species comparison of leaf nitrogen concentration (TKN) showed that Tamarix,

Pluchea and Salix had similar nitrogen concentrations, with Pluchea showing a

significant increase in leaf TKN over the hot, dry summer (Fig. 2-4A; Day X Species

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 35 Interaction F = 6.78, df = 3, 184). Prosopis had significantly higher leaf TKN than did

the other four species (Fig. 2-4A).

Leaf chlorophyll concentrations somewhat mirrored leaf TKN, with Prosopis

having the highest chlorophyll concentration among the four species (Fig. 2-4B).

Chlorophyll concentration in Tamarix declined between the June and August sampling

dates, whereas it increased in Pluchea and Prosopis (Fig. 2-4B).

Species comparison of mean photosynthetic rates showed that Prosopis had

comparable rates to Salix and Tamarix-, Salix was higher than Tamarix under early

drought and Prosopis under late drought. All three were higher than Pluchea (Fig. 2-

4C). None of the species showed a decline in photosynthetic rate from June to August,

and Pluchea actually exhibited a significant increase in August (Date X Species

Interaction F = 4.28, df = 3, 184).

1400 -June August Tamarix 1200 - Prosopis

1000 - Pluchea I - Salix 8 0 0 6 0 0 « E 4 0 0 s 200 0 -200 0 6 0 0 1200 1800 2 4 0 0 0 6 0 0 1200 1800 2 4 0 0 Time Figure 2-3. Mean sap flow per unit sapwood area (SWA) of T. ramosissima, P. pubescens, P. sericea, and S. exigua on 9 June 1994 and 23 August 1994. The number of stems used in each trace is indicated in the text.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 36

June

August

(0 1.5

XJ i O) £ _ 0.5 o E n . 0 600

OÔ to = 400 t"E |ï 200 I 5 0 Salix Tamarix Prosopis Pluchea Salix Tamarix Prosopis Pluchea Figure 2-4. Interspecific comparisons of leaf total Kjeldahl nitrogen (TKN) (A), leaf chlorophyll concentration (B), photosynthetic rate (C), stomatal conductance (D) and instantaneous water use efficiency (E) on 9 June 1994 (open bars) and 23 August 1994 (closed bars). All values are means ± SE. Values with the same letter are not significantly different (least squares means, a = 0.05)

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 37 Stomatal conductance declined with seasonal drying conditions and showed

significant between-species differences (Fig. 2-4D; Day X Species Interaction F = 10.54,

df = 3,184). Interspecific differences in gs tended to disappear with the imposition of

drought stress.

There were no significant species-specific drought responses in water use

efficiency (Day X Species Interaction F = 1.5, df = 3, 184). All species showed a large

significant increase in WUE over the hot, dry summer (Fig. 2-4E; F = 200, df = 1,184).

In both June and August, Pluchea demonstrated a significantly lower WUE than the

other three species (F = 6.25, df = 3, 184)

Factor analysis (Fig. 2-5) illustrated that the majority of variation in the gas-

exchange data (4 species X 2 dates) was due to water use (Factor 1 ; gs + E) and the extent

of environmental stress (Factor 2; T, - 'F|). A significant interaction existed between

species and day in the Factor 1 values (F = 11.3, df = 3, 184) in which Salix had

significantly higher water use values than Tamarix and Prosopis, which had significantly

higher values than Pluchea in June (all comparisons: Least Square Means, a = 0.05).

Day and species main effects were significant in sorting Factor 2 scores (F = 35.4, df = 1,

184 and F = 19.4, df = 3,184, respectively), whereas Factor 2 showed no day X species

interaction (F = 0.8, df = 3, 184). Salix had significantly lower Factor 2 values than the

other species, which corresponds to lower T, and less negative (Fig. 2-5; Fisher’s

Protected LSD, a = 0.05). Factor 2 values declined firom June to August (Fig. 2-5).

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 38

1 .5 June

0.5 ' f 0 }

•0.5 -

- 1

B -1 .5 + A August • Tamarix 1 1 □ Prosopis A Pluchea 5 Salix ■ 1 I 0 I ____ —

0 - % •0.5 -

- 1 -

-1 .5 j_ _L - 1 0 1 2 3 Factor 1

Figure 2-5. Factor analysis of the physiological data set from Fig. 2-4 on 9 June 1994 and 23 August 1994. Factor 1 (abscissa) is a linear combination corresponding to the greatest eigenvalue of the correlation matrix (Xj = 2.32, proportion = 46%, factor 1 = 0.09 T| + 0.25 A + 0.41 gs + 0.40 E + 0.18 'Pi). High values along factor 1 indicate high water use as a summation ftinction of stomatal conductance and transpiration. Factor 2 (ordinate) is a linear combination corresponding to the second greatest eigenvalue ÇK2 = 1.35, proportion = 27%, factor 2 = 0.66 T| - 0.25 A - 0.01 gs + 0.22 E - 0.45 'Pi). Greater values along factor 2 indicate higher leaf temperatures and more negative leaf water potentials. Values are means ± SE

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 39 Discussion

The results obtained in this study from a young successional, mixed-species

community are similar to our findings from previous studies with more mature Tamarix-

dominated communities. For instance, Tamarix possessed similar leaf-level transpiration

rate (Busch and Smith 1995) and sap flow (Sala et al. 1996) as did co-occurring native

phreatophytes. The tendency for Tamarix to operate at lower plant water potentials also

agrees with our past findings for both mature and post-bum communities (Busch and

Smith 1993,1995). Lower plant water potentials in Tamarix may be a consequence of its

ability to utilize unsaturated soil moisture sources, whereasSalix has been shown to be an

obligate phreatophyte (Busch et al. 1992). The ability to use water from unsaturated soil

layers can be a factor in both stress tolerance and nutrient uptake, as soil nutrients are

often more abundant above the saturated soil zone (Pinay et al. 1992).

The sap flow results from this study (Fig. 2-3) provide an interesting perspective

as to why Tamarix may be able to replace native phreatophytes over time in desert

fioodplain habitats (Christensen 1962; Robinson 1965; Brock 1994; Busch and Smith

1995). Although Tamarix has comparable transpiration rates as the other species at the

leaf level (as measured with gas exchange; Fig. 2-4) and per unit canopy leaf area (as

measured with xylem sap flow; data not shown), it exhibits much higher transpiration per

unit sapwood area (Fig. 2-3). This means that Tamarix is able to maintain higher leaf

area per unit sapwood area and invest much less biomass and energy into non

photosynthetic stems under non-stress conditions. The decline in the per unit sapwood

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 40 area sap flow in Tamarix with drought stress, without a concomitant decline in per unit

leaf area sap flow, may be caused by a differentially greater leaf loss in Tamarix over the

summer, a phenomenon that has yet to be tested. Because of its ability to maintain

sapflows at high canopy-level transpiration rate (Sala et al. 1996), Tamarix has the ability

to desiccate floodplains and lower water tables (Blackburn et al. 1982). This creates an

environment to which Tamarix is better adapted than are the native phreatophytes, which

are more intolerant of water stress (Busch and Smith 1995) and do not utilize unsaturated

soil moisture sources when water tables become depressed (Busch et al. 1992).

When exposed to a lack of soil moisture, Tamarix has been reported to shift

transpiration to an earlier time period in the day and to decrease transpiration later in the

day (Devitt et al. 1997). Tamarix, Pluchea, and Prosopis maintained highest sap flow

through the midday period, coincident with highest leaf-to-air VPD’s during the 1994

drought, whereas Salix shifted canopy transpiration to the morning hours (Fig. 2-3). This

indicates that Salix exhibits a more pronounced midday depression in stomatal

conductance late in the dry season than do the other three taxa, which has also been

observed in mature plants (Busch and Smith 1995).

Key trends in gas exchange behavior (Fig. 2-4) were that (1) Tamarix and Salix

exhibited lower leaf-nitrogen concentration but comparable photosynthetic rate as

Prosopis, indicating that they operate at higher nitrogen use efficiency (NUE, =

than the leguminous Prosopis, (2) Tamarix operated at equivalently lower g$ and

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 41 photosynthetic rate than Salix, indicating that Tamarix operates at similar WUE as Salix,

and (3) Pluchea had the lowest photosynthetic rate and WUE of the four species.

Tamarix ramosissima has been previously shown to exhibit a lower leaf carbon isotope

ratio, and thus higher WUE, than Pluchea sericea and Salix gooddingii, a more mesic

species of willow (Busch and Smith 1995). The low WUE of Pluchea is consistent with

its status as a ruderal shrub in this ecosystem, and its low photosynthetic rate is consistent

with its evergreen habit (Chabot and Hicks 1982). Furthermore, Pluchea was the only

species to show increased photosynthesis and leaf nitrogen and chlorophyll

concentrations in August, consistent with its status as a summer-active halophyte (Busch

and Smith 1993).

Factor analysis o f the gas exchange variables (Fig. 2-5) illuminated two factors

that might govern successional trajectories for these four woody species with respect to

environmental changes over time. The first factor (i.e., the abscissa), which was

characterized as explaining the greatest amount of variation in the physiological data set,

was related to plant water use (gs and E). The second factor, characterized as explaining

approximately one-half of the variation as did factor 1, was defined by T, and 'F,, where

high values indicate high absolute values of T( and 'Fi. The four species separated based

on factors 1 and 2 in June (early drought), with Salix having the highest water use, and

based on factor 2 in August (late drought), with Tamarix having the most negative 'F, and

highest T|. Because there was separation on factor 1 during the early drought conditions,

differences in factor 2 during early drought were of minimal importance. However,

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 42 when factor 1 lost importance toward the end of the drought, factor 2 primarily explained

the internal structure of the physiological data set In other words, the ability to use

water shows the greatest species discrimination under more mesic conditions (e.g.,

during high flow years or early in the growing season of dry years), and some function of

stress or stress tolerance affected the greatest discrimination under xeric conditions (e.g.,

during low flow years or during the summer dry season). Over the course of decades, it

appears that the cumulative enviromnent in the lower Virgin River favors stress tolerant

plants like Tamarix (Fig. 2-2), a relationship that is exacerbated by Tamarix's ability to

desiccate floodplains through the maintenance of high community leaf area. Salix may

thus be expected to be most successful during wet years or in early-successional

communities, while Tamarix, the most stress-tolerant species, would be expected to

exhibit greatest differential success during drought years and in late-successional

communities.

Stem growth further suggests Tamarix is a slow-growth species relative to the

other three woody phreatophytes (Table 2-1), typical of a stress tolerant species (Grime

1974). Salix, Prosopis and Pluchea have similarly high growth rates as Tamarix from

Navajo National Monument, Arizona (Brotherson et al. 1983), while Tamarix from three

different Mojave Desert sites demonstrate slower growth rates. While the high growth

rate for Pluchea is inconsistent with its evergreen form, it should be emphasized that

Pluchea stems are much shorter lived (all stems < 5 yrs old) than the stems of most of the

other species. Therefore, the high stem growth rate (Table 2-1) in Pluchea is an anomaly

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 43 of the allometric relationship between diameter (a linear measure) and surface area (i.e.,

Pluchea has a lower stem diameterzarea ratio than the other species).

This study reinforces our past findings with mature stands (Sala et al. 1996),

which indicated that Tamarix tends to dominate successional fioodplain communities in

the Southwest over time (Fig. 2-2). The similarity of these findings with earlier studies

indicates that either a 3-yr-old stand is sufficiently old to physiologically resemble more

mature stands or species-specific responses to the fluctuating and changing environment

are consistent throughout the lifespans of all of these species. If this young successional

stand does resemble more mature stands, different physiological relationships between

these four species could occur in younger seedling beds. On the other hand, seedling

beds would teU us exactly the same story if these fioodplain species do not respond to

age, size and succession as found in other systems (Knapp and Fahnestock 1990; Dawson

and Ehleringer 1991; Donovan and Ehleringer 1991; Bragg et al. 1993; Schoettle 1994).

In conclusion, Tamarix is able to dominate fioodplain communities in the desert

Southwest due to its ability to tolerate water stress late in the growing season or as an

effect of long-term drought. As a direct consequence of this stress tolerance adaptation,

Tamarix is able to maintain high leaf area (and high landscape transpiration rate; Sala et

al. 1996) under the extreme evaporative conditions that typify desert climates. As

Tamarix is the most stress tolerant of these putative competitors, reduction in streamflow

rates could further promote the invasion of desert floodplains by Tamarix.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 44 Acknowledgements

We would like to thank Simon Lei and JeffPiorkowski for assistance in the field,

Kim Mace for assistance in the laboratory and with data analysis and Matt Ronshaugen

for help with data analysis and graphics. Our further thanks to the two anonymous

reviewers who provided valuable editorial comments on this manuscript. This study was

supported by funding from the Las Vegas Valley Water District.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. CHAPTERS

A FLUID-DYNAMIC MODEL OF ADVECTIVE ENERGY EXCHANGE BETWEEN ADJACENT ARIDLAND SHRUB AND RIPARIAN ECOSYSTEMS

This chapter has been prepared for publication in Agricultural and Forest Meteorology and is presented in the style of that journal. The co-authors who have contributed substantially to this manuscript are Anna Sala, Dale A. Devitt, Lynn K. Shaulis and Stanley D. Smith.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 46

Abstract

Riparian ecosystems in arid landscapes have lower air temperature and higher

relative humidity than the surrounding desert, which is imposed by greater

évapotranspiration (ET) from the riparian vegetation and the desert shrubs. This

imbalance in ET rates creates conditions which drive sensible heat from the desert to the

fioodplain, allowing greater ET in the fioodplain than the net radiation energy should

permit. An analytical, atmospherically-based model was developed to investigate the

relationships between environment, lateral transfer of sensible heat energy and ET along

the Virgin River in the Mojave Desert. A Bowen Ratio energy balance system was used

in 1994 and 1996 (Devitt et al. 1998) to parameterize diel fluid-dynamic relationships

between heat and wind fiow under clear conditions. In 1994, mesoscale transfer of

sensible heat from the adjacent desert occurred following sundown and continued until

sunup; however, in 1996, advection only occurred during the latter portion of the night.

Furthermore, stream discharge was 51,462 m^ day'^ (two-fold) greater in 1994. Sensible

heat advection is demonstrated to promote the invasion of the exotic species Tamarix

ramosissima, and the presence of Tamarix, in turn, promotes both the advection of

sensible heat and stand-level water consumption. Topographical constraints, vertical and

horizontal eddy formation, plant vigor, streamfiow and regional air temperature are

associated with patterns of energy balance, sensible heat advection, and

évapotranspiration in an aridland riparian ecosystem.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 47 Introduction

Desert riparian corridors develop localized conditions of lower air temperature

and higher relative humidity relative to the surrounding aridland. The cause of these

gradients of temperature and humidity is augmented transpiration from the riparian

species (Malanson 1995). The magnitude of these differences between the riparian and

adjacent desert shrub ecosystems is often related to numerous characteristics of the

riparian plants in the corridor. In the southwestern U.S., key properties influencing leaf-

level evaporative demand and canopy relative humidity are leaf area index and species

composition (Sala et al. 1996). Tamarix ramosissima, an invasive weed responsible for

the degradation of riparian corridors throughout the western U.S., produces a thick

network of branches supporting very high leaf area index with little intracanopy air

movement. Actual évapotranspiration from such riparian vegetation affects river course

desiccation and large scale energy flux dynamics, promoting invasion of these

ecosystems by Tamarix. The study of évapotranspiration involves careful

characterization of both the physical and biological components of these ecosystems, for

physical and biological processes closely interact in their control of ecosystem processes.

Stand-level évapotranspiration can be estimated from an analysis of the energy

balance above a plant canopy. In such investigations, energy flux (W m'^) is partitioned

into the latent heat of évapotranspiration (XET), sensible heat flux (H), soil heat flux (G),

and net radiation (RJ. The most simple form of the energy balance considers these flux

components in a one-dimensional vertical model of canopy fluxes. Flux toward the

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 48 canopy (or radiant surface) is taken to be negative and away from the canopy is taken to

be positive, such that XET + H + G -R „ = 0 (Jury et al. 1991). It is common to assume

that the energy balance can be closed locally (i.e., phenomena outside the area of fetch do

not impact energy balance) and that storage of energy is minimal.

Numerous methods of estimating stand-level energy balance and

évapotranspiration have been developed, among which are micrometeorological

techniques such as Pemnan-Monteith potential évapotranspiration (ETq; Rao et al. 1990),

Bowen ratio (p = ; Fieri and Fuchs 1990; Devitt et al. 1998), and eddy covariance AET

(Anderson and Verma 1986; Kim and Verma 1990; Dugas et al. 1991), as well as remote

sensing techniques such as Lidar (Eichinger et al. 1993), infrared thermometry (Inoue et

al. 1990; Caselles et al. 1992; Courault et al. 1996), and multispectral analysis (Reginato

et al. 1985; Fenstermaker-Shaulis et al. 1997). Many of these methods integrate the

average values for an area of given fetch, and the footprint effect (i.e., weighting of

upstream contributions to AET; Brunet et al. 1994) can severely limit the usefulness of

such methods under advective conditions (i.e., when energy is transferred horizontally

rather than vertically; Verma et al. 1978; Lang et al. 1983). Such advective conditions

are common in arid and semiarid regions (Malek 1987; Lemeur and Zhang 1990).

Horizontal transfer of energy has been measured using eddy covariance, and the

magnitude ranges from -25 to -150 W m'^ in a semiarid region (Anderson and Verma

1986) to -100 to -300 W m'^ in an arid region (Dugas et al. 1991).

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 49 Under stable conditions (i.e., when temperature increases with height and sensible

heat flux is toward the canopy; Wu 1990), methods that depend upon energy balance and

its assumptions may be unreliable. Evapotranspiration estimated under advective

conditions is unreliable because (1) the ratio of turbulent exchange coefficients of water

and heat (Kh / Kw) deviates from unity (Verma et al. 1978), and (2) a drier adjacent

ecosystem can influence évapotranspiration from beyond the estimated fetch of the

measurement (de Vries 1959; Cooper et al. 1992). The magnitude o f advected energy

exchange between ecosystems depends upon the three-dimensional pathway of energy

transfer from one ecosystem to another, and the range of this footprint effect can be from

1 km (de Vries 1959; Eichinger et al. 1993) to 60 km (Weick and Rouse 1991).

Sensible heat advection occurs when a well-hydrated surface, such as an irrigated

field or a riparian forest, is juxtaposed with a hot, dry surface, such as a desert. When the

fioodplain is adequately hydrated, advection contributes to augmented AET, in excess of

that attributable to net solar radiation (i.e., AET > R„; Sala et al. 1996; Devitt et al. 1998).

This is because the cooling effect of latent energy flux creates a step-gradient in

temperature between the two ecosystems (Brunet et al. 1994; Hier et al. 1994). This

temperature gradient causes the establishment of a horizontal sensible heat flux between

ecosystems, oriented from higher temperature to lower (i.e., oriented toward the

fioodplain or irrigated ecosystem). Sensible heat advection has been investigated

primarily over irrigated plots (Hanks et al. 1971; Anderson and Verma 1986; Wu 1990;

Brunet et al. 1994) because they exhibit just such a simple step-up dry-to-irrigated

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 50 transition. At this scale, sensible heat advection (i.e., the border effect) occurs at the

margin of ecosystems (Hanks et al. 1971).

While the pathway of sensible heat transfer is defined explicitly over irrigated

plots, many topographical constraints are lacking because the irrigated and unirrigated

ecosystems are at the same elevation and are on a relatively flat plane. Riverine

environments pose a problem in that the riparian corridor occurs as both a heat sink (de

Vries 1959; Devitt et al. 1998) and a topographical depression. However, heat rises from

the surrounding aridland as a result of natural convection (Kreith and Bohn 1993), rather

than flowing laterally into the riparian ecosystem. Such topographical constraints have

been incorporated into a few energy balance studies, including the relationship between

mountain topography and Bowen ratio tower positioning (Fritschen and Qian 1990).

Even though horizontal sensible heat transport always occurs via wind, the

pathway of energy transfer depends upon the scale at which it occurs. Large scale (i.e.,

stand-level) sensible heat advection is characterized by a temperature inversion in which

the air above the canopy’s boundary layer is warmer than the canopy air temperature

(Hanks et al. 1971). In this case, sensible heat is horizontally transferred from the desert

above the fioodplain, then it is transferred through the boundary layer, rather than at the

fioodplain margin. Such conditions exist primarily during nighttime (Hanks et al. 1971)

and are believed to not impact évapotranspiration because sensible heat storage is

assumed to be negligible.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 51 This research was performed as a follow-up study to earlier research along the

Virgin River, Nevada (Devitt et al. 1998), in which Bowen ratio estimates of AET were

investigated over the 1994 and 1996 growth seasons. In such a habitat, advection of

sensible heat can favor stress-tolerant and invasive species at the expense of more stress-

sensitive native species (Smith et al. 1991; Busch et al. 1992; Busch and Smith 1995).

Analysis of the energy balance partitioning demonstrated that sensible heat advection is

most likely confounding the ability of the energy balance in general, and Bowen ratio

estimates of the energy balance in particular, to provide reliable estimates of AET.

Because AET exceeded R^ more often during 1996 than in 1994, the authors concluded

that greater sensible heat advection occurred during 1996 than during 1994 (Devitt et al.

1998). 1994 was a year characterized by extreme temperature and aridity (Chapter 2),

while water availability at the Bowen tower site declined in 1996 because of river

downcutting in the extreme flooding of 1995 (Devitt et al. 1998).

The main objective of this study was to investigate sensible heat advection over a

desert riparian corridor using a simple analytical model that can be parameterized from

variables collected by a Bowen Ratio Energy Balance (BREB) system. We tested four

hypotheses: (1) that large scale sensible-heat advection would occur at nighttime (Hanks

etal. 1971) as well as during the day; (2) sensible heat advection into aridland riparian

corridors would be more sensitive to topography and bulk airflow than to gradients in

energy flux because of the stable conditions imposed by topographical constraints; (3)

sensible heat advection at various scales would impact Bowen Ratio estimates of AET;

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 52 and (4) sensible heat advection at this location would be lesser in a dry year than in a

higher runoff year.

Fluid-dynamic Model

Natural convection drives sensible heat flux upward from desert surfaces during

the day. Because riparian corridors occur as both topographical depressions and heat

sinks, a one-dimensional model is inadequate to incorporate the convective cells that are

required to explain the bulk fluid flow of heat and moisture between the desert and

fioodplain ecosystems. Therefore,

a two-dimensional convection-cell

model was adopted as a system

Riparian Shrub analogous to thunderstorm- Figure 3-1. Heat transfer schematic model. The fioodplain is represented as the lower generating atmospheric conditions. bowl-shaped section, and the adjacent desert builds up to mesas in steps. Heat is driven in which heat from the surrounding off of the desert through natural convection (A), which draws the cooler, moist air from desert is naturally convected across the fioodplain (B). The heat then sinks back into the fioodplain (C) under stable the fioodplain (Fig. 3-1). Low conditions. U» represents the superboundary wind speed perpendicular to pressure induced by the bulk flow the riparian corridor. of heat from the surrounding desert draws cooler, moisture-laden air out of the fioodplain

and into the desert. This movement of latent heat out of the fioodplain creates vertical

plumes above the fioodplain through which the advected sensible heat is drawn down

into the riparian corridor. This pathway o f sensible heat advection describes the wind-

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 53 flow dynamics, implying the magnitude of neither the sensible heat advection, the related

temperature gradients, nor the extent of ET augmentation.

As advected sensible heat passes over the floodplain, the inertia of the

floodplain’s outward-flowing boundary layer is assumed to create turbulent conditions in

a supertending advection boundary layer; C is the downward flux through this boundary

layer (Fig. 3-1). It was assumed that the advection boundary layer behaves as a boundary

layer superimposing a solid surface. Given this assumption, advected sensible heat is

realized as a heat flux, directed downward through the advection boundary layer and

driven by eddy transfer within a turbulent boundary layer (Kreith and Bohn 1993).

Heat is transferred through the advection boundary layer by molecular conduction

and turbulent transfer (Kreith and Bohn 1993):

where q" (W m'^) is the total rate of heat transfer, Cp (J kg'" K'^) is the specific heat of air

at constant pressure, p (kg m'^) is the mass density of air, a (m^ s'‘) is the thermal

diSusivity due to molecular conduction, Eh (m^ s'*) is the thermal eddy difflisivity, and

dT — represents the time-averaged temperature gradient with respect to the boundary layer dz

thickness. Kreith and Bohn (1993) further demonstrate that, in fluids other than liquid

metals, a is negligible. So the difflisivity constant, Eh , is the key variable in determining

the transfer of sensible heat firom the upper, warmed advection boundary layer into the

lower, cooled floodplain boundary layer.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 54 The turbulent Prandtl number (Prt: ratio of the eddy viscosity to the eddy

difflisivity, Em/eh ) is approximately unity in air (Kreith and Bohn 1993). Furthermore, Em

= vY (Kreith and Bohn 1993), thus

£H = e M =

where v' is the vertical eddy velocity deviation from the time-averaged vertical velocity,

v; V is equal to zero in a boundary layer superimposing a solid surface (Kreith and Bohn

1993). i (m) represents the Prandtl mixing length, in which

u '= £ ^ , dz

where u' is the horizontal eddy velocity, u' is a function of the surface roughness o f the

floodplain boundary layer (upon which the advection layer lies), and — is a function of dz

the windspeed above the boundary layer (U»). As with v', u' equals the deviation from

the time averaged horizontal wind speed, ii.

Materials and Methods

Parameterization of step C (Fig. 3-1) in this model was performed using a Bowen

Ratio Energy Balance (BREB) system with a wind sentry cup-anemometer and wind

vane (Li-Cor, Lincoln, NE). This system was established on the Virgin River, Nevada

(36° 35' N, 114° 20' E, elevation 380 m), and was described more fully by Devitt et al

(1998). BREB systems are designed such that the lower arm is just above the

vegetation’s maximum boundary layer thickness. Thus, the lower arm is also taken to be

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 55

near the bottom of the advection boundary layer, where u is minimum. Because — dz

approaches zero in the upper boundary layer (Kreith and Bolm 1993), the upper arm was

well above the lower arm and could approximate the higher limit of the upper boundary

layer. The distance between the upper and lower arms (= dz) was 3.5 m, supertending

the 4 m tall canopy by 1.5 m (Devitt et al. 1998).

In each year of the study, four days of clear sky and advective conditions (as

indicated by XET > R^) were used to estimate all of the variables used in this model. The

BREB tower collected and recorded 20 minute average values of temperature, wind

speed and wind direction (Devitt et al. 1998). q" was solved for each o f those intervals

over the course of the four days, beginning at 0020 hours on June 27, 1994 and at 0020

hours on July 18,1996.

The values of Cp and p were interpolated by second-order linear regression (SAS,

SAS Institute, Cary, N.C.) of the temperature by Cp and p tables in Kreith and Bohn

(1993). The average temperature between the two BREB arms provided an estimate of

the mean temperature (° C) of the advection boundary layer, from which p = 1.18 —

0.0023 T + 0.0000014 T^ (r^ = 0.93) and Cp = 1009.2 + 0.13 T (i^ = 0.999) were

calculated.

The Virgin River flows from north to south within a >1 km-wide floodplain at

this location, so wind from the north and south will have originated above the floodplain;

such wind will not carry advected heat from the desert. Air originating from both the

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 56 west and east, however, will be fully capable of convecting heat into the floodplain. To

weight the wind speed by its origin, wind speed was replaced by the transverse wind

speed ( u t ),

Ut = (wind speed) | sin ( wind direction ) |.

Time averaging of temperature (in ^^), wind speed (in — ), and the covariance dz dz

between v' and ^ (in v’£) was based upon spectral and co-spectral time series analyses of

T and Uy (proc spectra, SAS, SAS Institute, Cary, NC; Bendat and Piersol 1993).

Coherence between the autocorrelation functions of T and uy estimated the frequency at

which these variables fluctuated in phase. The time constant was calculated as one-

fourth the periods of peak power spectrum and coherence. Time-averages were

calculated as moving averages, including one-half the time-averaging constant prior to

and one-half following the individual observations calculated.

As well as q", vertical wind speed is unmeasured by the BREB system. So, a

range of v' was used to investigate the effect of vertical eddy formation and topography

on q". Because vertical and horizontal eddy velocities are inversely related in a turbulent

boundary layer (Kreith and Bohn 1993), vertical eddy velocity was calculated as v' = / (-

u') at each time step.

The Bowen Ratio (p) during each year’s time series was compared to q" with a

single-factor analysis of covariance (ANCOVA; SuperANOVA, Abacus Concepts,

Berkeley, CA) in which year (1994,1996) was the factor, q" was the covariate, and the

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 57 dependent variable was p. The probability of a type I error was presumed to be a = 0.05

(p < 0.05).

The relationship between q" and environmental conditions between 1994 and

1996 were compared using streamflow and temperature as indicators of environmental

status. Streamflow data were collected from the USGS (1998) Littlefield (36° 53'N, 113°

55'E, elev. 538 m) gauge (upstream) and temperature data were collected from the

NOAA (1998) Boulder City (35° 981^, 114° 85'E, elev. 770 m) sensor.

Results

In both years, wind speed was higher and directed from the south during daytime

hours, while nighttime wind speed and direction was lesser and from the north (Fig. 3-2).

Wind speed was up to 1 m s'* higher in 1996 than in 1994, with a ten-degree easterly

influence during 1996 (Fig. 3-2) that wasn’t present in 1994.

A nocturnal temperature inversion, in which the upper atmosphere was warmer

than near the canopy, was more pronounced in 1994 than in 1996. This interannual

difference occurred particularly from midnight to dawn (Fig. 3-3 A). During daylight

hours in 1996, near the canopy was warmer than the overlying air (Fig. 3-3 A). Wind

speed perpendicular to the floodplain was greatest in the afternoon (Fig. 3-3B). The

period of strongest wind flow across the floodplain occurred as the evening temperature

inversion was developing (Fig. 3-3).

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 58

Day

Night

270' 90'

225

180° B 0°

270' 90'

180° Figure 3-2. Horizontal wind speed and direction during day (open circles) and night (closed circles) in 1994 (A) and 1996 (B). Distance from the origin represents wind speed (m s'*) and angle with the origin represents wind direction (°). O'* is wind from the North, 90° is East, 180° is South, and 270° is West. Values are 20 minute averages during the 4-day test runs described in the Materials and Methods.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 59

Nearly all of

the temperature Time 0:00 4:00 8:00 12:00 16:00 20:00 24:00 variation occurred 1.5

at a frequency of 1 1 994 1 1 996

cycle day'* (Fig. 3- Ê Ü 0.5 4). Likewise, the ux T3N

repeated at 1 cycle 0

day'* (Fig. 3-4), -0.5 although the wind 1.5 profile showed

higher frequency 1

harmonics of much 0.5 smaller magnitude. 0 Both functions are 0:00 4:00 8:00 12:00 16:00 20:00 24:00

Time in phase at 1 cycle Figure 3-3. Mean measured diel temperature gradient (dT/dz, day'* (Fig. 3-4), so a A) and transverse wind speed (uy, B) above the floodplain canopy for 1994 (solid line) and 1996 (dashed line). Positive period of one- values of dT/dz indicate cooler air within the canopy; i.e., stable conditions. Higher values of Uy indicate higher wind quarter days (i.e., 6 speed coincident with wind direction more directly crossing (rather than following) the corridor ______hours) was chosen

as the time averaging constant for T, % and 'v'i.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 60 Regional sensible heat advection (q") occurred during nighttime in both 1994 and

1996 (Fig. 3-5). In 1996, q" was greatest in the night between midnight and dawn, after

1 00

B 10 ns TX u (DCO "cB (DÜ Q. 0.1 CO

0.01 0 1

Frequency (cycles day’ )

Figure 3-4. Spectral (bars) and coherence (line) estimates of the measured temperature (T; open bars) and transverse wind speed (uy; closed bars) profiles.

which sensible heat flux was directed toward the sky (Fig. 3-5). For a given v', q" was

greater on these clear days in 1994 than in 1996.

There was not a meaningful relationship between q" and p in either year

(ANCOVA r^ = 0.10, p < 0.0001; Fig. 3-6). However, significant effects by year (F =

22.8, df = 1,488), q" (F = 27.5, df = 1, 488), and year X q" (F = 12.6, df= 1, 488) existed

in which

P = - 1.22 (year) - 0.01 (q") + 0.01 (year) (q")-

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 61 In 1994, when p was 1.22 fold higher (Fig. 3-6) and q" was lesser (Fig. 3-5),

environmental conditions were more moderate: streamflow was greater, vegetation more

vigorous (and not isolated on terraces; Devitt et al. 1998), and average temperature (both

maximum and minimum) was slightly lower (Table 3-1).

Discussion

We investigated sensible heat advection over a desert riparian corridor by

applying an analysis of natural convection to the topographical constraints normally

encountered across a desert-riparian landscape (Fig. 3-1). Over this monospecific

Tamarix ramosissima stand, large scale advection was indicated during both summers by

the imposition of a temperature inversion during evening and early morning hours (Fig.

3-3A; Hanks et al. 1971).

The key parameters (T and Uy) that control the convection of heat across a

boundary layer (Kreith and Bohn 1993) showed variability in very close agreement with

previous findings (Devitt et al. 1998), where wind direction was predominantly from the

north and south (Fig. 3-2). The predominate wind direction, however, did not preclude

the transverse transfer of sensible heat because of the secondary effect of wind fiow

across the predominate direction (compare Figs. 3-2 and 3-3). Furthermore, T and u

varied in phase at 1 cycle day * (Fig. 3-4; Devitt et al. 1998). Sensible heat flux and

temperature inversion formation also cycled in a more-or-less diel pattern (Figs. 3-3 and

3-5), certainly indicating that heat exchange is related to T and Uy. Secondary peaks in

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 62

Time

0:00 4:00 8:00 12:00 16:00 20:00 24:00 250 1 994

200

1 50 -0.05 u' -0.025 u' 1 00

§ 50 I- “ O CM

250 1 996

CO 200 § CO 1 50

1 00

0:00 4:00 8:00 12:00 16:00 20:00 24:00

Time

Figure 3-5. Diel pattern, of calculated sensible heat advection (q"; W m'^) in 1994 (A) and 1996 (B). Three functions o f the vertical eddy deviation velocity (v') with respect to the horizontal eddy deviation velocity (u') are presented: v' = -0.1 u', -0.05 u', and -0.025 u’.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 63

1 0

# 1 994

□ 1 996 CÙ

n n

- 5

1 0 100 200

q" (W m-2)

Figure 3-6. Relationship between the measured Bowen ratio (p) and calculated sensible heat advection (q") in 1994 (circles) and 1996 (sq u ares).______the coherence function are clearly aliases, as the T power spectrum shows no variability

at those frequencies. Therefore, no other time averaging constants were investigated.

Stand-level sensible heat advection occurred primarily at night (Hanks et al.

1971). In fact, stand-level sensible heat advection does not occur at all from early

morning through early evening (Fig. 3-3A). The temperature gradients established by a

wet-to-dry transition, on the other hand, occur during the daytime, when there is the

greatest imbalance of XET and between adjacent landscapes with high and low water

availability. While such sensible heat advection is undoubtedly occurring at the fringes

of the floodplain (Devitt et al. 1997), it is not detectable by stand-level measurement

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 64 techniques. The 12 hr time-lag in advection observed here (Fig. 3-5) indicates that stand-

level sensible heat advection over an aridland riparian corridor is sensitive to topography

and bulk airflow rather than gradients in energy flux (i.e., A forces B, which creates

atmospheric disturbance at C in Fig. 3-1). Although sensible heat advection is driven

primarily by topographical and aridland shrub energy balance, X£T augmentation is

affected by both the horizontal transfer of sensible heat (Devitt et al. 1998) and the earlier

transport of A£T to the desert (i.e., both B and C determine the magnitude of XET

enhancement).

Sensible heat advected at nighttime is assumed to have no impact on energy

balance or XET (Hanks et al. 1971). Such an assumption is a direct result of the BREB

Table 3-1. Environmental characteristics associated with sensible heat advection in 1994 and 1996. Yearly streamflow data were collected firom USGS (1998) and temperature data were collected firom NOAA (1998) for July. Vegetation appearance was reported in Devitt (1998). The percentile indicates that proportion of years (in percent) in which streamflow was lower. Statistical comparison of the July temperatures was not possible because NOAA only reports a single monthly value (i.e., n = 1 and df = 0). 1994 1996 Streamflow (m^ day ') 446,671 395,209 Percentile 47'" 28'" Vegetation appearance Vigorous Poor Tm«(°C) 37.8 38.5 Tmm (°C) 26.1 26.4 assumption that energy storage is inconsequential. This important assumption may be

invalidated under advective conditions, in which morning storage of sensible heat may be

released in the afternoon (McCaughey 1985). This study found no release of sensible

heat during 1994 and midmoming release of sensible heat during 1996 (Fig. 3-5),

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 65 suggesting that increased temperature stress (when water availability is insufficient of

full conversion of q" to XET) or increased A£T (when water availability is adequate) may

occur during midmoming hours, when stored sensible heat might be released.

Advected sensible heat can be stored in standing water, in the soil, in the

floodplain boundary layer, or in plant tissue. The soil heat capacity varies with soil water

content (Jury et al. 1991), making it difficult to investigate separately from the standing

water sink. However, the soil heat flux was constant and small (Devitt et al. 1998),

suggesting that substantial sensible heat storage does not occur in the soil (Malek 1993).

While standing water is a minor component during most summer months on the Virgin

River, both water availabihty and standing water undoubtedly affect the fate of sensible

heat advection toward augmenting heat stress conditions or lET.

Also correlated to water availability are the sensible heat storage sinks in the

boundary layer and in plant tissues. Decreased water availability can reduce the vigor of

Tamarix (Devitt et al. 1998), and the decreased density and LAI of unhealthy Tamarix

stands cause decreased boundary layer humidity (Sala et al. 1996), also decreasing its

heat capacity. The same is probably also true for the more sensitive native species along

the Virgin River.

The presence of Tamarix on the floodplain potentially lessens q" by reducing the

vertical temperature gradient. Just as humidification of the boundary layer by dense

Tamarix thickets can lessen the atmospheric demand for leaf-level transpiration (Sala et

al. 1996), boundary layer humidification reduces the magnitude of advection-related ÀET

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 66 augmentation. However, boundary layer humidification by Tamarix occurs during the

daytime, and has minimal effect on q". However, this leaf-density effect by Tamarix

would increase the magnitude of XET augmentation, contributing to greater water loss

from the ecosystem.

Water on the surface of saltcedar leaves comprises another reservoir for sensible

heat storage. Whatever the source of this water, whether guttation or nighttime

condensation (Decker 1961), the presence of saltcedar augments the effect of sensible

heat advection by absorbing that energy during the nighttime and releasing it during the

day. Increased q" due to this mechanism interacts in a positive feedback fashion with

leaf-density based XET augmentation by Tamarix described above. Absorbance of

sensible heat on leaf-bound water drops further favors Tamarix by conducting heat

directly to the leaf tissue (Butler 1985), buffering it against low temperatures that can

inhibit Tamarix^ growth (Chapter 6).

In addition to stand-level sensible heat advection, the presence of both within-

canopy advection and border advection have been inferred using heat-balance sapfiow

and lysimetry on the Virgin River (Devitt et al. 1997). Related to these other pathways

of advection, boundary layer humidification by Tamarix further impacts the contribution

of sensible heat advection at various scales. A negative feedback relationship between

saturation deficit and stomatal function tends to reduce border advection at the floodplain

margins (McAneney et al. 1994), and this feedback is weakest under dry conditions,

when stomatal physiology is constrained by factors other than sensible heat advection

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 67 (e.g., 1996; Table 3-1). Thus, lower stand-level sensible heat advection (Fig. 3-5B) was

somewhat offset by greater daytime border advection because plant performance was

compromised (Table 3-1). Such relationships between scales of advection, based as they

are upon energetic relationships in the boundary layer, also affect v' and can further affect

the measured value of q".

The impact of sensible heat advection at various scales can be further illustrated

by the poor relationship between p and q" (Fig. 3-6). Such insensitivity of P to sensible

heat advection is well understood (Verma et al. 1978). When there is adequate water

availability to support XET > (Smith et al. 1995; Sala et al. 1996; Devitt et al. 1998),

the additional energy input from stored q" will contribute to ET augmentation, the

denominator in P = . On the other hand, when there is not enough water available to lE T

achieve ETq, the energy released from stored q" will contribute to H augmentation, the

H numerator in p = ------, The negative q" values that occurred in the early morning 1996 AET

(Fig. 3-5) indicated augmented sensible heat flux into the atmosphere does occur under

drier conditions (Table 3-1; Devitt et al. 1998). Thus, vegetation responses to water

availability cause p to be affected in either direction by q", making it sensitive to sensible

heat advection but not in a way that allows understanding of the energy exchanges

occurring.

Interannual differences in the relationships between vertical energy gradients

(Fig. 3-3A) and sensible heat advection (Fig. 3-5) are best understood with respect to the

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 68 gross environmental conditions during each year (Table 3-1). Whereas sensible heat

advection occurred over a greater number of days in 1996 than in 1994 (Devitt et al.

1998), q" measured in each year illustrated that 1994 had higher maximal q" (Fig. 3-5)

during a 4-day period under clear, strongly advective conditions.

Clearly, techniques that quantify 3-dimensional wind profiles (e.g., Eddy

covariance; Motha et al. 1979; Anderson and Verma 1986; Kim and Verma 1990; Dugas

et al. 1991) can improve our understanding of q" by better characterizing vertical eddy

structure. Lidar (Eichinger et al. 1993) is a good companion to eddy covariance,

providing a spatial context for plume structure (Cooper et al. 1992) and allowing

relaxation of the relationship assumptions between horizontal and vertical eddy

formation. Further instrumentation across the landscape is also recommended,

investigating the applicability of this convection-cell analogy. In such a manner, sensible

and latent heat fluxes over entire landscapes may also contribute to understanding the

large spatial context under which the vegetation consumes water.

Acknowledgements

We would like to thank Tim Ball, Peter Ross, Greg Ross, and Kevin Griffin for

their technical support, and Stan ffillyard and Matthias Rillig for their conceptual

assistance in this project. This research was funded by a grant firom the Las Vegas Valley

Water District.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. CHAPTER 4

WATER, GROWTH AND CARBON RELATIONS FOLLOWING COMPETITIVE RELEASE IN SEEDLING POPULATIONS OF THREE MOJAVE DESERT WOODY FLOODPLAIN SPECIES

This chapter has been prepared for publication in Ecology and is presented in the style of that journal. The co-authors who have contributed substantially to this manuscript are Kent A. Sovocool, Dawn S. Neuman, Dale A. Devitt and Stanley D. Smith.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 70

Abstract

Tamarix spp. are exotic phreatophytes that have invaded much of the floodplain

lands surrounding riverine systems in the southwestern United States. Over two growing

seasons, we explored water relations, growth and carbon storage in a successional

community on a newly created system of sandbars along the Virgin River in southern

Nevada. Interspecific inhibition and facilitation among seedlings of Tamarix

ramosissima and two native phreatophytes {Salix exigua and Pluchea sericea) were

investigated by establishing plots in which all native seedlings were removed firom

Tamarix populations and vice versa.

First-year Tamarix density was reduced 500 plants m'^ by an autumn flood, while

native plant densities were not affected. Plant height was 30 to 50 percent lower for

Tamarix than for the native species, and competition intensity in both Tamarix and

Pluchea varied across stands of differing surface soil water content, water table depth

and soil texture. Tamarix growth was inhibited two-fold by the presence of Pluchea on

erosional surfaces, and growth of Tamarix and Pluchea was inhibited by the other

species in a wet stand and was stimulated by the other species in a dry stand.

The deciduous species (Tamarix and Salix) maintained two orders of magnitude

greater starch concentration in their taproots than did the evergreen Pluchea. Taproot

starch concentration in both deciduous species varied with both the presence o f another

species and with the soil moisture gradient adjacent. Tamarix, in particular, displayed

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 71 storage attributes that, when combined with reduced height growth, indicates that it is a

stress tolerant species. The results from this study suggest that abiotic stress,

physiological stress tolerance, and interspecific inhibition and facilitation mediate the

relative success of woody floodplain seedlings in this arid environment.

Key Words: arrowweed, carbohydrate, competition, coyote willow, environmental

gradients, facilitation, flooding, Pluchea, riparian, Salix, saltcedar, Tamarix

Key Phrases: riparian physiological ecology, abiotic stress and competition intensity,

environmental gradients and carbon allocation, measures o f competition intensity,

ecology o f invasive species, carbohydrate sequestration and energetics, flooding ecology

along aridland rivers, asymmetric interactions and seedling ecology

Introduction

Southwestern U.S. riparian areas have been invaded recently by the Eurasian

woody phreatophyte, Tamarix h . spp. (saltcedar) (Christensen 1962; Robinson 1965;

Brock 1994). Tamarix dominates most riparian systems it invades, replacing native

Populus-Salix (cottonwood-willow) communities (Busch and Smith 1995). The invasive

success ofTamarix is related to its tolerance of drought, salinity, and heat stresses

(Chapter 2; Kleinkopf and Wallace 1974; Busch and Smith 1993; Shafroth et al. 1995;

Devitt et al. 1997). Tamarix ability to recover from soil moisture deficit indicates its

stress resilience (Devitt et al. 1997).

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 72 The invasive capacity of Tamarix has been linked to the formation of dense

stands that create a greater draw on soil moisture resources available in the riparian

corridor (Sala et al. 1996) and with salinization of surface soils associated with its high-

salt litter (Smith et al. 1998). By drawing-down the water table, Tamarix may deprive

potential competitors of soil moisture (Blackburn et al. 1982), while its ability to tolerate

saline soils and utilize water from unsaturated soils confers an important advantage under

more xeric floodplain conditions (Busch et al. 1992; Smith et al. 1998). Clearly,

interspecific interactions associated with Tamarix invasive success in riparian areas of

the southwestern United States are strongly influenced by physiological responses to

abiotic stresses (Busch and Smith 1995).

The role of resource competition in Tamarix invasiveness has been proposed by

Busch and Smith (1995), who found the presence of Tamarix to detrimentally affect light

availability and water potential in Salix. In arid environments, both inhibition and

facilitation can be intense during seedling establishment (Callaway and Walker 1997),

and these interspecific interactions among seedlings can affect community composition

(Fowler 1986; Tilman 1987a; Wilson et al. 1992). As such, ecologists commonly

investigate the roles of inhibition and (more recently) facilitation in establishing

communities (Callaway et al. 1996). While both inhibition and facilitation can occur

simultaneously (Callaway and Walker 1997), the net interaction between two species is

affected strongly by abiotic stress (Holmgren et al. 1997) and biomass allocation (Tilman

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 73 1988) as well as by phenology, physiology and indirect interactions (Callaway and

Walker 1997).

The primary goals of this study were to elucidate the roles of abiotic stress on

interactions between Mojave Desert floodplain species, species effects on stress

amehoration or exacerbation, and how these, in turn, influence relative seedling

abundance and distribution. We tested four primary hypotheses: (1) water relations will

be influenced by both competition and abiotic stress, in which Tamarix is expected to be

more sensitive to the former and the native species are expected to be more sensitive to

the latter (Chapter 2); (2) during seedling establishment, native woody vegetation is

expected to have higher growth rates than Tamarix, as greater growth is found in mesic

versus xeric species (Myers and Landsberg 1989); (3) relative competition intensity

among study taxa is linked to soil moisture (Ware 1991); and (4) Tamarix will

accumulate greater carbohydrate reserves because it is a stress tolerant species (Quick et

al. 1992; Amundson et al. 1993). To test these hypotheses, water, growth and carbon

relations were investigated within neighbor removal plots between seedlings of exotic

(Tamarix ramosissima) and native (Salix exigua and Pluchea sericea) floodplain species

in the Mojave Desert.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 74 Materials and Methods

Study Site and Plant Removal

This study was conducted during the 1995 and 1996 growing seasons at the

confluence of Half-Way Wash and the Virgin River in southern Nevada (36°40’N,

114°20’E, elevation 380 m; Chapter 2; Sala et al. 1996). The co-dominant woody plant

species on the floodplain at this location were Tamarix ramosissima Ledeb. (saltcedar),

Pluchea sericea (Nutt.) Cov. (arrowweed), and Salix exigua Nutt, (coyote willow). For

clarity, these species will be referred to by their genus name hereafter.

Severe drought during 1994, followed by spring flooding in 1995, left a system of

depositional (silt loam) and erosional (sandy loam) bars available for germination and

seedling establishment. Seedlings of the three dominant species germinated within a

single week, during late July, 1995, after which no further germination occurred at the

study site. Piezometer wells were established and maintained throughout the

experimental period, over which time the water table depth was 3-5 cm during

germination, dropping to ca. 20 cm near the end of the first season (November, 1995),

and rem aining near 70 cm during the 1996 growth season. Near the end o f the first

(1995) season, a small four-day flood increased streamflow by a factor of 4.7 relative to

the previous week’s base stream discharge of 11,900 m^ day'^ (USGS 1998) and

deposited ca. 10 cm of silt. In 1996, the erosional sandbars were again scoured,

removing aU seedlings from these erosional surfaces. The depositional bars, on the other

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 75 hand, remained with their second-year seedling cohort, but the soil’s physical attributes

had changed such that the texture was a stony loamy sand.

In 1995, two sets of paired removal and reference (i.e., no manipulation) plots

were established within a fenced area that excluded herbivory. Each square plot was a

0.25 m^ with a 0.75 m^ buffer zone. Each set of paired plots included a Tam arix removal

plot, a Tamarix alone plot (i.e., a Salix/Pluchea removal) and a reference (no removal)

plot. Six groups of these fenced plots, three in the depositional and three in the erosional

bars, were established along 500 m of the Virgin River. For growth measurements,

Pluchea and Salix were combined into a single native vegetation type due to the

difficulty of distinguishing them when in the rosette and small seedling stages. No

difference in the height of Salix and Pluchea was found in the second year of the study

(when these species are more easily distinguished). During 1995 there was no further

recruitment or regrowth following the initial germination pulse, so all removals resulted

in 100% culling of the targeted species. All aboveground biomass of a given species

group was carefully removed, leaving the non-removed species and soil surfaces

undamaged. Thus, we believe experimental effects were due to interspecific interactions,

which were additional to the intraspecific interactions that were maintained in the plots.

The 1996 experiment evaluated biotic and abiotic interactions in second-year

communities composed of predominantly Tamarix and Pluchea. New removal plots,

0.25 m^ with 0.8 - 3.1 m^ buffer zones, were established in two second-year seedling

stands: one wet and one dry (Table 4-1). These plots, like those in 1995, were paired.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 76 but fenced exclosures were abandoned in favor of more cryptic plots, which were not

noticed by large herbivores. Because the 1995 removal protocol was a de-facto press

removal (i.e., new recruitment of seedlings were not permitted throughout the duration of

the study; Bender et al. 1984), in 1996 resprouts and new seedlings were removed when

found in the plots and buffer zones.

Soil samples were collected using intact cores firom each stand. Samples were

sealed in plastic bags to prevent evaporation during handling and transportation to the

laboratory. After weighing the sample, a subsample was weighed, oven dried at 105° C

for 48 hours, and reweighed to determine the gravimetric water content ( 6g; g water g'^

dry soil). The remainder of the soil sample was air dried in a low humidity glasshouse

for a minimum of 3 months. Saturation extracts were prepared on 200 g of the

glasshouse-dried sample for salinity (ECg) assessment, and another 40 g subsample of the

glasshouse-dried soil was used to determine texture using a modified hydrometer method

(Day 1979) in which density was measured after 40 seconds (~ % sand) and again after 2

hours of (~ % clay) settling.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 77 Water Relations

Water relations of the study taxa were evaluated in the field by monitoring

stomatal conductance (g j and leaf water potential (Y,). At the close of the 1996 season,

leaf samples were also collected to evaluate leaf abscisic acid concentration, which

Table 4-1. Soil characteristics in the experimental stands. Values represent the mean and standard error [se], and n represents the sample size. Only one soil salinity (ECg) value is presented because ECg showed very little variability between stands or years. Gravimetric water content ( 6g) was measured at the surface, and values with the same letter are not significantly different (F = 42.32, df = 3, 38, p = 0.0001); as the asterisk (*) indicates, water table values are significantly different (t = -4.65, d f = 8 , p = 0.002). n ECg(dSm') 7.1 [0.6] 19 1** year (1995) sandbars 0g (g H 2O g"' dry soil) depositional 0.27 [0.01] ' 9 erosional 0.26 [0.01] ' 14 2""' year (1996) sandbars 9g (g H 2O g ‘ dry soil) wet stand 0.16 [0.02] " 11 dry stand 0.014 [0.004] ■= 6 Water Table (cm) wet stand 64.6 [1.6] • 5 dry stand 75.4 [1.7] 4 increases in response to drought (Gaff and Loveys 1984; Davies and Zhang 1991;

Gallardo et al. 1994). Near the end of the 1995 growth season, & was estimated on

random terminal shoots of each species in the irmer buffer zones using a LI-1600 steady-

state porometer (Li-Cor, Lincoln, NE). During 1996, g; was again estimated on random

terminal shoots of each species in the inner buffer zones using a LI-1600 while

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 78 concurrent estimation of gs and photosynthetic rate (A) was made using a LI-6200 gas

exchange system (Li-Cor, Lincoln, NE). Leaf temperature (T,) and air temperature (TJ

were measured simultaneously with all gas exchange measurements using a fine-wire

(0.02 mm) copper-constantan thermocouple. All measurements were made between

sunrise and potential depression of gs (0830 to 1030 hours; Sala et al. 1996). Predawn Y,

measurements were collected between 0200 and 0430 hours on the morning preceding

the final gas exchange measurement in 1996. After each leaf was removed from the

cuvette, the tissue was transferred to a sealed plastic bag and transported on ice for

immediate estimation of Yi. was measured in a Scholander-type pressure chamber

(Soil Moisture Stress, Corvallis, OR). Following Y, measurement, specimens were

resealed in the plastic bags and kept on ice for transport back to the laboratory where leaf

area measurements were made using a Leaf Area Meter (Delta T Devices, Cambridge,

UK).

Apoplastic abscisic acid (ABAgp) samples were collected on 4 October 1996

during the early morning (0800 to 1000 h). Terminal leaf sub-samples of each species

were collected from each plot and placed into 7 ml vials filled with H 2O and stored at

4°C. Leaf area (cm^) of the ABAap sub-samples was calculated using a Delta-T Leaf

Area Meter, allowing evaluation of ABAap on a leaf area basis. Xylem sap was collected

by vacuum perfusion-centrifugation (Terry and Bonner 1980), in which water was

perfused into the apoplast under vacuum and then was collected from the leaf by

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 79 centrifugation (3000 RPM). The samples were stored at -20°C. Quantification of ABAgp

was accomplished using a radioimmunoassay technique (Weiler 1980). Scintillation

fluid was added to the tubes and they were counted for 5 min with a Beckman 1000

(Beckman, Fullerton, CA) radioactivity counter, where a higher concentration of [H 3]

ABA was indicative of less ABA in the sample vial. Sample ABAap was determined by

inference j&om a known standards curve run simultaneously with the samples.

Growth and Carbon Relations

During both years, plant height and density were measured biweekly. For each

species, the height of ten random plants firom each plot was measured, and density was

measured as the number of plants of a given species group within the plot. Neither of

these measurements were made on plants within the buffer zone.

Because the seed mass in these species is negligible, and the seedlings establish

within a small time frame, height was used as a measure of absolute growth during 1995;

relative growth rate is undefined during the first year because the denominator is

essentially zero. During 1996, on the other hand, relative growth rate was calculated as:

dh RGR = hodf

where the initial height (ho) was defined as the height measured before manipulations

were performed (Chiariello etal. 1991).

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 80 Relative competition intensity is a measurement of the effect of competitive

release or imposition on the growth of an organism and is calculated as

_ RGRrem - RGRref SEE:;;— •

where RGR^m and RGR^rare the aboveground growth rates of the removal and reference

plots, respectively (Grace 1993; Twolan-Strutt and Keddy 1996).

At the end of the 1996 growth season, starch concentration was determined in a

25 mg subsample of taproots and stems from each plot for each species. As with the

ABAap, samples for carbohydrate analysis were collected in the early morning (0800 to

1000 hours) and kept on ice for transport to the laboratory. In the laboratory, samples

were stored in a -80°C freezer until analysis. Tissue was then dried at 60°C for 48 hours

and a randomly selected 25 mg tissue subsample was ground. Free hexoses were

extracted in 80% ethanol. The remaining starch was extracted and converted to glucose

by enzyme hydrolysis using amyloglucosidase in 0.5 M sodium citrate. The solution

containing the glucose was assessed quantitatively relative to glucose standards with a

colorimetric assay technique (Haissig and Dickson 1979) in which the relative abundance

of glucose was proportional to the spectrophotometric (Titertek Multiskan Plus, Flow

Laboratories, McLean, VA) absorbance at A, = 450 nm.

Similar to CI rgr , taproot starch (storage carbohydrate) concentration was

compared between the reference and removal treatments using an analogous variable

which quantifies a change in starch sequestration with respect to competitor presence:

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 81 CIs = [Starch] rem - [Starch] ^ [Starch] rem

Whereas CIrgr quantifies inhibition and facilitation measured during the experiment’s

duration, CIs is a measure of these interactions with respect to carbon used in storage

rather than growth or maintenance.

Data Analysis

Normality in the data was tested using proc univariate normal (SAS, SAS

Institute, Cary, NC); none of the measured variables had a normal distribution (p < 0.05),

so only non-parametric hypothesis tests were applied. Three factor, split-plot

multivariate analysis of covariance (MANCOVA; SuperANOVA, Abacus Concepts,

Berkeley, CA) was performed on the ranked response variables ('Pi, gs. A, and leaf-to-air

temperature difference (AT)) in each year. Stand type (erosional or depositional in 1995,

wet or dry in 1996), treatment (removal or reference) and experimental taxa {Tamarix,

Salix, or Plucked) were the factors and time o f measurement was the covariate.

Likewise, split plot analysis of variance (ANOVA; SuperANOVA, Abacus Concepts,

Berkeley, CA) was performed on the ranked starch, ABA, height and density data. The

null hypothesis that mean competition intensity is zero was tested by comparing the ratio

of the mean and the standard error to the critical value of the two-tailed z-distribution

(Devore 1987).

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 82 Post hoc interpretation of significant effects in the MANCOVA models was

achieved by greatest characteristic root (gcr) analysis and ANOVA. Post hoc

interpretation of significant effects in ANOVA models was performed using least squares

means comparisons (on interaction effects) or Fisher’s Protected LSD (on main effects in

the absence of a significant interaction effect; SuperANOVA, Abacus Concepts,

Berkeley, CA). In all hypothesis testing, the probability of a type I error was presumed

to be a = 0.05 (p < 0.05).

Results

Water relations

Gas exchange variables (gs, 'P,, and AT) showed a significant stand-by-treatment-

by-species-by-measurement time interaction (Wilk’s A = 0.08, s = 3, m = 3.5, n = 11.5, p

= 0.0001). The eigenvectors significantly associated with the greatest rejection in the

MANCOVA model indicated that gs, and less so 'Pi, were most related to differences

between stands, treatments, and species after accounting for the time of measurement (Zi

= 0.15 A T -0.15'P |+ 1.0 gs. (A-i = 2.8) and Z 2 = -0 .4 AT + 0.8 'P,4-1.0 & (A.2 = 1.3)).

Tamarix predawn 'P| was 0.5 MPa higher (less negative) in the dry removal

treatment than in most other treatments and stands (Fig. 4-1 A). At this same location,

Tamarix 'Pi was similar to 'Pi in Pluchea. At midday, there were two responses to the

neighbor removal: midday Ÿi was more negative in Pluchea in the dry stand removal

treatment as well as in Tamarix in the depositional stand removal treatment (stand X

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 83 treatment X species X time of measurement (predawn or midday) F = 6.2, df = 29, 82, p

= 0.0001; Fig. 4-1). In Salix, predawn and midday Ÿ, was -0.63 ± 0.05 MPa (n = 4) and -

1.25 ± 0.05 MPa (n = 14), respectively.

Stomatal conductance in Tam arix and Pluchea was not significantly influenced

by treatment or each year’s stand type, although there was a large difference in values

between the 1995 and 1996 seasons; gs was reduced in the second year (Table 4-2). Salix

demonstrated a response to stand type where gs was significantly greater in the erosional

stand. In the depositional stand, Tamarix showed the greatest gs, Pluchea had the lowest

gs in the erosional and wet stands, and there were no significant differences between the

species in the dry stand (Table 4-2). There was a strong influence of stand and treatment

on leaf ABAap concentration for Tamarix, as ABAgp concentrations were elevated in the

dry Tamarix removal plots (Table 4-3). No significant responses in A to treatment or

stand type were observed.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 84

Stand Dry Depo 0 .0

-0.5

-1 .0

(B -1 .5 Q_ S -2.0 1 C ab b -2.5 ~ab bd bd S.o a. A Tamarix ramosissima 0.0 I S.« -0.5 c è CO -1 .0 "O 2 o_ -1 .5 Î -2.0 ab ab -2.5 Reference Pluchea sencea □ Neighbor Removal q -3.0 I______I______1 -3.0 Wet Dry Depo Ero Wet Dry Stand

Figure 4-1. Predawn (A & C) and midday (B & D) leaf water potential (MPa) for Tamarix ramosissima (A & B) and Pluchea sericea (C & D) seedlings on the Virgin River of southern Nevada. Bars represent mean and standard error for plants in reference (filled boxes) and neighbor removal (empty boxes) plots. Depo and Ero refer to the depositional and erosional stands, respectively. Water potential values with the same letter within each species are not significantly different.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 85

Table 4-2. Stomatal conductance to water vapor (mmol m'^ s ') for the species of riparian plant seedlings in four contrasting sites. Values represent the mean and standard error [se]; sites with different letters across a row are significantly different from the other sites, and species values with an asterisk are significantly different from the other species values in the same column (Stand X Species F = 18.7, df = 9, 61). The lack of Salix exigua occurring in the wet-dry plots during 1996 precluded gas exchange sampling, thus values indicated with — were unobtainable. Refer to Table 4- 1 and the text for stand descriptions. Stand Depositional Erosional Wet Dry Tamarix ramosissima \ 212.5 [7SAY 597.4 [282.0]“ 95.1 [20.8] 78.4 [13.6]

Pluchea sericea \ \29.1\25.QiY 153.6 [25.5]“* 49.8 [6.8]"' 65.3 [ 18 .8 ]"

Salix exigua\ 192.3 [8.8]" 260.4 [43.1]“

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 86

Growth and Carbon Relations

Native seedlings were taller than the Tamarix seedlings throughout this two-year

study (date X stand X treatment X species F = 89.0, df = 24, 2490, p = 0.0001 ; Fig. 4-

2A). In 1996, the native vegetation grew 1.4 times more rapidly than Tamarix (Fig. 4-

2A), although the preceding autumn’s (1995) flood slightly decreased average plant

height for the native species without doing the same for Tamarix (Fig. 4-2A). Tamarix

density, however, declined by a factor of 5 following the 1995 depositional flood (date X

stand X treatment X species F = 21.9, df = 24,269, p = 0.0001; Fig. 4-2B), after which

Table 4-3. Apoplastic ABA concentration (nmol cm'^) o f Tamarix ramosissima and Pluchea sericea in the wet and dry sites. Values represent the mean and standard error [se], except where n = 1 , indicated by [—]. The value indicated with an asterisk (*) was significantly different firom all other values in the table (stand X treatment X species F = 14.5, df = 7,14). Reference plots contained natural densities of all species in mixture. Removal plots contained natural densities of a single species; all others were removed. Refer to Table 4-1 for stand descriptions. Stand W et Dry Tamarix ramosissima reference 0.26 [0.03] Tamarix ramosissima alone (removal) 0.29 [0.02] 4.88 [1.4]

Pluchea sericea reference 0.13 [0.03] 0.36 [-] Pluchea sericea alone (removal) 0.22 [0.04] 0.19 [0.1]

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 87

7 0

6 0 Tamarix ramosissima Salix exigua, 5 0 Pluchea sericea E u 4 0 ic 3 0 5 20

7 5 0

CM Depositional E 5 0 0 Rood B c B a .

•t 250 be be 5 Q

Spring 1995 Autumn 1995 Spring 1996 Autumn 1996 Figure 4-2. Height (A) and density (B) of seedlings of Tamarix ramosissima (solid line) and Salix exigua and Pluchea sericea combined (dashed line) over the course of two years on the Virgin River. Spring 1995 shortly followed seedling germination and establishment. Autumn 1995 followed a late season (November) depositional event which buried numerous <10 cm tall seedlings. Spring 1996 shortly followed the breaking of winter dormancy, and autumn 1996 preceded end-of-season leaf senescence. No flooding occurred after the spring in the 1996 second-year sandbars. Values in each panel with the same letter are not significantly different. Salix exigua and Pluchea sericea were combined because their height and density were not significantly different.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 88 Tamarix density did not change. On the other hand, the density of Salix and Pluchea

declined linearly throughout the first three stages of this study (Fig. 4-2B).

Negligible starch was stored in Salix stems and Pluchea taproots and stems (stand

X treatment X species F = 8.2, d f = 9, 13, p = 0.0004; Fig. 4-3A). In contrast, high starch

Taproot □ Stem Tamarix ramosissima 1 0

C O) iCO ^ - 1.5 -K So 1 1 8 5 Q)c i 0.1 § -5 Ü 3 C cr Ü a> o

■ 5 E II E 0.0001 0.5 ^ — Tamarix Salix Pluchea Wet Dry

Species Stand

Figure 4-3. Taproot and stem carbon storage for Tamarix ramosissima, Salix exigua and Pluchea sericea (A) and taproot carbon storage of Tamarix ramosissima (B) in wet and dry sites. Starch concentration (mmol Glucose equivalent g"' dry mass) is illustrated on a logarithmic scale (A) to demonstrate the extreme differences between species and storage locations. Values represent mean and standard error, and values with the same letter within each panel are not significantly different. ______concentration (ca. 20% of dry weight) was found in Salix taproots and Tamarix taproots

and stems. There was a further significant increase in the starch concentration of

Tamarix roots from the dry stand relative to the starch storage in the wet stand Tamarix

(Fig. 4-3B)

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 89

Relative CI, as determined from RGR (CI rgr ), demonstrated significantly

positive values indicative of interspecific growth rate inhibition for Pluchea in the 1995

depositional sandbar and, more dramatically, for Tamarix in the erosional one (Fig. 4-

4A). During the second year, seedlings of Tamarix and Pluchea growing together in the

wet stand had reduced growth rates in the reference plots, but seedlings of Tamarix and

Pluchea had elevated growth rates in the reference plots in the dry stand (Fig. 4-4A).

Relative Cl, as determined from carbohydrate storage (CIj), was significantly

negative for Pluchea in the wet stand and for Tamarix in the dry stand. Only for Pluchea

in the dry stand was CI^ significantly positive (Fig. 4-4B).

Discussion

Our results show that the ability of Tamarix seedlings to invade riparian areas of

desert regions is due more to its responses to abiotic stress in this environment (Chapter

2; Busch and Smith 1995) than to aggressive growth. While microsite aridity coupled

with species interactions were the most crucial influences on the seedlings, it was the

alteration of plant carbon balance, and not plant water relations per se, that demonstrated

the most sensitivity to these influences. The similarity in pattern to Grime’s observations

and predictions (Grime 1974,1977) was striking given Grime’s assertion that abiotic

stress is lacking in riparian corridors (Grime 1974).

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 90

Stand

Depo Ero Wet Dry

I Tamarix ramosissima □ Pluchea sericea 2 -

- 1 0.50

- 0.25

0.00 Ü - -0.25

- -0.50

-0.75 Wet Dry Stand

Figure 4-4. Competition intensity (Cl) as a measure of either a growth (A) or carbon storage (B) response of Tamarix ramosissima and Pluchea sericea to experimental plant removals. Positive values indicate higher growth or storage in neighbor removal plots (i.e., inhibition) and negative values indicate higher growth or storage in the reference plots (i.e., facilitation). Depo and Ero refer to the depositional and erosional stands, respectively. Bars represent the mean and standard error of the ratio and an asterisk indicates a significant difference firom zero (i.e., no effect). The lack of Salix exigua occurring in the wet-dry stands during 1996 precluded measurements of competition intensity. ______

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 91 The responsiveness of Tamarix to putative competitors was revealed by its higher

(less negative) predawn 'Fi in the absence of neighbors in the dry stand (Fig. 4-1). An

increase in Y, generally indicates lower water stress (Nilsen et al. 1981; Stromberg et al.

1992) and higher soil moisture availability (Nilsen et al. 1984). The majority of midday

^1 comparisons were not significant (Fig. 4-1); although, when they were significant,

they were in the dry stand (Pluchea) or the depositional stand (Tamarix). In the dry

stand, soil moisture was lower (Table 4-1), and in the depositional stand, soil moisture

was probably less available than in the erosional stand due to the stand’s finer textured

soil. The pattern of response to neighbor removal is not consistent with the theory that

these plants were actively competing for soil water, as midday 'F, was more negative for

the target seedlings following removal of the interspecific neighbors. This unusual

response was not attributable to removal of shading vegetation, as it was observed for

both Pluchea and Tamarix upon neighbor removal, despite the great difference in height

between these two species (Fig. 4-2). These inconsistencies were likely due to seedlings

having developed sufficiently deep root systems to alleviate midday water stress (i.e.,

some plants quickly reached the water table, a result of their phreatophytic nature). Thus,

broad generalizations about phreatophyte water potentials during the seedling stage

would require experiments in which root growth patterns are fully and accurately

documented (Sala et al. 1996).

Whereas Pluchea failed to adjust leaf ABAap bi response to stress, the response of

Tamarix to more arid conditions was pronounced (Table 4-2). In the dry stand, Tamarix

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 92 increased leaf ABAap when the shading overstory of Pluchea was removed, suggesting

that water stress in Tamarix is ameliorated by the presence of Pluchea. The significant

increase in Tamarix ABAap concentration associated with both the loss of protective

cover and low soil moisture illustrates a typical ABAap threshold response to increasing

drought stress (Ackerson 1982). Although leaf ABAap levels did not demonstrate a

controlling influence over gs as has been suggested by previous investigations (Zhang

and Davies 1990; Davies and Zhang 1991), hormonal regulation may be obscured by a

lack of ABAap directly at the stomata or by the impairment of ABAap stomatal control

during severe soil drying (Correia and Pereira 1995). The greatest difference in gs was

between the first and second-year seedlings (Table 4-2), probably due to the wetter soils

in 1995 than in 1996 (Table 4-1).

The impact of flooding on newly established seedlings was more detrimental to

Tamarix than to Salix and Pluchea. Such asymmetry may have a strong influence on

competition with respect to the initial density of the species. Repeated short-term

instabilities, such as flooding, may help to maintain a community with native plants in

the long-term (Chesson and Huntly 1989). Anthropogenic modification of natural

disturbance regimes in Southwest floodplains (Smith et al. 1991), which is relatively

minor on the Virgin River, may further increase the magnitude of differences in variables

measured here as well as lead to greater invasibility by exotic taxa (Hobbs and Huenneke

1992). The more severe decrease in Tamarix seedling density relative to that of native

vegetation following the autumn 1995 flood (Fig. 4-2) may indicate that flood events

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 93 following germination can greatiy inhibit the relative success of and speed by which

Tamarix becomes a dominant member of the local flora in a floodplain with a shallow

water table.

Since both Tamarix and the natives germinated on new deposits simultaneously,

our ability to discern seedling growth rates was ideal (Fig. 4-2). An “aggressive”

competitor, as Tamarix has been described (Robinson 1965), should initially grow more

rapidly, even though differences in RGR tend to decline following the early seedling

stage (Eissenstat and Caldwell 1987). However, Tamarix never exceeded native

vegetation in height or aboveground biomass (data not shown), which is consistent with

hypothesis (2) predicting that Tamarix aboveground growth rate was lower than the more

mesic native species (Myers and Landsberg 1989). This suggests that the traits which

allow Tamarix ultimately to dominate southwestern riparian systems does not include a

high initial aboveground growth rate, rather it suggests that some other mechanism, such

as stress tolerance (Chapter 2; Grime 1974, 1977; Busch and Smith 1995), strongly

contributes to the invasive success ofTamarix under seasonal or longer-term drought

conditions.

CIrgr was significantly influenced by the abiotic conditions at the study site (Fig.

4-4). The new depositional and erosional surfaces of the 1995 study had greatly

contrasting influences on the interactions between Tamarix and the native phreatophytes.

Although our results show that native species growing on new depositional substrate

exhibited some decrease of growth rate due to competition with Tamarix, Tamarix was

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 94 initially at a disadvantage because of its lower growth rate on the erosional bar when in

the presence of the natives (Fig. 4-4).

In the established community on the depositional bank (1996), an interesting

interplay between interspecific interactions and abiotic conditions (i.e., aridity) was

observed (Fig. 4-4). Under the wet condition, competitive inhibition of aboveground

growth rate was observed (as per Grime 1977; Twolan-Strutt and Keddy 1996) for both

Tamarix and Pluchea in the presence of each other. An equally important facilitative

reaction in the dry stand occurred, indicating both positive and negative interactions

(Callaway and Walker 1997) are indeed important in this early succession community,

and the direction of the interaction is dependent on abiotic conditions (Holmgren et al.

1997). At the dry locations, the relative interaction strength was dependent on species

type, and the growth of Tamarix (in the presence of over-topping Pluchea) was more

greatly facilitated by Pluchea than Pluchea was facilitated by Tamarix (Fig. 4-4). There

is ample evidence to support hypothesis (3) and it appears that both inhibitory and

facilitative interactions direct aboveground growth of Tamarix and Pluchea along the

environmental gradients present at this site.

The deciduous species (Tamarix and Salix) store more starch than the evergreen

Pluchea (Fig. 4-3) as would be expected (Chapin et al. 1990). The increased taproot

starch storage by Tamarix in the dry stand may be a mechanism by which Tamarix

growing under stressful conditions can store carbon to increase the probability of survival

if water availability declines during the first few years of life. Increased starch

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 95 concentration in the stem may also permit Tamarix seedlings a competitive advantage by

preserving large long-term carbohydrate reserves when the taproot sink is at a maximum.

Contrasting patterns of root carbohydrate storage across treatments and stands

revealed different responses to competition and aridity. Pluchea’’s response to such

stresses was to allocate more carbohydrate to root storage in the presence of Tamarix in

the wet stand (as indicated by the negative CI^; Fig. 4-4). The facilitation of

carbohydrate storage in Pluchea by the presence of Tamarix indicates that Pluchea is

more sensitive to biotic stress than abiotic stress. However, in the presence of Tamarix at

the dry site, Pluchea may not have had this storage potential, as indicated by the positive

CIs value (Fig. 4-4); carbohydrate storage as a mechanism to survive potentially stressful

future conditions is a luxury available when only one type of potentially stressful

conditions is imposed. This needs to be viewed in the context of a species' functional

type, thus the ultimate impact of storage inhibition on an evergreen species may not be

important because evergreens do not store large amounts of starch in their taproots

(Chapin etal. 1990).

The response of Tamarix to competition and aridity was clearly different from

Pluchea in two ways. First, under wet conditions, the starch storage pattern of Tamarix

was not affected by the presence of a competitor as demonstrated by the null CIj value

(Fig. 4-4). Second, dry stand Tamarix showed a strongly negative Clg value to the

presence of Pluchea with respect to taproot starch accumulation (i.e., starch storage was

facilitated by the presence of Pluchea). This alteration of storage pattern to favor

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 96 carbohydrate storage may be employed by Tamarix under arid competitive conditions as

a mechanism to further its long-term survival. Carbon stored as starch may be

remobilized for growth as well as metaboUc functions and respiration (Chiariello et al.

1991). It has been observed that carbohydrate is more readily exported from the leaf to

woody storage organs in water-stressed plants (Quick et al. 1992). Though this has been

explained as an increased responsiveness to impending low temperature (Amundson et

al. 1993), cold tolerance seems to be an unlikely reason for increasing taproot starch

accumulation in this enviromnent, and thus energetic explanations are more plausible.

Stored carbohydrate promotes greater stress tolerance, at the expense of a high initial

growth rate. As with growth relations, carbon relations suggest that stress tolerance

contributes to the invasive success ofTamarix (Chapter 2). The suggestion that specific

stress-resistance properties are inherent to organisms which accumulate large metabolic

reserves, such as carbohydrates (Djawdan et al. 1997), is relatively new and there is little

agreement to date about its importance in plant stress tolerance. However, strategic

partitioning of carbon to starch reserves for later remobilization seems the most likely

reason for the patterns observed here, supporting hypothesis (4).

The results from this experiment support the assertion that naturally or

anthropogenically (Busch and Smith 1995) lowered water tables and reduced flood

occurrence in riparian areas positively influence Tamarix under competitive regimes in

the field while simultaneously being detrimental to co-occurring native phreatophytic

species. As demonstrated here, this seems to hold true across a spectrum of

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 97 physiological and ecological responses (Fig. 4-5), and the net effect of one species upon

another is difficult to determine, as inhibitory and facilitative interactions between

Tamarix and Pluchea depend upon the environmental conditions, just as other studies

have shown with other species (Callaway 1994; Chapin et al. 1994; Callaway et al. 1996;

Callaway and Walker 1997). Furthermore, in environments where long-term stress

tolerance is crucial to competitive dominance (e.g. desert riparian environments with

high spatial and temporal variability), acquisition and storage of reserve carbon is an

important (Komer 1991), though often neglected, consideration in assessing a species’

success.

Acknowledgments

We would like to thank Jeff'Piorkowski, Travis Huxman, and Catherine Heyne

for their conceptual and statistical assistance; Erik Hamerlynck, Chris Schaan and Lynn

Shaulis for their assistance in the field; and Janet Reiber and Nancy Sovocool for their

assistance in the laboratory. This study was supported by fimding firom the Las Vegas

Valley Water Authority to S.D. Smith and D.A. Devitt, and the UNLV Graduate Student

Association to K.A. Sovocool.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 98

Drought Stress

Tamarix - Pluchea f Tamarix Pluchea ^amarix ^sPluchea / / / / / I r . ▼ t drought: drought: drought: Inhibited Facilitated 1> Facilitated Facilitated Facilitated Inhibited wet: wet: wet: no effect no effect Inhibited Inhibited no effect Facilitated

Water Status Growth Carbon Storage (Fig. 4-1) (Fig. 4-4A) (Fig. 4-4B) Figure 4-5. Summary of drought effects on interspecific interactions among seedlings. Inhibited denotes that the species indicated is inhibited by the presence of putative competitors, facilitated indicated that the species A dashed line is placed over the water relations portion, indicating that these differences are not widespread throughout the study.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. CHAPTERS

THE EFFECT OF INTERACTING HEAT AND DROUGHT STRESSES ON COMPETITION AMONG MOJAVE DESERT RIPARIAN SPECIES

This chapter has been prepared for publication in Functional Ecology and is presented in the style of that journal. The co-authors who have contributed substantially to this manuscript are Kent A. Sovocool and Travis E. Huxman.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 100

Abstract

Physiological tolerance to heat, drought and competition were investigated in

seedlings of the Mojave Desert phreatophytes Tamarix ramosissima, Salix exigua and

Pluchea sericea under glasshouse conditions. Mortality ranged up to 30 % with biotic

and abiotic stresses in the native (Salix and Pluchea) seedlings, while survival of the

invasive Tamarix did not decline under the same conditions. Success of Tamarix was

further illustrated by its proclivity for very early basal ramet generation, whereas Salix

and Pluchea did not resprout. Predawn and midday xylem water potentials were around -

1.2 MPa for all species. In Salix, heat and drought stress together resulted in net

photosynthesis declining 10 pmol m'^ s‘‘ (three-fold) and stomatal conductance declining

0.3 mol m'^ s'^ (four-fold), with a concurrent two-fold increase in photochemical

quenching of excess radiant energy. Physiological characteristics in all species were

primarily sensitive to the heat and drought treatments, and density may mediate

interspecific interactions. When interspecific interactions were important, Tamarix was

facilitated by Salix and Pluchea , indicating that abiotic stress amelioration can occur

between species, as well as within clones. This study further illustrates that abiotic stress

and facilitation, rather than inhibition, promotes successful invasion of southwestern U.S.

riparian areas by Tamarix ramosissima.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 101 Introduction

The invasion of southwestern U.S. riparian ecosystems by Tamarix ram osissim a

(saltcedar) has been explained by its proclivity, its physiological tolerance to stress, and

its competitive superiority to native species (Robinson 1965; Kleinkopf and Wallace

1974; Busch and Smith 1995; Shafiroth et al. 1995). Riparian ecosystems in the arid

southwest are particularly open to invasion by Tamarix because river management

practices like stream diversion for agriculture and dam construction alter historical

streamflow conditions (Smith etal. 1991). Attention to the mechanisms by which these

explanations could contribute a great deal to developing more effective strategies for

controlling Tamarix.

Mechanistic studies have become more prevalent in ecology; for example,

facilitation and inhibition simply and generally represent the biotic factors that drive

succession and direct species interactions (Connell et al. 1987; Walker and Chapin 1987;

Callaway et al. 1996). Behind this simplistic framework of facilitation and inhibition,

interspecific variability in life histories and physiological responses to the abiotic

environment (Callaway and King 1996; Callaway and Walker 1997) provide mechanisms

for interspecific interactions (e.g., Fonteyn and Mahall 1981; Callaway et al. 1996).

Correlations in the field between competitive inhibition and the abiotic environment may

lead to a general understanding of interspecific interactions, but the better controlled

environment of the glasshouse or growth chamber provides the best design for inferring

mechanistic relationships between the physical environment and interspecific interactions

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 102 (Keddy 1989). Unfortunately, the problem of Tamarix invasion is infrequently tested

under glasshouse conditions.

Stress imposed by the abiotic environment directly affects the physiology of an

individual plant. A plant growing alongside another may also respond indirectly to that

stressful condition through a change in that neighbor’s physiology (due to the abiotic

stress) or in that neighbors ability to inhibit or facilitate its neighbors. Some of the

environmental conditions that have been shown to affect interspecific inhibition and

facilitation are drought (Bauder 1989), temperature extremes (Callaway and King 1996;

Greenlee and Callaway 1996), and nutrient deficiency (Aerts et al. 1991).

Floodplain ecosystems can provide valuable mechanistic insight into the interplay

between inhibition and facilitation (Walker et al. 1986). In desert riparian corridors,

stress (both heat and drought), disturbance (both flooding and fire), and high plant

density provide an ideal opportunity to explore the physiological explanations of

inhibition and facilitation (Chapters 2 and 4). In the southwestern U.S., riparian species

are physiologically suited to various environmental conditions (Chapter 2; Busch and

Smith 1995). Along the relatively unregulated Virgin River in southern Nevada,

Tamarix ramosissima, Salix exigua, and Pluchea sericea (hereafter referred to by their

genus name) are found in high density and close proximity. O f these species, Tamarix

comes to dominate the Virgin River floodplain.

The objective of this study was to investigate the roles of abiotic (heat and

drought) and biotic (competition) stresses on the physiology of Tamarix, Salix and

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 103 Pluchea in the seedling stage, when stress has its strongest impact upon survival and

reproduction (Osmond et al. 1987). To achieve this objective, four hypotheses were

tested with full-factorial temperature, water, and competition treatments in a glasshouse.

First, mortality due to stress was predicted to be lowest in Tamarix because of its

presumed stress tolerance (Chapters 2 and 4; Runeckles 1982) and its carbohydrate

storage reserves (Chapter 4). As a corollary to the first hypothesis, measures of

physiological integrity (e.g., chlorophyll fluorescence, stomatal conductance, and water

potential) was expected to be compromised by abiotic stress in Salix and Pluchea, but not

in Tamarix. Second, abovegroimd growth was expected to be enhanced by the presence

o f a neighboring plant (Tilman 1980, 1988). Third, we hypothesized that taproot growth

in the exotic species (Tamarix) would be greater than in the native species (Salix and

Pluchea), providing physiological and ecological advantages to Tamarix (Sala et al.

1996). Fourth, inhibition of Salix and Pluchea by Tamarix would occur under drought

and heat stress conditions, while Tamarix was expected to be inhibited by Salix and

Pluchea under stress-free conditions.

Materials and Methods

Seedlings of Tamarix ramosissima, Salix exigua, and Pluchea sericea were

collected on 15 June 1997 from the confluence of Half-Way Wash and the Virgin River

in southern Nevada (36°40’N, 114°20’E, elevation 380 m) ca. 1 week following

germination- Water table depth at that time was ca. 5 cm. Germination of these three

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 104 species coincided very closely, so all transplanted seedlings were of the same cohort and

age. Seedlings were allowed to recover from transplant shock in a glasshouse for 2

weeks before transplantation and initiation of the experiment. The experimental design

included the administration of 2 levels of temperature, water and competition stresses,

respectively. The experimental conditions were imposed on 27 June and continued for

six weeks, until 8 August 1997, when the experiment was terminated.

Individual Tamarix seedlings were grown either alone or with a single seedling of

Salix or Pluchea. Individual seedlings of Salix or Pluchea were likewise grown alone or

with a single seedling of Tamarix. On 27 Jime 1997, seedlings were transplanted into

cylindrical polyvinyl chloride (PVC) tubes of 90 cm length and radii of 3.8 cm and 5.1

cm for single seedlings and mixed seedlings, respectively. These two pot sizes provided

nearly single and double rooting volumes, maintaining a constant per-plant rooting

volume and avoiding the confounding effect of soil volume on root competition

(McConnaughay and Bazzaz 1992a).

The PVC pots were filled with very coarse sand to reduce capillarity in the soil

column, as well as to accentuate applied treatment differences in water table depth. Pots

were placed into large (208 L, 90 cm tall) barrels which were completely filled with

Colorado River water at an initial water table depth of 3-5 cm. The capillary fringe

within the PVC pots was observed at this time to be only 1-2 cm in height and responsive

within one day to changes in water table manipulated within the barrel.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 105 Two temperature treatments, hot and cool, were imposed in two glasshouse bays.

In the hot treatment, glasshouse temperature was allowed to fluctuate up to 45° C

through the normal diel pattern of the outside environment. In the cool treatment,

glasshouse temperature dielly fluctuated as with the hot treatment, but the temperature in

the cool bay was not allowed to exceed 37° C. In every case the cool bay was kept ca. 5°

C cooler than the hot bay at midday (Fig. 5-1 A). While neither of these temperature

regimes were unusual relative to summer field conditions (Chapter 2), the 5° C

temperature range is slightly greater than the range of normal photosynthetic acclimation

responses observed in Tamarix aphylla in Death Valley, CA (Downton et al. 1984).

Two water table drawdown rates, 15 cm wk'^ and 30 cm w k'\ were imposed as

wet and dry treatments, respectively (Fig. 5-IB). The proper amount of water was

removed firom each barrel weekly using a suction device. The in situ drawdown rate

(before water table manipulation) was 8 ± 1 cm wk'* (n =16) and 15 ± 1 cm wk‘* (n = 16)

in the cool and hot treatments, respectively. These drawdown rates are greater than

observed in the field (see Chapter 4), but they are not unreasonable because the 1995

growth season (see Chapter 4) followed an unusually wet spring and water table decline

was less rapid than in 1996 and 1997 (ca. 10 cm wk'*). Plants in the dry treatment were

allowed to continue drying following the third week (17 July), at which time the water

table was completely removed. Twenty seedlings of each species were planted into each

(temperature X drought X competition) treatment combination (N = 160).

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 106 Plant height was measured weekly, noting the height of each stem for individual

plants containing secondary stems; Tamarix seedlings branched profusely at their base

within 4 weeks of transplanting in the glasshouse. Extent of adventitious branching was

also noted weekly. Relative growth rate was determined from measurements of greatest

height (to infer overtopping-growth advantage; RGRh) and total sum height of the genet

(to infer growth-density advantage; RGRJ. Each relative growth rate was calculated as

RGR was calculated as in Chapter 4:

RGRh=

and

dZh RGRt = Zhodt

where the h^ax was the height of the tallest ramet, Zh was the total per-genet height, and

the initial height was demarked by a subscript 0 (i.e., ho, max and Zho) (Chiariello et al.

1991). Mortality was also noted during height measurements, and the resultant

experimental designs were unbalanced (i.e., samples sizes per species and treatment

varied from group to group).

All other measurements were made at the third (18 July) and sixth (8 August)

weeks of the experiment. Predawn water potential was measured using a Scholander-

type pressure chamber (Soil Moisture Stress, Corvallis, OR) on shoots that were severed

into a plastic bag and transported on ice to the pressure chamber.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 107 Later on the measurement day (10:00), seedlings were covered with aluminum

foil for 1 hour. Chlorophyll fluorescence of these dark-adapted leaves was performed

using a Hansatech MFMS/2S modulated fluorimeter (Loik and Harte 1996).

Photochemical efficiency of photosystem II (Fy / F^, where Fy = Fm - Fq and Fy, F^, and

Fq are the variable, maximal (measured with a saturating light pulse) and baseline

fluorescence in mV) and photochemical quenching (qP) were calculated firom the

primary (for Fy / Fm) and secondary (for qP) light pulses. After re-equilibrating the

leaves to natural light conditions, gas exchange measurements were taken using a LI-

6400 gas exchange system (Li-Cor, Lincoln, NE). Measurements of stomatal

conductance to water vapor and CO2 (gs) as well as net photosynthetic CO2 assimilation

(Anet), were made on 12 plants during each sampling period.

These plants and their intact soil column were then removed firom the pots.

Taproot length, soil water content at 10 cm and 75 cm depth, and midday water potential

of the shoot were measured immediately, and leaf subsamples firom gas exchange were

transferred to the laboratory on ice for leaf area measurement (Delta-T, Pullman, WA).

Soil water content was determined using a portable time-domain reflectometry (TDR)

probe (Delta-T, Pullman, WA) that was calibrated on soil samples of known density and

water content.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 108

Hot Bay Day of Year Cool Bay 200

0 .2 5

0.20

0 .1 5

0.10

0 .0 5

0.00 200 210 220 Day of Year Wet, 10 cm I - Wet, 60 cm Dry, 10 cm Dry, 60 cm

Figure 5-1. Temperature (A) and soil moisture (B) regimes imposed in the glasshouse experiment. Daily maximal and minimal temperatures are reported for the hot bay (open squares) and the cool bay (closed circles). Soil water content (0) was measured at depths o f 10 cm (solid lines) and 60 cm (dashed lines) under the wet treatment (squares) and the dry (circles) treatments. Values of 6 are represented as mean ± se.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 109 Normality in the data was tested using proc univariate normal (SAS, SAS

Institute, Cary, NC), and distribution free tests between rank-medians were used where

the observed probabiUty distribution function (pdf) was significantly different (p < 0.05)

from a normal pdf. Where possible (i.e., when degrees of freedom were not limiting),

full interaction, split-split plot, four factor ANOVA was used to test the null hypothesis

that there is no difference between means within the species {Tamarix, Salix, Pluchea) X

temperature (hot, cool) X water (wet, dry) X competition (monoculture, mixture)

treatment combination matrix. When a complete design was not possible, interaction

between species (i.e., each species responds uniquely to the stress matrix) was assumed,

so full interaction, split-split plot, three factor ANOVA was used for each species

individually, as well as single factor ANOVA between species.

In all hypothesis testing, the probability of a type 1 error was presumed to be a =

0.05 (p < 0.05). For brevity and clarity, only main or interaction effects that contained at

least one significantly different group mean are reported; any comparisons not illustrated

did not contain significant differences. Unless otherwise noted, interspecific

comparisons were presented across all treatment groups, and specific responses to stress

(interspecific and intraspecific) were presented where significant differences were found.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 110 Results

Growth

Only one of the Tamarix seedlings died following the imposition of stress

treatments (Table 5-1), while Salix and Pluchea had high mortality rates in the stress

treatments but not in the reference conditions (i.e., cool, wet, monoculture; Table 5-1).

Of those plants that survived, Tamarix had the highest RGR, in the wet treatment and

Salix had the lowest RGRt (species X water F = 12.0, p = 0.0001, df = 2, 272; Fig. 5-2).

RGRh was not significantly different between species or groups (data not shown).

Ramet generation did not occur in Pluchea or Salix seedlings, but Tamarix

produced basal shoots in all treatments (Fig. 5-3). Complex interactions with respect to

stress treatments were observed (water X competition F = 4.3, p = 0.04, df = 1, 72;

temperature X water F = 4.3, p = 0.04, df = 1, 72), in which branch formation was

inhibited when neighbors were present under cool, wet conditions and hot, dry conditions

(Fig. 5-3).

There were no differences in taproot elongation between species (species F =

0.47, p = 0.63, df = 2, 34). Taproot growth in Tamarix was responsive to heat stress

(temperature F = 6.0, p = 0.04, df = 1, 8), where taproot growth was significantly greater

in the hot treatment (Fig. 5-4A). Taproot growth was responsive to the combination of

heat and water stresses in Pluchea (temperature X water F = 11.0, p = 0.03, df = 1,4),

where taproot elongation was inhibited by wet and cool conditions (Fig. 5-4B).

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. I l l Stress Physiology

Predawn was most negative in Tamarix and least negative in Salix', Pluchea

had intermediate predawn V, that was not significantly different from either of the other

species (time of day X species F = 5.9, p = 0.004, df = 2,130; Fig. 5-5A). Midday 'Pi, on

the other hand, was least negative in Pluchea', midday in Tamarix was not

significantly different from midday 'Pi in Salix (Fig. 5-5A). The only species showing

Table 5-1. Percent mortality of exotic and native riparian seedlings in the glasshouse. Pluchea and Salix were difficult to distinguish when dead, so they have been grouped together. Numbers in parentheses indicate the sample size (n).

Tamarix ramosissima Wet Dry Monoculture Mixture Monoculture Mixture Cool 0 (20) 0 (20) 0 (20) 0 (20) Hot 0 (20) 0 (20) 0 (20) 5(20)

Pluchea sericea Salix exigua Wet Dry Monoculture Mixture Monoculture Mixture Cool 0 (20) 20 (20) 0 (20) 5(20) Hot 15 (20) 20 (20) 25 (20) 30 (20)

significant differences between predawn and midday 'P| was Salix, in which T'l was 0.4

MPa more negative during the daytime.

Both predawn and midday 'Pi declined in Tamarix when exposed to water stress

(water F = 5.4, p = 0.03, df = 1,31; Fig. 5-5B). Likewise, predawn (but not midday) 'Pi

in Pluchea was significantly more negative when grown under drought conditions (water

F = 11.7, p = 0.004, df = 1, 16; Fig. 5-5C). Predawn and midday 'Pi in Salix, on the other

hand, responded negatively to high temperature treatment, but not drought (temp X

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 112

0 .0 8 □ Wet

CD 0 .0 6

> « 0 .0 4

g E. 0.02

Tamarix Pluchea Salix Figure 5-2. Genet relative growth rate (RGRt), as it was affected by drought treatment, for each Tamarix ramosissima, Pluchea sericea and Salix exigua. Values with the same letter are not significantly different. _____ measurement F = 6.2, p = 0.001, df = 3,49; Fig. 5-5D). Predawn Ÿ, in Salix illustrated a

greater decline than did midday

Anet was significantly lower in Pluchea than in Tamarix', but A„et inSalix was not

significantly different firom Tamarix and Pluchea (species F = 3.5, p = 0.04, df = 2,46;

Fig. 5-6A). Anet in Salix was sensitive to the imposed treatment stresses, declining 3-4

fold under heat and drought stresses (temperature X water F = 10.2, p = 0.0002,,df= 3,

23; Fig. 5-6B). gs in Tamarix was significantly lower when seedlings were exposed to

drought stress (water F = 6.7, p = 0.02, df = 1,24; Fig. 5-6C). In Salix, gs was

significantly lower when both heat and drought stress were imposed (temperature X

water F = 9.4, p = 0.0003, df = 3,23; Fig. 5-6D).

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 113 Tamarix seedlings demonstrated a significantly higher photochemical efficiency

(Fy / Fm) than seedlings of Salix and Pluchea, which were not significantly different from

each other (species F = 14.3, p = 0.0001, df = 2,42; Fig. 5-7A). Furthermore, Fy / Fm

was greatest in Tamarix when released from water stress but exposed to competitors

0 .0 6 LJ Monoculture - ocI Mixture

0 .0 4 CO • “S ® oc i ' ' ^(D 0.02 DC

Wet Dry Wet Dry

Cool Hot

Figure 5-3. Relative branching rate, with respect to drought, heat and competition stresses, in Tamarix ramosissima. Values with the same letter are not significantly different, and values are represented as the mean ± 1 standard error. The number of branches genet'* doubled every 20 days at a value of 0.05. Salix exigua and Pluchea sericea did not produce further ramets during the course of the experiment (i.e., RBR = 0). _ (water X competition F = 5.5, p = 0.02, df = 1,42; Fig. 5-7B). Photochemical quenching

of excess light energy was greatest in Salix when exposed to heat stress and lowest in

Pluchea when protected from heat stress (species X temperature F = 3.5, p = 0.04, df = 2,

42; Fig. 5-7C).

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 114

Tamarix ramosissima

Hot Cool Figure 5-4. Taproot length, affected by heat in Tamarix ramosissima and affected by heat and drought stresses in Pluchea sericea. Values with the same letter are not significantly different, and values are represented as the mean ± 1 standard error. Water table depth when these measurements were taken was 60 cm (dry treatment) and 30 cm (wet treatment).______

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 115

Tamarix Piuchea Salix -0.4

- 0.8 - 0.8

-1 .2

-1 .6 .2 - 2.0 n predawn ■ midday Piuchea sericea QL . f f l -2.4 « 5 -0.4 \ -0.4

- 0.8 - 0.8 I'' X -1 .2

-1 .6

- 2.0

-2.4 - Tamarix ramosissima Salix exigua ______I______Wet Dry Cool Hot Figure 5-5. Predawn and midday water potential (Y,) measured between species {Tamarix ramosissima, Pluchea sericea and Salix exigua) and across all treatments (A), and affected by drought stress in Tamarix (B) and Pluchea (C) and heat stress in Salix (D). Treatments not presented demonstrated no significant differences between means. Values with the same letter are not significantly different, and values are represented as the mean ± 1 standard error. ______

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 116

Tamarix Piuchea Salix Wet Dry

20 - - 0.6

1 5 - 0 .4 ^ CO 1 0

O - 0.2 o E E Tamarix ramosissima s Salix exigua [ ] ctool ^ ° I c 20 - 0.6 f CO>. > ■ Hot o o O o sz 1 5 - CL 0 .4 « o5 2 z 1 0 - CO

- 0.2 5 -

Wet Dry Wet Dry Figure 5-6. Net photosynthesis (Aneb A and B) and stomatal conductance to water vapor (gs; C and D) between species (Tamarix ramosissima, Pluchea sericea and Salix exigua) and across all treatments (A), Salix exigua (B and D) and Tamarix ramosissima (C). Treatments not presented demonstrated no significant differences between means. Values with the same letter are not significantly different, and values are represented as the mean ± 1 standard error.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 117

Tamarix Piuchea Salix Tamarix Piuchea Salfx 1 1------T T 0.9 □ Cool 0.8 B Hot

0.7

0.6

0.5 0.0 Tamarix ramosissima 0.9 Monoculture O 0.8 Mixture H -

0.7

0.6

0.5

Wet Dry Figure 5-7. Fluorescence measurements of photochemical efficiency (Fy / Fm; A & B) and photochemical quenching (qP; C) in Tamarix ramosissima (A, B & C), Salix exigua (A & B) and Pluchea sericea (A & B) with respect to drought and competition stresses (B) and temperature stress (C). Panel A represents comparisons between species and across all treatments. Treatments not presented demonstrated no significant differences between means. Values with the same letter are not significantly different, and values are represented as the mean ± 1 standard error.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 118

Discussion

Among these young seedlings, various species-specific responses to abiotic and

biotic stress were observed, notwithstanding the episodic and unpredictable events that

can affect seedlings under field conditions (e.g., flooding; Chapter 4). In general, these

species were only on occasion responsive to competition stress. However, there were

widespread responses in these species to the imposition of abiotic stresses, and most of

the parameters investigated responded to both heat and drought stresses.

Mortality was minimal in Tamarix, as predicted. Salix and Pluchea, on the other

hand, experienced high mortality throughout this study, especially in the multiple stress

treatments (Table 5-1). Because the presence of abiotic stress is fairly constant in the

Virgin River floodplain, mortality in Salix and Pluchea is constantly occurring

throughout establishment, whereas morality in Tamarix is less constant, occurring in

random and episodic pulses (Chapter 4).

RGRh did not respond to any of the experimental manipulations, even though

height advantages were expected to occur under competitive conditions. However,

Tamarix RGRt was higher under drought-firee conditions (Fig. 5-2) as predicted. This

higher RGRt under stress-free conditions indicated that Tamarix invested in production

of ramets rather than height or overtopping growth. This thicket-forming characteristic

will eventually result in producing a canopy with higher leaf to stem-area ratio (Chapter

2) and humidification of the boundary layer (Sala et al. 1996). However, branch

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 119 production declined in Tamarix when exposed to biotic stress (i.e., competition) without

concomitant heat or drought stresses (Fig. 5-3). So, only when water and heat stress is

lacking and competitors are present, Tam arix may redirect aboveground resources away

from clonal reproduction (Fig. 5-3) because the neighboring plant may humidify the

boundary layer, protecting Tamarix from the drying effects of the atmosphere.

Tamarix did not produce longer taproots than the native species; in fact, it is not

difficult to imagine that obligate phreatophytes, like Salix (Busch et al. 1992), would be

well adapted for rapid root growth that is insensitive to environmental conditions.

Indeed, root growth in these species was high (Fig. 5-4); further growth through an entire

season would undoubtedly lead to taproots > 2 m in length, as previously observed in

Tamarix (D. Devitt, personal communication). Taproot growth was least in the cool

environment for Tamarix and the cool, wet environment for Pluchea (Fig. 5-4). Reduced

soil penetration in cool conditions (Jam arix and Pluchea) was likely due to reduced

respiration, and reduced taproot growth in the wet environment by Pluchea (Fig. 5-4B)

was likely a re-adjustment of root growth in response to soil hydrology (Ehleringer et al.

1992); as Tamarix is a stress tolerant species, it was unexpected that Tamarix did not

demonstrate a higher root growth rate at a higher drawdown rate. However, Tamarix

ability to utilize soil moisture from the unsaturated zone (Busch et al. 1992) doesn’t

impose as much survival necessity on reaching the water table as in obligate

phreatophytes.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 120 Predawn and midday Y; did not differ for either Tamarix or Pluchea (Fig. 5-5), as

previously observed in the field (Chapter 4). However, this anomalous similarity

between midday and predawn '?i was not due to the phreatophytic nature of these

seedlings, for predawn 'Fi > midday Y; in Salix, which did not show significantly

different root growth rates fi-om the other species. Because the predawn Ÿ, of Salix was

so much higher (i.e., less negative) than Ÿ, of Tamarix (Fig. 5-5), the Ÿ, of Tamarix is

probably dominated by the solute potential of Tamarix leaves, which overrides the diel

fluctuations in T, imposed by atmospheric demand, the salts in the leaves creating

tension much like the aridity of the atmosphere does during midday.

In Salix, A„et, g s and Fy / F^ were all sensitive to hot and dry treatment conditions

(Figs. 5-6 and 5-7). The concurrence between these related variables illustrates that Salix

is the most sensitive to abiotic stress, in which the absence of one stress can ameliorate

the physiological effects of the other stresses in Salix, and such interaction between

stresses allows temporal and spatial réfugia for Salix (Osmond et al. 1987). In Tamarix,

g s (but not Anet) was sensitive to the imposition of drought stress, but not to as great an

extent as in Salix (Fig. 5-6). Pluchea, in which Anet was lowest, did not demonstrate a

leaf-level gas exchange response to the imposition of abiotic or biotic stresses (Fig. 5-6).

The fluorescence property of PSII related to membrane stability (i.e., Fy / F^;

Lutts et al. 1996), was greatest in Tamarix (Fig. 5-7) as was hypothesized. Because Fy /

Fm was greatest in the wet-mixture treatment, the presence of interspecific neighbors

undoubtedly influenced the canopy structure in such a way that Tamarix benefited. This

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 121 was the same treatment in which ramet generation was suppressed in Tamarix (Figs. 5-3

and 5-7), further indicating that facilitation is an important factor contributing to the

invasive success ofTamarix when water stress is absent.

While both abiotic and biotic stresses impact physiological performance of these

species, physiological responses to abiotic stresses was more prevalent than responses to

biotic stress in these individual young seedlings. Where competition stress did affect

physiology (Table 5-1 and Figs. 5-3 and 5-7), early Tamarix seedlings were apparently

facilitated by the presence of neighbors. Young seedlings of Salix and Pluchea, on the

other hand, were insensitive to competition stress outside of a naturally occurring,

densely populated community (Chapter 4). The clonal nature of these species under field

conditions further increases the importance of inhibitory and facilitative relationships by

spatially ameliorating the effects of abiotic stress on physiology (Zekri and Parsons 1990;

Shard et al. 1993). The importance of facilitation in response to various environmental

conditions was again shown to contribute to the invasion of Tamarix along the Virgin

River in the Mojave Desert (Chapter 4).

Acknowledgements

The authors wish to thank Stan Smith, Arma Sala and Dale Devitt for their

assistance with development of the experimental design. Our further gratitude is offered

to Michael Loik for the use of his fluorimeter. Dawn Neuman for her laboratory space,

Fred Landau for glasshouse support, and Lyrm Shaulis and Erik Hamerlynck for

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 122 invaluable assistance in the glasshouse. This research was funded by grants from the Las

Vegas Valley Water Authority to D.A. Devitt and S.D. Smith, and UNLV B.A.G.S. and

the UNLV Graduate Student Association to J.R. Cleverly.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. CHAPTER 6

INFERENCE OF SUCCESSIONAL RELATIONSHIPS IN A SOUTHWESTERN FLOODPLAIN COMMUNITY THROUGH UTILIZATION OF CLIMATE AND ANNUAL TREE RING DATA

This chapter has been prepared for publication in Ecological Applications and is presented in the style of that journal.

123

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 124

Abstract

Allogenic succession refers to the long-term, sequential turnover of species in a

community when the pattern is dictated by the abiotic environment. Autogenic

succession, on the other hand, applies when a successional pattern is related to the biotic

environment (e.g., inhibition and facilitation by another species). Statistical models of

long-term, annual xylem production were developed to investigate the allogenic and

autogenic components of succession within a southwestern riparian community. Tree

ring surface area measurements were obtained for three riparian species (Tamarix

ramosissima, Salix exigua and Prosopis pubescens) that inhabit the Virgin River

floodplain in southern Nevada. Relationships between abiotic environment and long

term tree ring growth were investigated through multiple regression, and the effect of

interspecific interactions on long-term growth was investigated through power spectral

and coherence analyses of the tree ring growth-autocorrelation function. Over their tree

ring history, Tamarix was most responsive to maximum temperature during the previous

year’s summer and present year’s spring and summer maximum temperature (multiple

regression |3 = -0.55, -0.38 and -.49, respectively) and Salix growth did not respond to

those same maximum temperature regimes (multiple regression p = -0.10, -0.17 and -.06,

respectively). Furthermore, Tamarix demonstrated a typical wetness-growth relationship,

in which tree ring growth was significantly positively correlated to the present year’s

summer streamflow (multiple regression p = 0.41). Salix showed an atypical growth

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 125 response to the same streamflow regime, in which growth declined with increasing

streamflow (multiple regression p = 0.41). Thus, Salix was found to grow at the edge of

its drought tolerance along the Virgin River and probably experienced a great deal of

mortality episodes. The Virgin River experiences a yearly streamflow distribution that is

skewed toward low values, which together with the growth data explains the eventual

domination of the Virgin River floodplain by Tamarix. Growth in Tamarix and Prosopis

was strongly negatively correlated (power @ 0 cycles yr"* = 0.9 and 4.5 for Tam arix and

Prosopis, respectively; coherence = 0). There was no evidence of interspecific

interactions between Salix and Tamarix or Prosopis in the time series, and there were no

interspecific interactions with a time lag. Eventual dominance of the Virgin River

floodplain by Tamarix is inferred to result firom early colonization and long, slow growth,

rather than any marked competitive ability to invade already established stands.

Introduction

Ecological succession, in its widest sense, refers to long-term patterns of

vegetation associations (Drury and Nisbet 1973). Frequently, a more limited view of

ecological succession, driven by deterministic assumptions (Drury and Nisbet 1973),

requires climax-driven characteristics to demonstrate the pattern of succession (Clements

1936). It is firom this perspective that succession has been deemed not to occur in arid or

riparian communities, because early and late serai stages are often dominated by the

same species (Johnson et al. 1988), whether in the presence or the absence of Tamarix.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 126 The primary difficulty in studying the pattern of succession in aridland riparian

plant communities arises from environmental variability. Because the biota responds to

the fluctuations in the abiotic environment, pockets of successional patterns are scattered

spatially and temporally across the variable environment. Ultimately, environmental

conditions (both allogenic and autogenic) control a successional pathway, and more o f

those processes which drive ecological succession are exist in variable environments.

Desert floodplains in the southwestern U.S. are ideal for studies of successional

processes, particularly because they are continually disturbed and the time required for

the transition from one community composition to the next can be very short. Desert

floodplains are fru"ther useful in successional studies because of the close agreement

between community dynamics of their woody species and Egler’s concept of the Initial

Floristic Composition (IFC; Wilson et al. 1992). Van Auken and Bush (1988) showed

that, for Salix nigra and Populus fremontii, practically all successful seedling

establishment occurred in freshly opened sandbars near the river. Observations indicate

that Tamarix ramosissima, Pluchea sericea and Salix exigua are also restricted to

establishment on early sandbars along the Virgin River. In fact, all three species have

been observed to successfully germinate on a sandbar within the same 1-2 week period.

Prosopis pubescens doesn’t appear until the second year, after the water table has

dropped considerably (> 50 cm) below the surface.

Of particular use in the study of successional mechanisms are individual-based

models of physiological and life history traits over the life span of the longest-lived

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 127 organism in the ecological sequence (Huston and Smith 1987). The framework for such

models is already established as the field of dendroecology (Fritts 1972), in which the

effect of past and present environmental factors on tree growth is assessed. In fact, the

relative contributions of abiotic and biotic factors can be simultaneously investigated

through statistical modeling, in which allogenic succession can be inferred from multiple

regression relationships between tree growth and climate (Fritts 1976) and autogenic

succession can be inferred from coherence analysis of age-growth trends between species

(Fritts 1976).

This study was performed to investigate the relationships between abiotic

environment, growth and interspecific interactions over a 10 to 50 year time scale in a

Mojave Desert floodplain community. Two hypotheses were tested in this study. First, it

was predicted that there would be a relationship between the historical pattern of tree-

ring growth and seasonal temperature and streamflow, but not to species interactions

(Motzkin et al. 1993). Second, it was hypothesized that the succession of species in the

Virgin River floodplain would reflect climate. In other words, it was expected that

Tamarix comes to dominate these communities because of the climate of the region and

the growth response of Tamarix to that climate.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 128 Materials and Methods

Basai stem segments were collected from the confluence of Half-Way Wash with

the Virgin River, Nevada (36° 40’N, 114° 20’E, elevation 380 m; Appendix 1).

Collections were made during the winter of 1995, when the winter deciduous species

(i.e., Tamarix

ramosissima, Virgin River 18 Salix exigua 18 40 and Prosopis 100 m pubescens) 55 were dormant. Figure 6-1. Schematic showing stands from which tree ring specimens were collected. Stands are indicated by the age of the Stems were oldest collected specimen. ______obtained from five stands across the floodplain, ranging in age from 10 yrs to 55 yrs old

(as determined from the oldest specimen collected; see Chapter 2, Fig. 6-1). In the

laboratory, the stem sections were recut, sanded, varnished, oiled, scanned and analyzed.

These methods are described fully in Appendix 1.

Maximum and minimum monthly temperatures (1931 to 1996) were obtained

from the National Climatic Data Center (NCDC) from their Boulder City, Nevada station

(35° 98"N, 114° 85'E, elev. 770 m, NOAA 1998). Because there was no temperature data

available for Half-Way Wash, temperatures were also collected from 2 nearby stations

(Searchlight, NV (35° 47*N, 114° 92'E, elev. 1079 m) and Kingman, AZ (35° 02TST, 114°

02'E, elev. 1079 m)) to determine whether the temperatures at one station could be used

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 129 as a proxy for regional temperature. Daily streamflow data (1929 to 1995) were obtained

from the United States Geological Survey’s Littlefield, Arizona (36° 53"N, 113° 55'E,

elev. 538 m), station (USGS 1998). The Littlefield station has been collecting data for

over 60 years, while the USGS streamflow station at Half-Way Wash had been in

operation for only a six year subset of the 60 year period.

To reduce the number of variables (and their concomitant eflect on degrees of

freedom), monthly values were grouped into seasons, which were based loosely upon

phenology of these winter deciduous species. Spring was defined to be March, April and

May, wherein annual flooding occurs, plants break dormancy, and temperatures are still

moderate. Summer was defined as June, July, August and September. The end of

September coincides with the end of the water year and the beginning of senescence.

Winter was defined as the rest of the year.

Multiple linear regression (proc glm; SAS, SAS Institute, Cary, NC) was used to

build response functions between armual tree-ring surface area and climatic variables

(Fritts 1976). These climate-growth regression models were evaluated separately for

each species other than Plucheœ, Pluchea was not included in this analysis because the

youth of the stems created singularity all of the variable matrices. The first model

clumped all of the plants across all of the stands in the Half-Way Wash floodplain. The

rest of the models evaluated each species in each stand separately. In all hypothesis

testing, the probability of a type I error was presumed to be a = 0.05 (p < 0.05).

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 130 The effect of one year’s growth on succeeding year’s growth is frequently

inferred from the power spectral analysis in each individual tree’s growth time-series

autocorrelation function (Fritts 1976). Furthermore, co-cyclic behavior (coherence), both

phasic and aphasie, can be analyzed in the power spectra of more than one time-series to

infer interspecific relationships (Fritts 1976). Autocorrelation functions were calculated

for each species, upon which power spectra and coherence fimctions were constructed

using proc spectra (SAS, SAS Institute, Cary, NC). Investigation o f the raw growth

trajectory for each species was also used to illustrate growth-related successional

attributes of these riparian species.

Results

During the period of overlap, the correlation between streamflow at Half-Way

Wash (where tree bole sections were collected) and at Littlefield was very good (r^ =

0.96, Fig. 6-2A). Likewise, correlation between temperature measured at Boulder City

and at Kingman and Searchlight was very close (r^ = 0.98 and r^ = 0.99 for monthly

minimum and maximum temperature, respectively; Fig. 6-2B).

Tree ring surface area increased exponentially in Tamarix, Salix and Prosopis

over the last 55, 10 and 18 years, respectively (Fig. 6-3). Maximal growth rate was

achieved at 100, 5, and 35 cm^ yr*‘ in Tamarix, Salix and Prosopis, respectively, even

though the growth curve was steeper in Prosopis than in Tamarix (Fig. 6-3).

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 131

Littlefield Streamflow (10® m® day"’)

5 I Half-Way Wash = - 0.04 (Littlefield)^ ^ 1 4 + 0.99 (Littlefield) - 0.04; I ■o CO 3 CO

CO o 2

to 1 X 0

50 B o 40 2 3 30 0)2 Q. 20

- 1 0 _L -1 0 0 1 0 20 30 40 50

Boulder City Temperature (°C)

Figure 6-2. Reliability of USGS (1998) and NOAA (1998) data sets for predicting local streamflow (A) and regional temperature (B). Reference temperature stations used were in both Kingman, AZ, and Searchlight, NV.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 132

Tamarix 1 5 0 Salix • % S Prosopis (5 CO 2 00 < üCD oi E 3 o en 5 0 153 C

Tree Age (yr)

Figure 6-3. Tree age-xylem surface area growth relationship for Tamarix ramosissima, Salix exigua and Prosopis pubescens. Traces represent mean tree ring surface area across the floodplain. Inset: the first 10 years of the larger panel are expanded for easier viewing. Axes are the same variables as in the larger panel. ______Single and multiple relationships existed between environment and tree ring

growth at the individual stand scale in Tamarix, Salix, and Prosopis (Table 6-1). Across

sampled stands (Fig. 6-1), significant grcwth-climate relationships existed in Salix and

Prosopis, but not in Tamarix (Table 6-1). For all species, growth was negatively related

to maximum temperature and was positively related to minimum temperature, even

though the season and year (preceding or present with respect to a year’s growth) varied

between species (Table 6-2). Present summer and previous total streamflow were

negatively correlated to ring growth in Salix and Prosopis, respectively (Table 6-2).

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 133 Radial growth in Tamarix, on the other hand, responded positively to increased summer

streamflow (Table 6-2). The past history of streamflow in the Virgin River was skewed

toward lower values: there were very few large water years since 1930.

Variability in the growth-autocorrelation time series for each species was

predominantly acyclic, where Prosopis showed the greatest acyclic growth-

autocorrelation variability and Salix growth is least variable (Fig. 6-5A). Very low

coherence between these species in the acyclic region indicates 2-way negative

correlation between growth trajectories in Tamarix and Prosopis (Fig. 6-5B). High

coherence in the cyclic region is unimportant because none of the species demonstrated

variability at those frequencies (Fig. 6-5).

0 .4 r - T 1------1------1------1------1------r T T

0.3

2 0.2

0.1

f c _ J 3.2 4.8 6.3 7.9 9.4 11.0 12.5 14.1 15.7 17.2

streamflow (ICR day'^)

Figure 6-4. Histogram of annual streamflow discharge (10^ m^ day*') from the USGS Gauge at Littlefield, AZ. Water years, 1930 - 1996. Proportion indicates the percent of years that contributed to each category.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 134

Table 6-1. Multiple regression coefficients relating annual ring growth (cm^) to regional temperature and streamflow. Values indicated with an asterisk are significantly different from zero, s indicates that the matrices were singular because all of the specimens were too young, and np indicates that the given species was absent firom the given stand. Some species (e.g., Salix) were present in older stands but were not as old as representatives of other species (i.e., 37-40 year old Salix were not present). Stand age Regression coefficient (r^) Regression model (yr) Tamarix ramosissim, Salix exigua Prosopis pubescens Floodplain-wide -- 0.05 0.21 * 0.24 * Individual stands 8-13 0.30 s 0.57 * 18 0.30 * np 0.41 37-40 0.45 * 0.31 * 0.28 * 55 0.08 * np np

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 135

Table 6-2. Model coefficients (P) of the multiple regression (refer to Table 6-1) between tree ring surface area and climate, present and past. Values with an asterisk are significantly different firom zero. Positive values indicate a positive relationship between growth and the climate variable, given the other relationships in the matrix. (I.e., as growth increases, those variables with a positive value increases, too.)

Climate variable Model coefficient Tamarix ramosissima Salix exigua Prosopis pubescens Tmax Previous summe -0.55 ± 0.3 * -0.10 ± 0.14 -0.35 ± 0.1 * Present spring -0.38 ±0.1 * -0.17 ± 0.07 * -0.24 ± 0.08 * Present summer -0.49 ± 0.2 * -0.06 ±0.15 -0.15 ± 0.1 Tmin Previous spring 0.00 ± 0.07 -0.03 ± 0.03 0.06 ± 0.3 Present winter -0.03 ± 0.08 -0.01 ± 0.05 -0.03 ± 0.7 Present spring 0.48 ± 0.2 * 0.09 ± 0.1 0.33 ± 0.07 ’ Streamflow Previous summe 2.4 ± 2.1 0.88 ± 1.6 1.3 ± 1.0 Previous total -0.19 ± 0.1 -0.07 ± 0.07 -0.12 ± 0.04 * Present summer 0.41 ± 0.2 ' -1.6 ± 0.8 ’ -0.54 ± 0.75 Present total -0.07 ± 0.07 0.01 ± 0.04 -0.02 ± 0.03

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 136

Prosopis-Salix Tamarix-Salix Prosopis-Tamarix 5

4 Tamarix “ 0.75 Salix

0 0.250 0.5 0 0.25 0.5

Frequency (cycles yr’)

Figure 6-5. Spectral analysis of the tree ring growth-autocorrelation function. Power spectra estimates for Tamarix ramosissima, Salix exigua and Prosopis pubescens (A) are compared between species with coherence in power spectra (B). ______

Discussion

The climate data collected from public domain sources (NOAA 1998; USGS

1998) was consistent across a regional scale (Fig. 6-2B), so the relationships between

climate and interspecific growth patterns could be investigated by describing the multiple

correlations between growth, temperature, and streamflow. It was further encouraging

that the regression models on different experimental units (i.e., stands) were constructed

of similar significant model coefficients (p). Stand-based models of climate and growth

explained greater proportions of the variability in the data set (Table 6-1) because growth

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 137 and climate variability for clonal species like Salix and Tamarix are smoothed across

multiple ramets. The extensive root systems of these large genets can ameliorate

environmental drought and salinity stresses (Zekri and Parsons 1990; Shani et al. 1993).

The arborescent nature of Prosopis pubescens, in contrast to the thicket-forming

Tamarix ramosissima and Salix exigua, is clear from its very steep tree ring growth curve

(Fig. 6-3). However, large Prosopis trees are not found at this site, illustrated by its

foreshortened growth curve (Fig. 6-3). Domination of older stands by Tam arix at this

site (Fig. 2-2) is related to the slow growth but long-life of Tamarix, rather than rapid

growth, which Tamarix doesn’t demonstrate until after 40 years since seedling

establishment (Fig. 6-3).

Long-term growth in Tamarix was more responsive to the measured abiotic

environment than in Salix or Prosopis (Table 6-2). In fact, long-term growth in Salix and

Prosopis was negatively related to streamflow (Table 6-2). Such a negative relationship

is not unusual in the presence o f drought (Lane et al. 1993). In Salix, this negative

relationship indicates a potential response to cavitation and hydraulic loss, where the

plant could either produce additional xylem to replace dysfunctional conduits or suffer

from the greater water stress associated with compromised hydraulic conductivity (Tyree

and Ewers 1991). The widespread growth responses to temperature influences in

Tamarix relative to Salix are probably due to a greater proportion of Tamarix surviving

stress episodes that cause mortality in more sensitive species like Salix.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 138 Autogenic influences, inferred from the time series analysis, were primarily

competition between Tamarix and Prosopis, as illustrated by no coherence (i.e., perfect

aphasy) at 0 cycles yr'* (Fig. 6-5). This means that higher tree-ring growth in Tamarix is

correlated to lower tree-ring growth in Prosopis, which is consistent with competition

occurring between Tamarix and Prosopis with no time lag (Fritts 1976). Because these

two species are more drought-tolerant, their competition is consistent with the tendency

of this environment toward drier conditions (Fig. 5-4). This ecosystem exists at the

stressful extreme of multiple abiotic stress gradients (Osmond et al. 1987), and Salix is

probably inhabiting spatial and temporal réfugia from predominant environment.

Rather than finding that growth trends showed only allogenic succession, both

allogenic and autogenic succession have shaped this Virgin River floodplain community.

The abiotic and biotic environments interacted as a function of the predominant

streamflow record. Just as the physical environment has attributes favorable to invasion

by Tamarix, those same abiotic attributes sets the biotic arena, within which long-term

competition has been occurring to the benefit of Tamarix.

Acknowledgements

The author wished to thank Stan Hillyard for assistance with spectral and

coherence analyses. Gratitude is also offered for the intellectual and physical

contributions provided by Stan Smith, Dale Devitt, Anna Sala, Jeff Piorkowski, Chris

Schaan and Lynn Shaulis. Financial support was provided by a grant from the Las Vegas

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 139 Valley Water Authority (to D.A. Devitt and S.D. Smith), UNLV B.A.G.S. (to J.R.

Cleverly), and the Society of Wetland Scientists (to J.R. Cleverly).

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. CHAPTER?

CONCLUSIONS

What are the physiological bases o/'Tamarix invasion o f a shallow floodplain ecosystem

along the Virgin River, NV?

The physiology of Tamarix was extensively conducive to ecological success on in

the Virgin River floodplain. The water status of Tamarix was relatively stable under

various drought conditions (Chapters 2, 5, and 6; Fig. 7-1). While gas exchange in

sapling Tamarix leaves showed difficulty recovering from seasonal drought (Chapter 2),

photosynthesis and gj were unresponsive to drought in seedlings (Chapters 4 and 5).

Such leaf-level gas exchange indicates that continued normal gas exchange in Tamarix

occurs at a seasonal-scale cost to physiological performance. The short-term investment

in higher rates is expected to be successful if the native species experience higher

mortality while Tamarix does not (Chapter 5).

Tamarix does not experience mortality to stress (Chapter 5) because of its

impressive starch storage in taproots and stems (Chapter 4) coupled to its slow growth

rate (Chapters 4 and 6). Not only does starch storage and slow growth contribute to

lesser survival, but early formation of ramets (Chapter 5) provides sacrifice tissue that

can be lost under extremely dry conditions without complete mortality.

140

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 141 Lastly, Tamarix ability to modify the environment through fire and sedimentation

has been well documented (Blackburn et al. 1982; Busch and Smith 1995). Tamarix is

also capable of changing the atmospheric environment and can quite well protect itself

against cool nighttime temperatures through storage of sensible heat on surficial leaf

water (Chapter 3), through increasing the temperature and relative gradients between

floodplain and desert ecosystems (Chapter 3; Malanson 1995), and through boundary

layer humidification and leaf area production (Sala et al. 1996).

How will the dominant woody species respond physiologically to a range o f realistic

environmental conditions?

Even though Tamarix was expected to show complete unresponsiveness to stress,

the responses observed are consistent with its stress tolerant characteristics. For

example, the responsiveness of Tamarix radial growth to streamflow was consistent with

a species that is not experiencing drought stress, as well as not experiencing mortality

due to fluctuations in the abiotic environment (Chapter 6). It can be difficult

distinguishing between a response to stress that indicates compromised performance and

physiological readjustment to improve survival (Osmond et al. 1987).

Salix did show a decline in performance under abiotic stress (Chapters 2, 5, and 6;

Fig. 7-1). Some of the traits in Salix that were responsive to the abiotic environment

were growth, leaf-level gs, fluorescence and mortality. Some of these variables are

related to plant health (like chlorophyll fluorescence), while others indicate that

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 142 performance was compromised because they did not occur along with traits like starch

storage.

Pluchea responded dramatically to drought in some ways (e.g., in Fig. 7-1 A),

even though leaf-level ET remained unaffected (Fig. 7-IB). Pluchea can be quite

tolerant of abiotic stress, with a root elongation rate that is the rival of other

phreatophytes. In the short term, Pluchea was shown to unexpectedly not decline in

performance when exposed to drought.

The scarcity of Prosopis seedlings interfered with testing this hypothesis. Leaf-

level ET in Prosopis declined greatly upon the imposition of a seasonal drought (Chapter

2; Fig. 7-1), but not enough higher resolution information concerning specific

physiological responses of Prosopis to the abiotic environment could be collected to

determine whether the response observed in Chapter 2 is beneficial or detrimental to

Prosopis. Only Tamarix was able to compete with Prosopis in the long term (Chapter 6),

suggesting that the responsiveness of Prosopis was probably beneficial in the long term.

What is the pattern o frelative short-term performance under various environmental

conditions?

Under wet and cool conditions, leaf-level ET in Salix was higher (Chapter 2; Fig.

7-lB). Unexpectedly, Tamarix chlorophyll fluorescence was facilitated by the presence

of other species (Chapter 5). Because Pluchea and Salix contribute to the health and

vigor of Tamarix under wet conditions, the order of relative short-term performance was

modified to Salix > Tamarix > Pluchea > Prosopis to reflect that Salix was found to

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 143 perform the best of these species under abiotic stress, but that the benefit o f neighboring

species increases Tamarix performance above Pluchea.

Under dry and very dry conditions, Tamarix and Prosopis experience

competition, indicating they occupy fairly close habitats (MacArthur and Levins 1967;

Abrams 1983; Pacala and Tilman 1994). Therefore, their predicted dominance at the top

of the chain in dry and very dry environments was verified. Leaf-level physiology was

more stable in Pluchea (Fig. 7-1) than in Salix, and Pluchea^ s 'Fi was unresponsive to

diel variation, as with Tamarix (Chapters 4 and 5). Therefore, short-term relative

performance in dry and very dry environments was Tamarix > Prosopis > Pluchea >

Salix.

Will short-term relationships between environment, physiology, and

inhibition/facilitation patterns be reflected over the long-term (i.e., > 2 seasons)?

Long-term growth records showed Salix to be sensitive to drought, Tamarix to

gain a benefit from short-term storage of starch, and Prosopis to suffer premature

mortality (Chapter 6). Flooding is an episodic, rare event (Fig. 6-4) that causes mortality

in Tamarix (Chapter 4). The anaerobic soils following flooding may cause mortality in

Prosopis, thereby capping its growth potential. The same stress physiology was

operating in the short-term with Tamarix, Salix, and Pluchea.

The multitude of short-term interspecific responses observed in Chapters 4 and 5

were not reflected in succession. That is because Pluchea played a major role in

facilitating Tamarix, butPluchea stems don’t live long enough to detect their impact on

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 144 succession (i.e., they persist in a different temporal scale). The inhibitive growth

relationship between Tamarix and Prosopis in the long-term reflects their adaptation to

similar habitats, and Tamarix succeeds because of its survival of those episodic events

that Prosopis cannot avoid (Chapter 6).

— Tamarix ramosissima Prosopis pubescens — Pluchea sericea Salix exigua

•i0) p ^ n. (0 ÎÎ T3 T3 Î - 1 -2.5 175 200 225 175 200 225

Day of Year

Figure 7-1. Summary physiological responses (T, (A) and ET (B)) and to drought, imposed between days 175 and 225 of the year 1994. Data redrawn firom Fig. 2-5.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. APPENDIX 1

DIGITAL IMAGE ANALYSIS OF ANNUAL TREE-RING SURFACE AREA IN MOJAVE DESERT FLOODPLAIN SPECIES

This appendix has been prepared for publication in Tree Physiology and is presented in the style of that journal.

145

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 146

Abstract

A methodology was developed to correct for geometric constraints on tree ring

growth estimates, as well as incorporate physiologically meaningful measurements of

xylem production. Surface area estimates of annual ring growth were made on three

Mojave Desert riparian species: Tamarix ramosissima, Salix exigua and Prosopis

pubescens. Entire boles of each species were collected, and their transverse-section was

digitally rendered as 8-bit tagged image file format (TIFF) files for image enhancement

and surface area measurement. Excellent fit (r^ = 1.000) between actual and measured

surface area of simulated tree rings illustrated the accuracy of the digital medium. Using

digital image analysis for tree ring studies also corrects for age trends found in linear

estimates of tree ring growth, and these methods can be easily adapted for obtaining

precise measurements of cell volume, leaf area, and root density.

Introduction

A great deal of research has been performed on the pattern of tree ring growth, as

measured by ring width increments firom cores or bole sections. The time-series patterns

of radially linear growth collected firom such measurements can be used to reconstruct

past climate and to investigate biotic and abiotic correlates to long-term growth (Fritts

1976). However, there are some rather important limitations on the use of linear

estimates of tree ring growth imposed by growth trends with respect to tree age

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 147 (Cleaveland and Stable 1989; Meko et al. 1995), geometrical constraints between linear

and areal measurements (Visser 1995), and the role of xylem structure and function.

In tree ring growth series, younger rings tend to be wider than older rings (Meko

et al. 1995). Such trends have to be removed from the ring series when investigating

relationships between growth and climate (Cleaveland and Stable 1989), which is usually

achieved through a spline curve fit (ARSTAN; cf- Cleaveland and Stable 1989). Such a

transformation is ultimately necessary because this relationship between ring growth and

age is imposed by the geometric constraint of shape on the scaling of linear and areal

dimensions (Visser 1995). Because this constraint is purely physical, rather than

physiological or biological, it interferes with the reliability of the tree ring data and

should be removed. Geometrical constraints even further confound tree rings studies on

species that produce neither concentric nor regularly shaped rings, as with A rtem isia

tridentata (Ferguson 1964).

Measurements of tree ring surface area, on the other hand, do not suffer from the

geometric constraints between linear and areal measures. Furthermore, estimates of

surface area growth provide functional measures of radial growth because both xylem

transport processes (Tyree and Ewers 1991) and structural support are functions of

surface area rather than diameter.

Because of the difficulty in collecting surface area measurements of tree rings,

digitally enhanced methodologies have been investigated. Guay et al. (1992) provide an

extensive review of digital methods in tree ring measurement, as well as present another

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 148 line scan camera approach to collect tree ring measurements of tree ring linear

increments, even though the authors suggest that their system is easily adapted to tree

ring surface area measurements (Guay et al. 1992). Most of the methodologies presented

either required expensive instrumentation (e.g., robotics) or used low-resolution

techniques that are not easily upgradable (Clyde and Titus 1987).

The objective of developing an inexpensive, simple, high-resolution tree ring

surface area measurement method was developed. It was hypothesized (1) that such a

digital technique could render tree ring measurement simple and accurate and (2) that

surface area-based growth measurements would reflect physiological, rather than

geometric, characteristics. These hypotheses were tested on three Mojave Desert

floodplain species: Tamarix ramosissima, Salix exigua and Prosopis pubescens. The

former two species are thicket-forming species, so numerous samples could be collected

without damaging a large proportion of the individuals in the community.

Materials and Methods

This study was performed at two locations along the lower Virgin River

floodplain in the Mojave Desert of southern Nevada (Chapter 2; Sala et al. 1996). At the

mouth of Half-Way Wash (36° 40’N, 114° 20’E, elevation 380 m), the woody vegetation

consisted of saltcedar {Tamarix ramosissima), screwbean mesquite {Prosopis pubescens),

baccharus willow {Baccharis glutinosa), Gooding willow {Salix gooddingii), pickleweed

{Allenrolfea occidentalis), and a single cottonwood tree {Populus fremontii). On 4

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 149 January 1996, specimens o f the codominant species, Tamarix (n = 62), Salix (n = 28),

Pluchea (n = 47) and P. pubescens (n = 28), were collected from six stands of 8 to 55

years old. Tamarix, Salix spp., and P. pubescens were leafless, unlike the evergreen

Pluchea.

Basal stem segments, ranging from 3 cm to 15 cm in length, were collected from

1-5 cm above the soil surface. These stems were then sanded, then varnish was applied

to seal the wood and to enhance the delineation of the rings. Ring sequences were

visually inspected for crossdating (Fritts 1976).

Cedarwood oil was applied to the stem sections to maximize the surface’s

reflectiveness. These oil-coated stems were blotted (to discourage pooling of the oil and

associated visual aberrations) and placed face-down on a clean transparency film

mounted on a UMAX Vista S6E scanner (UMAX, Fremont, CA). Images of the stem

sections were captured at 236.22 pixels cm‘‘ and 100% magnification. Because the

monitor’s resolution is 29.5 pixels cm"*, images were effectively magnified by 8X.

Images were scanned into Adobe Photoshop v3.0 (Adobe Systems, Inc.,

Mountain View, CA) for enhancement. The autolevels algorithm was used to distribute

the pixel colors in three channels: red, green and blue. The enhanced images were then

rendered into 8-bit indexed color using the Photoshop adaptive palette and dithered

colors. Files were saved in tagged image file format (TIFF) for analysis using NIH

Image vl.62b4 (National Institutes of Health, Bethesda, MD). A precise area standard

was scanned with the images. It was discovered, however, that the scanning resolution

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 150 (at 100% magnification) is available automatically to the image analysis software.

making the area standard redundant.

Beginning with the pith and working outward, surface area was determined using

the freehand selection tool (for rings <1.0 cm^) and the polygon selection tool (for rings

>1.0 cm^) to correct for errors introduced from the selection method (see below). The

ring was traced, and NIH Image calculated the surface area of that ring as a function of

the number of pixels selected. Notations were made for false rings {sensu Fritts 1976).

Further verification of these methods was performed through the analysis of

known standards. Simulated tree rings, both circular and elliptical, were produced each

to a specific area in Adobe Illustrator v5.5 (Fig. Al-1; Adobe Systems, Inc., Mountain

View, CA). These simulated stems were

printed, scanned (at 236.22 pixels cm',

100% magnification), enhanced, and

analyzed as with the real stems.

Figure Al-1. Simulated tree rings used The selection tools used for in accuracy analysis. Rings were produced to sizes with random surface measurements were also tested for their area. Shapes were circular (A) or elliptical (B). ______accuracy with the simulated rings. Both

the freehand selection and the polygon selection tools were used to measure each ring

twice (for n = 2 psuedoreplicates). The accuracy was determined for each shape (Fig.

Al-1) and selection tool. Similarity between the actual and measured area was

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 151 determined as the percent difiference between the two values (i.e., measured area actual

area = % similarity).

After tree-ring surface area was measured, mean deviates of annual surface area

were calculated. Mean deviates of annual surface area were calculated as the difference

between an individual year’s growth and the mean growth of all rings averaged across

the stem:

mean deviate = x, - x,

where x,- represents the individual ring’s surface area, and x is the average annual growth

for each individual tree. Positive values indicate growth greater than an individual tree’s

mean growth, and negative values indicate lesser than mean growth

General linear regression models between surface areal and linear (i.e., ring

thickness or distance) measures of growth were prepared separately for each species

(SAS, SAS Institute, Cary, NC). Likewise, actual and measured surface areas of the

simulated stems were modeled by linear regression. In all statistical hypothesis testing,

the probability of a type I error was presumed to be a = 0.05.

Results

The measured area of each simulated tree ring was highly correlated with the

actual area (r^ = 1.000, n = 68, p = 0.0001; Fig. A1-2A). Underestimation errors were

found at the lower sizes using the polygon selection tool, while overestimation occurred

with larger sized rings using the freehand selection tool (Fig. A1-2B).

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 152 Tree ring growth in these species was lower than average for the first three years,

when Salix and Prosopis growth rose slightly above average (Fig. Al-3). Growth

circle polygon ellipse polygon circle freehand ellipse freehand 1 0 =1 % 0.95 >» (0 2 (0 0.9 1 T3 (0 gQ) 0.1 - 0.85 55

0.01 0.8 0.01 0.1 1 1 0 0.1 1 0

actual area (cm^) Figure Al-2. Accuracy analysis of simulated tree rings. Measured area = 0.001 + 1.001 (actual area) (A). The percent similarity (B) between actual and measured areas were measured on both circles and ellipses (Fig. A l- 1), as well as with the polygon and freehand selection tools. ______remained below average in Tamarix for the longest; positive values were not obtained

until well after 10 years old (Fig. Al-3). Growth in Prosopis began to decline after 17

yrs, but did not fall to lower than average while growth in Tamarix dropped well below

average for 10 yrs after dropping to zero at 45 yrs of age (Fig. Al-3).

Discussion

This tree ring measurement system was inexpensive, completed entirely with low-

tech devices. The free availability of NIH-Image easily allows for analysis of high

resolution images. Therefore, the objective of this study was met; a low-tech tree ring

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 153 research method was developed that was inexpensive, simple but still had high-

resolution.

The accuracy of digital area measurements is very high (Fig. Al-2), due to the

benefits of image enhancement and magnification. Very little crossdating had to be

accomplished because the characteristics of the ring could be seen continuously, rather

than in a small wedge as with tree ring studies from cores (Fritts 1976). Because the

rings can be made easier to see on the computer, accuracy of digital images is probably

higher than accuracy of non-digital images— even when magnification in a microscope

7.5 Tamarix 0.5 Salix Q Prosopis as 5 Q

o 2.5 0 Ü caQ>

o 0 ■ë3 CO

-2.5 0 1 0 20 30 40 50 60 Age (Yr)

Figure A 1-3. Surface area growth deviation from the mean lifetime growth (x; - x), averaged across all individuals of Tamarix ramosissima, Salix exigua, and Prosopis pubescens. Values above zero indicate periods of increasing growth rate, and values below zero indicate periods of decreasing growth rate. Inset: the first 10 years of the larger panel are expanded for easier viewing. Axes are the same variables as in the larger panel. ______

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 154 is required, micrographs can be transferred to a digital medium through scanning or by

mounting a digital camera to the microscope or a robotic device (Alfaro et al. 1984; Liu

1986; Guay et al. 1992; Schmidt et al. 1996).

By measuring xylem surface area production, rather than the greatest distance

between tree rings (Ferguson 1964), the geometric constraints that affect linear estimates

of annual ring growth are not reflected in the measurement of surface area (Fig. Al-3).

The pattern of surface area mean deviates in Tamarix ramosissima shows a distinct

senescence phase, when xylem production rate falls off after 45 years (Fig. Al-3). Such

a pattern confirms that measures of xylem surface area reflect physiologically meaningful

estimates of annual growth that are not bound by geometric constraints.

Acknowledgements

We would like to thank C. Schaan, D. Devitt and L. Shaulis for their invaluable

assistance in the field. We further appreciate the assistance of P. Territo with both

conceptual design and implementation, as well as D. Orange for his software and

hardware support of this project.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. APPENDIX 2

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155

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 156

PERMISSION TO USE COPYRIGHTED MATERIAL

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Graduate College University of Nevada, Las Vegas

James R. Cleverly

Local Address: 3021 E Karen Avenue Las Vegas, NV 89121

Degree: Bachelor of Science, Biology, 1993 University of Utah

Special Honors and Awards: Invited Participant, Colloquium on Terrestrial Ecosystems and the Atmosphere 1996, National Center for Atmospheric Research (NCAR), Boulder, CO

Best Student Poster, Physiological Ecology Section, 1996 Ecological Society of America, Providence, RI

Outstanding Graduate Student, 1997 Board of Regents, University and Community College System of Nevada

Nominated for Regents Scholar Award, 1997, 1998 Board of Regents, University and Community College System of Nevada

Invited Symposium Speaker, 1998 Southwestern Association of Naturalists, Albuquerque, NM

Publications: Barker, D.F., J. Cleverly and P.R. Fain. 1992. Two CA-dinucleotide polymorphisms at the COL4A5 (Alport syndrome) gene in Xq22. Nucleic Acids Research 20: 929

Smith, S.D., A. Sala, D A. Devitt and J.R. Cleverly. 1996. Evapotranspiration from a saltcedar-dominated desert floodplain: a scaling approach. Pages 199-204 184

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 185 In: Barrow, J.R., E.D. McArthur, R.E. Sosebee and R.J. Tausch, comps. Proceedings: symposium on shmbland ecosystem dynamics in a changing climate. 1995 May 23-25, Las Cmces, NM. Gen. Tech. Rep. INT-GTR-338. Ogden, UT: U.S. Department of Agriculture, Forest Service, Intermountain Research Station

Cleverly, J.R, S.D. Smith., A. Sala and D.A. Devitt. 1997. Invasive capacity of Tamarix ramosissima in a Mojave Desert floodplain: the role of drought. Oecologia. Ill: 12-18

Devitt, D.A., J.M. Piorkowski, S.D. Smith, J.R. Cleverly and A. Sala. 1997. Plant water relations of Tamarix ramosissima in response to the imposition and alleviation of soil moisture stress. Journal o f Arid Environments. 36: 527-540

Bonan, G., J. Cleverly and J. Shen. 1998. Land surface process modeling. Pages 39-58 In: Schimel, D. and R. Monson. Proceedings: colloquium on terrestrial ecosystems and the atmosphere. 1996 July 14-27, Boulder, CO. National Center for Atmospheric Research.

Devitt, D.A., A. Sala, S.D. Smith, J. Cleverly, L.K. Shaulis and R. Hammett. 1998. Bowen ratio estimates of évapotranspiration for Tamarix ramosissima stands on the Virgin River in southern Nevada. Water Resources Research. 34: 2407-2414

Smith, S.D., D.A. Devitt, A. Sala, J.R. Cleverly and D.E. Busch. 1998. Water relations of riparian plants from warm desert regions. Wetlands. 18: 687-696

Dissertation Title: Plant Physiology and Competition in a Mojave Desert Riparian Ecosystem: Proximate Solutions to Ultimate Questions

Dissertation Examination Conunittee: Chairperson, Dr. Stanley D. Smith, Ph. D. Committee Member, Dr. Dale A. Devitt, Ph. D. Committee Member, Dr. Lawrence R. Walker, Ph. D. Committee Member, Dr. Paul J. Schulte, Ph. D. Committee Member, Dr. Bruce E. Mahall, Ph. D. Graduate Faculty Representative, Dr. David K. Kreamer, Ph. D.

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