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dissertation entitled

WOODY PLANT ADAPTATIONS TO WATER STRESS IN ARID
SHRUB COMMUNITIES

presented by

Anna Linden Jacobsen

has been accepted towards fulﬁllment
of the requirements for the

Ph.D. degree in Plant Biologl

 

 

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WOODY PLANT ADAPTATIONS TO WATER STRESS IN ARID SHRUB
COMMUNITIES

By

Anna Linden J acobsen

A DISSERTATION
Submitted to
Michigan State University
in partial fulﬁllment of the requirements
for the degree of
DOCTOR OF PHILOSOPHY
Plant Biology

2008

ABSTACT

WOODY PLANT ADAPTATIONS TO WATER STRESS IN ARID SHRUB
COMMUNITIES

By
Anna Linden J acobsen

Plants vary greatly in the amount of water stress they experience and in their ability to
maintain water transport during periods of water stress. Woody plants in arid shrub
communities experience periods of extreme water stress and likely have evolved distinct
mechanisms for tolerating this stress. This may be particularly important in species that
maintain evergreen leaves and tolerate rather than avoid seasonal water stress. The
present dissertation examines, at the cellular, tissue, and community levels, what xylem
traits are associated with the xylem pressures experienced by arid woody plants and their
ability to maintain a functioning water transport system in the face of water stress.
Additionally, the role of xylem traits in community assembly and structure are examined.
Water stress tolerance strategies among woody shrub species from Californian and South
African shrub communities are compared to examine whether species from these
communities are utilizing common or different water stress tolerating strategies.

Across arid communities, communities composed of woody shrub species shared
a common mean water stress level although individual species varied greatly in the level
of water stress they experienced. Species that experienced very low xylem water
potentials seasonally had dense xylem due to reinforcement of both xylem vessel walls
and the surrounding ﬁber matrix. These cellular traits were associated with individual
and community level differences in cavitation resistance. Communities differed in the

suites of traits used by species within each community, including differences in their

xylem traits and in their stomatal response to water stress. These community speciﬁc
water use traits may play a role in community assembly and suggest that communities
may be differentially susceptible to invasion by non-native woody species. Comparable
plant communities from the Mediterranean-type climate regions of California and South
Africa appeared to be utilizing similar water use strategies, suggesting that there may be

convergence in water use strategy for communities in comparable arid environments.

ACKNOWLEDGEMENTS

I would like to that Michigan State University and the MSU Department of Plant Biology
faculty and staff for assistance and support in completion of this dissertation. I thank my
committee members, Dr. Frank Ewers, Dr. L. Alan Prather, Dr. Doug Schemske,pand Dr.
Frank Telewski, for their guidance and assistance. Many people have assisted in
completion of this dissertation, including Dr. Maynard Moe, Grant J acobsen, Dr. Kathryn
Jacobsen, Dr. Jason Kilgore, Dr. Karen Esler, Lize Agenbag, and others, for which I
thank them. Thanks go to my parents, Drs. Rhonda and Douglas J acobsen for their love
and support. I would like to specially thank Dr. Frank Ewers for being a wonderful
advisor, mentor, and friend, Dr. Stephen Davis for assistance, advice, hospitality, and use
of laboratory facilities, and Janet Davis for support, friendship, and hospitality. Finally, I
owe a great deal of thanks to my husband, Dr. R. Brandon Pratt, who has been unsparing
with his time, helpful with discussions and editing, inﬁnitely patient, and generous with
his laboratory space and facilities.

I thank the Michigan State University Department of Plant Biology, Pepperdine
University Natural Science Division, Stellenbosch University, and California State
University Bakersﬁeld for providing lab space and use of equipment and facilities. I
thank Mountain Restoration Trust, Pepperdine University, and the State of California
Department of Parks and Recreation for access to ﬁeld sites.

I thank the many funding sources that contributed to my completion of this
dissertation: National Science Foundation Graduate Research Fellowship, Michigan State

University-University Distinguished Fellowship, Paul Taylor Funds, Botanical Society of

iv

America Vernon Cheadle Student Travel Award, Fulbright Fellowship Program, and

National Science Foundation Doctoral Dissertation Improvement Grant.

TABLE OF CONTENTS

LIST OF TABLES .................................................................................... x
LIST OF FIGURES ................................................................................. xi
KEY TO SYMBOLS OR ABBREVIATIONS ................................................. xv
INTRODUCTION ................................................................................... 1
Plant water transport ........................................................................ 2
Hydraulic failure ............................................................................. 3
Xylem cellular and mechanical traits ...................................................... 5
Seasonal water relations ..................................................................... 5
Community structure ........................................................................ 6
Convergence among Mediterranean-type climate regions ............................. 6
CHAPTER 1
DO XYLEM FIBERS AFFECT VESSEL CAVITATION RESISTANCE? ................. 8
Abract .......................................................................................... 9
Introduction ................................................................................. 10
Results ....................................................................................... 12
Mechanical properties of stems .................................................. 12
Cavitation resistance .............................................................. 13
Stem traits .......................................................................... 14
Cellular traits ....................................................................... 14
Discussion ................................................................................... 15
Materials and Methods ..................................................................... 22
Study site ........................................................................... 22
Mechanical measurements ....................................................... 23
Hydraulic conductivity and cavitation resistance ............................. 25
Minimum Field Pressure Potentials ............................................. 27
Xylem anatomical measures ..................................................... 27
Data analysis ....................................................................... 28
CHAPTER 2
CAVITATION RESISTANCE AND SEASONAL HYDRAULICS DIFFER AMONG
THREE ARID CALIFORN IAN PLANT COMMUNITIES .................................. 37
Abstract ...................................................................................... 38
Introduction .................................................................................. 39
Materials and Methods ..................................................................... 41
Sites and species ................................................................... 41
Wet season vulnerability to cavitation .......................................... 43
Dry season predawn water potential and native PLC ........................ 45
Dry season vulnerability to cavitation .......................................... 46

vi

Statistical analyses ................................................................ 47

Results ....................................................................................... 48
Discussion ................................................................................... 5 1
Non-convergence of cavitation resistance ..................................... 51
Seasonal shifts in cavitation resistance ......................................... 53
Inﬂuence of seasonal shifts on interspeciﬁc and community
comparisons ........................................................................ 55
Physiology of seasonal shifts .................................................... 56
CHAPTER 3
COMPARATIVE COMMUNITY PHYSIOLOGY: NON-CONVERGENCE IN WATER
RELATIONS AMONG THREE SEMI-ARID SHRUB COMMUNITIES ................. 66
Abstract ...................................................................................... 66
Introduction ................................................................................. 67
Materials and Methods ..................................................................... 70
Sites and species ................................................................... 70
Weather ............................................................................. 71
Seasonal water potential .......................................................... 71
Seasonal stomatal conductance .................................................. 72
Speciﬁc leaf area ................................................................... 73
Leaf speciﬁc hydraulic conductivity ............................................ 73
Xylem density ...................................................................... 74
Data analysis ....................................................................... 74
Results ....................................................................................... 76
Weather ............................................................................. 76
Seasonal water potential .......................................................... 76
Seasonal stomatal conductance .................................................. 77
Water potential and stomatal conductance ..................................... 79
Speciﬁc leaf area ................................................................... 80
Xylem density ...................................................................... 80
Hydraulic conductivity ............................................................ 81
Xylem vulnerability to cavitation ............................................... 82
Water use “strategies” ............................................................ 82
Discussion ................................................................................... 83
CHAPTER 4
PHYLOGENETIC DISPERSION AND COMMUNITY STRUCTURE IN THREE
ARID PLANT COMMUNITIES ................................................................. 101
Abstract ..................................................................................... 101
Introduction ................................................................................ 102
Materials and Methods .................................................................... 105
Results ...................................................................................... 108
Community structure ............................................................ 108
Community assemblages ........................................................ 108
Conspeciﬁc occurrence .......................................................... 108
Species distributions within communities .................................... 109

vii

Functional traits and phylogeny ................................................ 109

Functional traits and species co—occurrence ................................. 110
Discussion .................................................................................. 11 1
Community assemblages and structure ....................................... 111
Conspeciﬁc co-occurrence ...................................................... 1 11
Species distributions and communities ........................................ 113
Functional traits and community structure .................................... 115
CHAPTER 5
DRY SEASON SOIL MOISTURE CONTENT AND INVASIBILITY OF ARID
SHRUBLANDS .................................................................................... 124
Abstract ..................................................................................... 124
Introduction ................................................................................ 125
Materials and Methods .................................................................... 127
Results ...................................................................................... 128
Discussion ................................................................................. 129
CHAPTER 6

XYLEM DENSITY, BIOMECHANICS, AND AN ATOMICAL TRAITS CORRELATE
WITH WATER STRESS IN SEVENTEEN EVERGREEN SHRUB SPECIES OF THE

MEDITERRANEAN -TYPE CLIMATE REGION OF SOUTH AFRICA ................. 136
Summary ................................................................................... 137
Introduction ................................................................................ 138
Materials and Methods ................................................................... 140
Results ...................................................................................... 145

Intraspeciﬁc comparison of sexes .............................................. 145

Minimum seasonal pressure potential ......................................... 146

Correlations of raw trait values ................................................. 147

Phylogenetic independent contrast correlations .............................. 148

Principal components analysis .................................................. 149

Discussion ................................................................................. 150
CHAPTER 7

CAVITATION RESISTANCE IN FYNBOS AND SUCCULENT KAROO SHRUB
SPECIES AND MEDITERRANEAN -TYPE CLIMATE REGION

CONVERGENCE .................................................................................. 169
Summary ................................................................................... 169
Introduction ................................................................................ 170
Materials and Methods ................................................................... 172
Results ...................................................................................... 175

Vulnerability to cavitation ...................................................... 175
Xylem anatomy and cavitation resistance ..................................... 176
Water use “strategies” ........................................................... 177
Convergence among Mediterranean-type climate regions ................. 178
Discussion ................................................................................. 179
Resistance to cavitation .......................................................... 179

viii

Water use “strategies” of fynbos and succulent karoo shrub ............... 182
Convergence among South African and Californian plant

communities ...................................................................... 1 84
CHAPTER 8
CONCLUSION .................................................................................... 195
LITERATURE CITED ........................................................................... 197

LIST OF TABLES

Table 1.1: Xylem functional properties for six Chaparral shrub species ..................... 29

Table 2.1: Vegetation community, location and sampled species within each community
along with families, codes and leaf habits ....................................................... 59

Table 3.1: Species listed by vegetation type, family, species code, cavitation resistance
(W50), xylem speciﬁc conductivity (Ks), speciﬁc leaf area (SLA), and xylem density for
28 shrub species from three sites in southern California ....................................... 91

Table 4.1: Species and families from three arid plant communities, species codes, and
species characteristics including height, crown diameter, and basal diameter ............ 116

Table 4.2: Plant community traits of canopy height, mean species crown diameter, mean
basal diameter, and average distance between individual plant bases and crowns in three
plant communities, Chaparral, coastal sage, and Mojave Desert scrub ..................... 118

Table 4.3: Observed and expected numbers of conspeciﬁc and heterospeciﬁc neighbors
and nearest neighbors among the dominant woody plant species from three plant
communities, Chaparral, coastal sage, and Mojave Desert scrub ............................ 119

Table 6.1: The species of evergreen shrubs located on J onaskop in the Riviersonderend
Mountain Range in the Western Cape Province, South Africa, along with the elevation at
which the species was sampled (rounded to the nearest 10 m) .............................. 159

Table 6.2: The coefﬁcients of determination (r2) and probability values (P) for
regressions of raw trait values and phylogenetic independent contrast (PIC) values of
several xylem structural and functional traits as measured on 17 evergreen shrub

species ............................................................................................... 160

Table 7.1: Species of evergreen shrubs located on Jonaskop in the Riviersonderend
Mountain Range in the Western Cape Province, South Africa including species families
and the code used for each species in Figures 7.1, 7.2, 7.5, and 7.6 ........................ 186

Table 7.2: Xylem functional and anatomical traits for several xylem functional and
anatomical traits previously published in J acobsen et al. (2007a) and included in analyses
in the present study .............................................................................. 187

LIST OF FIGURES

Figure 1.1: Load versus displacement in four-point bending tests for stems of six species
of Chaparral shrubs .................................................................................. 31

Figure 1.2: Modulus of rupture (MOR) versus modulus of elasticity (MOE) for wet and
dry treatments of stems of six species of Chaparral shrubs .................................... 32

Figure 1.3: Percentage of loss of hydraulic conductivity of stems as a function of xylem
pressure potential (PX) .............................................................................. 33

Figure 1.4: A. Modulus of rupture (MOR), B. xylem density, and C. minimum seasonal
pressure potential (Pm) as functions of xylem pressure at 50% loss of conductivity (P50)
and D. xylem density and E. Pm as functions of MOR for six species of Chaparral

shrubs ................................................................................................. 34

Figure 1.5: Xylem anatomical measures as functions of the xylem pressure at which
there is a 50% loss of conductivity (P50) and MOR, including estimated vessel implosion
resistance [(t/b)h2; A and D], percentage of ﬁber wall area (B and E), and ﬁber lumen
diameter (C and F) in six species of Chaparral shrubs .......................................... 35

Figure 1.6: Some possible causes of embolism in a woody angiosperm stem ............. 36

Figure 2.1: Vulnerability to cavitation curves measured on 10 Chaparral shrub species (a-
j; see Table 1 for full species names) during the wet season (February-May 2006; closed
circles, mean :1: 1 SE; n = 6-12) and for four species measured during the dry season
(August-December 2006; open circles, mean :I: 1 SE; n = 6) ................................. 60

Figure 2.2: Vulnerability to cavitation curves measured on nine coastal sage scrub
species (a—i; see Table 2.1 for full species names) during the wet season (February-May
2006; closed circles, mean :I: 1 SE; n = 6-12) and for four species measured during the dry
season (August-December 2006; open circles, mean :t 1 SE; n = 6) ......................... 61

Figure 2.3: Vulnerability to cavitation curves measured on nine Mojave Desert scrub
species (a—i; see Table 2.1 for full species names) during the wet season (February-May
2006; closed circles, mean :t 1 SE; n = 6—12) and for ﬁve species measured during the dry
season (August-December 2006; open circles, mean :1: 1 SE; n = 6) ......................... 62

Figure 2.4: Water potential at 50% loss in hydraulic conductivity (W50) for 27 species
from three arid plant communities ................................................................ 63

Figure 2.5: Xylem speciﬁc conductivity (Ks) for 27 species from three different arid
plant communities: Chaparral (a), coastal sage scrub (b) and Mojave scrub (c), as

xi

determined during the wet season (black and grey bars, mean t 1 SE; n = 6-12) and dry
season (open bars, mean :l: 1 SE, n = 6) .......................................................... 64

Figure 2.6: Mean water potential at 50% loss in hydraulic conductivity (W50) (a) and T75
(b) for 13 species from three arid plant communities (black and grey bars :1: 1 SE). .......65

Figure 3.1: Monthly mean, minimum, and maximum temperature and precipitation for
three sites located in southern California for February 2006 through April 2007 .......... 93

Figure 3.2: Water potential and stomatal conductance (gs) measured approximately
monthly on species from three arid plant communities in southern California ............. 94

Figure 3.3: Maximum and minimum water potential (‘I’Wmax and ‘Pwmin, respectively)
measured from February 2006 through April 2007 on 28 shrub species from three plant
communities in southern California: Chaparral, coastal sage scrub (CSS), and Mojave
Desert scrub .......................................................................................... 95

Figure 3.4: Maximum and minimum stomatal conductance (gsmax and gsmin, respectively)
measured from April 2006 through April 2007 on 27 shrub species from three plant
communities in southern California: Chaparral, coastal sage scrub (CSS), and Mojave
Desert scrub .......................................................................................... 96

Figure 3.5: Water potential as a predictor of stomatal conductance (gs) for 28 species
from three arid plant communities of southern California: Chaparral (A and D), coastal
sage (B and E), and Mojave Desert scrub (C and F) ........................................... 97

Figure 3.6: Xylem density as a predictor of ‘1’me and ‘I’wmin pooled across communities
(P < 0.001, r2 = 0.52 for Wm... and P = 0.012, r2 = 0.21 for ‘11....) .......................... 98

Figure 3.7: Minimum seasonal water potential (Twin) as a predictor of resistance to
water stress induced cavitation (W50) pooled across communities ........................... 99

Figure 3.8: Results of a principle component analysis using multiple traits measured on
species occurring in three shrub communities of the winter rainfall area of southern
California ........................................................................................... 100

Figure 4.1: Phylogeny of species included in the present study including the plant
community in which they occur (Chaparral, coastal sage, or Mojave Desert scrub). . . 120

Figure 4.2: Histogram representing the phylogenetic distance of randomly generated
communities drawn from a pool of the species analyzed in the present study (grey bars
and solid line, n = 1000) .......................................................................... 121

Figure 4.3: Phylogenetic distance as a predictor of the percent co-occurrence among
species for neighbors (ﬁlled circles and solid line) and nearest neighbors (open circles

xii

and dashed line) for three communities, Chaparral (A and D), coastal sage (B and E), and
Mojave Desert scrub (C and F) .................................................................. 122

Figure 4.4: The relationship between various functional parameters and species co-
occurrence as either neighbors (ﬁlled circles) or nearest neighbors (open circles) in the
coastal sage (A and B) or Mojave Desert scrub (C, D, and E) communities ............... 123

Figure 5.1: Solid curves show the dependence of population growth rate on resource
availability (A; based on Tilman 1982) and the dependence of species communities on
resource availability (B) if a single resource is limiting ...................................... 133

Figure 5.2: Volumetric soil moisture content of the upper soil layers (upper 30 cm)
measured from late August 2006 through April 2007 at each of the three arid shrub
communities (Chaparral, coastal sage, Mojave Desert) ....................................... 134

Figure 5.3: The frequency of water potential occurrence in three arid plant communities,
the Chaparral (medium gray ﬁll, solid line), coastal sage scrub (black ﬁll and dashed line)
and Mojave Desert scrub (light grey ﬁll, dashed-dotted line) (A and B) and the minimum
seasonal volumetric soil water content for these same three communities (C) ............ 135

Figure 6.1: Phylogeny of 17 species of evergreen shrubs sampled from Jonaskop, in the
south-westem Cape of South Africa ............................................................ 161

Figure 6.2: Xylem speciﬁc hydraulic conductivity (K5) (3), mean hydraulic vessel
diameter (dh) (b), percentage vessel area per transverse xylem area (c), and percentage
ﬁber wall area per transverse xylem area (d) of females (black bars :t 1 SE; n = 6) and
males (grey bars :1: 1 SE; n = 6) of two dioecious species, Leucadendron laureolum and L.
salignum ............................................................................................. 162

Figure 6.3: Minimum seasonal pressure potentials (Pmin) measured in 2004 on 17
evergreen shrub species (:1: 1 SE; n = 5-12) .................................................... 163

Figure 6.4: Xylem density (a), mechanical strength against breakage (modulus of
rupture, MOR) (b) and the ratio of vessel wall thickness to lumen diameter squared, an
estimate of vessel implosion resistance ((t/b)h2) (c), as functions of minimum seasonal
pressure potential (ijn) ........................................................................... 164

Figure 6.5: Mechanical strength against breakage (modulus of rupture, MOR) (a),
percentage ﬁbre wall area per transverse xylem area (b and d), and the ratio of vessel wall
thickness to lumen diameter squared, an estimate of vessel implosion resistance ((t/b)h2)
(c and e) as functions of xylem density or MOR .............................................. 165

Figure 6.6: Xylem speciﬁc conductivity (Ks) as a function of hydraulic vessel diameter
(dh) ................................................................................................... 166

xiii

Figure 6.7: Relationship among xylem traits along two axes as determined by principle
component analyses on raw data (a) and phylogenetic independent contrasts (b) ........ 167

Figure 6.8: Light micrographs of xylem transverse sections illustrating differences in the
ratio of the double cell wall between two vessels to the vessel lumen diameter
((t/b)h2) .............................................................................................. 168

Figure 7.1: Vulnerability to cavitation curves for 15 evergreen shrub species from South
Africa depicting the percentage loss in hydraulic conductivity for a given decrease in
water potential generated using a customized rotor and centrifuge (see Methods for
details) ............................................................................................... 189

Figure 7.2: Cavitation resistance (W50) of 15 evergreen shrub species from South Africa,
estimated from fatigue-corrected vulnerability to cavitation curves (see Methods for
details) ............................................................................................... 190

Figure 7.3: Xylem ﬁber and vessel anatomical traits as predictors of cavitation resistance
(9’50) among 15 evergreen shrub species from South Africa ................................. 191

Figure 7.4: Light micrographs of xylem longitudinal sections demonstrating some of the
xylem vessel anatomical differences among species .......................................... 192

Figure 7.5: Cavitation resistance (T50) plotted against minimum seasonal water potential
(Twin) for 15 species of evergreen shrubs from South Africa ............................... 193

Figure 7.6: Relationships among species from South Africa to those from climatically

similar plant communities in California, USA as determined by principle components
analysis .............................................................................................. 194

xiv

dh
85
85min

gsmax

MOE
MOR
PIC

PLC

\Pmin 01' \Pwmin

\Pwmax

KEY TO SYMBOLS OR ABBREVIATIONS

vessel diameter

mean hydraulic vessel diameter

stomatal conductance

minimum seasonal stomatal conductance

maximum seasonal stomatal conductance

hydraulic conductivity

maximum hydraulic conductivity

leaf speciﬁc hydraulic conductivity

xylem speciﬁc hydraulic conductivity

Modulus of Elasticity

Modulus of Rupture

phylogenetic independent contrast

percentage loss in hydraulic conductivity

xylem pressure potential

minimum seasonal xylem pressure potential

xylem pressure potential at 50% loss in hydraulic conductivity
xylem pressure potential at 75% loss in hydraulic conductivity
xylem water potential

water potential

minimum seasonal water potential

maximum seasonal water potential

XV

‘Pso

R*
SLA

(t/b)h2

water potential at 50% loss in hydraulic conductivity

water potential at 75 % loss in hydraulic conductivity

level of a limiting resource at which there is no population growth
speciﬁc leaf area

theoretical vessel implosion resistance where t is the thickness of

the double vessel wall between two vessels and b is the lumen
breadth of a vessel near the hydraulic mean vessel diameter (h).

xvi

INTRODUCTION

Woody plant species differ in their ability to transport water and in their ability to resist
failure of their hydraulic transport system during periods of water stress. Concomitantly,
species also differ in the level of water stress that they experience, even among plants
growing together at a common microsite. Arid woody plants, particularly evergreen
species, experience extremely negative xylem pressures yet must also be able to maintain
their water transport pathway to supply leaves. Thus, arid evergreen shrub species likely
exhibit unique xylem adaptations in order to cope with the extreme negative pressures
that can develop within their xylem during periods of limited soil moisture and high
evaporative demand.

The present dissertation examines, at the cellular and tissue level, what xylem
traits are associated with xylem pressures experienced by arid woody plants and their
ability to maintain a functioning water transport system in the face of severe water stress.
At the organismal and community levels, seasonal water relations of shrub species are
compared. The relationship between plant water stress tolerance, functional traits, and
the phylogenic relations among and distribution of species within and between
communities is examined. Finally, water stress tolerance strategies among woody shrub
species from two comparable regions global are examined as a test of how climate and
plant morphological convergence may relate to how arid woody shrub species respond to

water SII'CSS.

Plant water transport
Water is transported in plants under negative pressure via the soil-plant-atmosphere
continuum (Cowan 1965). Water is “pulled” from the soil, through the plant, and out of
leaves by the evaporative pull of the atmosphere. Water molecules are connected by
cohesive forces among water molecules and adhesive forces to cell walls, allowing a
column of water molecules to persist under considerable tension (1'. e. the cohesion-
tension theory of xylem sap ascent; Tyree & Zimmermann 2002).

The theoretical tensile strength of water quite is great (—130 to -150 MPa; Apfel
1972 cited in Tyree & Zimmermann 2002) and water columns have been measured
withstanding pressures of -28 MPa (Briggs 1950), yet water columns within tracheary
elements are subject to failure at much higher (less negative) pressures. Riparian plants
may experience failure of all of the water conduits within stem xylem at relatively high
pressures (> -1.0 MPa), while water columns within the xylem conduits of xeric
angiosperrns and many gymnosperms may remain intact at considerably lower pressures
(< -12 MPa) (e. g. Pockman & Sperry 2000). These differences are likely due to size and
structure of tracheary elements and inter-conduit pits and pit membranes (Sperry & Tyree
1988; Sperry et al. 1991; Sperry & Hacke 2004; Hacke et al. 2004). Differences may
also be related to the mechanical strength of xylem vessels and their surrounding tissues,
which may be susceptible to implosion under extreme negative pressures (Hacke et al.
2001a). Additionally, wall differences, damage to cell walls, or degradation or damage
to vessel pits can affect the ability of the water column in a conduit to resist tension

(Sperry et al. 1991; Hacke et al. 2001a; Tyree & Zimmermann 2002) as can changes in

the concentration of solutes in the xylem which may lower the energy required to break

the hydrogen bonds between water molecules (Sperry & Tyree 1988).

Hydraulic failure

Water stress induced cavitation of the xylem occurs when the cohesive bonds
between water molecules fail. Because water columns are under negative pressure in the
xylem, breakage of these intermolecular bonds results in rapid expansion of the gap in the
water column and the ﬁlling of the created void in the water column with gas from
adjacent gas ﬁlled cells or intercellular spaces and water vapor, in a process termed air-
seeding (Sperry & Tyree 1988; Tyree & Zimmermann 2002). The resulting blockage of
the xylem conduit by a gas bubble is a xylem embolism. Because cavitation events are
rapidly followed by embolism formation, these terms are often used interchangeably.

Water stress induced failure of water transport in conduits may also occur due to
mechanical implosion or inward bending of vessel or tracheid walls. Xylem conduits
have been shown to collapse inward as xylem tensions increase (1'. e. become more
negative) (Cochard et al. 2004; Brodribb & Holbrook 2005). Resistance of xylem to
failure has been shown to correlate to the mechanical strength of conduits against
implosion which is estimated by the square of the thickness of the double vessel wall
between two conduits (t) divided by the vessel lumen diameter (b) ((t/b)h2; Hacke et al.
2001a).

Cavitation and subsequent embolism can also be caused by freezing and thawing
of the xylem sap, although the mechanism of embolism formation differs from that of

water stress induced cavitation. Freezing-induced embolism is dependent on conduit

volume (Ewers 1985; Davis et al. 1999b; Pitterrnann & Sperry 2003). When xylem sap
freezes, gas that was dissolved in the xylem sap comes out of solution and forms bubbles.
The larger the conduit, the larger are the bubbles which form in the xylem sap and larger
bubbles take longer to dissolve back into solution upon thawing of the xylem sap
increasing the likelihood that xylem tensions will pull on these bubbles causing them to
expand. Xylem conduits with diameters greater that 43 to 44 um appear to be
particularly susceptible to freezing induced cavitation (Davis et al. 1999b; Pitterrnann &
Sperry 2003).

Xylem embolism repair has been shown to occur in some species. Positive
pressure of the xylem may occur through loading of solutes into the xylem when
transpiration is limited. This may dissolve embolisms in the xylem, although positive
root pressures are usually not great enough to dissolve embolisms in relatively tall woody
plants, with few notable exceptions (Sperry et al. 1987; Fisher et al. 1997; Williams et al.
1997). Xylem embolism repair has also been shown to occur under negative pressures,
but these pressures are generally very near to zero (Salleo et al. 1996; 2004; however see,
Melcher et al. 2001). Thus, for most woody angiosperrns, especially those in semi-arid
or arid regions, repair of xylem embolism is unlikely and plants must either avoid high
levels of embolism or be able to rapidly grow new xylem when water is available.

Woody plants vary greatly in their cavitation resistance (Maherali et al. 2004).
The ability of woody plants to avoid cavitation can be estimated using a vulnerability to
cavitation curve. Woody stems or roots can be dried down to known tensions (i. e. xylem
pressure potentials or xylem water potentials) and the amount of embolism can be

estimated by determining the loss in conductivity of the xylem. Negative xylem

pressures can be generated using air-desiccation of shoots (Sperry et al. 1988) or by
spinning stem or root segments in a centrifuge (Alder et al. 1997). Pressures in the xylem

can also be generated using air-injection (Sperry & Saliendra 1994).

Xylem cellular and mechanical traits

Chapter 1 is a study of anatomical and biomechanical traits related to water stress
tolerance in six Chaparral species. This chapter investigates the possible mechanical and
hydraulic costs to increased cavitation resistance. Not all plants in arid environments
display high resistance to cavitation and woody angiosperms are seldom able to resist
cavitation at pressures that are more negative than they regularly experience in the ﬁeld

suggesting that increased cavitation resistance may come at a cost.

Seasonal water relations

In Chapters 2 and 3 the seasonal water relations of shrub species in three different arid
shrub communities, Chaparral, coastal sage, and Mojave Desert scrub, are examined.
Shrub species in these communities experience similar levels of water stress seasonally,
yet differ in their resistance to cavitation. What are the xylem and leaf traits associated
with different water stress tolerating strategies among species from these communities?
Chapter 2 is a study of seasonal differences in cavitation resistance and seasonal
hydraulics. In Chapter 3, seasonal measures of water status and stomatal conductance are
compared across communities. This expands on the prior chapters, which have focused

on xylem function and structure, to include other plant traits correlated with water stress

tolerance, including speciﬁc leaf area (leaf area per leaf dry weight), stomatal response to

water stress, and vegetative phenology (leaf longevity and abscission).

Community structure

In Chapters 4 and 5, plant structural and functional traits relating to water stress tolerance
are used to predict species distributions within and between communities. In Chapter 4,
the relationship between species traits and the phylogenetic relatedness of species are
examined. The phylogenetic relationships among species have the potential to inﬂuence
community assemblages and community structure. Additionally, plant functional traits
may be associated with patterns of co-occurrence at local and regional scales. In Chapter
5, plant water status and soil moisture are used to predict community water use. This is

then used to predict comparative invasibility among communities.

Convergence among Mediterranean-type climate regions.

In the last two chapters of this dissertation (Chapters 6 and 7), xylem tension, cavitation
resistance, and xylem functional and anatomical traits are examined among several shrub
species from the Mediterranean-type climate region of South Africa. This region is
climatically similar to southern California, receiving primarily winter rain and
experiencing along, dry summer. In Chapter 6 (Jacobsen et al. 2007a), the negative
tensions experience by 17 shrub species and the xylem anatomical and functional traits
that are associated with experiencing more negative xylem tensions seasonally are
examined. In Chapter 7, cavitation resistance of 15 South African shrub species is

measured. These data are then analyzed in tandem with data from Chapters 2, 3, and 6 to

examine how the water stress tolerating strategies of woody shrubs from South Africa
and California compare. Are all woody arid shrubs utilizing a common water stress
tolerating strategy or are there many different solutions to the mutual problem of seasonal

water stress among aridland woody shrub species?

CHAPTER ONE

Jacobsen, A.L., Ewers, F.W., Pratt, R.B., Paddock, W.A., HI & Davis, SD. (2005) Do
xylem ﬁbers affect vessel cavitation resistance? Plant Physiology, 139, 546-556.

DO XYLEM FIBERS AFFECT VESSEL CAVITATION RESISTANCE?

Abstract

Possible mechanical and hydraulic costs to increased cavitation resistance were examined
among six co-occurring species of Chaparral shrubs in southern California. We measured
cavitation resistance (xylem pressure at 50% loss of hydraulic conductivity; P50), seasonal
low pressure potential (Pm), xylem conductive efﬁciency (speciﬁc conductivity; ks),
mechanical strength of stems (modulus of elasticity and modulus of rupture; MOE and
MOR, respectively), and xylem density. At the cellular level, we measured vessel and
ﬁber wall thickness and lumen diameter, transverse ﬁber wall and total lumen area, and
estimated vessel implosion resistance using (t/b)h2 where “t” is the thickness of adjoining
vessel walls and “b” is the vessel lumen diameter. Increased cavitation resistance was
correlated with increased mechanical strength (r2 = 0.74 and 0.76 for MOE and MOR,
respectively), xylem density (r2 = 0.88), and Pm," (r2 = 0.96). In contrast, cavitation
resistance and Pmin were not correlated with decreased ks suggesting no tradeoff between
these traits. At the cellular level, increased cavitation resistance was correlated with
increased (t/b)h2 (r2 = 0.95), increased transverse ﬁber wall area (r2 = 0.89), and decreased
ﬁber lumen area (r2 = 0.76). The correlation between cavitation resistance and ﬁber wall
area has not been previously shown and suggests a mechanical role for ﬁbers in
cavitation resistance. Fiber efﬁcacy in prevention of vessel implosion, deﬁned as inward

bending or collapse of vessels, is discussed.

Introduction
Among vascular plants water is transported through xylem under negative pressure.
Xylem must withstand both the mechanical stresses associated with negative pressure as
well as the risk of air entering the hydraulic pathway. Failure to do so may lead to
cavitation of water columns and blockage of water transport. Failure may occur when
gas is pulled into water-ﬁlled xylem conduits from gas-ﬁlled cells or intercellular spaces
through pores in the xylem pit membrane in a process referred to as air-seeding
(Zimmermann 1983; Sperry & Tyree 1988; Baas et al. 2004). Failure may also occur
when negative pressures overcome the ability of the xylem conduit walls to resist
implosion (i.e. inward bending or collapse) (Carlquist 1975; Hacke et al. 2001a;
Donaldson 2002; Cochard et al. 2004; Brodribb & Holbrook 2005). Implosion may
trigger cavitation or, in leaves, may restrict hydraulic transport by reducing conduit
diameter (Brodribb & Holbrook 2005). In addition to negative pressures, freezing can
lead to failure when sap in the xylem freezes and the gas dissolved in the sap comes out
of solution. This can lead to cavitation upon thawing if the bubbles do not go back into
solution but instead expand (Yang & Tyree 1992). The result of cavitation is embolism
or gas-blockage which reduces hydraulic transport and can result in reduced stomatal
conductance (Pratt et al. 2005), reduced photosynthesis (Brodribb & Feild 2000), and
dieback of branchlets (Rood et al. 2000; Davis et al. 2002).

Natural selection favors increased cavitation resistance among woody evergreen
plants occurring in drought-prone environments; however, not all plants adapted to arid
environments have high cavitation resistance (Pockman & Sperry 2000; Maherali et al.

2004). One explanation for this is that increased cavitation resistance may come at the

10

cost of decreased xylem conductive efﬁciency, preventing plants from developing high
levels of cavitation resistance. Additionally, a plant may have to develop thicker xylem
walls and/or smaller conduit diameters to strengthen the resistance of a conduit to
implosion under negative pressure (Hacke et al. 2001a). Such changes may increase
xylem construction costs or decrease conductive efﬁciency.

Selection to resist freezing-induced cavitation is also linked to decreased xylem
conductive efﬁciency. To resist freezing-induced cavitation a plant must have narrow
vessel or tracheid diameters as resistance to freezing-induced cavitation is directly related
to conduit diameter (Langan et al. 1997; Davis et al. 1999; Pittermann & Sperry 2003;
Pratt et al. 2005). Narrowing of conduits to resist freezing-induced cavitation would
lead to a decrease in hydraulic conductivity. Therefore, attempts to examine the
relationship between resistance to water-stress induced cavitation and hydraulic
efﬁciency may be confounded by selection to resist freezing-induced cavitation in
environments that experience freezing temperatures.

In the present study, we examine the cost of increased cavitation resistance at a
non-freezing site using a combined physiological and anatomical approach. We tested
for several tradeoffs to increased cavitation resistance, including decreased conductive
efﬁciency and increased xylem construction cost. Additionally, we expanded these
traditional tradeoffs to include examination of a possible role for ﬁbers in cavitation
resistance. We sampled six species, examining cavitation resistance (xylem pressure at
50% loss of hydraulic conductivity; P50), minimum seasonal pressure potential (Pm),
xylem biomechanics (modulus of elasticity and modulus of rupture; MOE and MOR,

respectively), xylem density, vessel and ﬁber anatomy, and xylem conductive efﬁciency

11

(speciﬁc conductivity; ks). These species correspond to three species pairs of Chaparral
shrubs from three angiosperm families all growing at the same coastal site where freezing
temperatures and, presumably, freezing-induced cavitation do not occur. Using the
species at this site allowed us to examine possible costs to water stress induced cavitation
relatively independent of environmental differences including any limitations on vessel
diameter resulting from selection to resist freezing-induced cavitation.

We hypothesized that increased mechanical strength (MOE and MOR) as well as
xylem density would be correlated with increased cavitation resistance. We further
hypothesized that the mechanical strength of stems would decrease with increasing water
stress, since tension in the water column should exacerbate external mechanical stresses
(Sperry & Hacke 2004). We hypothesized that increased cavitation resistance would
come at the cost of decreased hydraulic efﬁciency. At the cellular level, we hypothesized
that cavitation resistance would come at the cost of decreased vessel lumen diameter and
increased thickness of xylem cell walls. Changes in either or both of these cellular
dimensions would result in a greater thickness-to-diameter ratio ((t/b)h2) and would result
in increased strength of cells against implosion under negative pressure (Hacke et al.

2001a).

Results

Mechanical properties of stems

Adenostoma fasciculatum, A. sparsifolium, and Ceanothus megacarpus showed great
resistance to bending (high load required for displacement) followed by very sharp drop-

offs, indicating sudden complete failure of stems (Figure 1.1 A and B). In contrast

12

Malosma laurina and Rhus ovata required less force for displacement and the resistance
to displacement soon ﬂattened out such that there was an extended period before
complete failure; thus both partial and complete failure of stems occurred at very low
load levels (Figure 1.1 C). Ceanothus spinosus had intermediate results compared to the
other species (Figure 1.1 B).

The MOE and MOR were not different between our wet and dry treatments with
two exceptions: the dry treatment did result in signiﬁcantly greater MOR values in C.
megacarpus and in signiﬁcantly greater MOE in C. spinosus (Table 1.1). Stems of C.
spinosus were dried down below the Pmin measured in the ﬁeld (-10.1 MPa compared to a
Pm of -5.3 MPa); however, this value is not different from the Pmin measured in previous
years on this species (Pm,n < -9 MPa in 2002, data not shown) and is therefore still within
the physiological range of this species. Modulus of rupture was positively correlated to
MOE, both for the wet (r2 = 0.79) and dry treatments (r2 = 0.87; Figure 1.2). Linear
regressions of MOE and MOR did not differ for wet and dry treatments in slope (p =
0.72) or intercept (p = 0.84; Figure 1.2); therefore, we used averaged results from the wet

and dry treatments in our comparisons with other xylem parameters.

Cavitation resistance

The vulnerability curves are simpliﬁed down to one value, P50, shown for each species in
Table 1.1. The stems of A. fasciculatum (Figure 1.3 A) and C. megacarpus (Figure 1.3
B) were the most resistant to water stress induced cavitation, followed by C. spinosus and
A. sparsifolium. The species most vulnerable to cavitation were M. laurina and R. ovata

(Figure 1.3 C). Malosma laurina and R. ovata both displayed high levels of embolism at

13

relatively high pressures (29 and 28% loss of hydraulic conductivity (PLC) at 2-05 MPa)
compared to the remaining four species (3.2 i 1.6 PLC at 205 MPa). This indicates that
cavitation fatigue (sensu Hacke et al. 2001b) may have been present in M. laurina and R.

ovata.

Stem traits
Stems that were more resistant to cavitation had stiffer (greater MOE) and stronger
(greater MOR) stem tissue and experienced lower seasonal pressure potentials. Greater
cavitation resistance was correlated to increased MOE (r2 = 0.74; not shown), MOR (r2 =
0.76; Figure 1.4 A), and xylem density (r2 = 0.88; Figure 1.4 B). Resistance to cavitation
(P50) was positively correlated with Pm," (r2 = 0.96; Figure 1.4 C). Similarly, MOR was
positively correlated with xylem density (r2 = 0.95; Figure 1.4 D) and negatively
correlated with Pm," (r2 = 0.60; Figure 1.4 E).

In contrast, xylem conductive efﬁciency (ks) was not related to cavitation
resistance or to measures of stem mechanical strength. Xylem conductive efﬁciency
varied independently of P50 (p = 0.15), Pmin (p = 0.19), MOE (p = 0.20), MOR (p = 0.15),

and xylem density (p = 0.11; not shown).

Cellular traits

Percent transverse ﬁber wall area per total transverse xylem area ranged from 41.0% in
M. laurina to 60.7% in C. megacarpus, with an across species mean of 53.3 i 3.1%.
Percent transverse vessel wall area per transverse xylem area occupied considerably less

area and ranged from 3.5 to 5.5%, with an across species mean of 4.5 :l: 0.3%.

14

At the cellular level, increased cavitation resistance and stem mechanical strength
were associated with increased thickness of ﬁber cell walls. Resistance to cavitation (P50)
and MOR were correlated with increased strength against implosion of xylem vessel
walls ((t/b)h2; r2 = 0.95 and 0.85, respectively; Figure 1.5 A and D), increased percent
transverse ﬁber wall area (r2 = 0.89 and 0.71, respectively; Figure 1.5 B and E),
decreased ﬁber lumen diameter (r2 = 0.84 and 0.79, respectively; Figure 1.5 C and F), and
decreased percent transverse lumen area (r2 = 0.76 and 0.86, respectively; not shown).
Modulus of rupture was also correlated with an increase in ﬁber wall thickness (r2 = 0.86;
not shown).

Increased vessel wall thickness was not correlated with increased cavitation
resistance and mechanical strength. Vessel wall thickness was not correlated to P50 (p =
0.56), Pm,“ (p = 0.80), MOE (p = 0.37), MOR (0.37), or xylem density (p = 0.40). Vessel
wall thickness also was not correlated with ﬁber wall thickness (p = 0.15). Hydraulic
vessel lumen diameter was correlated with xylem density (r2 = 0.67), but was not
correlated with cavitation resistance (p = 0.07; not shown).

Xylem conductive efﬁciency (ks) was correlated with increased hydraulic vessel
lumen diameter (r2 = 0.75; not shown) and decreased ﬁber wall area (r2 = 0.75 ; not
shown). Xylem conductive efﬁciency was not correlated with total lumen area (p = 0.06;

not shown).

DISCUSSION
Water stress induced cavitation in woody plants occurs when air is seeded into a

functional conduit from an adjacent gas-ﬁlled cell or intercellular space (Jarbeau et al.

15

1995; Sperry et al. 1996; Tyree & Zimmermann 2002). Conduits may also cavitate
following collapse under negative pressure. Conduit collapse may be reversible,
depending on conduit structure and biomechanics (Cochard et al. 2004; Brodribb &
Holbrook 2005). Although some have questioned the existence of these extreme
negative pressures in the water transport system of woody plants (Zimmermann et al.
2004), the existence of tensions in the xylem is widely supported (see Angeles et al.
2004) and, presumably, plants have adapted to tolerate such stresses.

Hacke et al. (2001a) suggested that to resist collapse of conduits, plants that
exhibit a high degree of cavitation resistance and that experience greater negative
pressures display thicker vessel walls relative to their lumen diameter (i.e. higher (t/b)h2)
and that such plants also have denser xylem. The link between vessel (t/b)h2 and xylem
density is apparently due to correlated changes in vessel and ﬁber lumen to wall ratios
(Hacke et al. 2001a; Sperry & Hacke 2004). Although data are lacking on the correlated
nature of vessel and ﬁber lumen to wall ratios, its seems that the link between vessel
(t/b)h2 and xylem density is dependent on this correlation since the density of xylem in
angiosperrns is primarily affected by the abundance and properties of ﬁbers and only
minimally affected by changes in vessel (t/b)h2. Our data supports the suggestion by
Hacke et al. (2001a) that ﬁber and vessel properties are indeed correlated. Additionally,
our results point to a possible role for ﬁbers in increased vessel implosion resistance, an
idea that was hypothesized, but not previously tested (Hacke et al. 2001a). Previous
studies have not analyzed ﬁber anatomical properties independently and have relied on

assumptions of ﬁber anatomical measures and mechanical properties. Here, we examine

16

the role of changes in vessel and ﬁber anatomy and mechanical strength on cavitation
resistance.

Vessel implosion resistance can be increased by a decrease in vessel lumen
diameter, an increase in wall thickness, or both; however, the species included in this
study did not appear to utilize all of these anatomical options. The variation in (t/b)h2
among species was largely due to changes in vessel lumen diameter and not to changes in
vessel wall thickness. The range of vessel wall thicknesses among our sampled species
was narrow (2.3 to 3.8 pm) and was not correlated with cavitation resistance (P50) or
minimum seasonal pressure potential (Pmin). One interpretation would be that the
sampled species were limited in their ability to alter their vessel wall thickness, limiting
changes in vessel mechanics to changes in the lumen diameter. However, this would
suggest that increased (t/b)h2 would correlate with decreased conduit efﬁciency, a tradeoff
that was not observed. A second interpretation would be that other surrounding tissues,
such as ﬁbers, may act to strengthen vessel walls, somehow increasing resistance to
cavitation without a necessary change in either vessel wall thickness or lumen diameter.
Our data supports this second interpretation and suggests that viewing vessels as isolated
pipes (i.e. (t/b)h2) may not fully describe their ability to resist mechanical stresses
imposed by negative pressures. Indeed, strong correlations between ﬁber characters,
cavitation resistance, and xylem density suggest ﬁbers may be involved in cavitation
resistance of woody plants. In the present study, ﬁber wall area was, on average, 53.3%
of the total transverse xylem area, compared to less than 5% vessel wall area per

transverse xylem area. Since more than ten times the biomass goes into ﬁber walls than

17

vessel walls, the cost of ﬁber support for mechanical safety may be considerable in plants
that experience very low xylem pressure potentials.

Direct evidence for ﬁbers in preventing vessel collapse in stems is lacking;
however, recent studies in leaves have demonstrated the importance of supportive tissue
in the prevention of collapse. Under severe water stress, tracheids in conifer needles
collapse preferentially when xylem conduits are adjacent non-strengthening parenchyma
(Cochard et al. 2004), suggesting that the cells adjacent to a xylem conduit are important
in preventing conduit collapse under negative pressure. The importance of the strength of
the surrounding tissue is further supported by the ﬁnding that conifer stem tracheids,
which are surrounded by a mechanically supportive tracheid matrix, did not exhibit
collapse (Cochard et al. 2004). Brodribb and Holbrook (2005) similarly found that
tracheids occurring outside leaf midveins exhibited collapse whereas tracheids within the
more supported midveins did not display evidence of collapse. Vessel implosion has also
been observed in stems of genetically modiﬁed angiosperms with weakened cell walls
(Turner & Somerville 1997; Franke et al. 2002) demonstrating that mechanical strength
of supportive tissue may be important in preventing implosion. The idea that the
mechanical strength of stems is related to vessel implosion resistance contrasts with the
idea that stem mechanical strength is mainly the result of selection for resistance to stem
breakage due to wind or fruit-load (Wagner et al. 1998).

It has been hypothesized that stronger stems may be needed to resist whole stem
bending which would exacerbate the internal stresses that occur during severe water
stress (Sperry 2003; Sperry & Hacke 2004); however, our data do not support this. We

found that stem mechanical strength did not vary between hydrated stems and stems dried

l8

down to their seasonal low pressure potential. Although C. megacarpus had greater
MOR and C. spinosus had greater MOE in the dry treatment compared to the wet
treatment, for ﬁve out of six species there was no difference in MOE or MOR with the
treatments. This ﬁnding suggests that negative internal stresses within the stem do not
affect whole stem bending strength. A caveat of these ﬁndings is that we do not know
the xylem pressures while stems were being bent. Bending of vessels may have reduced
vessel volume thereby reducing the negative pressures within the xylem. Regardless, the
experiment did recreate the stresses that would occur with bending in intact hydrated and
water-stressed stems in the ﬁeld. A further criticism would be that we do not have
evidence as to whether the ﬁbers were embolized during the wet or dry treatments and,
therefore, did not fully test the mechanism suggested by Sperry and Hacke (2004) of
exacerbated bending stress with water stress. Thus, while we found no evidence that
pressures are intensiﬁed in stems experiencing both water and bending stresses, this
mechanism has not yet been fully tested.

It has also been hypothesized that stiffer and denser stems, which may be more
resistant to vessel implosion, would be a mechanical liability because they are less
ﬂexible and more likely to break (Hacke et al. 2001a). Our data do not support this
suggestion. For the species in this study, stems that were stiffer (i.e. less ﬂexible; high
MOE) and denser displayed the greatest strength (i.e. resistance to breakage; high MOR).
This relationship did not vary with stem water stress suggesting that even under extreme
water stress the stiffest stems remain the strongest and least likely to break.

Stem mechanical properties and cavitation resistance were unrelated to xylem

conductive efﬁciency in the present study. This is consistent with previous studies that

19

have surveyed many angiosperm families and found that there is only a weak tradeoff
between hydraulic conductivity and cavitation resistance at best (Tyree et al. 1994;
Maherali et al. 2004) and weak evidence for a tradeoff between conductivity and
mechanical strength (Wagner et al. 1998). Tradeoffs may be present in the case of
freezing-induced embolism where vessel diameter is directly related to susceptibility to
cavitation (Cochard & Tyree 1990; Langan et al. 1997; Davis et al. 1999). The lack of a
tradeoff between stem biomechanical traits and conductivity is perhaps because stem
mechanics are largely dependent on ﬁber properties while conductivity is controlled by
vessel properties. Xylem can be constructed in many different ways such that it can have
a relatively high mechanical strength and simultaneously have high transport efﬁciency
(W oodrum et al. 2003; Kern et al. 2005). In addition, certain factors impact mechanical
properties of xylem but are independent of the number and diameter of vessels, including
the amount of lignin in the ﬁbers and the cellulose microﬁbril angle (Panshin & deZeeuw
1980; Niklas 1992).

Reinforcement of xylem tissue may represent a signiﬁcant cost limiting increased
cavitation resistance. Modulus of elasticity, MOR, and xylem density showed strong
correlations with P50, suggesting that stems that are mechanically stronger and denser are
apparently able to withstand more negative pressures. This suggests that the ﬁber matrix
may be important in increased resistance to cavitation. Partial implosion of vessel walls
under negative pressure could lead to increased likelihood of air-seeding due to stretching
or rupture of pit membranes (Zimmermann 1983; Sperry & Tyree 1988) or micro-
fractures in other parts of the wall that could initiate cavitation (Pickard 1981) (Figure

1.6). The correlation between increased allocation to the ﬁber matrix and P50 support the

20

suggestion by Niklas (1997) and Hacke et al. (2001a) that ﬁbers play a key role in
buttressing vessel walls against implosion under extreme negative pressure.

Pit membrane tears and microfracture of vessel walls may be more common than
previously realized. Permanent implosion of stem tracheary elements has been observed
only in plants with weakened cell walls that were deﬁcient in lignin (Franke et al. 2002;
Donaldson, 2002) or cellulose (Turner & Somerville 1997). The implosion observed by
Cochard et al. (2004) and Brodribb and Holbrook (2005) was temporary and completely
reversible, either with rehydration of the tissue or upon cavitation of the water columns,
either of which would relieve tension on the walls. The reversibility of implosion means
that implosion and resultant tears in the pit membrane or microfracture of the ligniﬁed
cell walls might not be visible with conventional light microscopy and would be difﬁcult
to distinguish from artifacts with electron microscopy. However, some authors consider
“checks” that are often seen in wood to be damage caused by negative pressure (Hunter
2001; Donaldson 2002).

For some species, once a tracheary element cavitates due to water stress it
becomes more susceptible to cavitation following reﬁlling and with subsequent water
stress, i.e. a tracheary element is more susceptible to cavitation after a prior cavitation
event. The phenomenon has been called “cavitation fatigue” (Hacke et al. 2001b). It has
been suggested that cavitation fatigue may be the result of pit membrane damage or
tearing (Hacke et al. 2001b). Consistent with our suggestion that the ﬁber matrix may
play an important role in the prevention of implosion and possible permanent damage or
weakening of vessels, we found evidence for fatigue in two species, M. laurina and R.

ovata. Both of these species have weak stems (low MOR), low transverse ﬁber wall area,

21

and vessels that are predominantly surrounded by ﬁbers. Additionally, the ﬁber walls are
much thinner in these species (1.9 pm for both) compared to their vessel walls (3.8 and
3.4 pm, respectively), meaning that risk of implosion ((t/b)h2) may greatest between a
vessel and its surrounding ﬁbers rather than between two vessels. It is possible that the
support of ﬁbers helps to minimize cavitation fatigue; however, the mechanism for this
remains to be elucidated.

Previous studies have found correlations between wood density and resistance to
cavitation (Hacke et al. 2001a; Baas et al. 2004); however, no previous study has tested
the relationship between stem mechanical strength and cavitation resistance. The
correlations we found between wood anatomical traits and cavitation resistance suggest a
greater role for ﬁbers in imparting conductive safety than previously considered. While it
is thought that resistance to cavitation is primarily a function of pore size in pit
membranes (Jarbeau et al. 1995; Sperry et al. 1996), it may be that the mechanical
properties of xylem ﬁbers, as well as of other cell types associated with vessels including
xylem parenchyma and, in some species, tracheids, are important in determining
resistance to cavitation. Fibers may impact vessel implosion risk by reducing stresses
that exacerbate pit membrane deﬂection or stresses that lead to vessel collapse and

microfracture of the cell wall.

Materials and Methods
Study site
All plant material was collected at a site in the Santa Monica Mountains, 0.5 km south of

Encinal Canyon Road, at an elevation of 480 m (34° 05' 27" N, 1180 50' 29" W). This

22

site, described as "site 3" in Wagner et al. (1998), is a mixed stand of Chaparral with a
coastal exposure. Wildﬁres occurred at the site in 1956 and 1978, meaning that at the
time of the study, in 2003, this was a mature Chaparral stand with above ground shoots up
to 26 years old. Measurements were made on six species of Chaparral shrub, including:
Adenostoma fasciculatum Hook. and Am., A. sparsifolium Torrey, Ceanothus
megacarpus Nutt., C.spinosus Nutt., Malosma laurina (Nutt.) Abrams (formerly Rhus

laurina), and Rhus ovata S. Watson (nomenclature follows Hickman 1993).

Mechanical measurements

Twelve plants per species were marked and used for all measures. For comparison
between stems dehydrated to their seasonal low water potentials and well hydrated stems,
on each plant, two stems were identiﬁed that were very similar in size, appearance,
exposure to the sun, and angle of inclination. The shoots, 1.5 to 2.0 min length, were cut
from the plant, immediately placed into plastic bags, and transported to the laboratory at
Pepperdine University. In the laboratory, one shoot of each pair was re-cut at the base
under water and the base was kept in water overnight with the aerial portions covered
with a plastic bag. For the "wet" treatment twigs or leaves were sampled the next
morning to measure the xylem pressure potential (PX) using a pressure chamber (PMS,
Corvalis, OR, USA) in order to conﬁrm that the stems were rehydrated. The stems were
then re-cut under water to a length of between 0.26 and 0.29 m and kept entirely
submerged for another 24 hours. The "dry" treatment shoot of each pair was allowed to
dehydrate in an air conditioned laboratory until their Px values were close to the lowest

pressures that the plants experience in the ﬁeld. The shoots were then double bagged and

23

allowed to equilibrate overnight. The next morning branchlets or leaves were sampled
for P. and the stems were cut to a length of slightly over 0.3 m. Stems of the wet and dry
treatments were tightly wrapped in plastic and placed in separate bags before being
shipped via overnight express to Michigan State University, where an lnstron Universal
Machine (model 4202, lnstron Corporation, Canton, MA, USA) was used to measure
MOE and MOR.

Stem segments were kept at approximately 10° C until MOE and MOR were
measured. A four-point bending test with a compression load cell of 500 N was
conducted as described by Woodrum et al. (2003). However, the stem segments used
were longer (about 0.275 m) than were used in previous studies, so that most of the
vessels would be intact during the bending experiments on wet versus dry treated stems.
The span length (L), the distance between the two supported ends, was 0.21 m. The load
was applied at two points along the span length with a crosshead speed of 20 mm/min
and stems were stressed until the load reached a maximum value (Fm), determined as
the maximum force obtained in the bending test prior to stem failure (Fig. 1). The
distance between one supported end and the nearest loading point (a in the equations
below) was 0.07 m. The elastic limit was always exceeded with the bending test, thus
stems did not return to their original shape.

Flexural rigidity (EI) was calculated using slope (FN) of the linear (elastic)
portion of the curve (Fig. 1) and the equation E1 = (F/V)(a2/12)(3L-4a) (modiﬁed from
Gere and Timoshenko, 1997). Flexural rigidity was divided by I to determine MOE.

Modulus of rupture (MOR) was estimated from the equation: MOR = (Fmax* a *

Rmajo,)/I, modiﬁed from Ugural ( 1991), where Fmax is the load at stem failure and Rmajor is

24

the radius of the xylem. The second moment of area, I, was calculated as it (Rm-o,4 -
Rminor4)/4, with Rminor as the radius of the pith, based upon I of a hollow cylinder (Niklas
1992).

Adjacent stem segments were used to estimate xylem density (in kg m'3) as the
dry mass per saturated volume of xylem. For this measurement the pith and bark

(including the phloem and vascular cambium) were removed from the xylem.

Hydraulic conductivity and cavitation resistance

Six plants per species were sampled for hydraulic conductivity (kh), speciﬁc conductivity
(kh/sapwood area; k,), and cavitation resistance of their stem xylem. One branch per
plant, approximately 2 min length, was excised, bagged in the ﬁeld and taken to the
laboratory. The branch was re-cut under water to obtain one "distal" stern segment 6 to 8
mm in diameter and 0.10 min length for measurements of kS and xylem anatomical
features. An adjacent "proximal" segment was used for measurement of resistance to
cavitation using the centrifuge technique.

Both the proximal and distal stems were connected to a tubing system and ﬂushed
with water that had been passed through a 0.1 pm ﬁlter and adjusted to a pH 2 with HCl
in order to discourage microbial growth. The stems were ﬂushed at a pressure of 100 kPa
for one hour to remove gas emboli from the xylem vessels. The kh (in m4 MPa'1 5") was
then measured gravimetrically and the high pressure perfusion process repeated until a
maximum value (km) was obtained for each segment (Sperry et al. 1988).

The distal segments were then attached to a tubing system that allowed uptake of

a 0.1% (mass/volume) dye solution of crystal violet under a suction of 5-6 kPa for 25

25

min. The dye solution had been passed through a 0.1 um ﬁlter. The midpoints of the
distal segments were transversely sectioned at a thickness of 40 pm with a sliding
microtome. The active sapwood area, indicated by the dye, was measured with a light
microscope (Nikon microscope, Model Microphot-FX, Japan and Spot RT Color camera,
Diagnostic Instruments, USA) and analyzed using image analysis software (Image v.1.61,
National Institute of Health). The kS value (in m2 MPa’1 5") was then calculated as
kmax/active sapwood area.

The proximal stem segments, following determination of their kmax were spun in a
centrifuge (RCSG Plus, Sorvall, Kendro Laboratory Products, Asheville, NC, USA),
using a modiﬁed rotor to accommodate stem segments. Stems were spun at a prescribed
RPM in order to generate a known negative pressure on the water column in the xylem
vessels (Alder et al. 1997). The proximal segments were 0.271 m long (for use with a
large centrifuge rotor) in the case of C. megacarpus and A. fasciculatum and 0.14 m long
(for use with a smaller rotor) in the case of the other four species. The larger rotor was
needed to create greater centrifugal force for the species that, based upon previous
studies, required greater tensions (measured as lower Px in previous studies) to induce
embolism (Kolb & Davis 1994; Redtfeldt & Davis 1996; Davis et al. 1999).
Vulnerability curves were constructed by plotting decreasing values of xylem pressure
potential versus the percent loss in hydraulic conductivity (PLC). Two species, M.
laurina and R. ovata, demonstrated evidence of cavitation fatigue (Hacke et al. 2001b).
For these species, a correction for fatigue was done by calculating PLC using the kh

measure from a centrifuge spin at 2-05 MPa instead of kmax. For each stem the PLC

26

values were ﬁtted with a polynomial model, which was used to predict the pressure
potential at 50 PLC (P50). The mean P50 value was thus determined for each species.
While this is a relatively arbitrary value, it is one that is widely used and can be

objectively applied to a wide-range of vulnerability curves.

Minimum field pressure potentials

The lowest xylem pressure potentials (Pmm) occurred following the summer drought but
before the ﬁrst rains in autumn (Kolb & Davis 1994; Redtfeldt & Davis 1996; Davis et
al. 1999). On October 13, 2004 we sampled six of the marked plants of each species for
midday xylem pressure potential, measured from branchlets with the pressure chamber
technique (Scholander et al. 1965). Since the ﬁrst rain of the fall season fell on October
17, 2004, ending a greater than 7 month period with no rain, we assumed the October
13th measurements were representative of the lowest pressure potentials that the plants

would experience in 2004.

Xylem anatomical measures

Images were taken of wedge-shaped sectors, using vascular rays as the borders, to sample
for vessel and ﬁber features. Vessel lumen diameter (d in urn), ﬁber lumen diameter,
ﬁber wall thickness, total transverse lumen area (vessel + ﬁber lumen area/sapwood
area), and transverse ﬁber wall area/sapwood area were measured with these images. All
of the vessels and ﬁbers in sectors were measured until a sample size of 200 vessels and
100 ﬁbers was obtained for a stem. The hydraulic vessel diameter (dh) was calculated

from the formula db = (22d5 )/(Xd4 ), based upon all the sampled vessels in a stem. The

27

vessel implosion resistance ((t/b)h2) (Hacke et al. 2001a) was determined for those
vessels, within the sampled 200 vessels per stem, that formed pairs in which one or both
vessels fell within 15 pm of the calculated dh, with "t" as the thickness of adjoining vessel

walls and "b" as the lumen diameter of the vessel.

Data analysis

Modulus of elasticity and MOR of wet and dry treatments were compared within a
species using t-tests. An ANCOVA was used to compare the relationship between MOE
and MOR for wet and dry treatments. Parameters were compared across species using an
AN OVA followed by a Fisher’s LSD post-hoc analysis. Linear regression analysis was
used to examine the correlations between parameters as predicted in our a priori
hypotheses (StatView, SAS Institute Inc., Cary, NC, USA). We used an a of 0.05 to

determine statistical signiﬁcance.

28

Table 1.1. Xylem functional properties for six Chaparral shrub species. Xylem speciﬁc
conductivity (Ks), xylem density, stem modulus of rupture (MOR), modulus of
elasciticity (MOE), xylem pressure potential (PX) of the dry and wet treatments and at
50% loss of hydraulic conductivity (P50), and the 2004 seasonal low xylem pressure
potential (Pm-m) measured in six co—occurring Chaparral species. All values are means 1 1
SE and the sample sizes are given in column “11.” An asterisk indicates signiﬁcant
different (P < 0.05) between fully saturated “wet” stems and “dry” stems dehydrated to
approximate minimum water potentials experienced in the ﬁeld. Letters indicate
signiﬁcant difference between species for a given parameter.

Adenostoma Ceanothus
Species fascicqu A.sparsifolium megacarpus
Family 11 Rosaceae Rosaceae Rhamnaceae

-3 2 -l -1
Ks(10 m MPa s) 6 0.8810.01a 1.6010.l2a 1.5410.12a

Xylem Density (kg m'3) 12 891 1 65.0 a 684 1 26.4 bc 779 1 34.6 b

MOR (N mm'z)
dry 12 23517.5 a 17517.8b 212:8.3C *
wet 12 237111.221 178 15.2b 16418.1 b

-2

MOE (N mm )
dry 12 10794 1 505 ac 7104 i 498 b 8617 :l: 955 be
wet 12 10804 :1: 707 a 7353 :l: 608 be 7722 1 1526 b

Px (MPa)

dry 12 -8.l310.39a* 4.4510.20b* 401010.316 *
wet 3-12 -0.18 :l: 0.06 a -0.14 3: 0.03 a -O.26 1 0.05 ab
P50 6 -8.23 i 0.19 a -5.09 i 0.34 b -9.30 3: 0.66 c
Pm,“ 6 -6.53 :l: 0.15 a -4.06 3: 0.18 b —7.99 1 0.44 c

29

Table 1.1 (cont’d).

C. spinosus Malosma laurina Rhus ovata

Rhamnaceae Anacardiaceae Anacardiaceae
1.8210.29a 6.4611.36b 19510.15 a

659127.40 48916.2d 529121.1d

15215.3d 11414.76 11216.1e
13218.7c 11214.2c 130110.0c

9505 1 369 c * 5392 1 265 d 4661 1 349 d
6689 1 417 c 5450 1 339 c 5349 1 620 C

-10.05 1 0.62 c * -2.53 1 0.96 d * -2.85 1 0.50 d *
-0.16 1 0.02 a -0.43 1 0.09 b -0.43 1 0.10 b

-5.38 1 0.46 b -O.98 1 0.31 d -1.23 1 0.08 d
-5.34 1 0.31 d -2.34 1 0.09 e -2.65 1 0.10 e

30

Load (N)

 

 

 

I I

— Afasciculatum
— — Asparsifolium -

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

A
I I I I
— C. megacarpus
250 .. — — C. spinosis . -
. ........................... F l
200 .. m” -
150 ~- -
1m ‘:OOO 0;»wm‘? 0000000000 F'T‘ax ‘
’ I
/
50.. I i .
l B
1 11 l I
300 I I I I I I
—M. laurina
250 -- —- Fl. ovata - t .
200 -- - r -
150 .. - - -
Fm
ax
1m n.000}0‘ 000:2: ......... Fn‘ax "
50 -- \\ - - -
'« c
o 1 1 1 1 1 1 1
O 20 4O 60 80 O 5 1O 15

Displacement (mm)

31

Displacement (mm)

Figure 1.1. Load versus displacement in four-point bending tests for stems of six species
of Chaparral shrubs. The graphs on the left show the entire test for representative stems,
the graphs on the right are a close-up of the earlier part of the bending tests. The slope of
the initial, linear portion of the function (F/V) is used to calculate ﬂexural stiffness and
modulus of elasticity (MOE), whereas the maximum load (Fm) is used to calculate the
modulus of rupture (MOR).

260 ‘F I I
0 wet; r2 = 0.79
0 dry, r2 = 0.87 ' .

 

T

240 ‘

 

 

 

 

 

 

l
l
80 1 1 1
4000 6000 8000 10000 12000
MOE (N mm'z)

Figure 1.2. Modulus of rupture (MOR) versus modulus of elasticity (MOE) for wet and
dry treatments of stems of six species of Chaparral shrubs (n = 12 plants per treatment per

species).

32

 

 

 

 

 

 

 

 

 

100
A
80 --
60 --
40 .- l
20 -- ,
.Afascmulatum
OA.sparsifoIium
2\: 100
3‘ B
E l
*5 80 -
a
'c
8
60 ,_
0
.9
'5
40 -- -
‘3
'o
>
I 20 -
“5 l .C.magacarpus
g OC.sprnosus
O .
.1
100
C
80 ~1 4
60 -_
40 --
2 -~ .
0 .MJaunna l
OR.ovata
O t 1 ‘r I . 1
-14 -12 -10 -8 -6 -4 -2 0

PX (MPa)

Figure 1.3. Percent loss of hydraulic conductivity of stems as a function of xylem
pressure potential (PX). Curves were ﬁt with a second order polynomial (r2 2 0.99 and p
S 0.01, for all curves). Means 1 1 SE are shown with n = 6 plants per species. The
graphs were used to calculate for each species the xylem pressure at which there was
50% loss of conductivity (P50 in Figures 1.4 and 1.5).

33

 

 

 

1000 r . . T

(D
O
O

600 i
500 1»

 

I

 

Xylem Density (kg m'3)
\l
o
o

 

o
i

2 2 _
-2 ltr = 0.96 . .rm- 0.60

J:
1
1'

Pmin (M Pa)
‘3’

1

 

 

 

 

 

_'.1
o

-2 0 120 140 160 180 200 220 240 260
MOR (N mm'2)

l
T

-10 -8

_'..
N

-6 -4
P50 (M Pa)

Figure 1.4. A. Modulus of rupture (MOR), B. xylem density, and C. minimum seasonal
pressure potential (Pm) as functions of xylem pressure at 50% loss of conductivity (P50)
and D. xylem density and E. Pm," as functions of MOR for six species of Chaparral
shrubs. Means 1 1 SE are shown and n = 12 plants per species, except for P50 where n =
6 plants per species.

34

 

 

 

 

 

 

 

 

 

 

 

 

 

 

D
005 1 "2:0'85 “I“ +
N
50.041
"’ 0.03«
A '1
0.021-r2=0.95
g 70 r
a
.1 ..
To
3 501 i
I. i
.8
i: B 1. 1 l
4" r2=0.89
E 10 1
3- c F
b 2- 2:
% 8 _r —0.84 .9- _r 0.79
E
.2
o 6 *
: i—i—l
0
E 4-~ 1 1:4
3 1—{—1 1*“ i—§—1 1—1—1
.l
I-
3 I; : U I 1 1 1 1 1 1 1 1
it 42 40 -3 .5 .4 -2 0 120140160180 200 220 240 260

P50 (MPa) MOR (N mm")

Figure 1.5. Xylem anatomical measures as functions of the xylem pressure at which
there is a 50% loss of conductivity (P50) and modulus of rupture (MOR) including
estimated vessel implosion resistance ((t/b)h2) (A and D), percent ﬁber wall area (B and
E), and ﬁber lumen diameter (C and F) in six species of Chaparral shrubs. Means 1 1 SE
are shown and n = 6 plants per species for P50 and n = 12 for MOR.

 

   
    
 

   
  

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

A V -6 MPa
0 MPa
o ~
0:: ...... - 1.0
0 V
v N
. ,,,,, . ,L .
\r
PIIS l\. {'30 ID 50'}
....... ' \ .\
i336? ' '
61 5:9. \
‘
0 MPa
31 Pit membrane
V F‘ A
0 MPa -6 MPa 0
MPa
Air-seeding

 

 

 

 

 

 

 

 

Figure 1.6. Some possible causes of embolism in a woody angiosperm stern. Depicted in
the diagram is a segment of an embolized vessel represented by several vessel elements
(V; 0 MPa), adjacent a functional water-ﬁlled vessel (V; -6 MPa) and surrounded by a
matrix of ﬁbers (F). In this diagram we have assumed that the ﬁbers are embolized (0
MPa). The lower panels represent more detailed diagrams of an intervessel pit, and are
close-ups of the rectangular areas indicated in panels A and B. With thick ﬁber and
vessel walls (A), membrane deﬂection may occur, but it is not exacerbated by wall-
buckling, limiting possible causes of hydraulic failure to air-seeding at the pit pore or
membrane rupture (a1). With thin vessel and ﬁber cell walls (B), there is partial
implosion of the water-ﬁlled vessel (indicated by thick arrows). With partial implosion
there is stretching of the pit membrane with water stress, stretching the pores in the pit
membrane and increasing the likelihood that air-seeding will occur either at the pit pore
or following membrane rupture (b1). Additionally, implosion of vessel walls could lead
to microfractures, another source of nucleation which would lead to cavitation of the
water column (b2).

36

CHAPTER TWO

Jacobsen, A.L., Pratt, R.B., Davis, S.D. & Ewers, F.W. (2007) Cavitation resistance and
seasonal hydraulics differ among three arid Californian plant communities. Plant, Cell
and Environment, 30, 1599-1609.

37

CAVITATION RESISTANCE AND SEASONAL HYDRAULICS DIFFER AMONG

THREE ARID CALIFORNIAN PLANT COMMUNITIES

Abstract

Vulnerability to water stress induced cavitation was measured on 27 woody shrub species
from three arid plant communities, including Chaparral, coastal sage, and Mojave Desert
scrub. Dry season native embolism and predawn water potential and both wet and dry
season xylem speciﬁc hydraulic conductivity (Ks) were measured. Cavitation resistance,
estimated as water potential at 50% loss in conductivity (9150), was measured on all
species during the wet season and on a subset of species during the dry season.
Cavitation resistance varied with sampling season, with 8 of 13 sampled species
displaying signiﬁcant seasonal shifts. Native embolism and water potential were useful
in identiﬁcation of species displaying seasonal shifts. The K8 was not different among
sites or seasons. The ‘1’50 varied among species and communities. Within communities,
interspeciﬁc variation may be partially explained by differences in rooting depth or leaf
habit (evergreen, semi-deciduous, deciduous). Communities diverged in their ‘I’50 with
Chaparral species displaying the greatest cavitation resistance regardless of sampling
season. The greater cavitation resistance of Chaparral species is surprising considering
the greater aridity of the Mojave Desert site. Adaptation to arid environments is due to
many plant traits and aridity does not necessarily lead to convergence in cavitation

resistance.

38

Introduction

Woody plant species from arid communities are more resistant to water stress induced
cavitation than species from more mesic regions when compared across broad spatial
scales (Brodribb & Hill 1999, Maherali, Pockman & Jackson 2004). This same pattern is
present across smaller scales, such as the transition from riparian to upland communities
in the Sonoran Desert (Pockman & Sperry 2000). In addition to moisture availability,
growth form and leaf habit may also inﬂuence cavitation resistance, with shrubs having
greater resistance to cavitation than trees (Maherali et al. 2004) and a trend for evergreen
shrubs to have greater resistance to cavitation than deciduous shrubs (Martinez-Vilalta et
al. 2002; Maherali et al. 2004). Aridland shrub communities, particularly those with
evergreen species, may be convergent in containing species that are highly cavitation
resistant (water potential at 50% loss in hydraulic conducticity [‘I’so] < -4 MPa).

There have been several studies examining cavitation resistance of species within
arid plant communities (c.f. Sobrado 1997; Hacke, Sperry & Pittermann 2000; Pockman
& Sperry 2000; Martinez-Vilalta et al. 2002; Sperry & Hacke 200; Jacobsen et al.
2007b); however, there have been far fewer studies comparing species across different
types of arid communities. These studies have often been limited to few species (Kolb &
Davis 1994, however see Pockman & Sperry 2000) or investigations of a few widely
distributed generalist species whose ranges overlap different communities (Mencuccini &
Comstock 1997; Kolb & Sperry 1999b; Stout & Sala 2003). While a recent meta-
analysis compared resistance to cavitation across expansive vegetation types (Maherali et
al. 2004), such broad studies can be problematical because they do not control for data

gathered across different seasons and years and the utilization of different methods.

39

There have been few, if any, comparisons among arid plant communities utilizing
common methods and taking into account seasonal variation.

Vulnerability of stems to cavitation has been shown to vary greatly over the
course of the growing season (from a ‘1‘50 of approximately -1.6 to -4.5 MPa over three
months for Artemisia tridentata; Kolb & Sperry 1999a) as well as following drought or
freezing stress (Hacke et al. 2001 and Sperry et al. 1994, respectively). Such shifts can
lead to signiﬁcant changes in the vulnerability of stems to cavitation seasonally and, if
widespread, may have a great effect on species and community comparisons. The season
in which species are sampled is rarely reported; however, for studies that do report
sampling season, there is considerable variation (c.f. Sobrado 1997; Tyree, Patifio &
Becker 1998; Kolb & Sperry 1999b; Hacke et al. 2000; Martinez-Vilalta et al. 2002;
Stout & Sala 2003; Ewers et al. 2004; Jacobsen et al. 2007b). While techniques have
been developed for correcting for freezing or water stress induced cavitation fatigue, such
as calculating loss in conductivity relative to the conductivity after application of a
modest negative pressure (> -0.5 MPa; Hacke et al. 2000; Sperry & Hacke 2002;
Maherali et al. 2006), it is possible that shifts occurring during the growing season may
be harder to standardize.

In the current study, we examined, in the same year and season, resistance to
water stress induced cavitation (estimated by ‘1’50 and T75) among three arid plant
communities of southern California, including Chaparral, coastal sage scrub, and Mojave
Desert scrub communities. Vulnerability to cavitation curves were determined for 27
shrub species, including 12 for which no vulnerability curves have previously been

published. In addition to vulnerability curves, native percent loss in hydraulic

40

conductivity (i. e. native embolism) and predawn water potential were measured on plants
during the dry season and xylem speciﬁc conductivity (K5) was measured in both the wet
and dry seasons. In order to evaluate the possibility of seasonal shifts in cavitation
resistance among these species, which may complicate comparisons with previously
published curves, vulnerability to cavitation curves were measured during both the wet
and dry seasons on a subset of these species.

We predicted that among these three arid communities, species would show
similar mean xylem resistance to water stress induced cavitation and a similar range in
values. This is consistent with ﬁndings of similar ranges and means in ‘1’50 among woody
species from Mediterranean-type climate regions compared to deserts in a recent meta-
analysis (Maherali et al. 2004). Additionally, this is consistent with predictions of plant

functional convergence in response to similar environments (Meinzer 2003).

Methods

Sites and Species

Three diverse aridland plant communities were selected based on their high prevalence of
woody shrub species. All sites were located in the winter rainfall—summer dry area of
southern California, USA. The Chaparral site was located in Cold Creek Canyon
Preserve in the Santa Monica Mountains. The coastal sage scrub site was located on the
campus of Pepperdine University in an ecological preserve also located in the Santa
Monica Mountains. These two sites experienced similar precipitation over the course of
the study (Feb 2006-Feb 2007: 433 and 406 mm, respectively) and similar cold season

mean temperatures (10°C compared to 9°C at the Chaparral site) but the coastal sage scrub

41

site had slightly higher mean summer temperatures (26°C compared to 23°C at the
Chaparral site) and a narrower daily temperature range (approximately 10°C compared to
16°C for the coastal sage and Chaparral sites, respectively). The Mojave Desert site was
located in Red Rock Canyon State Park and experienced less annual precipitation for the
year sampled than the other two sites (138 mm). This site had similar summer mean
temperatures as the coastal sage scrub (26°C) site but had cooler mean winter
temperatures than either of the other two sites (4°C).

All of the woody shrub species with unbranched, straight stems longer than 14 cm
that had at least 12 individuals present at a site were included in the present study (Table
2.1) with two exceptions. Arctostaphylos glauca was excluded from the Chaparral site
because it is locally rare and we did not have permission to sample it and Gutierrezia
microcephala was excluded from the Mojave Desert site because we were unable to
measure hydraulic ﬂow due to vessel blockage in this species. The remaining species
included 10 Chaparral species, 9 coastal sage scrub species, and 9 Mojave Desert scrub
species. These species represent 15 families and several leaf habits (Table 2.1).
Nomenclature follows Hickman (1993). One species, Malosma laurina, occurred at both
the Chaparral and coastal sage scrub sites and was sampled at both making the total
number of sampled species 27.

Soil texture, which can inﬂuence xylem cavitation resistance (Sperry and Hacke
2002), was measured beneath one individual of each species at each site (n = 9-10 per
site). Soil was collected from surface level to a depth of 30 cm and texture determined
using the hydrometer method (Soil hydrometer, VWR Scientiﬁc, West Chester, PA,

USA) described in Sheldrick and Wang (1993).

42

Wet Season Vulnerability to Cavitation
Wet season vulnerability to cavitation was measured from February through early July
2006 on at least 6 individuals per species. The last rainfall of the wet season at all sites
occurred May 18-23 and water potentials of plants did not begin to decline until late July.
Stems were trimmed under water in the ﬁeld to a length of approximately 30 cm, sealed
in plastic bags with a moist paper towel, placed in a cooler on ice, and transported to the
laboratory at California State University, Bakersﬁeld (CSUB) where they were
refrigerated until measured (within 4 days of ﬁeld collection). Stems were trimmed
under water from both ends until a segment 4—8 mm in diameter and 14 cm in length was
obtained, except for stems of Adenostoma fasciculatum, Ceanothus cuneatus, C.
megacarpus, and Larrea tridentata. For these species, stem segments at least 50 cm long
where collected in the ﬁeld. These stems were then trimmed under water to 27 cm in
length in the lab. The longer stem sizes were needed for use in a larger rotor which could
generate more negative pressures since prior studies indicated this may be needed for
these species (Pockman & Sperry 2000; J acobsen et al. 2007b).

Vulnerability to cavitation was determined for stem segments as described in
J acobsen et al. 2005. In brief, stems were connected to a tubing system and ﬂushed for l
h at 100 kPa and the maximum hydraulic conductivity (Khmax) of stems was measured
gravimetrically (Sperry, Donnelly & Tyree 1988) using an analytical balance (CP124S,
Sartorius, Goettingen, Germany). Following determination of their Khmax, stems were
spun in a centrifuge (Sorvall RC-SB Refridgerated Superspeed Centrifuge or RC-SC,

Therrno Fisher Scientiﬁc, Waltham, MA, USA), using either a small (for 14 cm stem

43

segments) or a large (for 27 cm stem segments) custom built rotor (Alder et al. 1997).
Vulnerability to cavitation curves were constructed by plotting the water potential
(generated using the centrifuge) versus the percent loss in hydraulic conductivity (PLC).
For each stem, curves were ﬁt with a second order polynomial model (J acobsen et al.
2007b).

Additionally, PLCs were calculated and curves were generated using the Kh from
an initial spin of -0.25 to -0.5 MPa in place of the Khmam in order to correct for cavitation
fatigue of the xylem (Hacke et al. 2000; Sperry and Hacke 2002; Maherali et al. 2006).
This is done since xylem conduits that were previously embolized or damaged may
become conductive following ﬂushing resulting in an elevated Khmax. Using Ki, following
a relatively mild pressure (>-0.5 MPa) embolizes these non-functional conduits while
leaving functional conduits intact thus yielding a more realistic Khmax. These corrected
curves were then used to predict the water potential at 50% and 75% loss in hydraulic
conductivity (‘1’50 and T75, respectively) for each stem and these values were averaged to
get a species mean (n = 6-12 per species with a greater number of samples for those
species for which no prior data existed on vulnerability to cavitation).

The xylem speciﬁc hydraulic conductivity (K,) of stems was determined using the
methods described in J acobsen et al. (2007a). Stained active xylem area was determined
using a digital camera and image analysis software (Olympus SP-500UZ, Olympus
Imaging Corp., Center Valley, Pennsylvania, USA and Scion Image v. Beta 4.0.3, Scion
Corp., Frederick, Maryland, USA). The whole xylem area in cross-section (minus the

pith) was also determined. The Kim)( was then divided by either the active (stained)

xylem area or the whole xylem area to obtain two different measures of xylem speciﬁc

conductivity (Ks).

Dry Season Predawn Water Potential and Native Percent Loss in Hydraulic Conductivity
In September 2006, branchlets from six individuals of each of four species, A. polycarpa,
H. salsola, I. arborea, and L. tridentata, were collected predawn and water potential was
immediately determined in the ﬁeld using a pressure chamber (Model 2000 Pressure
Chamber Instrument, PMS Instrument Company, Albany, OR, USA). A second set of
branchlets were collected at the same time from the same individuals, double bagged,
placed in a cooler on ice, and transported to CSUB where they were rapidly processed in
an air-conditioned lab using the same pressure chamber. Additionally, stem segments
from the same individuals were collected predawn. Leaves were removed from these
branches prior to the branches being removed from the plant, stems were then double
bagged, placed in a cooler on ice, and transported to CSUB where xylem segments of
approximately 4 mm were rapidly excised and placed into calibrated psychrometers
(PST-55-30—SF, Wescor Inc., Logan, UT, USA) connected to a microvolt meter (HR-33T
Dew Point Microvoltmeter, Wescor Inc., Logan, UT, USA) for determination of the stem
xylem water potential. For these four species, there was no signiﬁcant difference
between water potential measured on branchlets in the ﬁeld or laboratory (P > 0.05 for
all); therefore, for the remaining 23 species branchlets were transported to the lab at
CSUB (for the Mojave Desert species) or Pepperdine University (for the Chaparral and

coastal sage scrub species) for measures of branchlet water potential.

45

Predawn water potential was measured during the dry season (measurements
made 30 August 2006 through 6 September 2006). Six individuals were measured per
species. On the same mornings that predawn branchlet water potential was determined,
stems approximately 0.5 min length where collected from the same individuals to
determine native embolism. Stems were cut from the plant while underwater to prevent
the introduction of air into the xylem. The end of each stem was covered with a small
piece of moist paper towel and sealed with Paraﬁlm Laboratory Film and the whole
branch was double bagged in plastic bags containing moist paper towels. Branches were
rapidly transported to the lab at CSUB or Pepperdine University and measured within 5 h
of collection. Stems were trimmed underwater from both ends until an unbranched
straight stem segment 10 cm in length and 4-8 mm in diameter was obtained. These
stems were connected to a tubing manifold and the native Kh determined gravimetrically.
Stems were then ﬂushed following the procedure describe previously and Km
determined. Using these values, the native PLC of stems was determined. Native PLC
was not measured on Malacothamnusfasciculatus due to mucilaginous clogging of
stems. Stems were then sectioned at their midpoint and whole xylem area in cross-
section (minus the pith) determined. The Khm was then divided by the whole xylem

area to obtain the xylem speciﬁc conductivity (Ks) for the dry season.

Dry Season Vulnerability to Cavitation
Four or ﬁve species were selected at each site for determination of dry season
vulnerability to cavitation. We attempted to measure the species with the most negative

wet season ‘I’so in order to determine the species with greatest cavitation resistance at

46

each site and also to sample phylogenetically diverse species. Dry season vulnerability
curves were constructed using the same methods as described for the wet season
vulnerability curves. Dry season curves were measured during November and December
2006 when plants were at or near their annual minimum water potential (J acobsen,
unpublished data). Dry season measures were halted after the onset of signiﬁcant winter
rain in mid-December and for this reason we were unable to measure dry season curves

on additional species.

Statistical Analyses
Statistical analyses were preformed using Minitab (Release 14.12.0, Minitab Inc., State
College, PA, USA) and/or Statview (v. 5.0.1, SAS Institute Inc., Cary, NC, USA). Alpha
was set at 0.05 for all comparisons. Water potential as measured on branchlets using the
pressure chamber in the lab or ﬁeld or on stem xylem using psychrometers where
compared within species using AN OVAs followed by a Fisher’s PLSD post-hoe analysis
when appropriate. Interspeciﬁc differences in ‘1’50 were analyzed within site using
ANOVAs, and AN OVAs were also used to analyze across site differences in ‘1’50, Tim",
and Ks. For comparisons of ‘1150 and ‘1’75 among species with different leaf habits, species
were grouped into three categories, evergreen, semi-deciduous, or deciduous, and
ANOVAs were used.

Non-fatigue corrected vulnerability to cavitation curves were used to predict the
expected PLC at the predawn water potential for comparison with the dry season ﬁeld
measured native PLC. For comparison of the measured native PLC with the wet and/or

dry season calculated PLC, t-tests were used. For seasonal comparisons of wet and dry

47

season ‘I’so and ‘P75 within species, t-tests were used and species were considered to have
a signiﬁcant seasonal shift in their vulnerability to cavitation if either of those parameters
differed signiﬁcantly. For comparisons within individual species of wet season stained

Ks, wet season Ks, and dry season Ks, ANOVAs were used.

Results

The 27 species showed a range of cavitation resistances. This is indicated by the variation
in the size and magnitude of their wet season vulnerability to cavitation curves, with
curves ranging in shape from convex to linear to concave (Figures 2.1, 2.2, & 2.3). In
regression analyses of these vulnerability to cavitation curves, water potential described
more than 82% of the variation in percent loss in hydraulic conductivity (PLC) in all
cases (i.e. r2 > 0.82), and often much more (most r2 > 0.95).

Soil texture was not different among sites, with no signiﬁcant differences in the
sand, clay, or silt fractions among sites (P > 0.05 for all). All soil samples fell within the
Sand to Loamy Sand categories.

Wet season vulnerability to cavitation (estimated by the mean water potential at
50% loss in hydraulic conductivity; 1'50) was signiﬁcantly different among the three arid
communities (P = 0.003). The ‘Pso ranged from -0.5 (Malosma laurina) to -9.5 MPa
(Adenostoma fasciculatum) (Figure 2.4). The Chaparral species were signiﬁcantly more
cavitation resistant (lower 9’50) than the coastal sage scrub (P = 0.003) and the Mojave
Desert scrub species (P = 0.003) with 7 out of 10 Chaparral species displaying greater
resistance than the most resistant species of either of the other two communities. The

Mojave Desert and coastal sage scrub species were not different from one another (P =

48

0.909) (Figure 2.4 B inset). Water potential at 75% loss in hydraulic conductivity
followed the same pattern as ‘1’50 (not shown) and non-fatigue corrected values were
positively correlated with fatigue corrected values (P < 0.001; not shown). Malosma
laurina was the only species that occurred at more than one site, in both the Chaparral and
coastal sage scrub, and its ‘1’50 and ‘P75 did not vary between sites (P = 0.471 and 0.652
for ‘1’50 and ‘1’75, respectively).

Species displaying different leaf habits (i. e. species with evergreen, semi-
deciduous, or deciduous leaves) did not signiﬁcantly differ in either ‘1'50 or Wu (P =
0.186 and 0.188, respectively; see Table 2.1 for leaf habits of individual species).
However, there was a trend for evergreen species to be more resistant to cavitation.
Evergreen species had a mean ‘1’50 of -3.1 1 0.6 MPa compared to -1.8 1 0.2 and -l.4 1
0.5 MPa for the semi-deciduous and deciduous species, respectively.

Mean native percent loss in hydraulic conductivity (native PLC) measured in
September was near 50% for all communities and was not different among communities
(Figures 2.1, 2.2, & 2.3; P = 0.417). Mean native PLC for the Chaparral was 41.8 1 7.6%
versus 49.0 1 6.7% for the coastal sage scrub and 55.6 1 7.7% for the Mojave Desert
scrub. Among individual species, native PLC ranged from 10.2% in Hazardia squarrosa
to 91.9% in Quercus berberidifolia. Native PLC signiﬁcantly differed from the PLC
predicted by wet season vulnerability curves and predawn branchlet water potential in 14
out of 26 species (Figures 2.1, 2.2, & 2.3; P > 0.05). Note, only 26 species were included
in this analysis because we were unable to measure native PLC on M. fasciculatus (see

Methods).

49

Predawn branchlet water potential (Tpd) measured in September during the
collection of native PLC values was not different among the three communities (P =
0.151). The mean ‘I’pd 1 1 SE was -3.32 1 0.59 MPa for the Chaparral, -2.42 1 0.26 MPa
for the coastal sage scrub, and -4.06 1 0.70 MPa for the Mojave Desert scrub (grey bars
in Figures 2.1, 2.2, & 2.3).

Xylem speciﬁc conductivity (KS) did not differ among the three communities
(Figure 2.5 C inset; P = 0.107). None of the measured species experienced a signiﬁcant
change in xylem speciﬁc conductivity from the wet season to the dry season (grey versus
open bars in Figure 2.5). For several species, not all growth rings in the xylem area were
active as indicated by a signiﬁcant difference between the stained area wet season KS
versus the whole xylem area wet season Ks (black versus grey bars in Figure 2.5).

For four species in which water potentials were measured on branchlets in the
ﬁeld and laboratory, there was no signiﬁcant difference between these water potentials (P
> 0.05 for all; data not shown). For three out of four species, these branchlet water
potentials were also not different from stem xylem water potentials as measured with
psychrometers (P > 0.05; data not shown); however, for one species, Larrea tridentata,
the stern xylem water potential measured by psychrometers was signiﬁcantly more
hydrated than branchlet water potential measured using a pressure chamber (P < 0.001
for stem water potential compared to both the lab and ﬁeld measured branchlet water
potentials; data not shown).

Among the 13 species for which dry season vulnerability to cavitation curves
were measured, there was great variability in seasonal response when compared to wet

season vulnerability curves. In some species the dry season curve was more vulnerable

50

(Figure 2.1 A & Figure 2.3 G), in others there was no signiﬁcant difference (Figure 2.1 D
& H, Figure 2.2 A, Figure 2.3 D & E), and in others the dry season curve was more
resistant (Figure 2.1 F, Figure 2.2 D, H, & I, & Figure 2.3 C & F). Of the 13 species for
which dry season vulnerability to cavitation curves were measured, 5 had predicted PLC
that was signiﬁcantly different from the measured native PLC (Figures 2.1, 2.2, & 2.3; P
> 0.05). However, if the stem xylem water potential for Larrea tridentata is used instead
of the branchlet value, both the dry season and wet season curves predict PLC for Larrea
(open bar Figure 2.3 G) reducing this to 4 of 13 species that have predicted PLC that are
different from the measured native PLC.

Dry season ‘1’50 and ‘1’75 values differed signiﬁcantly from wet season values in
eight of 13 species (Figure 2.6). In most of these cases, the dry season value was lower
than the wet season value, indicating a shift toward being more resistant to cavitation
during the dry season. However, in two cases the dry season value was higher than the
wet season value (Adenostoma fasciculatum and Larrea tridentata). Wet season and dry

season ‘1’50 were signiﬁcantly correlated (P < 0.001).

Discussion

Non-convergence of cavitation resistance

Across three arid plant communities, shrub species appear to diverge in their cavitation
resistance in spite of similar growth form and environment. Among 27 woody shrub
species from three arid shrub plant communities there is considerable variability in
vulnerability to water stress induced cavitation. Within communities, this variability may

be due to differences in rooting depth or heterogeneity of soil moisture availability within

51

sites (J acobsen et al. 2005; Jacobsen et al. 2007b). While soil texture of shallow soils
was similar among sites and did not vary greatly within sites, deeper soil layers may
exhibit greater heterogeneity (c.f. Davis & Mooney 1985). Differences in rooting depths
and physiological traits among species are likely primary determinants of variability in
vulnerability to cavitation. Indeed, a previous investigation found a similar range in
cavitation resistance (9’50) as found in the current study when comparing 6 co—occurring
species of even—aged Chaparral shrubs growing at the same microsite (J acobsen et al.
2005).

While all three communities include species that are relatively vulnerable, the
Chaparral has many more species that are highly resistant to cavitation, including 7
species with ‘1’50 lower than —4 MPa. These species are more resistant than any species
measured in either the coastal sage or Mojave Desert scrub. Indeed, Chaparral species
are, on average, more resistant to water stress induced cavitation than species from the
other two arid communities. This contrasts with ﬁndings of similar ranges and means in
T50 among woody species from deserts and winter rainfall regions when compared across
a much broader scale (Maherali et al. 2004). Thus, species in these communities do not
converge to a common level of xylem cavitation resistance as predicted. Additionally,
the greater resistance of Chaparral species to water stress induced cavitation is surprising
considering the greater aridity of the Mojave Desert site (Maherali et al. 2004). This
highlights that habitat aridity is not necessarily a good predictor of species resistance to
water stress induced cavitation across arid ecosystems.

Species in the coastal sage scrub and Mojave Desert scrub may have traits

allowing them to mitigate extreme water stress in xylem tissues. This is supported by

52

similar levels of native embolism among species in all three communities of
approximately 50% loss in hydraulic conductivity during the dry season. This suggests
that species are similarly avoiding high levels of xylem cavitation in spite of differences
in cavitation resistance. Variation in leaf habit or rooting depth among the sampled
species may partially explain the different water stress tolerating strategies among
species, both within communities as well as between them. For instance, while the
Chaparral retain a near complete canopy throughout the dry season, many of the shrub
species of the coastal sage and Mojave Desert are semi-deciduous or facultatively
drought deciduous and adjust their canopy size during the dry season. Additionally,
Chaparral species tend to be larger and have fuller canopies than species occurring in the

other two communities (J acobsen, unpublished data).

Seasonal shifts in cavitation resistance

Vulnerability to water stress induced cavitation signiﬁcantly varied depending on the
season in which stems were measured. In many cases, non-fatigue corrected wet season
vulnerability curves were predictive of dry season native PLC. Native PLC values agreed
with the percent loss in hydraulic conductivity predicted by 13 out of 26 wet season
curves suggesting that seasonal shifts are not likely in these species. However, in 13
other species, native PLC was signiﬁcantly different than that predicted by wet season
vulnerability to cavitation curves. This suggested that shifts were likely or, alternatively,
that branchlet water potential was in disequilibrium with stem xylem water potential in
these other species. Indeed, of the 13 species for which vulnerability to cavitation curves

were measured in both the wet and dry seasons, 8 species displayed signiﬁcant seasonal

53

shifts. Most species shifted to become more resistant later in the season as was observed
previously in Artemisia tridentata (Kolb & Sperry 1999a), whereas a few species became
more vulnerable during the dry season. Species in the present study experienced as much
as a twofold change in vulnerability to cavitation from the wet season to the dry season
and seasonal shifts appear to be relatively common among shrub species in all three
communities.

For a few species, Ceanothus cuneatus, Malosma laurina, Hazardia squarrosa,
and Larrea tridentata, dry season vulnerability to cavitation curves predicted PLC values
signiﬁcantly higher than the measured dry season native PLC. This pattern has been
reported previously for tropical shrubs and trees (Lopez et al. 2005) and may be due to
branchlet water potentials that are more negative than the pressure experienced by the
stem xylem on which native PLC is measured. This leads to artiﬁcially high predictions
of PLC similar to the pattern seen in these species. Nighttime transpiration and solutes in
the xylem sap have been found to partially explain this disequilibrium in arid plants
(Donovan et al. 1999; Donovan, Linton & Richards 2001; Donovan, Richards & Linton
2003); however, solutes in the xylem sap do not seem likely for the species in the current
study because we did not ﬁnd signiﬁcant xylem sap osmotic potential in individuals in
which this was examined (J acobsen, unpublished data). Evidence of predawn
disequilibrium between stem xylem and branchlets was found in one species. For L.
tridentata, native PLC was not different from that predicted by either wet or dry curves if
the water potential of stem xylem measured by psychrometers was used instead of
branchlet water potential measured by pressure chamber (Figure 2.3 G). For the 5

species in the present study for which native PLC differed signiﬁcantly from predictions

54

based on wet season vulnerability curves but for which dry season vulnerability curves
were not measured, seasonal shifts and/or disequilibrium are likely.

Shifts in vulnerability to cavitation may explain some of the variability among
published curves. Vulnerability to cavitation of Chaparral species, both from the wet and
dry seasons are similar in range to those previously reported for these species (c.f.

J acobsen et al. 2005; Jacobsen et al. 2007b; Pratt et al. 2007). There have been relatively
few vulnerability curves published for coastal sage scrub species, but for the species for
which there are published curves, Malosma laurina and Salvia melltfera, our results are
within the same range of published values (Kolb & Davis 1994; Langan, Ewers & Davis
1997; J acobsen et al. 2005; Jacobsen et al. 2007b). For the Mojave Desert species, the
curves for Larrea tridentata and Hymenoclea salsola are similar and within the range of
other published curves for these species (Pockman & Sperry 2000 and Mencuccini &
Comstock 1997, respectively). For the other two species for which curves have been
published, Ambrosia dumosa and Atriplex canescens, the curves in the present study were
more vulnerable than those reported elsewhere (Mencuccini & Comstock 1997 and
Hacke et al. 2000, respectively). This may have resulted because the curves in the
present study for these species were wet season curves. A shift in A. canescens of similar
magnitude to that found in the closely related species A. polycarpa would produce a dry

season curve similar to that reported by Hacke et al. (2000).

Inﬂuence of seasonal shifts on interspeciﬁc and community comparisons

Wet season cavitation resistance was correlated to dry season cavitation resistance in the

present study and similar differences were found among communities when data were

55

compared within a season (i. e. mean ‘1’50 is approximately 2 MPa lower in the Chaparral
compared to the other two communities when either wet or dry season values are
compared). However, results could be altered signiﬁcantly if ‘1’50 values from different
seasons were used to compare communities. This suggests that care must be taken in
comparison of vulnerability curves completed during different seasons or for which no
sampling season is reported. This may complicate attempts to use published values in
broad scale meta-analyses. Measures of native embolism and water potential may be
useful in identifying species in which seasonal shifts are likely or to validate existing

CUI’VCS.

Physiology of seasonal shifts

Seasonal shifts in vulnerability to water stress induced cavitation are likely of
physiological signiﬁcance and may be due to maturation of xylem as suggested by Kolb
& Sperry (1999a) or to changes in pit membranes or mechanical strength. Several of the
species that experienced signiﬁcant shifts in xylem vulnerability to cavitation in the
present study also have a large portion of inactive xylem as indicated by the signiﬁcant
difference between stained xylem speciﬁc hydraulic conductivity (Ks) and whole xylem
K3 in these species, including Ceanothus megacarpus, Ambrosia dumosa, and Isomeris
arborea. This suggests that vulnerability to cavitation curves in these species largely
measure the vulnerability of newer xylem and may therefore be sensitive to maturation of
the xylem over the course of the growing season. It is unlikely that the shifts seen in the
present study are the result of loss of function or sealing off of old wood or early wood

over the course of the growing season as is seen in ring-porous species because these

56

would likely affecth or would result in high levels of cavitation fatigue, neither of
which were observed. Additionally, such shifts could be explained by seasonal hydrogel
or other pit membrane changes (Gascé et al. 2006; Gascé et al. 2007) although such
changes would also likely have resulted in signiﬁcant differences in KS seasonally.

Seasonal changes in xylem mechanical strength may inﬂuence xylem cavitation
without affecting seasonal hydraulic conductivity. Young xylem may not contain enough
mature and mechanically robust cells to buttress newly functional vessels against
implosion when exposed to high tensions (J acobsen et al. 2005). Indeed, seasonal
changes in mechanical strength against stem breakage have been found among several
species of Rhamnaceae shrubs of the California Chaparral, including the four Ceanothus
species included in the present study (Pratt, unpublished data). These species
experienced signiﬁcant increases in modulus of rupture (MOR) from the wet season to
the dry season. Seasonal changes in xylem biomechanics may have important
implications for dry season acclimation of woody shrubs, perhaps through increased
resistance to implosion (J acobsen et al. 2005). This suggests that care should be taken in
interpreting vulnerability curves collected on non-hardened xylem which may be not be
indicative of dry season values. Thus, dry season vulnerability to cavitation curves may
be preferable in determination of the resistance to cavitation of the hardened xylem that
actually tolerates low seasonal water potentials. Additionally, while dry season curves are
likely to have greater levels of xylem fatigue compared to wet season curves, a standard
fatigue correction can be applied to curves minimizing the inﬂuence of fatigue on

comparisons (Hacke et al. 2000; Sperry & Hacke 2002; Maherali et al. 2006).

57

In the present study, the greater resistance to cavitation of Chaparral shrub species
compared to coastal sage or Mojave Desert shrub species is similar regardless of whether
wet or dry season curves are examined. Curves for all 27 species were completed during
the wet season providing a more comprehensive comparison of these communities and
similar differences in cavitation resistance were also found when the fewer dry season
curves were compared. To conclude, in spite of environmental similarities and the
common stress of summer drought, species from these three communities have diverged
in their xylem physiology with Chaparral species displaying the greatest resistance to
water stress induced xylem cavitation regardless of sampling season. Among these
communities, species are likely utilizing differing suites of whole plant traits in order to

persist in these arid environments.

58

Table 2.1. Vegetation community, location, and sampled species within each community
along with families, codes, and leaf habits.

 

 

 

 

 

 

Vegetation
type & Species 1
Location SEcies Famil Code Leaf Habit
Chaparral--Cold Creek Canyon Preserve, Santa Monica Mountains, CA, USA (34.5 N 118.4 W)
Adenostomafasciculatum Hook. & Arn. Rosaceae Af E
Adenostoma sparsifolium Torrey Rosaceae As E
Arctostaphylos glandulosa Eastw. Ericaceae Ag E
Ceanothus cuneatus (Hook) Nutt. Rhamnaceae Cc E
Ceanothus megacarpus Nutt. Rhamnaceae Cm E
Ceanothus oliganthus Nutt. Rhamnaceae Co E
Ceanothus spinosus Nutt. Rhamnaceae Cs E
Malosma laurina (Nutt.) Abrams2 Anacardiaceae M1 E
Quercus berberidifolia Liebm. Fagaceae Qb E'FDD
Rhus ovata S. Watson Anacardiaceae Ro E

 

Coastal Sage Scrub—Preserve located on Pepperdine University's campus, Malibu, CA. USA (34.2 N

 

 

 

118.4 W) _
Artemisia califomica Less. Asteraceae Ac SD,FDD
Encelia califomica Nutt. Asteraceae Eca D
Eriogonum cinereum Benth. Polygonaceae Eci E
Hazardia squarrosa (Hook. & Am.) E. Asteraceae HS E
Greene
Lotus scopan'us (Nutt.) Ottley Fabaceae Ls D,PS
Malacothamnusfasciculatus (Torrey & Malvaceae Mf SD,FDD
A. Gray) E. Greene
Malosma laurina (Nutt.) Abrams2 Anacardiaceae M] E
Salvia leucophylla E. Greene Lamiaceae Sl SD,FDD
Salvia mellifera E. Greene Lamiaceae Sm SD,FDD
Mojave Desert Scrub--Red Rock Canyon State Park, CA, USA (35.2 N 117.6 W)
Ambrosia dumosa (A. Gray) Payne Asteraceae Ad SD,DD
Am‘plex canescens (Pursh) Nutt. Chenopodiaceae Ac E
Atriplex polycarpa (Torrey) S. Watson Chenopodiaceae Ap E
Coleogyne ramosissima Torrey Rosaceae Cr E,FDD
Hymenoclea salsola A. Gray Asteraceae Hs SD,FDD,PS
Isomeris arborea Nutt. Capparaceae Ia SD,FDD,PS
Larrea tridentata (DC.) Cov. Zygophyllaceae Lt E
Lepidospartum squamatum (A. Gray) A. Asteraceae Ls E
Gray4
Lycium andersonii A. Gray Solanaceae La D

 

 

 

 

lE (evergreen), SD (semi-deciduous), FDD (facultatively drought deciduous), D
(deciduous), PS (photosynthetic stems)
2Formerly Rhus laurina; this species was present at both the Chaparral and coastal sage

scrub sites

3May be facultatively drought deciduous during extreme drought events (Pratt and Davis,
unpublished data) but was not during the studied time period in the present study
4Scale-like leaves

59

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A. califomica

 

 

 

 

 

 

 

 

 

  

 

 

 

 

100 A I B' E. caldomma 7
75 i - -
50 -r .4 .-
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2\: 25 _r2-0.99 _ 2
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O 100 r r r I l
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Water Potential (MPa)

8. me__ifera

 

 

 

 

Figure 2.2. Vulnerability to cavitation curves measured on 9 coastal sage scrub species
during the wet season (Feb-May 2006; closed circles, mean :I: 1 SE; n = 6—12) and for 4
species measured during the dry season (Aug-Dec 2006; open circles, mean :1: 1 SE; n =
6). Curves shown are uncorrected for xylem fatigue (see Methods). Native percent loss
in conductivity (PLC) and predawn water potential from the dry season are also shown
(grey bars, mean :I: 1 SE; n = 6). A “w” indicates that native PLC are signiﬁcantly
different from those predicted by wet season vulnerability curves and a “d” indicates
native values are signiﬁcantly different from those predicted by dry season vulnerability

CUI'VCS.

61

 

A. canescens
I l

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

100 l u
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o I I l
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I HI I T I l
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-12 -8 -4 0 -12 0

   

Water Potential (MPa)

Figure 2.3. Vulnerability to cavitation curves measured on 9 Mojave Desert scrub
species during the wet season (Feb-May 2006; closed circles, mean i 1 SE; n = 6-12) and
for 5 species measured during the dry season (Aug-Dec 2006; open circles, mean :t: 1 SE;
n = 6). Curves shown are uncorrected for xylem fatigue (see Methods). Native percent
loss in conductivity (PLC) and predawn water potential from the dry season are also
shown (grey bars, mean :t 1 SE; for predawn water potential as measured with
psychrometers, white bar :t 1 SE; n = 6). A “w” indicates that native PLC are
signiﬁcantly different from those predicted by wet season vulnerability curves and a “(1”
indicates native values are signiﬁcantly different from those predicted by dry season

vulnerability curves.

62

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A Chaparral

- wet season stained area a
6 _ wet season xylem area
:1 dry season xylem area

  

Af As Ag Cc Cm Co Cs Ml Qb Ho

 

B Coastal Sage Scrub

KB (:112 s" We" '10'3)
A

 

 

Ac Eca Eci Hs Ls Mf Ml SI Sm

C Mojave Scrub 4
6 -- 2 _
|
0

4 -- Chap. 088 Mojave ‘

 

 

 

Ad Ac Ap Cr Hs la Lt Ls La
Figure 2.5. Xylem speciﬁc conductivity (Ks) for 27 species from three different and plant
communities as determined during the wet season (black and grey bars, mean :l: 1 SE; n =
6-12) and dry season (open bars, mean 1- 1 SE; n = 6). See Table 2.1 for species codes.
Wet season K8 was determined by dividing the maximum hydraulic conductivity (Km)
by either the stained active area (black bars) or the whole xylem area (grey bars). Dry
season KS was determined by dividing Km by the whole xylem area only (open bars).
Unique letters indicated signiﬁcant differences between measures within a species. Inset
in C shows the mean wet season stained KS for each community (black bars, mean i 1
SE) and letters indicate that there was not a signiﬁcant difference in Ks among
communities.

 

   

Cha arral Coastal Sa e Scrub Mo'ave Desert Scrub
Af Cc Co MllAc Hs SI SmIAp Cr Hs la Lt

         

  
  

 

0 .7
l ' l
-2 —— .1
a -4 -- l
n- 1
a -6 __ * _
8
B-i
-8 _- _

- Wet Season —
l:l Dry Season

 

 

 

 

 

 

 

Figure 2.6. Mean water potential at 50% loss in hydraulic conductivity (T50) (A) and ‘P75
(B) for 13 species from three arid plant communities (black and grey bars :l: 1 SE)
corrected for fatigue (see Methods for details). See Table 2.1 for species codes. Species
means were determined from vulnerability to cavitation curves measured during the wet
season (black bars) and dry season (grey bars). See Figures 2.1—2.3 for vulnerability to
cavitation curves. An asterisk beneath the dry season bar indicates that the dry season
and wet season ‘1’50 or ‘1’75 values were signiﬁcantly different for that species.

65

CHAPTER THREE

COMPARATIVE COMMUNITY PHYSIOLOGY: NON-CONVERGENCE IN WATER

RELATIONS AMONG THREE SEMI-ARID SHRUB COMMUNITIES

Abstract

Plant adaptations to the environment are limited and plants in similar environments may
display similar functional and physiological traits, a pattern termed functional
convergence. Evidence was examined for functional convergence among 28 evergreen
woody shrubs occurring in three different plant communities in the semi-arid winter
rainfall region of southern California. These communities included Chaparral, coastal
sage scrub, and Mojave Desert scrub. Both leaf and water relations traits were examined,
including seasonal stomatal conductance (gs), speciﬁc leaf area (SLA), leaf speciﬁc
conductivity of stems (K1), seasonal water potential (WW), stem cavitation resistance (1’50),
and stem xylem density. These communities displayed a similar level of water stress,
with a community level average minimum seasonal water potential (mein) of
approximately -4.6 MPa which agrees with average ‘I’wmin reported for other arid
communities. Pooled across sites, there was a strong correlation between ‘I’wmin and
xylem density suggesting that these traits are broadly related and predictive of one
another. In contrast, the relationship between ‘Pwmin and ‘P50 appears to be community
speciﬁc and may be related to differential ability of species to tolerate or avoid high
seasonal levels of embolism. Speciﬁc leaf area differed among communities with the

coastal sage scrub community displaying greater SLA than the other two communities.

66

Speciﬁc leaf area was not a good predictor of water relations traits within or across
communities. The relationship between g5 and ‘Pw also appears to be community speciﬁc
and likely reﬂects differential water use by shrubs in these communities, with coastal
sage scrub species adapted to utilizing shallow pulses of water, Mojave Desert scrub
species relying on deeper water reserves, and Chaparral species utilizing both shallow and
deep moisture reserves. The comparative community physiology approach used here
may provide a useful tool to test hypotheses of functional convergence across structurally

similar semi-arid communities.

Introduction

Plant functional convergence studies both at the global and community levels have
suggested that plants may be limited in their physiological solutions to environmental
stresses and that plants in similar environments may therefore display similar functional
and physiological traits (Reich et al. 1997; Paruelo et al. 1998; Meinzer 2003; Reich et
al. 2003; Bucci et al. 2004; Swenson & Enquist 2007). Such ﬁndings suggest that there
is potential to predict plant traits and related ecological processes across broad regions
based on environmental conditions. Additionally, such correlations may be useful in
predicting plant traits in regions that have been poorly studied. Many studies examining
plant functional traits have examined plant form (Paruelo et al. 1998), xylem density
(Swenson & Enquist 2007), water relations (Ackerly 2004; Bucci et al. 2004; Bhaskar &
Ackerly 2006), and leaf traits (Reich et al. 1997; Ackerly 2004) as traits associated with

speciﬁc aspects of plant functional variation.

67

Across broad scales, plant form appears convergent leading to the recognition of
vegetatively similar biomes. A classic example of this is convergence to a shrub
dominated landscape in Mediterranean—type climate regions (Aschmann 1973; Paruelo et
al. 1998). These plant communities from around the world have often been compared to
one another, although not in terms of the detailed physiological parameters used in the
present study (e. g. Aschmann 1973; di Castri & Mooney 1973; Parsons & Moldenke
1975; Cody & Mooney 1978; Cowling & Campbell 1980; Kruger et al. 1983). While
there appears to be great similarity in plant form among species occurring in these
regions (i.e. shrubs with evergreen, tough leathery leaves), it is not clear that this
morphological similarity corresponds with similar functional traits among species.

We examined evidence for functional convergence among the evergreen woody
shrubs occurring in three semi-arid plant communities in the winter rainfall region of
southern California. These communities included Chaparral, coastal sage scrub, and
Mojave Desert scrub. In the present study we included leaf, stem, and water relations
traits. Leaf level measurements included speciﬁc leaf area (SLA). Stem level
measurements included leaf and xylem speciﬁc conductivity (K1 and Ks, respectively),
xylem resistance to cavitation (T50), and xylem density (KS and Wm were previously
reported by J acobsen et al. (2007c)). To characterize plant water relations, seasonal
measures were made of stomatal conductance (gs) and leaf branchlet water potential (WW)
for 12 to 14 months. Additionally, temperature and precipitation were monitored at each
site.

We predicted that the species occurring in these communities would display

similar water relations and functional traits in response to their common arid winter

68

rainfall environment. We predicted that, among sites, species would experience dry
season water potentials (mein) similar to their xylem cavitation resistance (W50) that have
already been reported (see J acobsen et al. 2007c). This would be consistent with the 1:1
relationship between ‘I’wmin and T50 reported for arid communities, including 26 species
of Chaparral (J acobsen et al. 2007b; Pratt et al. 2007a) and six shrubs from the Great
Basin Desert (Hacke et al. 2000). Based upon previously reported ‘Pso, a 1:1 relationship
would result in differential ‘Pwmin among the sites such that the Chaparral species would
experience the lowest ‘I’wmin and species in the other two sites would experience less
negative ‘I’wmin relative to the Chaparral.

We predicted gS would decline with declining ‘1’“, during the course of the dry
season when plant water status declined and the vapor pressure deﬁcit increased (Poole &
Miller 1975; Davis & Mooney 1985; Schulze 1986; Thomas & Eamus 1999; Brodribb &
Holbrook 2003; Barradas et al. 2004; Brodribb & Holbrook 2004; Ladjal et al. 2005;
Galmés et al. 2007). Such a stomatal response is presumably necessary in order for
plants to avoid extreme negative pressures and runaway cavitation during the dry season
especially among evergreen plants (Cochard et al. 2002; Sperry et al. 2002).
Additionally, we predicted that Chaparral species would have a shallower slope in their
relationship between ‘Pw and g5 (i.e. delayed stomatal closure) consistent with their more
cavitation resistant xylem (Ladjal et al. 2005; J acobsen et al. 2007c).

Relationships among traits were also examined in order to determine the
predictability of functional traits using traits that are commonly used as indices of plant
functional variation. We predicted that xylem density would be correlated with ‘11an

(J acobsen et al. 2007a; Jacobsen et al. 2007b), ‘1’50 (Hacke et al. 2000; J acobsen et al.

69

2007b), and g5 (Bucci et al. 2004). We predicted that SLA would be correlated with
‘Pwmin and ‘P50 since SLA is associated with increased aridity tolerance (Wright et al.
2002). Lastly, we predicted that SLA, Ks, and K. would be associated with gS (Sperry
2000; Gulias et al. 2003; Santiago et al. 2005; Poorter & Bongers 2006). Correlations
between these traits were also analyzed using phylogenetic independent contrasts in order

to account for the phylogenetic relationships among species in analyses (Felsenstein

1985).

Materials and Methods

Sites and Species

Three diverse aridland plant communities were selected based on their high diversity of
woody shrub species. All sites were located in the winter rainfall-summer dry area of
southern California, USA. The Chaparral site was located in Cold Creek Canyon
Preserve in the Santa Monica Mountains, the coastal sage scrub site was located on the
campus of Pepperdine University also located in the Santa Monica Mountains, and the
Mojave Desert site was located in Red Rock Canyon State Park (see Chapter 2; Jacobsen
et al. 2007c for site descriptions).

All of the shrub species that occurred in sufﬁcient numbers and for which we
were able to obtain permission to sample were studied at each of these sites. This
included 10 Chaparral species, 9 coastal sage scrub species, and 10 Mojave Desert species
(see Table 3.1). Most of these species are evergreen (see Jacobsen et al. 2007c). At each

site, six individuals of each species were tagged at the beginning of the study. All

70

measurements throughout the course of this study were conducted on these same
individuals.

Xylem speciﬁc conductivity (Ks) and xylem vulnerability to cavitation (9150) were
also measured on these same individuals or individuals of the same species located in
close proximity to the sampled individuals. These data were published as part of a

separate study (J acobsen et al. 2007c).

Weather

Temperature and precipitation were monitored at sites via Remote Automated Weather
Stations (RAWS) run by the Western Regional Climate Center for which temperature and
precipitation at weather stations is monitored hourly and available online
(http://www.wrcc.dri.edu/wraws/). Conditions at the Chaparral site were approximated
using the Malibu Canyon California RAWS, at the coastal sage scrub site using the
Malibu Hills California RAWS, and for the Mojave Desert scrub site using the Jawbone

California RAWS.

Seasonal water potential

Water potential CPw) was measured on all species approximately monthly beginning in
February 2006 and continuing through April 2007. Leaves or branchlets were removed
from plants at midday, double-bagged, and placed in a cooler on ice. Samples were then
rapidly transported to an air-conditioned laboratory at Pepperdine University, Malibu,
CA, USA for the Chaparral and coastal sage scrub species or California State University,

Bakersﬁeld, CA, USA (CSUB) for the Mojave Desert scrub species. Samples were

71

rapidly processed using a pressure chamber (Model 2000 Pressure Chamber Instrument,
PMS Instruments, Corvalis, Oregon, USA). A previous study concluded that laboratory
measured ‘I’w samples were no different from those measured immediately in the ﬁeld

(J acobsen et al. 2007c).

Seasonal stomatal conductance

Stomatal conductance (gs) was measured on all species approximately monthly beginning
in April 2006 and continuing through April 2007. Stomatal conductance was measured
on a leaf or branchlet of six individuals per species at each sampling time using a steady
state porometer (LI-COR, Inc., LI-16OO Steady State Porometer with a 1600-07
Cylindrical Chamber, Lincoln, Nebraska, USA). For each sampling time, all species
within a site were measured within a single day beginning around 10:00 am and ending
around noon. Leaf and air temperatures were periodically checked using an infrared
thermometer for leaf temperatures (Fluke Corporation, Fluke 572 CF IR thermometer,
Germany) and a thermocouple for air temperatures (Control Company, 4015 Traceable
Total Range Thermometer with a beaded Type-K thermocouple probe, Friendswood, TX,
USA). Sampled leaves or branchlets were collected and the sampled leaf area determined
using a leaf area meter (LI-3100, LI—COR, Inc., Lincoln, Nebraska, USA). Stomatal
conductances of species where then corrected using the area of the leaves containing
stomata (i.e. species with stomata on only one side of the leaf where corrected using the
one-sided leaf area, species with amphistomatic leaves were corrected using the two-
sided leaf area, and species with needle like leaves were corrected by calculating the

surface area of the leaf based on cross sectional measures of leaf geometry).

72

Speciﬁc Leaf Area

Speciﬁc leaf area (SLA) was measured on fully mature leaves at the start of the summer
dry period. Branchlets were collected from individuals in the ﬁeld, placed in plastic
bags, and transported to the laboratory at CSUB. Individual leaves were then taken from
each branchlet with a total of 10 leaves from 10 individuals for each species and their
area was measured using a leaf area meter. Leaves were then placed in a drying oven at
60°C for four days and their dry mass was determined using an electronic balance
(CP124S, Sartorius, Goettingen, Germany). Speciﬁc leaf area was calculated as the leaf
area per dry leaf mass (mm2 mg'l). The SLA was not determined for Lepidospartum

squamatum separating its small adherent scale—like leaves from the stem.

Leaf Speciﬁc Hydraulic Conductivity

Leaf speciﬁc hydraulic conductivity was measured during the dry season in August and
September 2006 on 24 of the 28 species included in the present study. The remaining 4
species had very small, scale-like, or adherent leaves which prevent accurate
determination of leaf area. Stems approximately 0.5 m in length were collected predawn.
Stems were cut from the plant while underwater, the end of each stem was covered with a
small piece of moist paper towel and sealed with Paraﬁlm Laboratory Film, and the
whole branch was double bagged in plastic bags containing moist paper towels.

Branches were rapidly transported to the lab and native conductivity was measured on a
stem segment 10 cm in length and 4-8 mm in diameter within 5 h of collection following

the methods in Jacobsen et al. (2007c). All leaves distal to the measured stem were

73

collected and their leaf area determined using a leaf area meter. The native conductivity
was then divided by this leaf area to determine the dry season leaf speciﬁc xylem

conductivity (KI).

Xylem Density

Xylem density was determined as the dry mass per water saturated volume. Stem
segments approximately 5 cm long and 6-8 mm in diameter were collected adjacent to
those used for determination of vulnerability to xylem cavitation in a prior study

(J acobsen et al. 2007c). Stem segments were split longitudinally and their pith and bark
removed. Xylem segments were then soaked in degassed water adjusted to a pH of 2
overnight and saturated volume was determined using the methods of Hacke et al.
(2000). Samples were then placed in a drying oven at 60°C for four days and their dry

mass determined.

Data analysis

Statistical analyses were preformed using Minitab (Release 14.12.0, Minitab Inc., State
College, PA, USA) and/or Statview (v. 5.0.1, SAS Institute Inc., Cary, NC, USA). Alpha
was set at 0.05 for all comparisons. Differences in minimum and maximum seasonal ‘l’w
and minimum and maximum gs were analyzed among species at a single site and among
sites using AN OVAs followed by Bonferroni/Dunn post-hoc analyses when appropriate.
Seasonal changes in ‘I’w and g8 were analyzed using repeated measures AN OVAs

followed by Bonferroni/Dunn post-hoc analyses when appropriate.

74

Linear regression models were used to analyze the within and among species
relationships between gS and ll’W and ANOVAs were used to examine differences in the
slopes and intercepts of these regressions among species and sites. Linear regressions
were also used to examine the relationship between these seasonal measures and SLA, K1,
K5, ‘1’50, and xylem density.

A principle components analysis was used to examine differences among the
suites of xylem traits used by species and communities. Minimum seasonal water
potential (mean), ‘1’50, Ks, and xylem density were included in this analysis. A MANOVA
was used to determine if communities differed in the relationships among these multiple
traits.

The phylogeny used for phylogenetic independent contrast (PIC) calculations was
constructed based on the relationships among families and species reported in recent
molecular—based published phylogenies (Morgan et al. 1994; Bayer & Starr 1998; Hardig
et al. 2000; Goertzen et al. 2003; Hilu et al. 2003; Urbatsch et al. 2003; Soltis & Soltis
2004; Soltis et al. 2005). Contrasts were calculated using COMPARE (Martins 2004)
and linear regressions were used to examine the relationship between SLA, K1, K5, ‘P50,
and xylem density contrasts pooled across communities. Correlations among PICS were
similarly signiﬁcant or non-signiﬁcant to correlations among raw trait values in most
cases; therefore, only correlations of raw trait values, which have more easily
interpretable values, are discussed in the Results. There was only one case in which the

raw trait correlation and PICS correlation did not agree and this is discussed below.

75

Results

Weather

Spring rains occurred across all sites from February 2006 though May 2006 (Figure 3.1).
The summer rainless period began in June 2006 and extended through September 2006
for the Mojave Desert and through October 2006 for the Chaparral and coastal sage scrub
at which time a few small precipitation events occurred (< 10 mm). Substantial rain did
not fall at the sites until the months of December 2006 and January 2007 when several
precipitation events (> 20 mm) occurred across the sites. Rainfall during the 2005 to
2006 rainy season was 510 mm for the Chaparral site, 460 mm for the coastal sage scrub
site, and 230 mm for the Mojave Desert site. Rainfall for the 2006 to 2007 rainy season
was considerably lower and was 130, 80, and 100 mm for the Chaparral, coastal sage, and

Mojave Desert sites, respectively.

Seasonal water potential

All Chaparral, coastal sage, and Mojave Desert species experienced signiﬁcant changes in
their water potential over the course of this study (Figure 3.2; P < 0.05 for all). Chaparral
species reached their maximum ‘l‘w (81%”) during the wet season in February, April, or
May 2006. Most Chaparral species reached their minimum ‘l’w (mein) during the dry
season in August, October, or November 2006. Rhus ovata differed from these species in
reaching its ‘I’wmm during the wet winter months (February 2007). All coastal sage scrub
species experienced their ‘l’wnm during the wet season in April 2006. Most coastal sage
scrub species experienced their ‘l’wmjn at the end of the summer dry season in October and

November 2006. Only one species experienced its seasonal low during the winter cool

76

period, M. laurina (February 2007). Most Mojave Desert scrub species reached their
‘I'wm during the wet season in April and May 2006 and January and February 2007.
Lepidospartum squamatum differed from these species in displaying its ‘l’wmx during the
dry summer period (August 2006). Most species reached their ‘Pwmin during the dry
summer season in July, August, and September 2006. However, a few species displayed
seasonal lows during the wet winter months of January 2007 (H. salsola), February 2007
(L. andersonii), and March 2007 (C. ramosissima).

The average monthly ‘I’wm occurred in the coastal sage scrub and Mojave Desert
scrub in April 2006 and in the Chaparral in May 2006 (Figure 3.2). The three sites
differed in their ‘Pwm (Figure 3.3; P < 0.001) with the Chaparral and coastal sage scrub
species experiencing signiﬁcantly less negative water potentials than the Mojave Desert
species (P < 0.001 for both). The Chaparral species and coastal sage scrub species did not
signiﬁcantly differ in their ‘I’wmax (P = 0.723).

The average monthly minimum water potential (Twin) occurred in the Chaparral
and coastal sage scrub in November 2006 and in the Mojave Desert in September 2006

(Figure 3.2). There was no difference among sites in ‘Pwmin (Figure 3.3; P = 0.376).

Seasonal stomatal conductance

All Chaparral and coastal sage species experienced signiﬁcant changes in their stomatal
conductance (gs) over the course of this study (Figure 3.2; P < 0.05 for all). All of the
Chaparral species experienced their maximum 38 (gsm) in the spring in April and May
2006. Several species displayed their minimum gS (85min) during the end at the end of the

summer dry period in November 2006 (A. glandulosa, C. cuneatus, C. megacarpus, C.

77

oliganthus, and C. spinosus). Several other species displayed their gsmin in February (R.
ovata) and April 2007 (A. fasciculatum, M. laurina, and Q. berberidifolia). All of the
coastal sage scrub species displayed their gmIx during the spring season during April,
May, and June 2006. Several coastal sage scrub species experienced their 85min at the end
of the summer dry season in November 2006 (A. califomica, L. scoparius, S. leucophylla,
and S. mellifera). However, several other species did not experience their gsmin until
February (E. califomica and M. laurina) and April 2007 (E. cinereum, H. squarrosa, and
M. fasciculatus).

Stomatal conductance for the Mojave Desert species A. dumosa and L. andersonii
did not change signiﬁcantly over the course of this study (Figure 3.2; P = 0.449 and
0.052, respectively) although this includes only two months of data from L. andersonii
due to it being fully drought deciduous. For the remaining Mojave Desert species, gs
- underwent signiﬁcant seasonal change (Figure 3.2; P < 0.001 for all). Most species
reached their gsmax in the wet spring season in April 2006 (A. canescens, C. ramosissima,
and L. tridentata) and May 2006 (H. salsola and G. microcephala). However, several
species reached their gsm later in the dry season including A. polycarpa (August 2006),
I. arborea (November 2006), and L squamatum (November 2006). All species reached
their gsmin during the cool winter months in December 2006 (G. microcephala), January
2007 (C. ramosissima, H. salsola, I. arborea, and L. tridentata), and March 2007 (A.
canescens, A. polycarpa, and L. squamatum).

The average monthly high stomatal conductance (gsm) occurred in the coastal
sage scrub and Mojave Desert scrub in April 2006 but was delayed in the Chaparral until

May 2006 (Figure 3.2). These months also coincided with the average monthly high

78

water potentials across sites; however ‘Pwm is not correlated with gsmax either within or
across communities (P > 0.05 for all). The three sites differed in their gsmax (Figure 3.4;
P = 0.007) with the coastal sage scrub species experiencing signiﬁcantly greater gsmax
than the Chaparral or Mojave Desert species (P = 0.019 and 0.002 for coastal sage
compared to the Chaparral and Mojave Desert, respectively). Chaparral and Mojave
Desert species did not signiﬁcantly differ in their gsmax (P = 0.425).

The average monthly minimum stomatal conductance (gsmrn) occurred in the
Chaparral and coastal sage scrub in April 2007 and in the Mojave Desert in January 2007

(Figure 3.2). There was no difference among sites in gsmin (P = 0.267).

Water potential and stomatal conductance

Among the different sites, the relationship between ‘Pw and g8 varied (Figure 3.5; P <
0.001 for both slopes and intercepts across communities). For the Chaparral and coastal
sage scrub, ‘Pw was correlated to gs pooled across species (P < 0.001 for both, 1'2 = 0.27
and 0.22, respectively); however, there was no relationship between ‘I’w and g8 pooled
across species from the Mojave Desert (P = 0.132). Species from the coastal sage scrub
had a signiﬁcantly greater slope (64.89 :I: 13.49) than either the Chaparral (27.08 :1: 4.60)
or the Mojave Desert scrub species (12.07 i 6.18) (Figure 3.5; P = 0.007 and 0.001 for
the coastal sage scrub compared to the Chaparral and Mojave desert scrub, respectively).
Species from the Chaparral and Mojave Desert did not differ signiﬁcantly in their slopes
of T“, and g8 pooled across species (P = 0.264). Species from the coastal sage scrub also
had a signiﬁcantly greater intercepts (273.77 :I: 40.36) than either the Chaparral (141.54 :1:

13.67) or the Mojave Desert scrub species (106.56 :1: 29.91) (Figure 3.5; P = 0.004 and

79

0.001 for the coastal sage scrub compared to the Chaparral and Mojave desert scrub,
respectively). Species from the Chaparral and Mojave Desert did not differ signiﬁcantly

in their intercepts (Figure 3.5; P = 0.452).

Speciﬁc Leaf Area

Speciﬁc leaf area (SLA) was different among sites (P = 0.014) with the coastal sage
having signiﬁcantly higher SLA compared to the Chaparral (P = 0.004) and the Mojave
Desert scrub (P = 0.047). Speciﬁc leaf area was not different between the Chaparral and
Mojave Desert scrub (P = 0.321). Speciﬁc leaf area of species was not correlated with
‘Pwmax, ‘I’wmrn, K5, K1, or gsmin either within or across communities (P > 0.05 for all; data
not shown). Speciﬁc leaf area was also not correlated with gsmax across communities (P >
0.05 for all; data not shown); however, SLA was correlated with gsmax among Mojave
Desert species (P = 0.016, r2 = 0.59; data not shown) such that species with lower SLA
also had lower gsmax. Speciﬁc leaf area was not correlated with gsmax among species in

either Chaparral or coastal sage scrub communities (P > 0.05 for both; data not shown).

Xylem density

Xylem density was signiﬁcantly different among the sites (P = 0.007) with the Mojave
Desert scrub having signiﬁcantly denser xylem than the Chaparral (P = 0.035) or coastal
sage scrub (P = 0.002). Xylem density was not different between the coastal sage and
Chaparral (P = 0.215). Xylem density was correlated with ‘1’me and ‘l’wmin when pooled
across communities such that species with denser xylem had more negative ‘1’me and

mm... (Figure 3.6; P < 0.001, r2 = 0.52 for WW”... and P = 0.012, r2 = 0.21 for L11mm).

80

Xylem density was not correlated with ‘l’wmax and ‘Pwmm within individual communities
(P > 0.05 for all). Xylem density was correlated with gsmax across communities such that
species with denser xylem had lower maximum stomatal conductance (P = 0.046, r2 =
0.14; data not shown). Xylem density was not correlated to gsmax within communities (P
> 0.05 for all; data not shown). Xylem density was not correlated to gsmin within or

across communities (P > 0.05 for all; data not shown).

Hydraulic conductivity
Xylem speciﬁc conductivity (KS) did not differ among the three communities (P = 0.107;
sec J acobsen et al. 2007c). Xylem speciﬁc conductivity was correlated with ‘I’wm (P <
0.001, r2 = 0.46; data not shown) across communities and within the coastal sage scrub
(P = 0.036, r2 = 0.55; data not shown) such that species with greater KS experienced
higher ‘Pwm. Xylem speciﬁc conductivity was not correlated with ‘Pwmax among species
within the Chaparral or Mojave Desert communities (P > 0.05 for both). Xylem speciﬁc
conductivity was also not correlated with ‘Pwm, gsmax, or gsmin within or across
communities (P > 0.05 for all; data not shown); however, Ks was correlated with ‘I’wmin
when data were analyzed using phylogenetic independent contrasts (P = 0.039).

Leaf speciﬁc conductivity (K.) was correlated with gsmax (P = 0.004, r2 = 0.337,
data not shown) and gsmjn (P = 0.030, r2 = 0.206; not shown) across communities such
that species with great Kl displayed higher gsmax or gsmin- The K. was not signiﬁcantly

different among communities (P = 0.227, data not shown).

81

Xylem vulnerability to cavitation

The xylem and leaf traits included in the present study were not generally good predictors
of species vulnerability to xylem cavitation. In contrast, minimum seasonal ‘1’“, was
predictive of resistance to water stress induced cavitation (T50) across communities
(Figure 3.7; P = 0.013, 12 = 0.22) and within the chaparral community (Figure 3.7; P =
0.013, r2 = 0.56) but not within the coastal sage or Mojave Desert communities (P =
0.461 and 0.773, respectively). Other traits included in the present study, including
‘I’wm, gsm, gsmin, SLA, xylem density, and Ks, were not predictive of Wm either across
or within communities (P > 0.05 for all; data not shown) with one exception. Minimum
gS was predictive of ‘P50 within the coastal sage scrub community with species
experiencing lower gsmin also having more negative ‘1’50 (P = 0.032; r2 = 0.50; data not

shown).

Water use “strategies ”

Communities differed in the suites of xylem traits utilized by species (P = 0.006). A
principle components analysis resulted in two components (P < 0.001, Fig. 3.8).
Component I explained 56.2 % of species variability and was associated mainly with
mein. K3, and xylem density. Component 2 explained 22.9% of species variability and
was associated mainly with ‘1’50. Species from the chaparral, coastal sage, and Mojave
Desert communities occupy largely non-overlapping areas when the species values of
these components are graphed, consistent with a signiﬁcant difference between these

communities in multivariate strategies utilized by species (Fig. 3.8).

82

Discussion

Among shrub species occurring in three different winter rainfall plant communities of
southern California, plants experienced similar patterns in their seasonal water status and
stomatal conductance (gs) such that across sites species tended to reach their seasonal
high water potentials (WWW) and maximum gS (gsmax) in spring during the wet season.
Species tended to reach their seasonal low water potentials (Twin) at the end of the dry
season and seasonal low gs (gsmin) during the cool winter months. This matches the
annual precipitation and temperature pattern for these sites and indicates that species are
responding similarly to rainfall events and that cooler winter temperatures may limit gas
exchange in Californian winter rainfall communities.

Several species from each of the three sites deviated from these average patterns
of seasonal water status illustrating phenological diversity among species. These
included R. ovata, M. laurina, H. salsola, L. andersonii, and C. ramosissima which
reached their minimum seasonal water potentials (Twin) during the winter wet season in
2007. This pattern has been described previously for R. ovata (Pratt et al. 2005) and is
likely caused by high winter embolism in the stems of this species which reduces water
supply to leaves. However, below ground factors may be involved in other species,
including root phenology and soil moisture distribution. Lepidospartum squamatum
differed from other species in displaying its maximum seasonal water potential (meu)
during the dry summer period (August). The range of this species extends into summer
rainfall regions and this species appears to be tuned to a summer rainfall regime. A

similar pattern was also evident in the Mojave Desert shrub C. ramosissima which was

83

able to rapidly respond to a small late summer rain pulse in the present study but which
slowly responded to a pulse of winter rain. This pattern has been previously described
for this species (Lin et al. 1996; Gebauer & Ehleringer 2000).

While across sites species tended to respond similarly to seasonal changes in
precipitation, plant water status varied signiﬁcantly among the sites during the wet
season. Species in the chaparral and coastal sage scrub experienced similarly high ‘I’wm
while species from the Mojave Desert did not reach similarly high water potentials. This
may be due to lower wet season soil moisture in the Mojave Desert site compared to the
other two sites (J acobsen, unpublished data). Relatively low soil moisture values of
shallow soil layers have been previously reported for the Mojave Desert (Smith et al.
1995; Yoder & Nowak 1999) and comparatively higher values have been reported for the
chaparral (J ohnson-Maynard et al. 2004) suggesting this may be a consistent difference
among these shrub communities. Additionally, desert shrubs may be accessing deeper
soil moisture reserves which are fairly stable and recharge mainly during above average
precipitation years as has been described for the Chihuahuan Desert (Snyder et al. 2006).

During the dry season, ‘l’wmrn was not different among the sites suggesting that
species at these sites are experiencing a common level of water stress. The across species
mean ‘I’Wﬁn was -4.6 MPa. This value is similar to the average ‘l’wmin reported for 26
chaparral species in years of average precipitation (J acobsen et al. 2007b), for 17 species
from the winter rainfall region of South Africa (J acobsen et al. 2007b), and for 6 species
from the Great Basin Desert (Hacke et al. 2000). This suggests this ‘I’wmm may represent
a common physiological limit of arid and semi-arid shrub communities. This is also

consistent with a mean cavitation resistance (W50) of approximately -4 to -5 MPa which

84

has been found across Mediterranean—type and Desert ecosystems (Hacke et al. 2000;
Maherali et al. 2004; J acobsen et al. 2007b).

Minimum ‘I’w was correlated with ‘1’50 with a 1:1 relationship between these traits
for the chaparral species as has been reported in previous studies (Hacke et al. 2000;

J acobsen et al. 2007b; Pratt et al. 2007a); however, there was no correlation among these
traits within the coastal sage scrub or Mojave Desert scrub. This suggests that these
communities may vary considerably in the levels of water stress induced embolism that
they experience seasonally. While chaparral shrubs appear to reach approximately 50%
native embolism seasonally, it appears that shrubs in other arid systems may have
alternative thresholds and may regularly reach signiﬁcantly higher levels of xylem
embolism. Indeed, high seasonal levels of embolism have been reported for species of
the Sonoran Desert (Pockman & Sperry 2000) and for the coastal sage (Hargrave et al.
1994; Kolb & Davis 1994). Thus, while ‘Pwmin and ‘1’50 may be correlated in some
communities it does not appear that these traits are always correlated and Twin may not
be a generally useful predictor of T50 in arid and semi-arid communities as has been
suggested (J acobsen et al. 2007b).

Among these three communities, species displayed differential stomatal
sensitivity to water stress with the relationship between ‘Pw and g8 signiﬁcantly varying
among communities. Among coastal sage scrub species, gS declined rapidly with
declining ‘1’... suggesting high stomatal sensitivity to water stress. Consistent with our
predictions, the chaparral had a much shallower slope between g5 and WW when compared

to the coastal sage scrub species. This implies that chaparral species, which have stem

85

xylem that is more resistant to cavitation, can tolerant greater declines in ‘l’w before
limiting stomatal gas exchange.

In contrast to these ﬁrst two communities, on average, species from the Mojave
Desert scrub showed no change in gs in response to changes in ‘Pw when data were pooled
across species. This suggests that these species do not alter their stomatal conductance in
response to water stress and that they may be using alternative strategies to limit water
loss. However, it should be noted that while this is the general pattern across species
there are some species from the Desert community that displayed rather sensitive
stomatal responses. For instance, both Coleogyne ramosissima and Larrea tridentata
displayed relatively steep declines in stomatal conductance with declining water potential
(Figure 3.5 C; medium dashed line for C. ramosissima and dotted line for L. tridentata).
Many of the Mojave Desert scrub species may be reducing total leaf area rather than
reducing water loss through individual leaves. Indeed, during the course of the present
study individuals of many desert species reduced their leaf area, although only one
species (L. andersonii) is completely deciduous and lost all of its leaves. This pattern of
leaf drop as a means of regulating whole plant stomatal conductance appeared most
pronounced in Ambrosia dumosa. In this species, stomatal conductance increased as
water potential declined largely as a result of reduced leaf area which likely increased the
water supply to individual leaves even though whole plant water status was reduced
(Figure 3.5 C solid line). Signiﬁcant leaf drop during drought has been described
previously in desert shrubs during the dry season (Smith et al. 1995).

Consistent with the idea that species in these three communities are employing

different suites of traits in response to water stress, species appear to be differentially

86

adjusting leaf area to maintain similar dry season K. and 39, in response differences in
cavitation resistance and therefore seasonal embolism. Stomatal conductivity was
correlated with K. when pooled across sites, with species with greater K. displaying
greater gm... and gs...ax consistent with previously reported correlations between K. and 3S
(Sperry 2000; Santiago et al. 2004). Additionally, dry season K. and gsmin were not
different among sites suggesting that perhaps there is a common minimum hydraulic ﬂow
which much be sustained in order to maintain evergreen leaves in arid and semi-arid
environments. This is consistent with the greater level of leaf drop observed in the
coastal sage and Mojave Desert communities concomitant with their greater susceptibility
to cavitation and presumably higher levels of dry season embolism. Coastal sage scrub
species displayed signiﬁcantly higher gsm than the other two communities which may
partially result from their high stomatal sensitivity to changes in water status. Xylem
speciﬁc conductivity was not correlated with most water relations and leaf traits,
including ‘Pso, Ks, K., and g8 ; however, across sites ‘I’wm and Ks were correlated.

Thus, species among these three sites are divergent in their functional traits
related to available water resources. The pattern of water use displayed by the coastal
sage scrub species is consistent with adaptation to utilize shallow temporarily available
water (Schwinning & Ehleringer 2001). Coastal sage scrub species tend to have shallow
roots (Hellmers et al. 1955) and display signiﬁcantly higher wet seasonal gs than species
in the other two sites, and have high stomatal sensitivity to plant water status. In contrast,
shrub species from the desert likely have deeper root systems (Gibbens & Lenz 2001),
have low maximum stomatal conductivity, and have low stomatal sensitivity to plant

water status consistent with a strategy of tapping mostly deeper soil moisture reserves

87

(Schwinning & Ehleringer 2001). Chaparral shrub species are a blend of these two
extremes with species exhibiting both deep and shallow rooting systems (Cooper 1922;
Hellmers et al. 1955), intermediate stomatal sensitivity to water stress (Poole & Miller
1975), and low maximum stomatal conductivity not signiﬁcantly different from that of
the Mojave Desert species. Recent work has shown that deep and shallow water use
strategies are linked with life history type in the chaparral (Pratt et al. 2007b). Species
that are utilizing suites of traits that occur in overlapping areas between communities (see
Fig. 3.8) tend to be species with broad ranges that occur across communities, suggesting
there are certain suites of traits that may be successful in many communities.

Speciﬁc leaf area (SLA) does not correlate well with plant functional traits among
these arid shrub species. SLA was different among the sites, with the coastal sage scrub
species having signiﬁcantly higher SLA compared to the chaparral and Mojave Desert
scrub. However, SLA was highly variable among species within a site suggesting lack of
convergence to a single SLA within these environments. Additionally, SLA was not
correlated with water relations or leaf traits including, ‘1’50, ‘Pwmax, ‘Pwmin, Ks, K., and g8
and thus was not useful as a predictor of these physiological traits. SLA is likely
correlated to other plant traits not included in the present study such as leaf life span and
photosynthetic capacity (Ackerly 2004; Poorter & Bongers 2006; Gulr’as et al. 2003) or
may be responding to microsite differences in nutrient availability (Wright et al. 2002).

The strong relationship between seasonal water potential and xylem density
among data pooled across communities suggests that xylem density may indeed be a
useful tool in categorizing plant functional strategies and plant functional variation both

across broad regions and within communities (cf Ackerly et al. 2004; Preston et al.

88

2006; Swenson & Enquist 2007). Xylem density was strongly correlated with ‘l’wmax and
‘l’wm... across communities with species having denser xylem displaying more negative
‘Pwma.x and ‘Pwmm. Xylem density was also correlated with gs".ax across communities such
that species with denser xylem had lower maximum stomatal conductance.

The ‘Pwmm that plants experienced was a better predictor of xylem traits than
xylem cavitation resistance (W50). Additionally, xylem density was not predictive of
xylem cavitation resistance (9’50) within any of the three plant communities examined
contrary to what has been found in other studies (Hacke et al. 2001a; J acobsen et al.
2007b). This may be due to the 1:1 relationship between T5.) and ‘I’wm... found in these
prior studies. In the present study where ‘13.. and ‘Pwm... are not correlated or are
correlated in a non-1:1 relationship, xylem density appears to be non-predictive of
cavitation resistance (Pratt & Black 2006). This suggests that xylem density should not
be used to predict cavitation resistance in communities unless the relationship between
‘Pso and ‘l’wm... has been determined. In contrast, the strong correlation between ‘l’wm... and
xylem density suggests that these traits may be functionally related and predictive of one
another. This is supported by previous studies that have found these traits to be related
(Hacke et al. 2000; Ackerly 2004; J acobsen et al. 2007a, J acobsen et al. 2007b). This
relationship may be useful in development of global plant functional trait models.

Arid shrub communities appear divergent in their adaptation to water stress even
though they experience similar levels of water stress with a community level average
‘I’wmm of approximately -4.6 MPa. The relationship between TM“... and ‘1150 appears to be
community speciﬁc and may be related to differential ability of species to tolerate or

avoid high seasonal levels of embolism. The relationship between gS and ‘1’... also appears

89

to be community speciﬁc and may reﬂect differential water use by shrubs in these
communities perhaps in response to different rainfall predictability, soil moisture,
precipitation, or soil nutrients among sites. Trait relationships that are community
speciﬁc in the present study may provide the basis for tests of community convergence; it
may be that shrub communities in some of the other Mediterranean-type climate regions
worldwide display similar relationships as those found in the three communities sampled

in the present study.

90

Table 3.1. Species listed by vegetation type, family, species code, cavitation resistance
(W50), xylem speciﬁc conductivity (Ks), speciﬁc leaf area (SLA), and xylem density for
28 shrub species from three sites in southern California.

 

 

 

 

 

 

Vegetation type and Species Family Species C°d°
Chaparral

Adenostomafasciculatum Hook. & Am. Rosaceae Af
Adenostoma sparsifolium Torrey Rosaceae As
Arctostaphylos glandulosa Eastw. Ericaceae Ag
Ceanothus cuneatus (Hook.) Nutt. Rhamnaceae Cc
Ceanothus megacarpus Nutt. Rhamnaceae Cm
Ceanothus oliganthus Nutt. Rhamnaceae Co
Ceanothus spinosus Nutt. Rhamnaceae Cs
Malosma laurina (Nutt.) Abrams Anacardiaceae Ml
Quercus berberidifolia Liebm. Fagaceae Qb
Rhus ovata S. Watson Anacardiaceae Ro
Coastal Sage Scrub

Artemisia califomica Less. Asteraceae Ac
Encelia califomica Nutt. Asteraceae Eca
Eriogonum cinereum Benth. Polygonaceae Eci
Hazardia squarrosa (Hook. & Am.) B. Greene Asteraceae Hs
Lotus scoparius (Nutt.) Ottley Fabaceae Ls
Malacothamnusfasciculatus (Torrey & A. Gray) E. Greene Malvaceae Mf
Malosma laurina (Nutt.) Abrams Anacardiaceae Ml
Salvia leucophylla E. Greene Lamiaceae Sl
Salvia mellifera E. Greene Lamiaceae Sm
Mojave Desert Scrub

Ambrosia dumosa (A. Gray) Payne Asteraceae Ad
Atriplex canescens (Pursh) Nutt. Chenopodiaceae Ac
Atriplex polycarpa (Torrey) S. Watson Chenopodiaceae Ap
Coleogyne ramosissima Torrey Rosaceae Cr
Gutierrezia microcephala (DC.) A. Gray Asteraceae Gm
Hymenoclea salsola A. Gray Asteraceae Hs
Isomeris arborea Nutt. Capparaceae Ia
Larrea tridentata (DC.) Cov. Zygophyllaceae Lt
Lepidospartum squamatum (A. Gray) A. Gray Asteraceae Ls
Lycium andersonii A. Gray Solanaceae La

Note: Data for ‘1’50, Ks, SLA, and xylem density are means :1: 1 SE.
# from Chapter 2; J acobsen et al. 2007c
§ from Chapter 2; J acobsen et al. 2007c

91

Table 3.1 (cont’d).

#

§

 

 

 

 

 

 

qlso Ks SLA Density

-7.33 1 0.45 0.88 1 0.13 5.91 1 0.42 679.3 1 12.8
-4.65 1 0.27 1.55 1 0.19 11.43 1 1.38 619.8 1 10.9
-5.09 1 0.34 1.04 1 0.18 5.20 1 0.29 661.5 1 18.5
-7.19 1 0.58 0.83 1 0.19 4.27 1 0.13 678.1 1 10.4
-6.44 1 0.43 1.91 1 0.27 4.06 1 0.16 638.9 1 11.4
-4.05 1 0.37 1.24 1 0.11 11.06 1 1.23 647.1 1 8.2
4.14 1 0.61 1.33 1 0.21 6.91 1 0.62 614.9 110.8
-0.52 1 0.12 5.55 1 1.05 5.24 1 0.16 496.6 1 16.9
-1.51 1 0.24 1.59 1 0.51 7.38 1 0.37 724.2 1 8.9
-0.56 1 0.07 1.64 1 0.36 4.41 1 0.37 523.1 1 8.9
-2.15 1 0.16 1.21 1 0.20 20.09 1 1.20 685.7 1 14.7
-0.82 1 0.08 1.44 1 0.29 14.01 1 0.47 637.8 1 16.9
-1.9710.18 09310.13 5.411019 67121240
-1.42 1 0.16 0.64 1 0.08 12.26 1 0.59 557.9 1 12.5
-2.34 1 0.25 1.41 1 0.25 15.39 1 0.85 613.7 1 16.7
-0.94 1 0.14 0.77 1 0.13 12.03 1 0.69 571.8 1 19.2
-0.68 1 0.10 4.80 1 1.67 4.41 1 0.18 467.2 1 7.7
-1.70 1 0.07 2.07 1 0.28 12.96 1 1.36 503.1 1 19.1
-2.39 1 0.26 1.50 1 0.21 8.89 1 0.37 528.9 1 10.0
-1.0510.24 0.6510.12 11.691109 7112116.]
-0.97 1 0.17 0.17 1 0.03 4.92 1 0.45 797.8 1 9.9
-1.98 1 0.14 0.36 1 0.05 4.62 1 0.83 810.7 1 10.4
-1.50 1 0.21 0.39 1 0.05 10.57 1 1.35 678.3 1 18.0

no data no data 7.03 1 0.59 647.2 1 10.0
-2.09 1 0.35 1.60 1 0.40 10.75 1 0.84 690.2 1 18.3
-2.51 1 0.23 0.34 1 0.04 8.97 1 0.73 612.6 1 10.7
-3.31 1 0.32 0.63 1 0.10 6.17 1 0.43 854.1 1 8.4
-0.79 1 0.06 1.54 1 0.39 no data 566.1 1 12.0
-1.02 1 0.10 0.60 1 0.16 9.36 1 0.76 706.9 1 16.9

92

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----I Cm _'¢_ HS —0— Gm
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Mojave Desert Scrub

 

 

 

01 m'2 5") Water Potential (M Pa)

 

 

 

 

 

 

 

Date (mmldlyy)

Figure 3.2. Water potential and stomatal conductance (gs) measured approximately
monthly on species from three arid plant communities in southern California. Water
potential was measured on 29 species from February 2006 through April 2007 and gS was
measured on 28 species from April 2006 through April 2007. See Table 3.1 for species
codes. The same symbols are used to represent the same species for water potential and
gS panels for each community. Symbols are species means 1 1 SE (n = 6).

94

Chaparral Coastal Sage Scrub Mojave Desert Scrub
MI As RoQb Al Ag Cs CoCch MI Ls Mf Hs Eci Ac SI EcaSm Ls la Hs La AchAd Ap Ll Cr

 

 

 

 

-2 _- _
a
A a a a a a
a? -4 -*- b b a -
g b b [)0 b
C C
E 0 Cd cd b be be
9"; -6 'L C C Chaparral CSS Mojave d m C -
o c
-8 -r d ~
e d
-10 l l l | l l l I l l l l L L l l l l l l 1
Chaparral Coastal Sage Scrub Mojave Desert Scrub

Ro Cs Cc QmeCoAs Ml Ag Af Sl SmEcaLs Ml Hs Mt Ac Eci Ls la Ap Lf Hs Ad La Cr Ac Lt

 

Chaparral CSS Mojave
-6 - 0 : . ,,

 

 

 

.10 l l l l l l l I I l

 

Figure 3.3. Maximum and minimum water potential (‘I’wmx and ‘Pwmin, respectively)
measured from February 2006 through April 2007 on 28 shrub species from three plant
communities in southern California: chaparral, coastal sage scrub (CSS), and Mojave
Desert scrub. Each black bar represents the lowest or highest monthly value for a species
(mean :t 1 SE; see Table 3.1 for species codes). Different letters below bars indicate
signiﬁcant differences among species within a community. Grey bars in insets represent
means :l: 1 SE across communities and different letters indicate signiﬁcant differences.

95

Chaparral Coastal Sage Scrub Mojave Desert Scrub
Cch Cs Co Ag At Qb MI Flo Ml Ac SmEcaHs Ls SI Eci Ml Lt Hs CerAc Ia Ap Ls Ad La
1 I J I I l l I I I l l I

 

 

 

 

 

500 I I + i‘: JI i i i I i i I I I I i i; I i I l I I I l I I
Chaparral CSS Mojave
400 r r 4

400 -
Ta) 200-
‘t‘
E 300 - a a a
E
E

j
l

V200 "i i
l

 

 

 

 

c
b bC Cd
Chaparral Coastal Sage Scrub Mojave Desert Scrub
Ag Af Ml Flo Cs CchQbCo Ac MI Ls Hs Sm Mf Eci SI Eca Lt ApAchHs Ls Ia Cr Ad La
500'l—lllllll lllllllll li%llli%%t
Chaparral CSS Mojave
400
A 400 e- e r
F”, 200 de e |
c}: de
5 300 -- d . e -
g be de
E c
‘;200 -- cd d «
g b
63’ b be be“
-- ab ‘
a
0 ..

 

 

Figure 3.4. Maximum and minimum stomatal conductance (gsmax and gsmin, respectively)
measured from April 2006 through April 2007 on 27 shrub species from three plant
communities in southern California: chaparral, coastal sage scrub (CSS), and Mojave
Desert scrub. Each black bar represents the highest or lowest monthly value for a species
(mean :t 1 SE; see Table 3.1 for species codes). Different letters below bars indicate
signiﬁcant differences among species within a community. Grey bars in insets represent
means :t 1 SE across communities and different letters indicate signiﬁcant differences.

96

 

 

Chaparral Coastal Sage Scrub Mojave Desert Scrub
b A‘ ﬂ 1 ‘li B. I l I I c. I I I I

  

 

 

 

 

 

 

 

 

 

 

Water Potential (MPa)

Figure 3.5. Water potential as a predictor of stomatal conductance (gs) for 28 species
from three arid plant communities of southern California: chaparral (A and D), coastal
sage (B and E), and Mojave Desert scrub (C and F). Linear regressions were modeled for
each species (A, B, and C) and for each community with data pooled across species (D,
E, and F). Species from the coastal sage scrub had a signiﬁcantly greater slopes and
intercepts when compared to either the chaparral or the Mojave Desert scrub species.
Species from the chaparral and Mojave Desert did not differ signiﬁcantly in their slopes
or intercepts. Within each community, different symbols represent different species. See
Table 3.1 for species codes in Panel C and see Figure 3.2 for species legend for A, B, and
C.

97

 

 

 

 

 

 

 

 

 

O 0
O C Q. C
-2 4 v t”. v _2 _
a. ' H :r.
- -l .. -j
E E
g -6 ' .s -6 a
E 0 Chaparral Bf
9" '3 ‘ 0 Coastal sage scrub '3 ‘ .
v Mojave Desert V
-10 r r r 1 -10 I r r u
400 500 600 700 800 900 400 500 600 700 800 900
Xylem density (kg m'3) Xylem density (kg m'a)

Figure 3.6. Xylem density as a predictor of ‘Pwmax and ‘l’wmin pooled across communities
(P < 0.001, r2 = 0.52 for ‘Pwmax and P = 0.012, r2 = 0.21 for men). Xylem density was
not correlated with ‘Pwmax and Twin within individual communities. Different symbols
indicate data from the different arid plant communities.

98

 

 

all
0“ Chap.
CSS
Majavej
l

 

 

 

 

 

O

‘Pmm (MPa)

Figure 3.7. Minimum seasonal water potential (Twin) as a predictor of resistance to
water stress induced cavitation (W50) pooled across communities. Different symbols
indicate data from a different arid plant community: chaparral (Chap), coastal sage scrub
(CSS), or Mojave Desert scrub (Mojave). Linear regressions were modeled both across
all communities and for each community. Only signiﬁcant regressions are shown (P <
0.05).

99

 

 

 

 

 

2 T _
I’M MI
N
o o -- 0 -
O.
-2 -7 -
{é} Chaparral \gc Cm,’
0 Coastal Sage Scrub ‘ ~~~~~
4 13‘- Mojave Desert Scrub . I
-4 -2 o 2 4

P01

Figure 3.8. Results of a principle component analysis using multiple traits measured on
species occurring in three shrub communities of the winter rainfall area of southern
California. Component 1 (PCI) is strongly associated with water relations traits
including minimum seasonal water potential (Wu/min). xylem density, and xylem speciﬁc
conductivity (Ks) such that species with higher values have greater Ks, lower xylem
density, and higher (less negative) ‘Pwmin. Component 2 (PC2) is strongly associated with
water stress tolerance (W50), such that higher values are less resistant to cavitation (i.e.
have higher W50). The suites of traits utilized by each community signiﬁcantly differ (P =
0.006). Each symbol represents a different community and species codes are shown in
Table 3.1.

100

CHAPTER FOUR

PHYLOGENETIC DISPERSION AND COMMUNITY STRUCTURE IN THREE

ARID PLANT COMMUNITIES

Abstract

The phylogenetic relationships among species have the potential to inﬂuence community
assemblages and community structure. Communities that are the product of
environmental ﬁltering will likely contain species that are more closely related than
randomly constructed communities, while communities that are biotically shaped through
competitive interactions will likely contain species that are more distantly related than
randomly constructed communities. These patterns rely on the assumption that more
closely related species display more similar functional traits compared to distantly related
species. Using woody shrub species from three arid communities of southern California,
including the chaparral, coastal sage, and Mojave Desert scrub, I examined whether
functional traits related to water stress tolerance and water use were indeed more similar
among more closely related species. Additionally, I examined whether phylogenetic
relationships among species inﬂuence species distributions among and within these
communities (at the B and a scales, respectively). At the a level, I examined what
functional traits may be associated with species co-occurrence in each community. The
three communities examined in this study differed in their species compositions and stand
structures, yet they all tended to be composed of species assemblages that were more

closely related than expected. This suggests that species were “ﬁltered” into these

101

communities based on preexisting functional traits and that in these stressful arid
environments species persistence at the B scale is likely related to traits conserved within
certain lineages. Minimum seasonal water potential (mein) was signiﬁcantly correlated
with phylogeny and may be related to phylogenetically linked traits important for species
persistence in these communities (P = 0.001). Within communities, at the a scale,
phylogeny was unrelated to species co-occurrence, perhaps because the traits associated
with co-occurrence and niche segregation within communities are phylogenetically labile.
Traits that varied independent of phylogeny in the present study and which were
correlated with species co-occurrence within some communities included water potential
at 50% loss in hydraulic conductivity for the coastal sage and stomatal conductance,
xylem speciﬁc conductivity, and xylem density for the Mojave Desert. Frequent co-
occurrence of conspeciﬁcs within stands, particularly in the chaparral, and of species
displaying similar functional traits, in the Mojave Desert and coastal sage scrub, suggests
that habitat heterogeneity or dispersal limitation may inﬂuence within community species

distributions.

Introduction

In arid communities competition for water is likely one of the key community structuring
processes and likely inﬂuences within community interactions (Flores-Martinez er al.
1998; Vila & Sardans 1999). Water use differences among species may be involved in
community assembly and may facilitate species co-occurrence within communities.
Functional traits related to water use and water stress tolerance may also inﬂuence

species distribution and abundance within a community.

102

Among 28 shrub species from three arid plant communities in southern
California, including the chaparral, coastal sage scrub, and Mojave Desert scrub, species
display great variation in water use and response to water stress (Harrison et al. 1971.;
Poole & Miller 1975; Smith et al. 1995; J acobsen et al. 2007c; Chapter 3). This
divergence in species response includes considerable within and between community
variation in species resistance to water stress induced cavitation (J acobsen et al. 2007c),
water potential (Chapter 3), and stomatal response (Chapter 3). Among these
communities, community speciﬁc traits and trait relationships may reﬂect selective
ﬁltering of species during community assembly. That is, only species and lineages with
certain traits or suites of traits were able to persist within a speciﬁc community. Within
communities, variation among species in these traits may be related to niche segregation
and interspeciﬁc partitioning of available resources.

More closely related species likely share more functional traits than distantly
related species (Webb et al. 2002; Swenson et al. 2007) leading to predictions of
phylogenetic structuring both between and within communities (at the B and a scales,
respectively). At the community ([3) level, presence of a functional trait that allows for
persistence of a lineage in a given environment may lead to environmental ﬁltering of
these species. Thus, communities assembled through ﬁltering would be composed of
species that are more closely related than would occur in randomly assembled
communities (i. e. phylogenetic under-dispersion). Patterns of phylogenetic under-
dispersion have been found previously among bacterial communities (Homer-Devine &
Bohannan 2006), a neotroprical forest tree community (Kembel & Hubbe112006),

tropical insect herbivores (Weiblen er al. 2006), and among diverse Floridian plant

103

communities (Cavender-Bares et al. 2006). Alternatively, functionally similar species
could competitively exclude one another (Hardin 1960), leading to communities being
composed of species that are more distantly related than would occur in randomly
assembled communities (1'. e. phylogenetic over-dispersion). Phylogenetic over-
dispersion has been described in Floridian oak communities (Cavender-Bares er al. 2004)
and among Adenostoma species occurring in southern California (Beatty 1987). Both
environmental ﬁltering and competitive exclusion could operate to create community
level ([3 scale) species assemblages. Within communities, at the a scale, these same
processes can create similar patterns. In an under-dispersed community, more closely
related species are more likely to occur near one another whereas in an over-dispersed
community, more distantly related species are more likely to occur near one another.

We examined whether, at the community scale, functional traits of species
relating to water stress tolerance and water use were correlated with species phylogenetic
relationships. Additionally, we examined whether arid communities displayed evidence
of the processes of ﬁltering or competitive exclusion in their community composition.
We predicted that ﬁltering would be more important than competition in these
communities based on the work of Grime (1977) in which it is suggested that competition
may be less important in stressful environments (see also Goldberg & Novoplansky
1997). Thus, we would expect phylogenetic under-dispersion among species in these
communities if the traits related to persistence within the community are phylogenetically
constrained. We also examined whether the phylogenetic relationships among species
relates to the distribution of species within these communities. We predicted

phylogenetic over-dispersion within communities, consistent with what has been found in

104

prior studies (Beatty 1987; Cavender-Bares et al. 2006; Swenson er al. 2006) although
other phylogenetic patterns have also been found within communities (Homer-Devine &
Bohannan 2006; Kembel & Hubbel 2006). We used published values for various
physiological and functional traits for the species included in the present study (J acobsen
et al. 2007c; Chapter 3) to determine which traits may be correlated with species
distributions within communities (Redtfeldt & Davis 1996).

We examined the dominant woody shrub species occurring at sites in each of
these communities. We focused on woody plant species because these species are of
similar form and habit and would likely occupy relatively similar niches and they are the

dominant plants in these communities.

Materials and Methods
The dominant woody shrub species in each of three aridland plant communities located in
the winter-rainfall region of southern California were sampled. These three sites
included a chaparral site where 10 woody plant species were dominant, a coastal sage
scrub site where 9 woody plant species were dominant, and a Mojave Desert scrub
community where 10 woody plant species were dominant (see Table 4.1 for species
names). These species accounted for 89, 99, and 73 % of the woody plants in each
community, respectively. The location of these sites is described in J acobsen et al.
(2007c).

At each site, woody shrub species were sampled using a modiﬁed point-quarter
sampling method (Cox 1985). Fifty-four to 60 points were established at each site using

six randomly chosen individuals of each of the dominant woody species at each site as

105

points. At each point, the distance from the central plant to the nearest plant in each of
four quadrants was measured and the species identiﬁed. By this analysis a plant had four
neighbors but only one nearest neighbor. For each of the ﬁve plants at each point, the
basal diameter, crown diameter, and crown height were measured. The percentage of co-
occurrence of species within each site was calculated as the percentage that species were
neighbors in any of the four quadrants measured at each point and also as the percentage
that species occurred as nearest neighbors irrespective of quadrant. AN OVAs were used
to test for differences in these traits among species and communities. These data were
also divided into cases in which the neighbors or nearest neighbors were conspeciﬁc or
heterospeciﬁc. The expected counts of conspeciﬁc and heterospeciﬁc co-occurrence
were predicted based on species abundance within each community and random species
distribution within the community. A chi-squared test was then used to determine if the
actual co—occurrence of conspeciﬁcs and heterospeciﬁcs were different than predicted
values.

Phylogenetic relationships among species were established using published
phylogenetic data (Figure 4.1). The phylogeny was constructed using recent molecular-
based phylogenies (Morgan et al. 1994; Bayer & Starr 1998; Hardig et al. 2000; Goertzen
et al. 2003; Hilu et al. 2003; Urbatsch er al. 2003; Soltis & Soltis 2004; Soltis et al.
2005). Since we combined several trees to create this phylogeny we lacked branch length
information; therefore, all analyses were run assuming equal branch lengths (Ackerly
2000). The phylogenetic distances between species pairs were determined based on the
number of steps between each pair. More closely related species pairs have fewer steps

between them (small phylogenetic distance), whereas distantly related species have more

106

steps between them (greater phylogenetic distance). The maximum phylogenetic
distance in our study was 15. Individuals of the same species would have the minimum
phylogenetic distance (zero).

To examine phylogenetic dispersion among communities, phylogenetic distances
were calculated between all of the species examined in the present study. From the pool
of 28 studied species, species were randomly selected to create hypothetical communities
each containing 10 species (n = 1000 randomly assembled communities). Phylogenetic
distances among species were calculated for these randomly assembled communities and
community average phylogenetic distances determined. Community average
phylogenetic distances for the three communities examined in the present study were then
compared to the distribution of mean phylogenetic distance values from the randomly
assembled communities.

To examine phylogenetic dispersion within communities, phylogenetic distances
among species pairs within each community were correlated to the percentage species co-
occurrence within each community. We also used published trait values (Chapter 3;

J acobsen et al. 2007c) to examine if co-occurrence within communities was correlated
with species differences in several physiological and functional species traits. The traits
included differences among species pairs in minimum and maximum seasonal water
potential (A ‘Pwmin and A WWW), water potential at 50% loss in hydraulic conductivity (A
W50), minimum and maximum stomatal conductance (A gm,ax and A gsmin), xylem density
(A density), speciﬁc leaf area (A SLA), and xylem speciﬁc conductivity (A K.,) among
species pairs. All statistical analyses were run using Minitab (Release 14.120, Minitab

Inc., State College, PA, USA) and the alpha-level was set at 0.05.

107

Results

Community structure

Within each community the height, crown diameter, and basal diameter of species varied
signiﬁcantly (Table 4.1). Overall, chaparral species were taller and had greater crown
diameters relative to the other two communities (Table 4.2). The distance between plants
was not different among the chaparral and coastal sage communities although crown
overlap was greater in the chaparral due to their signiﬁcantly wider crown diameters.
Individuals occurring at the Mojave Desert site were further apart than in the other two
communities and this, combined with their smaller canopy sizes, resulted in an open

canopy (Table 4.2).

Community assemblages

Among communities, the chaparral community was phylogenetically under-dispersed
compared to the phylogenetic dispersion of randomly generated communities (based on
95% conﬁdence interval; Figure 4.2). The coastal sage and Mojave Desert scrub
communities were not different in their phylogenetic dispersion from randomly generated

communities (Figure 4.2).

Conspeciﬁc occurrence
Within each of the three communities, there were more conspeciﬁc neighbors than
predicted based on species abundances in the community (Table 4.3). When only nearest

neighbors were considered, chaparral species remained more likely to be nearest a

108

conspeciﬁc than predicted, while coastal sage and Mojave Desert scrub species were not

more likely to be nearest a conspeciﬁc than predicted (Table 4.3).

Species distributions within communities

The percent co-occurrence among more closely related individuals increased when
conspeciﬁcs were included in analyses (Figure 4.3 A, B, C; P < 0.001 for the chaparral, P
= 0.023 for the coastal sage, and P = 0.014 for the Mojave Desert). This relationship is
also signiﬁcant among chaparral and Mojave Desert species when only nearest neighbors
are included in the analysis (Figure 4.3 A, B, C; P < 0.001 for the chaparral, P > 0.05 for
the coastal sage, and P = 0.003 for the Mojave Desert). When conspeciﬁcs were
excluded from analyses, there was no relationship between either neighbor or nearest
neighbor co-occurrence and phylogenetic distance in any of the three communities

(Figure 4.3 D, E, F; P > 0.05 for all).

Functional traits and phylogeny

Only one trait of those examined, A ‘I’wmin was correlated with phylogenetic distance
among species (P = 0.001), such that more closely related species had more similar
‘l’wmin. All other functional traits included in the present study, including A ‘Pso, A ‘I’wmax,
A gsmax, A gsmin, A xylem density, A SLA, and A Ks varied independently of phylogenetic

distance (P > 0.05 for all).

109

Functional traits and species co-occurrence
Within the chaparral community, there was no correlation between differences among
species pairs in any of the traits included in the present study, including A ‘1’50, A ‘I’wmin, A
‘Pwm, A gsmax, A gsmin, A xylem density, A SLA, and A Ks and the percentage co-
occurrence of those species either as neighbors or nearest neighbors (P > 0.05 for all).
Within the coastal sage scrub community, A ‘I’wmm was correlated with co-
occurrence as neighbors and nearest neighbors (Figure 4.4 A; r2 = 0.146, P = 0.022 for
neighbors and r2 = 0.166, P = 0.014 for nearest neighbors). Differences between species
in ‘I’so were also correlated with occurring as neighbors and nearest neighbors (Figure 4.4
B; r2 = 0.15, P = 0.020 for neighbors and r2 = 0.107, P = 0.05 for nearest neighbors). For
both ‘Pwmin and ‘P50 the species that showed the greatest differences in these traits were
less likely to occur near one another. All other traits included in the present study were
not correlated with co-occurrence in the coastal sage scrub community (P > 0.05 for all).
Within the Mojave Desert scrub community, A density was correlated with co-
occurrence as neighbors and nearest neighbors (Figure 4.4 C; r2 = 0.099, P = 0.035 for
neighbors and r2 = 0.114, P = 0.023 for nearest neighbors). Differences between species
in gsm were also correlated with occurring as neighbors and nearest neighbors (Figure
4.4 D; r2 = 0.094, P = 0.041for neighbors and :2 = 0.091, P = 0.044 for nearest
neighbors). For both gsm and xylem density the species that showed the greatest
differences in these traits were less likely to occur near one another. In contrast, A K8
was correlated with co-occurrence as neighbors and nearest neighbors (Figure 4.4 E; r2 =
0.221, P = 0.001 for neighbors and 12 = 0.198, P = 0.002 for nearest neighbors) and

species with the greatest differences in Ks were more likely to occur together. All other

110

traits included in the present study were not correlated with co-occurrence in the Mojave

Desert scrub community (P > 0.05 for all).

Discussion
Community assemblages and structure
Among three arid shrub communities, species utilize community speciﬁc suites of traits
related to water stress tolerance and water use (J acobsen et al. 2007c; Chapter 3). These
community speciﬁc differences may partially be due to environmental ﬁltering of species
with speciﬁc traits into these communities. This is evident in the under-dispersion of the
chaparral community. Indeed, niche conservatism of many chaparral species has been
described previously (Ackerly 2004) suggesting that species may have been “ﬁltered”
into the chaparral community based on traits that were already present. The coastal sage
and Mojave Desert scrub communities were not signiﬁcantly more or less
phylogenetically dispersed than randomly assembled communities, although they tended
to be under-dispersed. This pattern of under-dispersion in arid communities is consistent
with the predictions of Grime (1977) that in stressful communities competition may be
less important in the determination of community structure and species traits compared to
stress tolerance traits. Disturbance in these communities could also mitigate interspeciﬁc
competition, for instance, the coastal sage scrub and chaparral communities are prone to
wildﬁre. Fire may also lead to under-dispersion due to ﬁltering based on ﬁre-related life
history types that are often phylogenetically linked (Verdt’r & Pausas 2007).

The stand structure of these communities suggests that species occurring in these

communities may be more tolerant of stress or disturbance than competition. In the

111

Mojave Desert scrub, individuals are signiﬁcantly further apart than in the other two
communities and the crowns of individuals do not overlap. This suggests that as adults
these individuals are not strongly competing for space and light, although competition for
below ground resources may still be great (Casper & Jackson 1997). Above ground, the
stands are denser in the coastal sage scrub and chaparral although disturbance by wildﬁre

may mitigate competition in these more productive communities.

Conspeczﬁc co-occurrence

Across all three communities, individuals were more likely than predicted to occur near
another individual of the same species. This pattern was strongest in the chaparral
community where the nearest neighbor of any individual was signiﬁcantly more likely to
be an individual of the same species than would be predicted based on species
abundances and random species distribution within the community. This suggests that
species distributions and abundances in these communities may be, at least partially, due
to a scale environmental heterogeneity within the communities. It also is consistent with
evidence of community level environmental ﬁltering.

While conspeciﬁc co-occurrence may suggest that certain species possess traits
that allow them to best utilize a local abiotic resource, such a pattern could also be
explained by dispersal limitation (Levine er al. 2003; Levin & Murrell 2003), particularly
in the chaparral community. Many of the coastal sage and Mojave Desert species are
relatively small seeded (Baker 1972) or have modiﬁcations for wind or animal dispersal
and thus are able to relatively broadly disperse. Several chaparral species are also

broadly dispersed, usually by vertebrate animals, including Quercus berberidifolia,

112

Arctostaphylos glandulosa, and Rhus ovata (Willson 1993); however, many of the
species are short to intermediate dispersers including the Ceanothus species which utilize
ballistic seed dispersal (Evans et al. 1987). Localized dispersal may allow species to take
advantage of clustered favorable microsites within the chaparral community.
Alternatively, the evolution of short range dispersal mechanisms due to other selective
pressures may constrain species dispersal across the landscape leading to species
clustering in the absence of microsite differences. The high intraspeciﬁc competition this
pattern creates may also partially explain the high tolerances to water stress found in
chaparral shrubs (J acobsen et al. 2007c) and selection for increased competitive ability in

some of these species (Pratt et al. 2007).

Species distributions within communities

By the niche concept, species co-existence is predicted to depend on species
specialization resulting in reduced competition within a community (Darlington 1972;
Vandermeer 1973; Case 1981; Futuyrna & Moreno 1988; Chase & Leibold 2003;
Silvertown 2004). This suggests that the distribution of species will be non-random, with
functionally dissimilar species more likely to co-occur than species that are functionally
more similar. If functional traits are phylogenetically constrained, one would expect a
pattern of phylogenetic over-dispersion within communities. This pattern has been found
previously among oak species occurring across different habitats (Cavender-Bares et al.
2004) and among Adenostoma species occurring in southern California (Beatty 1987).
Alternatively, heterogeneity across the landscape may combine with niche conservatism

(e. g. trait conservatism) within lineages resulting in more closely related species co-

113

occurring more often than distantly related species as seen at the across community level
(Ackerly 2004). However, in the present study no relationships were found between
phylogeny and species co-occurrence within a stand.

The phylogenetic independence of species distributions within these three
communities could be due to several factors. It may be that the effects of environmental
ﬁltering (which would lead to under-dispersion) and competition (which would lead to
over-dispersion) are balancing or weak within these arid communities (Toft & Fraizer
2003; Kembel & Hubbell 2006). Alternatively, it may be that the species speciﬁc traits
related to resource use segregation are not phylogenetically constrained (Silvertown et al.
2006). Indeed, xylem cavitation resistance, a trait that is often used as an estimate of
woody plant water stress tolerance, and which is highly variable among species in these
communities, has been shown to vary more adaptively rather than be conserved across a
broad range of plant taxa (Maherali et al. 2004). Xylem speciﬁc hydraulic conductivity,
a measure of the efﬁciency that water can be transported through the xylem, also displays
more adaptive variability than conservation (Maherali et al. 2004). Thus, phylogenetic
relationships may not strongly inﬂuence plant functional traits and community structure
among species within these communities. This is consistent with the ﬁndings of
Carlquist and Hoekman (1985) that anatomical traits associated with drought tolerance
appears to have developed independently in many lineages in these communities. In
other communities a poor relationship between phylogeny and co-occurrence at local

scales has also been reported (the or scale; Silvertown et al. 2006).

114

Functional traits and community structure

Communities that are not phylogenetically structured may be structured instead
by evolutionarily labile traits. We examined the relationship between species co-
occurrence and several traits related to water stress and water stress tolerance. In the
chaparral community, none of the traits included in the present study were related to
species co—occurrence. In contrast, among the coastal sage scrub and Mojave Desert
scrub communities, trait relationships among species support habitat heterogeneity as
important in driving community structure. Species in these communities are most likely
to occur near other species that display similar traits including similar ‘Pwmin and T50 for
the coastal sage and similar xylem density and gsmin for the Mojave Desert species. Thus,
it is likely that species displaying these traits, regardless of phylogenetic relationships, are
able to do well within certain microsites within these communities. One trait, Ks, did
appear to display a pattern consistent with niche segregation among co—occurring species
with species that were very different in this trait being more likely to co-occur than
species with similar Ks.

The three arid communities discussed in this study differ in their species
compositions and stand structures, yet they all tend to be composed of species
assemblages that are more closely related than expected by chance. This suggests that in
these stressful environments species persistence is likely related to traits conserved within
certain lineages. These arid systems may offer a unique opportunity to examine the
evolution of aridity tolerance of woody species among a diverse range of plant families
and to identify which plant functional traits may be important in the ﬁltering of species

into arid communities.

115

Table 4.1. Species and families from three arid plant communities, species codes, and
species characteristics including height, crown diameter, and basal diameter. Different

letters in each column indicate signiﬁcant differences among species within each

 

 

 

 

 

 

community.

Species
Vegetation type and Species Family Code
Chaparral
Adenostomafasciculatum Hook. & Am. Rosaceae Af
Adenostoma sparsifolium Torrey Rosaceae As
Arctostaphylos glandulosa Eastw. Ericaceae Ag
Ceanothus cuneatus (Hook) Nutt. Rhamnaceae Cc
Ceanothus megacarpus Nutt. Rhamnaceae Cm
Ceanothus oliganthus Nutt. Rhamnaceae Co
Ceanothus spinosus Nutt. Rhamnaceae Cs
Malosma laurina (Nutt.) Abrams Anacardiaceae Ml
Quercus berberidifolia Liebm. Fagaceae Qb
Rhus ovata S. Watson Anacardiaceae R0
Coastal Sage Scrub
Artemisia califomica Less. Asteraceae Ac
Encelia califomica Nutt. Asteraceae Eca
Eriogonum cinereum Benth. Polygonaceae Eci
Hazardia squarrosa (Hook. & Am.) E. Greene Asteraceae qu
Lotus scoparius (Nutt.) Ottley Fabaceae Ls
Malacothamnusfasciculatus (Torrey & A. Gray) Malvaceae Mf
E. Greene
Malosma laurina (Nutt.) Abrams Anacardiaceae Ml
Salvia leucophylla E. Greene Lamiaceae Sl
Salvia mellifera E. Greene Lamiaceae Sm
Mojave Desert Scrub
Ambrosia dumosa (A. Gray) Payne Asteraceae Ad
Atriplex canescens (Pursh) N utt. Chenopodiaceae Aca
Atriplex polycarpa (Torrey) S. Watson Chenopodiaceae Ap
Coleogyne ramosissima Torrey Rosaceae Cr
Gutierrezia microcephala (DC.) A. Gray Asteraceae Gm
H ymenoclea salsola A. Gray Asteraceae Hs
Isomeris arborea Nutt. Capparaceae Ia
Larrea tridentata (DC.) Cov. Zygophyllaceae Lt
Lepidospartum squamatum (A. Gray) A. Gray Asteraceae qu
Lycium andersonii A. Gray Solanaceae La

116

Table 4.1 (cont’d)

Crown diameter Basal diameter

 

 

 

 

 

 

Height (m) (m) (m)
2.51 1 0.12 b 2.53 1 0.26 bc 0.31 1 0.05 bc
5.18 1 0.23 a 4.37 1 0.62 a 0.72 1 0.09 a
1.8210.l4d 1.6210.18cd 0.4110.07b
2.96 1 0.24 bc 1.64 1 0.20 cd 0.06 1 0.01 d
2.1810.16d 0.8010.11d 0.0310.00d
2.98 1 0.19 be 1.25 1 0.14 d 0.07 1 0.02 d
3.16 1 0.23 b 2.24 1 0.51 cd 0.14 1 0.03 cd
3.34 1 0.31 b 3.37 1 0.82 ab 0.30 1 0.09 be
3.02 1 0.31 be 2.39 1 0.36 be 0.39 1 O. 12 b
2.41 1 0.43 cd 2.57 1 0.39 be 0.38 1 0.07 b
1.001010 bc 1.2210.18b 0.0910.01bc
0.85 1 0.05 c 1.46 1 0.21 b 0.13 1 0.03 bc
0.75 1 0.08 c 1.04 1 0.10 b 0.08 1 0.01 c
0.73 1 0.08 c 1.32 1 0.21 b 0.12 1 0.01 bc
0.89 1 0.03 c 1.37 1 0.11 b 0.05 1 0.01 c
2.07 1 0.12 a 1.62 1 0.45 b 0.08 1 0.02 c
2.22 1 0.10 a 3.40 1 0.45 a 0.75 1 0.14 a
10310.16 ab 1.1910.24b 0.161003 be
0.87 1 0.07 c 1.66 1 0.21 b 0.23 1 0.01 b
0.35 1 0.03 e 0.62 1 0.11 f 0.08 1 0.02 d
0.99 1 0.06 be 1.26 1 0.18 cd 0.25 1 0.05 bcd
1.07 1 0.08 bc 1.90 1 0.12 b 0.35 1 0.08 b
0.95 1 0.19 cd 1.42 1 0.13 bcd 0.20 1 0.03 bcd
0.61 1 0.08 de 0.92 1 0.13 def 0.14 1 0.03 cd
0.69 1 0.06 d 1.25 1 0.09 cde 0.30 1 0.04 be
0.90 1 0.08 cd 1.12 1 0.20 cdef 0.12 1 0.03 d
2.11 1 0.21 a 3.27 1 0.39 a 0.89 1 0.14 a
1.26 1 0.11 b 1.62 1 0.21 be 0.23 1 0.05 bcd
0.48 1 0.04 e 0.87 1 0.12 ef 0.13 1 0.02 ed

117

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119

Adenostomafasciculatum -
Adenostoma sparsifolium -

Chaparral Coleogyne ramosissima
m coasml Sage Scrub Ceanothus oliganthus
[:I Mojave Desert Scrub —-:

Ceanothus spinosus
*— —‘l: Ceanothus cuneatus
Ceanothus megacarpus
Quercus berberidifolia
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Larrea tridentata
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Rhus ovata
Arctostaphylos glandulosa
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Hymenoclea salsola
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Cl

[:1

[———Salvia leucophylla

l——Salvia mellifera

Atriplex canescens |:I

Atriplex polycarpa l:
L—Eriogonum cinereum

 

Figure 4.1. Phylogeny of species included in the present study including the plant
community in which they occur (chaparral, coastal sage, or Mojave Desert scrub). See
Methods for description of how the phylogeny was constructed.

120

Chaparral Coastal Sage Scrub Mojave Desert Scrub

100

 

80-

Count

401

20-

 

/

0 l I I

8 9 1o 11
Phylogenetic distance

 

 

 

 

 

 

Figure 4.2. Histogram representing the phylogenetic distance of randomly generated
communities drawn from a pool of the species analyzed in the present study (grey bars
and solid line, n = 1000). Mean phylogenetic distances for species occurring within three

communities, chaparral, coastal sage scrub, and Mojave Desert scrub, are shown as open
bars.

121

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122

 

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—°- Nearest neighbors

A Density

 

 

 

 

 

 

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60
Co-occurrence (%) Co-occurrence (%)

Figure 4.4. The relationship between various functional parameters and species co-
occurrence as either neighbors (ﬁlled circles) or nearest neighbors (open circles) in the
coastal sage (A and B) or Mojave Desert scrub (C, D, and E) communities.

123

CHAPTER FIVE

DRY SEASON SOIL MOISTURE CONTENT AND INVASIBILITY OF ARID

SHRUBLANDS

Abstract

Soil moisture is a limiting resource in arid environments for woody shrub species. We
assessed if three arid communities differed in their level of dry season soil moisture
content and in their ability to use soil moisture reserves. Water potential of all of the
dominant woody plant species occurring in a chaparral, coastal sage, and Mojave Desert
community were measured seasonally and dry season soil moisture content was
determined. Individuals occurring in the Mojave Desert were able to persist with the
lowest water potentials while the coastal sage community displayed the highest minimum
water potentials. Volumetric soil moisture content (m3/m3) of the Mojave Desert site was
lowest during the dry season (7 %), the chaparral site was intermediate (10 %), and the
coastal sage scrub site had the moistest dry season soil (20 %). Previous work ﬁnds that
18 % soil moisture seems to be an important threshold for woody plant seedling
recruitment and the coastal sage community remains above this soil moisture threshold
year round. Of the three communities, the coastal sage community may therefore be
particularly susceptible to invasion by woody shrub species since its soil moisture content
would allow for germination and persistence of a wider range of potential invaders,
although all three of these communities are relatively little invader compared to adjacent

riparian communities.

124

Introduction

Competition among species should lead to the exclusion of species that rely on utilization
of similar resources (i.e. species that occupy the same niche). This principle was
described by Gause and is given the name “competitive exclusion” (Hardin 1960). While
a species niche is deﬁned by many variables, it is likely that in any given environment
there is one resource that is most limiting to species persistence. Where species are in
competition for a single limiting resource, species resource use can be used to predict
limiting resource levels and to predict the outcome of competitive interactions (R* rule;
Tilman 1982). This pattern of resource competition has also been termed exploitation
competition (Levine 1976; Vance 1985).

The R* rule predicts the outcome of competitive interactions based on differential
dependence of species on a given resource level for positive population growth (Figure
5.1 A; Tilman 1982). The growth rate of a population will decline as the availability of
the limiting resource declines. The level of resource availability at which the population
growth rate equals zero is the R*. If the resource is available in levels exceeding the R*
the population will grow and if the limiting resource is available in levels less than R* the
population will decline. If two species have different R* then the species with the lower
R* will be able to competitively exclude the species with the higher R*. This is because
the species with lower R* can draw resource availability down to a level that results in a
decline in the population of the species with the higher R* (Figure 5.1 A). The same
model may also be applied to interactions among plant communities (Figure 5.1 B).

The R* rule and similar models have been used to predict the outcome of

competition in controlled experiments (Titman 1976; Ciros-Pérez et al. 2001; Fox 2002),

125

patterns of species abundance within communities (Koiv & Kangro 2005; Harpole &
Tilman 2006), and patterns of species succession (Herron et al. 2001). Recently, these
models have also been applied to species invasions and determination of community
invisibility and native versus non-native competitive interactions (Herron et al. 2001;
Booth et al. 2003; Fargoine et al. 2003; Krueger-Mangold et al. 2006; Funk & Vitousek
2007). While many of these studies have focused on nutrient availability (for plants) or
food availability (for animals), moisture availability has also been shown to predict
competitive outcomes in some plant communities (Cleverly et al. 1997; Booth et al.
2003).

We examined differences among three arid plant communities in plant water
potential and soil moisture to assess whether these communities differed in their
invasibility based on these parameters. Water is likely a limiting resource in these
communities, particularly for the evergreen woody shrub species which remain active
year-round. Indeed, drought induced mortality of species in these communities at both
the seedling and adult stages have been reported (Frazer & Davis 1988; Williams et al.
1997; Davis et al. 2002; Paddock HI 2006). Water potential of woody plant branchlets or
leaves estimates the negative pressure in the xylem and is related to the availability of
soil moisture. More negative values indicate less available soil moisture reserves. Plants
that can tolerate more negative water potentials can continue to extract soil water when
plants that are less tolerant no longer are able to obtain enough moisture. Thus, species
and communities that tolerate more negative pressure have a lower R* and would be
predicted to be invasible by fewer invaders (i.e. only the limited number of potential

invaders that are most water stress tolerant) (Pratt & Black 2006). In the present study, I

126

did not attempt to compare across functional groups because predictions of competitive
outcomes based on limiting resources appear most useful among similar functional
groups (Krueger-Mangold et al. 2006). Thus, results are discussed in the context of

woody shrub species only.

Materials and Methods
Three diverse arid sites were selected based on their abundance of woody shrub species.
These sites represented chaparral, coastal sage, and Mojave Desert plant communities
(see J acobsen et al. 2007c, Chapter 2 for site descriptions). The average annual
precipitation for these sites is approximately 440 mm for the chaparral and coastal sage
communities and 180 mm for the Mojave Desert site (average annual precipitation from
1999-2007 based on the July to June rain year).

Volumetric soil moisture content was measured from late August 2006 through
April 2007 at each of the three sites. Moisture content of the upper soil layers (upper 30
cm) was measured at the base of the same individuals at each sampling time (n = 14-26)
using one TDR probe (CS615, Campbell Scientiﬁc, Inc., Logan, Utah, USA) attached to
a datalogger (CR23X Micrologger, Campbell Scientiﬁc, Inc., Logan, Utah, USA). These
sites do not differ in soil texture at this soil depth (J acobsen et al. 2007c). Within each
site, monthly values were compared using repeated measures ANOVAs. Minimum
seasonal soil moisture of each site was determined as a community wide mean from the
month with the lowest soil moisture values. An AN OVA was used to compare minimum
volumetric soil moisture across communities followed by a Bonferroni/Dunn post-hoe

analysis (Statview v. 5.0.1, SAS Institute Inc., Cary, NC, USA).

127

Water potential was measured at midday on all dominant woody shrub species at
each site approximately monthly from February 2006 and continuing through April 2007
(see Chapter 3 for detailed Methods) using a pressure chamber (Model 2000 Pressure
Chamber Instrument, PMS Instruments, Corvalis, Oregon, USA). Water potential was
measured on leaves or branchlets from six individuals per species at each sampling
period. Mean water potentials were calculated for each species at each sampling time.
These values were pooled across species and the frequency of water potentials were
calculated for each community in order to determine the community wide range in soil

moisture resource use.

Results

Dry season volumetric soil moisture of the shallow soil layers signiﬁcantly differed
among the sites and with season (Figure 5.2; Figure 5.3 C). Dry season soil moisture
values for fall 2006 followed an average rain year and thus should be representative for
soil moisture conditions in normal years during the dry season. The three communities
signiﬁcantly differed in their dry season volumetric soil moisture content (Figure 5.3 C; P
< 0.001). Minimum volumetric soil moisture content of the Mojave Desert site was the
driest (0.071 :1: 0.001; P 5 0.001 compared to the chaparral and coastal sage scrub), the
chaparral site was intermediate (0.103 :1: 0.006; P < 0.001 compared to the coastal sage
scrub), and the coastal sage scrub site had the moistest dry season soil (0.202 :t 0.010).
All of the sites exhibited signiﬁcantly higher soil moisture values during the wet season
from December to March (Figure 5.2); however, rainfall during the winter 2006-2007 wet

season was much less than normal (approximately 100-130 mm across all sites), so wet

128

season soil moisture values are likely not as high as would be typical in an average
rainfall year.

The three communities examined in the present study differed in the minimum
water potentials that could be tolerated by species within each community (Figure 5.3 A
and B). The Mojave Desert community experienced the lowest water potentials (-9.2
MPa), the chaparral was intermediate (~-8.7 MPa), and the coastal sage scrub community
experienced the least negative water potentials (~-5.4 MPa). All of the communities had
some species that maintained relatively high water potentials even in the dry season
(Figure 5.3 A and B). These minimum water potential values are consistent with site

differences in dry seasonal soil moisture content (Figure 5.3).

Discussion

Arid low productivity sites appear to be less broadly invasible than more moist and
productive sites (Stohlgren et al. 2002; Otto et al. 2006); however, arid plant
communities in southern California have still experienced considerable invasion by non-
native species. Most of these invasive species are annual herbs and grasses (Knops et al.
1995; Sax 2002; Salo 2004; Keeley 2006; Lanbrinos 2006) although there are several
woody non-native species naturalized in these communities. In the coastal sage and
chaparral communities woody invaders include, Acacia spp., Nicotiana glauca, Cytisus
spp. and Spartium spp. (Knops et al. 1995; Keeley 2006). While annual invasions into
arid regions appear to be at least partially dependent on increased nitrogen availability

(Brooks 2003), the timing and availability of soil moisture is also important (Salo 2004).

129

Species of woody shrubs in the chaparral, coastal sage, and Mojave Desert
communities are able to tolerate relatively low water potentials (less than -7 MPa in all
communities compared to a limit of -2 MPa for most crop plants; Tyree & Zimmerman
2002). Among these three communities, the Mojave Desert contains species that
experience the lowest water potentials seasonally and therefore are able to utilize more
limited soil moisture reserves than species in the other two communities. This suggests
that among these communities the Mojave Desert is the least invasible by woody shrub
species if soil moisture is the limiting resource in these communities. In contrast, the
coastal sage does not have species that reach as low water potentials as species in the
other communities. This suggests that this community may be the most invasible of the
three communities examined in the present study.

The dry season soil moisture of these communities is related to the water
potentials that the woody shrub species in these communities experience. This is
particularly evident when comparing between the chaparral and coastal sage
communities. Both of these communities experience similar annual rainfall
(approximately 400-500 mm) and have similar soil texture (J acobsen et al. 2007c) yet
they have very different dry season soil moisture levels. This is presumably because
species in the chaparral community are able to attain and survive lower water potentials
and are therefore able to draw soil moisture levels down to a lower level.

Differences in dry season soil moisture content may be particularly important in
determining the invasibility of these communities. A recent study examined ﬁve woody
species from the Mediterranean Basin (Spain) and found that among these species at soil

moistures over 18% there was 100% survival, while very few seedlings were able to

130

survive dry season soil moistures of less then 12% (Padilla & Pugnaire 2007). If this
result is general, this suggests that while the chaparral and Mojave Desert communities
would be able to resist seedling establishment by these woody species (10% and 7% dry
season soil moisture content, respectively) nearly all seedlings of these Mediterranean
species would be able to persist in the coastal sage community through the dry season
(20% dry season soil moisture content). Since most of the invasive or naturalized species
already present in these communities are native to other regions globally that experience
similar environmental conditions including the Mediterranean Basin (Knops 1995; Salo
2004; Keeley 2006) the results of this recent study may be particularly applicable to these
southern Californian communities.

Current numbers of non-native woody species in these communities, are
consistent with the predicted differences in susceptible to non-native species among these
communities. Based on recent species lists and floras of these communities (McAuley
1996 for the chaparral and coastal sage; Faull, unpublished data for Mojave Desert), 15 %
of the woody species present in the coastal sage are non-native compared to only 11 %
for the chaparral and 8% for the Mojave Desert.

The R* rule and similar models have been useful for prediction of invasibility of
some communities. Using this model to predict susceptibility to invasion by woody
shrub species in these three woody shrub communities of southern California suggests
that the coastal sage community may be most susceptible to woody species invasion if
soil moisture is a limiting resource in these communities. This suggests that monitoring

and control of woody naturalized shrubs may be most efﬁcient if efforts are focused on

131

this southern Californian plant community, as the chaparral and Mojave Desert

communities appear to be more impervious to shrub invasion.

132

 

 

  

 

 

 

 

 

 

 

 

 

 

 

 

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High

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Resource availability

Figure 5.1. Solid curves show the dependence of population growth rate on resource
availability (A; based on Tilman 1982) and the dependence of species communities on
resource availability (B) if a single resource is limiting. In panel A, the dashed line
indicates the point at which the mortality rate in a population equals the replacement rate.
The R* indicates the amount of resource needed for the population to increase. Species B
requires a higher amount of resource than Species A for the population to increase (i.e.
RB* > RA“); therefore, the long term outcome of competition between Species A and
Species B would be the competitive exclusion of Species B. This results because Species
A is able to reduce resources below the level at which Species B can maintain positive
population growth. In panel B, the dashed line indicates the point at which individuals
are so infrequent in the community that the community cannot be sustained. In this
example, Community A would be able to competitively exclude Community B.

133

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134

 

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Volumetric Soil Moisture Content (%)

Figure 5.3. The frequency of water potential occurrence in three arid plant communities,
the chaparral (medium gray ﬁll, solid line), coastal sage scrub (black ﬁll and dashed line)
and Mojave Desert scrub (light grey ﬁll, dashed-dotted line) (A and B) and the minimum
seasonal volumetric soil water content for these same three communities (C). Different
letters after bars in panel C indicated soil moisture values that are signiﬁcantly different.

135

CHAPTER SIX

Jacobsen, A.L., Agenbag, L., Esler, K.J., Pratt, R.B., Ewers, F.W. & Davis, SD. (2007)
Xylem density, biomechanics, and anatomical traits correlate with water stress in

seventeen evergreen shrub species of the Mediterranean-type climate region of South
Africa. Journal of Ecology, 95, 171-183.

136

XYLEM DENSITY, BIOMECHANICS, AND AN ATOMICAL TRAIT S CORRELATE
WITH WATER STRESS IN SEVENTEEN EVERGREEN SHRUB SPECIES OF THE

MEDITERRANEAN-TYPE CLIMATE REGION OF SOUTH AFRICA

Summary

1 Climate change in South Africa may threaten the sclerophyllous evergreen shrubs of
this region. Available data suggest that they are not as tolerant of water stress as
chaparral shrubs occurring in climatically similar California, USA.

2 Seventeen species from nine angiosperm families, including both fynbos and succulent
karoo species, were studied at a ﬁeld site in Western Cape Province, South Africa.
Minimum seasonal pressure potential (Pmin), xylem speciﬁc conductivity (Ks), stem
strength against breakage (modulus of rupture; MOR), xylem density, theoretical vessel
implosion resistance ((t/b)h2), and several ﬁber and vessel anatomical traits were
measured.

3 Species displayed great variability in Pmin, similar to the range reported for chaparral
and karoo shrub species, but in contrast to previous reports for fynbos shrubs.

4 More negative Pmin was associated with having greater xylem density, MOR, and
(t/b)h2. There was no relationship between Pm and traits associated with increased water
transport efﬁciency.

5 Xylem density integrates many xylem traits related to water stress tolerance including
Pmin, MOR, and (t/b)h2 as well as percent ﬁber wall, parenchyma, and vessel area, and

ﬁber lumen diameter.

137

6 Xylem density may be an integral trait for predicting the impact of climate change on

evergreen shrubs.

Introduction
The Cape Floristic Region of South Africa is dominated by evergreen shrubs with tough,
leathery leaves collectively referred to as fynbos. This region is classiﬁed as a
Mediterranean-type climate region, referring to its climatic similarity with the
Mediterranean Basin Region. This climate type is exempliﬁed by hot dry summers and
cool moist winters, with greater than 65% of annual precipitation occurring during the
winter months (Aschmann 1973). In the more arid areas adjacent to fynbos, fynbos is
replaced by more succulent vegetation called succulent karoo (Cowling & Holmes 1992).
These biogeographical regions contain some of the highest levels of regional diversity in
the world (Cowling et al. 1996) and are particularly threatened by global climate change
(McCarthy et al. 2001; Lovett, Midgley & Barnard 2005). Predictions for future climate
in the region point to signiﬁcant changes in water availability (Shulze & Perks 2000;
McCarthy et al. 2001) yet seasonal water relations (Miller, Miller & Miller 1983; M011 &
Sommerville 1985; van der Heyden & Lewis 1989; Richardson & Kruger 1990; Smith &
Richardson 1990) and associated xylem traits (February & Manders 1999) have only
been studied among very few species.

Minimum seasonal pressure potential (Pm) is a measure of the maximum water
stress that a plant experiences in the ﬁeld and is often correlated with plant water stress
tolerance (Hacke, Sperry & Pittermann 2000; Sperry & Hacke 2002; J acobsen et al.

2005; Jacobsen et al. 2006). Differential Pmin among co-occurring plants may indicate

138

variation in water availability and differential susceptibility to depleted water resources.
A less negative Pmin annually indicates greater access to soil moisture and suggests
greater rooting depth (Moll & Sommerville 1985; Smith & Richardson 1990) but may be
coupled with greater susceptibility to water stress. Conversely, a lower Pm,“ annually and
associated greater plant water stress tolerance may be coupled to lower water availability,
more extreme drought in dry years (J acobsen et al. 2006), and greater risk of drought
induced dieback and mortality (Davis et al. 2002; Paddock 2006).

The evergreen shrubs which occur in the Mediterranean-type climate region of
South Africa experience a predictable annual summer dry period (Cowling et al. 2005).
Thus, the evergreen shrubs of this region must be able to both resist the negative
pressures that develop within the xylem with water stress as well as maintain water
transport to evergreen leaves and actively expanding shoots during the summer dry
period (Agenbag 2006). We examined xylem traits associated with water transport
efﬁciency and water stress tolerance as well as Pm," in 17 evergreen shrub species
occurring in the southwestern region of the Western Cape Province, South Africa.

Several xylem anatomical traits were measured to ascertain what xylem structural
traits may be associated with decreased Pm“. including increased stem mechanical
strength (modulus of rupture), increased vessel and ﬁber wall thickness, increased
percent ﬁber wall area per transverse area, and decreased ﬁber lumen diameter. These
traits have been shown to be related to Pm, perhaps due to the increased structural
support needed to buttress xylem against negative pressure (J acobsen et al. 2005). We
also estimated the resistance of xylem vessels to implosion under negative pressure as an

additional estimate of water stress tolerance, by calculating the square of the ratio of the

139

inter-vessel wall thickness to vessel lumen diameter (i.e. (t/b)h2; Hacke et al. 2001). A
greater (t/b)h2 is associated with greater vessel mechanical strength against implosion
under negative pressure. Traits associated with greater hydraulic conductivity and
capacitance, including increased vessel and ﬁber lumen diameter and vessel and
parenchyma area per transverse xylem area, were also measured.

Sensitivity to water stress varied greatly among fynbos species exposed to an
experimental reduction in rainfall (Agenbag 2006). Xylem traits may be useful in
explaining this variation. Increased knowledge of xylem traits associated with water
stress tolerance in fynbos species may improve our ability to predict how plants will
respond to changes in temperature and precipitation in the face of regional climate

change.

Materials and Methods

Xylem traits were measured in 17 species of evergreen sclerophyllous shrubs from nine
angiosperm families located on J onaskop in the Riviersonderend Mountain Range in the
Western Cape Province, South Africa (Table 6.1; Figure 6.1). This site falls within the
Mediterranean-type climate region of South Africa. Individuals were sampled from the
north facing slope of the mountain at approximately 33° 56.08’ S 19 ° 31.26’ E. Eight
species were sampled at 920 m elevation (approximately 410 mm annual precipitation),
two species were collected from as high as 1160 m elevation, and the remaining 7 species
were collected from between 845 and 540 m elevation (Table 6.1). The steep elevational

gradient at this site corresponds to considerable variation in precipitation (approximately

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315 to 600 mm annual precipitation) and temperature (see Agenbag 2006 for a complete
description of the study site).

Species were identiﬁed by the Compton Herbarium of the South African National
Biodiversity Institute and specimens are housed at the University of Stellenbosch.
Identiﬁcation of one species was not possible, although it was identiﬁed as being within
the genus Euclea.

Twelve individuals of each species were tagged at the site and the same
individuals were used for each of the measured parameters. Two of the studied species
are dioecious (Leucadendron laureolum & L. salignum Proteaceae). For these two
species, twelve female and twelve male individuals of each were tagged and measured.

Xylem pressure potentials were measured at predawn and midday on 19 February
and at midday on 26 February and 24 March 2004 using a pressure chamber (Model
1001, PMS Instrument Company, Corvallis, Oregon, USA). At each sampling time, we
measured xylem pressure potentials (Pm) on branchlets on a minimum of ﬁve plants per
species with the pressure chamber technique (Scholander et al. 1965). The last rainfall
event prior to the onset of the summer dry period occurred on 27 September 2003 (~17
mm). There were several small rain events over the course of the summer (less than 10
mm each) although xylem pressure potentials for most species declined over the
measurement period. The summer drought ended on 1 April 2004 with a rainfall event of
21 mm, one week after the 24 March sample date. Thus, the duration of the seasonal
drought period was about 6 months.

Xylem density was determined as the dry mass per fresh volume of mature stems

from at least six individuals per species or sex (Wagner, Ewers & Davis 1998; Hacke et

141

al. 2001). The bark and pith were removed from stems prior to determination of xylem
density. The stems were saturated in degassed HCl solution adjusted to a pH of 2 until
they reached their maximum wet weight. Water-saturated volume was determined by
water displacement in a graduated cylinder. The stems were dried at 60°C to a constant
weight and dry mass was determined.

Stem xylem modulus of rupture (MOR) was measured using a four-point bending
test on an Instron Universal Testing Machine (model 4202, lnstron Corporation, Canton,
MA, USA) at Michigan State University (East Lansing, MI, USA) following the methods
of J acobsen et al. (2005). Twelve stems per species or per sex and approximately 0.3 m
in length and 6-8 mm in diameter were collected in the ﬁeld, wrapped in moist paper
towels, and placed in plastic bags. Stems were then express shipped, in a chilled cooler,
to Michigan State University for mechanical analysis. All stems were measured within 4
days of ﬁeld collection. A four-point bending test with a compression load cell of 500 N
was conducted following the methods of J acobsen et al. (2005). We were unable to
collect stems from four species for mechanical analysis due to difﬁculty in obtaining
straight stems of the required dimensions for measures: Erica cerinthoides, Euclea sp.,
C liﬁ‘ortia ruscifolia, and Metalasia densa.

Xylem speciﬁc hydraulic conductivity (Ks) was calculated following removal of
air embolism by high pressure perfusion (Sperry, Donnelly & Tyree 1988). One branch
from a minimum 'of six different individuals per species was collected from the ﬁeld.
The collected branches were approximately 0.3 m in length and 6-8 mm in diameter.
They were wrapped in wet paper towels, sealed in plastic bags, and placed in a cooler for

transport back to the laboratory. All stems were measured in less than 24 hrs from the

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time they were collected. Once in the laboratory, branches were submerged in water and
trimmed from alternate ends until a ﬁnal stem segment, 0.1 m in length, was obtained.
Stems were connected to a tubing system and ﬂushed with low pH degassed water (pH 2
HCl) that had been passed through a 0.1 pm ﬁlter. The stems were ﬂushed at a pressure
of 100 kPa for one hour to remove gas emboli from the xylem vessels. The Kh (kg m
MPa'1 3") was then measured gravimetrically on each stem segment (Sperry et al. 1988)
using an analytical balance (AE260, Delta Range Balance, Mettler Instrument Corp).
The segments were then attached to a tubing system that allowed uptake of a 0.1%
(mass/volume) ﬁltered (0.1 mm ﬁlter) dye solution of crystal violet under a suction of 4-6
kPa for 20 min (Hargrave et al. 1994). The midpoint of each segment was then sectioned
to a thickness of 30-40 pm using a sliding microtome. The stained xylem area was then
measured using a digital camera (C-730 Ultra Zoom Camedia, Oympus America Inc.)
and image analysis software (Image v.1.61, National Institute of Health). The KS value
(kg 111'1 MPa'1 5") was calculated as K.,/active xylem area.

The same sections used for determination of active xylem area were also used for
xylem anatomical measures. For each stem, images were taken of several wedge-shaped
sectors to sample for vessel and ﬁber features using a digital camera (J VC TK-C1381
Colour Digital Video Camera) attached to a light microscope (DM LB, Leica
Microsystems). Vessel lumen diameter (d) and wall thickness, ﬁber lumen diameter and
wall thickness, and percent transverse ﬁber, vessel, and parenchyma area were measured.
All of the vessels and ﬁbers in sectors were measured until 100 vessels and 100 ﬁbers
had been measured in a given stem. The hydraulic vessel diameter (dh) was calculated

from the formula dh = (Zd5)/(Zd4), based upon all the sampled vessels in a stem. This

143

parameter weights the vessel diameters by their hydraulic contribution which is a
function of the diameter to the fourth power (Tyree & Zimmermann 2002). This was
used in our analyses instead of mean d because it is more directly related to xylem water
transport. The vessel implosion resistance ((t/b)h2) (Hacke et al. 2001) was determined for
those vessels, within the sampled 100 vessels per stem, that formed pairs in which one or
both vessels fell within i 5 pm of the calculated db, with t as the combined wall thickness
of adjoining vessels and b as the lumen diameter of the selected vessel. Percent
transverse area was estimated through measurements of vessel, ﬁber, and parenchyma
area in four randomly chosen cross-sectional sectors per stem.

We calculated phylogenetic independent contrasts (PICS) to test for patterns of
correlated evolutionary change between traits (Felsenstein 1985) using COMPARE (v
4.6, EP Martins, Department of Biology, Indiana University). A correlation among PICs
for two traits indicates that these traits have undergone changes of similar direction and
magnitude across the phylogeny and supports a possible functional link between these
traits. The phylogeny used for these analyses was constructed by hand using published
phylogenetic data (Fig 1). Relationships among families, genera, and species were based
on recent molecular phylogenies (Morton et al. 1996; Soltis et al. 1997; Bayer & Starr
1998; Soltis et al. 2000; Miller, Young & Wen 2001; Hilu et al. 2003; Barker et al. 2004;
Yi, Miller & Wen 2004; McGuire & Fron 2005). All analyses were run assuming equal
branch lengths (Ackerly 2000). This is a conservative approach, thus there is less
certainty associated with lack of correlation among contrasts but high conﬁdence when

there is a signiﬁcant correlation among contrasts.

144

Unpaired t—tests were used to compare xylem traits of male and female individuals
of dioecious species and linear regression analyses were used to examine interspeciﬁc
trait correlations (Minitab v. 14. 12, Minitab, Inc. and Statview v.5.0.1, SAS Institute Inc.).
Regressions or differences were considered to be signiﬁcant if a S 0.05. Where females
were found to differ from males, they are included as separate data points in analyses. A
power ﬁt was used to compare db and K, because according to the Hagen-Poiseuille
equation K, is a function of diameter raised to the fourth power (Tyree & Zimmermann
2002). Principle component analysis was used to determine correlation patterns among
multiple traits. This analysis is useful in summarizing the relationships between multiple
traits into a single two dimensional ﬁgure that may be easier to interpret than many
separate regressions. Principle component analysis was used to examine both raw data as
well as PICS. Data were transformed as necessary to meet the assumptions of statistical

models.

Results

Intraspeciﬁc comparison of sexes

Two of the studied species, Leucadendron laureolum and L. salignum are dioecious.
Females and males of L laureolum did not signiﬁcantly differ in any of the xylem traits
measured in this study (Figure 6.2; P > 0.05 for all comparisons). Data from both sexes
of L. laureolum were therefore pooled for regression analyses. In contrast, females and
males of L salignum were different in their xylem traits related to conductive efﬁciency,
such as xylem speciﬁc hydraulic conductivity (Ks), mean hydraulic vessel diameter (dh),

and percent vessel area per transverse xylem area. Males of L. salignum had higher Ks

145

(Figure 6.2a; P = 0.046), greater dh (Figure 6.2b; P = 0.003), and greater percent vessel
area per transverse xylem area (Figure 6.2c; P = 0.020) relative to females. In addition to
these hydraulic traits, males also had a lower percent ﬁber wall area per transverse xylem
area compared to females (Figure 6.2d; P = 0.001). Female and male L. salignum are
thus included as separate data points in regressions involving these traits in which they
differ signiﬁcantly. Female and male L. salignum did not differ in the other xylem traits
measured, including xylem density, modulus of rupture (MOR), (t/b)h2, minimum
seasonal pressure potential (Pmin), ﬁber lumen diameter, ﬁber wall thickness, and percent

parenchyma per transverse xylem area (P > 0.05 for all).

Minimum seasonal pressure potential
Branchlet pressure potentials (PX) were measured over three sample dates towards the end
of the summer dry period. Over the course of the sample period pressure potentials of
most species did not change or declined, indicating steady or declining water status.
Pressure potential increased on the sampling date 24 March 2004 for a single species,
Searsia undulata (P = 0.016). Pressure potentials for the two Pteronia spp. were
approximately -8.5 MPa on 26 February 2004, and declined to below - 10 MPa
(exceeding the limits of the pressure chamber) on 24 March 2004. Thus, for these two
species minimum seasonal pressure potential (Pmin) is unknown, but is lower than -10
MPa. For the remaining species, the lowest measured pressure potential was used to
estimate Pmin.

Minimum seasonal pressure potentials (Pm) varied greatly among the 17 species

examined, ranging from a high of -1.89 MPa (Leucadendron salignum) to a low of less

146

than —10 MPa (Pteronia fasciculata & P. paniculata) (Figure 6.3). The mean Pm," across
species, excluding the two Pteronia species for which their Pm," values are lacking was -
3.4 i 0.34 MPa. The mean Pm," across species, assuming that the two Pteronia spp. had
Pmin of -10 MPa, was —4.34 i 0.61 MPa. Because speciﬁc Pmin values for the Pteronia

spp. are lacking and they were presumably lower than ~10 MPa, the mean Pmin across all

species may actually be more negative.

Correlations of raw trait values

Lower Pm was correlated with greater xylem density (Figure 6.4a; Table 6.2), greater
stem mechanical strength against breakage (Figure 6.4b; modulus of rupture, MOR;
Table 6.2), and increased ratio of vessel wall thickness to lumen diameter (Figure 6.4c;
Table 6.2). Minimum seasonal pressure potential was not correlated to other stem xylem
properties, including ﬁber lumen diameter and wall thickness, percent vessel,
parenchyma, or ﬁber wall area per transverse xylem area, Ks, or dh (Table 6.2).

Xylem density was correlated with stem mechanical and cellular properties. At
the stem level, increased xylem density was correlated to increased MOR (Figure 6.5a;
Table 6.2), increased percent ﬁber wall area per transverse xylem area (Figure 6.5b;
Table 6.2), and decreased percent parenchyma area and percent vessel area per transverse
xylem area (Table 6.2). At the cellular level, greater xylem density was correlated to
smaller ﬁber lumen diameters (Table 6.2) and increased (t/b)h2 (Figure 6.5c; r2 = 0.53, P
= 0.003 for 14 species). Three species, Passerina obtusifolia, Pteroniafasciculata, and
Pteronia paniculata, had (t/b)h2 values outside the range previously reported for

angiosperms and which signiﬁcantly impacted the slope of the regression (Figure 6.5c; P

147

= 0.004). Because of the signiﬁcant impact of these few points on the regression, values
for those species were excluded from the regression analysis, although the regression was
still signiﬁcant when they were included (r2 = 0.65, P < 0.001 for all 17 species). Xylem
density was not correlated with estimates of hydraulic efﬁciency, including Ks and dh, nor
to ﬁber wall thickness (Table 6.2).

Modulus of rupture was negatively correlated with percent vessel area and percent
parenchyma area per transverse xylem area, ﬁber lumen diameter, and dh (Table 6.2).
MOR was positively correlated with percent ﬁber wall area (Fig 5d) and (t/b)h2 (Figure
6.5c; Table 6.2). MOR was not correlated with Ks or ﬁber wall thickness (Table 6.2).

Xylem speciﬁc hydraulic conductivity (K.,) was correlated with dh using a power
ﬁt (Figure 6.6; r2 = 0.71, P < 0.001) and the exponent was not different from 4 (3.55 i
0.63). K8 was not correlated to (t/b)h2, ﬁber lumen diameter, ﬁber wall thickness, or

percent parenchyma, vessel, or ﬁber wall area per transverse xylem area (Table 6.2).

Phylogenetic independent contrasts correlations
Phylogenetic independent contrasts (PICS) of Pm,“ and xylem density were correlated
(Table 6.2), but PICS of Pm," were not correlated to any other contrasts of measured
xylem traits including ﬁber wall thickness, ﬁber lumen diameter, Ks, dh, and percent ﬁber
wall, parenchyma, or vessel area (Table 6.2).

Phylogenetic independent contrasts of xylem density were correlated to contrasts
of MOR, ﬁber lumen diameter, (t/b)h2, and ﬁber wall thickness, but not to percent

parenchyma, vessel, or ﬁber wall area per transverse xylem area contrasts (Table 6.2).

148

Xylem density contrasts were also not correlated to contrasts of hydraulic traits (Table
6.2).

Phylogenetic independent contrasts of MOR were correlated with contrasts of
several xylem parameters including ﬁber lumen diameter, dh, (t/b)h2, percent vessel area,
percent ﬁber wall area, and percent parenchyma area per transverse xylem area (Table
6.2). MOR contrasts were not correlated with K, or ﬁber wall thickness contrasts (Table
6.2).

Phylogenetic independent contrasts of Ks were correlated with d.., ﬁber wall
thickness, percent vessel area, and percent ﬁber wall area per transverse xylem area
contrasts, but not to (t/b)h2, ﬁber lumen diameter, or percent parenchyma area contrasts

(Table 6.2).

Principal components analysis

Principal Components analysis of the raw data, not taking phylogenetic relatedness into
account, supported a division between pressure potential and structural traits compared to
hydraulic traits (Figure 6.7a). The ﬁrst component described 61.4% of the variation
among 11 traits and associated with Pmin, xylem density, MOR, (t/b)h2, ﬁber lumen
diameter, and percent ﬁber wall area and parenchyma area per transverse xylem area.
The second component described 17.7% of the variation among 11 traits and was
associated with hydraulic efﬁciency traits including, Ks, db, and percent vessel area per
transverse xylem area. A third component described 9.4% of the variation and was
associated with ﬁber wall thickness. Xylem density, (t/b)h2, MOR, and percent ﬁber wall

area are all positively related with one another and are negatively related to Pmin, ﬁber

149

lumen diameter, and percent parenchyma. Measures of transport efﬁciency, Ks, (In, and
percent vessel area, are positively related. This analysis helps elucidate the relationships
among many traits Simultaneously and summarizes them on a single graph. In this case,
this analysis illustrates the relationship among the many xylem structural traits associated
with water stress versus the relationships among the vessel traits associated with
increased hydraulic efﬁciency.

Principal component analysis of PICS suggest that the traits that are correlated
when raw data are analyzed are also evolutionarily correlated (Figure 6.7b). The ﬁrst
component described 57.8% of the variability among 11 traits and was associated with
Pmrn, xylem density, and MOR contrasts as well as the xylem anatomical trait contrasts of
percent ﬁber wall and parenchyma area per transverse xylem area, (t/b)h2, ﬁber lumen
diameter, and db. The second component described 23.2% of trait variability and was
associated with trait contrasts of xylem density, Ks, and ﬁber wall thickness. A third
component explained 10% of trait variance and was associated with percent vessel area
per transverse xylem area. The positions of traits along the x-axis (component 1) appears
to divide traits associated with greater transport efﬁciency and capacitance (Ks, dh,
percent vessel area, percent parenchyma area, and ﬁber lumen diameter) from those
associated with greater tissue density and increased drought tolerance (Pmin, xylem

density, MOR, percent ﬁber wall area, and (t/b)h2).
Discussion

The wide range of Pmin found among species occurring within close proximity (-1.9 to

less than -10 MPa) suggests that these plant species differ in their utilization of water

150

resources. Lower pressure potentials at midday were accompanied by lower predawn
pressure potentials. Thus, heterogeneity of Pm," indicates variable access to soil moisture
and water utilization patterns among species perhaps due to variable rooting depth, root
phenology, or soil characteristics among species. This variability may be an important
factor in the great species richness of the area (Richardson et al. 2001).

All of the species included in this study occur within the Mediterranean-type
climate region of South Africa (Aschmann 1973). Because of the Similarities in climate
among the ﬁve Mediterranean-type climate regions of the world, Species occurring in
these regions have often been compared (e. g. di Castri & Mooney 1973; Cody & Mooney
1978; Cowling & Campbell 1980; Kruger, Mitchell & Jarvis 1983; Cowling et al. 1996).
Studies that have compared minimum seasonal pressure potentials (Pmin) 0f species
across regions, speciﬁcally to the California chaparral, have found that Pmin of South
African fynbos are often much less negative (most were higher than -4 MPa; of Miller et
al. 1983; M011 & Sommerville 1985; Jeffery, Moll & van der Heyden 1987; Davis &
Midgley 1990; Smith et al. 1992) compared to those found in California (c. f. Miller &
Poole 1979; Poole & Miller 1981; Burk 1978; Williams, Davis & Portwood 1997; Davis
et al. 2002; Jacobsen et al. 2005; J acobsen et al. 2006). Other studies have found
similarly high pressure potentials among South African fynbos species (van der Heyden
& Lewis 1989; von Willert, Herppich & Miller 1989; Richardson & Kruger 1990; Smith
& Richardson 1990).

In the present study, we found several Species that had Pmin lower than -4 MPa
and the mean Pm across all Species did not differ from the recently published mean Pmin

of 26 species in California (-4.34 i 0.61 for South Africa compared to -4.9 i- 0.42 MPa

151

for California, P = 0.50; J acobsen et al. 2006). The more negative Pm," values found in
this study than in previous studies are likely due to an inclusion of different and a greater
number of species, including some species associated with succulent karoo vegetation.
When the two Pteronia species (characteristic of the arid, low elevation of the study
gradient) are excluded from this analysis the Pm," for the 15 remaining species do differ
from that of the California species (P = 0.013). For species that have been included in
previous investigations and were part of the current study, our Pm," are consistent with
published values limiting the likelihood that Site, sampling technique, or sampling year
Signiﬁcantly impacted results (Miller et al. 1983; van der Heyden & Lewis 1989; von
Willert et al. 1989; Richardson & Fruger 1990; Smith & Richardson 1990). For the two
Pteronia species, whose distributions extend into the more arid succulent karoo
shrubland, Similarly low values (less than -10 MPa) have been reported for individuals
occurring within the succulent karoo (Midgley & van der Heyden 1999).

The greater range of Pmin found in this study may be due to the steep elevation
and precipitation gradient of this site (Agenbag 2006). The ﬁve species experiencing the
most negative Pmin occurred at lower elevations (lower than 660 m) at the ecotone
between fynbos and succulent karoo and receive less annual precipitation than species
occurring at higher elevations. For the remaining 12 Species, there does not appear to be
any relation between elevation and Pmin. For instance, the species collected in this Study
from the highest elevations, Nebelia laevis and Brunia noduliﬂora have Pmin of
approximately -4 MPa even though they likely receive more rainfall than many of the

other species.

152

Species that experienced greater seasonal water Stress (lower Pmin) had greater
xylem density and greater stem mechanical strength (MOR). The xylem of species
experiencing more negative Pm," also had xylem vessels with greater theoretical
implosion resistance (i.e. (t/b)h2; Hacke et al. 2001). These results are consistent with
what has been reported in the literature for shrubs of the Mediterranean-type climate
region of California (Wagner et al. 1998; J acobsen et al. 2005; J acobsen et al. 2006).
Interestingly, Pmin is not correlated with changes in ﬁber properties, including ﬁber lumen
diameter and wall thickness and transverse ﬁber wall area. This differs from what has
been reported for the chaparral of California (J acobsen et al. 2005; J acobsen et al.2006)
and suggests that xylem anatomical traits associated with drought tolerance may differ
between these two regions. The relationship between measurements made on bulk xylem
tissues and stems, such as density and MOR, and Pmin appear more consistent between
California and South Africa than measurements made on cellular properties (Hacke et al.
2001; Ackerly 2004; J acobsen et al. 2005). Thus, increased allocation of carbon
resources to support xylem vessels against implosion under increasing negative pressure
may be necessary at the bulk tissue level, but this may be accomplished at the cellular
level by varied adjustments across cell types (e. g. vessels, tracheids, ﬁbers, or
parenchyma). For example, increased cellular support against implosion can result from
either increased vessel wall to lumen ratio (South Africa; this study) or increased ﬁber
matrix support (California; J acobsen et al. 2006). Both types of cellular adjustments
would result in increased xylem density and MOR. Differences in cellular level

adjustments and Pm... between South Africa and California might be due to phylogenetic

153

differences, differences in the chemical makeup of cell walls or some yet to be
determined factor.

While most species had (t/b)h2 values within the range of previously reported data
(approximately 0.01-0.08; Hacke et al. 2001; J acobsen et al. 2005; Jacobsen et al. 2006),
there were three species that had exceptionally high (t/b)h2 values. Two of these species,
Pteronia fasciculata and P. paniculata, had values that exceed those previously reported
for all woody species including conifers ((t/b)h2 = 0.24 and 0.20, respectively; c. f. Hacke
et al. 2001). Figure 6.8 shows micrographs of these species in comparison to those of
Species with (t/b)h2 values falling within the previously reported range of values.
Individuals of the two Pteronia species experienced pressure potentials that exceeded the
range of our pressure chamber (less than -10 MPa), but their (t/b)h2 values, as well as
their high MOR values, suggest that their xylem could resist implosion at pressures much
more negative than ~10 MPa (see Figures 6.4b & c). This is consistent with prior reports
of great desiccation tolerance in these species (Midgley & van der Heyden 1999).
Additionally, it appears that these species have altered patterns of xylem allocation in line
with the need to resist greater pressures within the xylem. This is evidenced by the
relatively large (t/b)h2 values of these species for a lesser whole xylem investment
compared to other species (see Figures 6.4a & c and Figure 6.5c) which suggests they
have preferentially developed vessels that are more implosion resistant without
equivalent changes to the whole xylem tissue. This may have been necessary because
these Species already have the highest percent ﬁber wall areas (76 and 79%) and the
lowest percent parenchyma areas (less than 3%) of all of the species examined. Thus,

they may have reached the maximum xylem strength and density possible while still

154

maintaining an adequate conductive area (i.e. vessel area). As a result, Pteronia
fasciculata and P. paniculata differ from other species in the study in the effectiveness of
their vessel mechanical resistance for a given xylem density (i.e. these species fall well
above the trend line for density versus (t/b)h2 in Figure 6.5c).

Xylem density and MOR were correlated with xylem tissue and cellular
properties, including percent ﬁber wall, parenchyma, and vessel area, ﬁber lumen
diameter, and (t/b)h2, consistent with previous studies (Wagner et al. 1998; Hacke et al.
2001; Woodrum, Ewers & Telewski 2003; J acobsen et al. 2005; Jacobsen et al. 2006).
However, one species, Searsia undulata, appeared to have relatively low MOR, ﬁber wall
area, and (t/b)h2 for its xylem density. This species also had one of the highest levels of
transverse parenchyma area of the species examined. Presumably, the higher percentage
of parenchyma and their associated stored starch contributed to xylem density in this
species, but did not offer the mechanical strength that displaced ﬁber area would have,
resulting in low MOR. Interesting, while this species has a higher parenchyma and lower
ﬁber area, which may be associated with higher capacitance (Borchert & Pockman 2005),
it still experienced a relatively low Pmin (-6.7 MPa) suggesting high risk of cavitation. It
may be that this species differs from other Species included in this Study in being able to
tolerate a greater degree of seasonal embolism such as has been found in the chaparral
shrub Rhus ovata (Pratt et al. 2005).

AS predicted, K8 was correlated with increased hydraulic vessel diameter (db) and
the exponent of the power ﬁt relating these two variables was not different from 4
consistent with the Hagen-Poiseuille equation (Tyree & Zimmermann 2002). Thus,

among these species, vessel diameter is a strong predictor of Ks regardless of interspeciﬁc

155

differences in vessel area (8.6 — 18.7%) or possible differences in pitted area and vessel
sculpturing. Increased K.,, which is associated with greater potential growth rate (Vander
Willigen & Pammenter 1998), varied independent of xylem traits associated with strength
(ﬁber and tissue parameters) or drought tolerance (ijn and (t/b)h2) consistent with
previous ﬁndings (Woodrum et al. 2003; Kern et al. 2005; J acobsen et al. 2005).

Species of the genus Leucadendron are dioecious with some species displaying
vegetative dimorphism between sexes, such as differences in leaf morphology and
branching, while in other species the sexes display little vegetative divergence (Bond &
Midgley 1988; Bond & Maze 1999; Rebelo 2001). The two Leucadendron species
included in this study, L. laureolum and L. salignum, are vegetatively dimorphic.
Consistent with this, sexes in L. salignum also display xylem trait dimorphism.
Conversely, sexes in L. laureolum do not appear to vary in the xylem traits we examined.

Males of L. salignum have greater xylem speciﬁc conductivity (Ks), hydraulic
vessel diameters (db), and percent vessel area, suggesting that for a given xylem area they
have more efﬁcient hydraulic conductivity compared to females. Males also have a
lower percentage of ﬁber wall area for a given xylem area due to a combination of ﬁber
displacement in favor of increased vessel area and greater ﬁber lumen diameter. These
changes in cell type abundance apparently do not affect whole stem strength or
drastically alter carbon allocation, Since males and females do not differ in stem
mechanical strength (MOR) or xylem density. Consistent with what has been reported
for other Leucadendron species (Bond & Midgley 1988; Bond & Maze 1999), males of
L. salignum at our study site appear to have smaller leaves, thinner branches, and greater

branch ramiﬁcation than females. Selection for greater ramiﬁcation in males may be due

156

to sexual selection for greater inﬂorescence number (Bond & Midgley 1988; Geber 1995;
Bond & Maze 1999), since inﬂorescences are terminal in L. salignum. It may be that
selection for greater inflorescence number has affected xylem hydraulic traits. Males,
with more ramiﬁed and narrow branches may have increased hydraulic conductivity per
xylem area (higher K.,) as a means to maintain ﬂow to leaves through a smaller xylem
area. Additionally, although it was not measured in this study, smaller leaves in males
may also lead to greater leaf speciﬁc hydraulic conductivity (K) in males versus females.
These results suggest a link between ﬂoral and hydraulic traits.

Correlations among phylogenetic independent contrasts (PICS) of xylem
characteristics generally agree with correlations obtained from the raw trait values that
did not incorporate phylogenetic relatedness. Thus, many of the traits that are correlated
using raw data have also experienced correlated evolutionary change across the
phylogeny, suggesting that they may be functionally related. Evolutionary changes in
xylem density are correlated with evolutionary changes in Pmin, MOR, ﬁber lumen
diameter, (t/b)h2, and ﬁber wall thickness, supporting utility of xylem density in
prediction of other xylem traits. Similarly, KS and d1. contrasts were correlated,
supporting a functional relationship between these hydraulic traits.

Unlike the raw trait regression, percent vessel area contrasts were correlated to Ks
contrasts. This suggests that these traits may be functionally related as predicted (i.e.
greater vessel area could mean either larger vessels or a greater number of vessels, both
of which would be predicted to increase ﬂow; Ewers 1985). However, it should be noted

that PIC analyses should be viewed with caution, especially where they vary from raw

157

analyses, because of the uncertainty in phylogeny topography and branch length and non-
random species sampling (Donoghue & Ackerly 1996; Ackerly 2000).

Principal components analyses of both raw trait values and PICS conﬁrm the
above relationships between a suite of mechanical and drought tolerance xylem traits and
a suite of hydraulic traits. The mechanical and drought tolerance traits include xylem
density, MOR, Pmim (t/b)h2, ﬁber lumen diameter, percent ﬁber wall area, and percent
parenchyma area. The hydraulic traits include Ks, db, and percent vessel area. We found
no evidence of a trade-off between these hydraulic and the mechanical-drought traits.

The great variability in Pm... found among Species suggests that water use and
availability may be important factors in the structuring of fynbos and succulent karoo
evergreen woody Shrub communities of the Mediterranean-type climate region of South
Africa. This range of Pm among the species included in this study is Similar to the
evergreen sclerophyllous Shrubs of the Mediterranean-type climate region of California
and suggests that co-occurring Shrubs in these regions may similarly utilize water
resources in spite of differences in rainfall reliability among the regions (Cowling et al.
2005). The ease of measuring xylem density and its use in predicting xylem
characteristics as well as Pmin, may make it a useful tool in estimating the xylem
characteristics and drought tolerance of large numbers of Species. This may be
particularly useful in South Africa, where the region is vulnerable to changes in climate
and where plant distributions and diversity will likely impacted (McCarthy et al. 2001;

McClean et al. 2005; Lovett et al. 2005).

158

Table 6.1. The Species of evergreen shrubs located on Jonaskop in the Riviersonderend
Mountain Range in the Western Cape Province, South Africa along with the elevation at
which the Species was sampled (rounded to the nearest 10 m). Nomenclature follows
Germishuizen & Meyer (2003) except for Searsia undulata which follows Yi et al.
(2004).

 

Species Elevation (111)
Brunia noduliﬂora (E. Mey.) Kuntze 1160
Nebelia laevis O. Kuntze 1020
Aspalathus pachyloba R. Dahlgren 920
Cliﬁortia ruscifolia L. 920
Erica cerinthoides L. 920
Leucadendron laureolum (Lam.) Fourc. 920
Leucadendron salignum P.J. Bergius 920
Metalasia densa (Lam.) Karis 920
Protea laurifolia Thunb. 920
Protea repens (L.) L. 920
Aspalathus hirta E. Mey. 850
Erica plukenetti L. 850
Passerina obtusifolia Thoday 660
Euclea Sp. 540
Pteronia fasciculata L.f. 540
Pteronia paniculata Thunb. 540
Searsia undulata (J acq.) T.S. Yi, A.J. Miller & J. Wen1 540

1formerly Rhus undulata

159

Table 6.2. The coefﬁcients of determination (r2) and probability values (P) for
regressions of raw trait values and phylogenetic independent contrast (PIC) values of
several xylem structural and functional traits as measured on 17 evergreen shrub Species.
Bold text indicates a Signiﬁcant correlation. See Methods for abbreviations and trait
descriptions.

 

 

 

 

 

 

 

Phylogenetic
Correlations of Raw Independent Contrast

Traits Trait Values Correlations

2 2
Independent Dependent r P I' P
Xylem Density 0.76 <0.001 0.50 0.005
MOR 0.39 0.023 0.07 0.45
Fiber wall thickness 0.00 0.97 0.22 0.09
Fiber lumen diameter 0.23 0.06 0.05 0.44
P 'n (t lb )h2 0.49 0.002 0.13 0.20
mi
% Fiber wall area 0.19 0.08 0.00 0.99
% Parenchyma area 0.03 0.51 0.00 0.88
% Vessel area 0.15 0.13 0.00 0.86
dh 0.01 0.73 0.03 0.54
K S 0.19 0.08 0.20 0.11
MOR 0.72 <0.001 0.32 0.034
Fiber wall thickness 0.03 0.46 0.26 0.043
Fiber lumen diameter 0.58 <0.001 0.31 0.026
x 16m (t lb )h2 0.65 <0.001 0.38 0.011
Deynsity % Fiber wall area 0.52 <0.001 0.14 0.16
% Parenchyma area 0.28 0.021 0.13 0.16
% Vessel area 0.26 0.026 0.03 0.55
dh 0.08 0.24 0.00 0.94
K S 0.01 0.72 0.06 0.35
Fiber wall thickness 0.01 0.731 0.02 0.68
Fiber lumen diameter 0.67 <0.001 0.50 0.011
(t/b )h2 0.93 <0.001 0.86 <0.001
MOR % Fiber wall area 0.83 <0.001 0.78 <0.001
% Parenchyma area 0.45 0.006 0.44 0.019
% Vessel area 0.41 0.010 0.42 0.023
dh 0.43 0.008 0.44 0.018
K S 0.11 0.221 0.32 0.06
Fiber wall thickness 0.10 0.179 0.35 0.015
Fiber lumen diameter 0.03 0.500 0.03 0.56
K (t/b)h2 0.04 0.387 0.08 0.30
S

% Fiber wall area 0.16 0.093 0.38 0.011
% Parenchyma area 0.04 0.428 0.09 0.25
% Vessel area 0.17 0.078 0.33 0.019

 

 

160

—- Brunia noduliflora .
Brunlaceae

 

 

Nebelia Iaevis

 

 

— Metalasia densa

 

 

 

—— Pteronia fasciculata Asteraceae

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

-— Pteronia panicula ta
1— Erica cerinthoides
Ericaceae
— Erica plukenetti
‘— Euclea sp. l Ebenaceae
— Aspa Ia thus pachyloba
Fabaceae
*— Aspalathus hirta
*— Cliffortia ruscifolia l Rosaceae
— ~—— Passerina obtusifolia I Thymelaeaceae
—- Searsia undulata I Anacardiaceae
Leucadendron laureolum
-— Leucadendron salignum
Proteaceae

--- Protea la urifolia

 

 

 

 

—— Protea repens

Figure 6.1. Phylogeny of 17 Species of evergreen shrubs sampled from J onaskop, in the
southwestern Cape of South Africa. The phylogeny was constructed using published
results referenced in the text and all branch lengths are assumed to be equal for
determination of phylogenetic independent contrasts. Family divisions are indicated by
the broken line on the right Side of the ﬁgure. We were unable to identify one species
(Euclea Sp.) beyond the level of genus (see Methods for details).

161

25 _ Leucadendron

(a) _ Female
. Male

2.0 -

lg (kg m'1 MPa" s")

 

4.0m)

 

Vessel Area (%)

 

 

80

(d)

Fiber Wall Area (%)

 

 

 

Figure 6.2. Xylem specific hydraulic conductivity (Ks) (a), mean hydraulic vessel
diameter (dh) (b), percent vessel area per transverse xylem area (c), and percent ﬁber wall
area per transverse xylem area (d) of females (black bars i 1 SE; n = 6) and males (grey
bars :1: 1 SE; n = 6) of two dioecious Species, Leucadendron laureolum and L. salignum.
Data were analyzed using unpaired t-tests and asterisks indicate signiﬁcance (* P S 0.05,
** P S 0.01, *** P 5 0.001, no asterisk = not signiﬁcant).

162

 

 

 

 

 

Figure 6.3. Minimum seasonal pressure potentials (ijn) measured in 2004 on 17
evergreen shrub species (1- 1 SE; n = 5-12). Pressure potentials for two Species (Pteronia
fasciculata and P. paniculata) exceeded the range of the pressure chamber (less than -10
MPa) and therefore their Pmin are unknown and error bars are lacking (see Results for
details). The horizontal line indicates the mean Pmin for 15 species (—3.4 MPa). The two
Pteronia Species have been excluded from this mean because Pmin for these species
exceeded the measurable range (less than -10 MPa) and are therefore lacking.

163

 

 

a
O
l-G-D-l

Xylem Density (kg m'3)

 

 

MOR (N mm'2)

 

 

r = 0.49‘

 

 

 

 

Pm." (M Pa)

Figure 6.4. Xylem density (a), mechanical strength against breakage (modulus of
rupture, MOR) (b) and the ratio of vessel wall thickness to lumen diameter squared, an
estimate of vessel implosion resistance ((t/b)h2) (c), as functions of minimum seasonal
pressure potential (Pm). Data points are means :1: 1 SE. Speciﬁc Pm," values for two
species (Pteronia spp.) are not known (see Results for details) and thus were not included
in regression analyses although they are included in the graphs (open squares). There is a
break in the y-axis in panel (c) and a change in scale above the break. In panels (13) and
(c) Su =' Searsia undulata. All regressions shown were signiﬁcant (P < 0.05).

164

 

700 (a) I +

MOR (N mm'2)

 

 

 

‘1
GI

50 l-

 

Fiber Wall Area (%)

 

 

 

 

 

 

 

 

400 500 600 700 800 200 350 500 650
Xylem Density (kg m'3) MOR (N mm'z)

Figure 6.5. Mechanical strength against breakage (modulus of rupture, MOR) (a),
percent ﬁber wall area per transverse xylem area (b & d), and the ratio of vessel wall
thickness to lumen diameter squared, an estimate of vessel implosion resistance ((t/b)h2)
(c & e) as functions of xylem density or MOR. Three data points signiﬁcantly inﬂuenced
the slope of the regression in panel (c) (open circles) and were excluded from the
regression Shown (see Results for details). In panels (a) and (b) Su = Searsia undulata.
To accomadate elevated (t/b)h2 values in three species, there is a break in the y-axis in
panels (c) and (e) and a change in scale above the breaks. All regressions were
signiﬁcant (P < 0.05).

165

 

r2=0.71

OD

 

h

Ks (kg 111'1 MPa" s")
N

 

 

 

 

O

20 30 40 50
Hydraulic Vessel Diameter (um)

Figure 6.6. Xylem Speciﬁc conductivity (Ks) as a function of hydraulic vessel diameter
(dh). Data points are Shown :1: 1 SE. A power model was used to ﬁt the data (P < 0.001;
y = 4.115'6 x3547).

166

.000 00:05:00 E00? :00 :03 .m 000 00.0 _03 0000 0:00:00 0:0 .3 00v 000

0830:0000 0:00:00 A> 000 000 0000., 0:00:00 0:0 .CIIC 0.005000 _03 :25 .00 0000800 :082 0000 .03 0000800 00.00.» 02:00.3
Add 50500080 050000 800? A0030: 000000: 50003:: _0mm0> 0000:0000 AMOS: 0.5000: .00 02:00:: 50:00 :00? .0050:
00:08: 0.50000: 0:808 8:800: ”030:8 00 0.0 m0m>0:0 0.0 E 000205 30.: E0§X .30 0:000:00 0:00:00005 000:0w00E:
0:0 00 0000 B0: :0 830:0 0:008:80 090500 .3 00580000 00 0000 030 w:o0 300 E00? w:o.:0 35:000—3— 80 0.5me

0.0.0.3 .002

 

 

 

 

0.0.50 .002

 

 

 

 

 

o. _. m6 cd m6. 0. _.I o. w md ad m6. c. T
a . u 0..- a a 0. P-
E 0
I .. 0.0. I . -I 00.
mo: .0". w :0»; u. .x. W
o 0 ﬂ. 0 mo: m.
:0... .u. .\. n. s 7. «=33 5...: z
1 ad \I 011 ad \I
70 a .x. .I.
.. > s . /o /o
I N 33 ._ . -I 0.0 0 - -I 0.0 hx
. 0 > .0
3.0000 . 0. . . . .
_ _ Ev . 0. . .0 I 00

 

 

a...

 

0;.

167

 

Figure 6.8. Light micrographs of xylem transverse sections illustrating differences in the
ratio of the double cell wall between two vessels to the vessel lumen diameter ((t/b).1 ).
Two of the species shown have extremely large (t/b)h2 values, Pteroniafasciculata (a)
and Pteronia paniculata (b), while two other species have (t/b)h2 values that fall within
the range of published values, Aspalathus pachyloba (c) and Protea repens (d). The inset
in panel (b) shows two vessels from a transverse section of P. paniculata enlarged to a
size comparable to vessels present in panels (c) and (d) to facilitate comparison of vessel
wall to lumen ratios. The black bar in each panel is 100 pm in length.

168

CHAPTER SEVEN

CAVITATION RESISTANCE IN FYNBOS AND SUCCULENT KAROO SHRUB

SPECIES AND MEDITERRANEAN -TYPE CLIMATE REGION CONVERGENCE

Summary

1 Arid and semi-arid shrub communities may differ in their water use strategies in
response to seasonal water deﬁcit and may be differentially susceptible to extreme
weather events.

2 Resistance to water stress induced xylem cavitation (W50) and xylem hydraulic
efﬁciency (Ks) were measured in 15 species from two shrub communities, fynbos and
succulent karoo, from the winter rainfall Mediterranean-type climate region of South
Africa. These data were correlated with anatomical and physiological data.

3 Species varied in the Shape and magnitude of their vulnerability to cavitation curves,
with a range in water potentials at 50% loss in hydraulic conductivity (T50) of -1.9 MPa
to -10.3 MPa. The mean ‘I‘so across species was -4.5 i 1.5 MPa. Fynbos and succulent
karoo species were not different in their T50.

4 The males and females of the dioecious species Leucadendron salignum were
signiﬁcantly different in their ‘I’so suggesting that, even within a species, this trait may be
a useful indicator of differential water use strategies.

5 Based on principle components analysis, fynbos species display a Similar water use
strategy to the vegetative and climatically similar chaparral Shrub vegetation community

of California as deﬁned by their ‘1150, minimum seasonal water potential (Twin), xylem

169

speciﬁc hydraulic conductivity (Ks), and xylem density, while succulent karoo Species
utilize a strategy that overlaps with that of the woody shrubs of the Mojave Desert.

6 The data suggest convergence of community and. species speciﬁc strategies between
these Mediterranean-type climate regions with respect to their xylem traits. The results

are discussed in the context of global climate change.

Introduction
The ﬁve Mediterranean-type climate regions are among the most biodiverse and
threatened in the world. These ﬁve regions contain nearly 20% of all vascular plant
Species but only occupy 5% of the earth's surface (Cowling et al. 1996). In a recent study
examining global biodiversity conservation priorities, these regions were recognized as
highly vulnerable to losses in biodiversity and regions in which recovery of degraded
ecosystems was highly unlikely (Brooks et al. 2006). Additionally, these regions have
been identiﬁed as being particullarly threatened by global climate change (IPCC 2007).
The Mediterranean-type climate region of south-westem South Africa stands out
as being uniquely diverse and particularly threatened. Additionally, predictions for future
climate in the region point to Signiﬁcant changes in water availability (Shulze & Perks
2000) and suggest that the ecology of the region may be highly threatened by such
changes (Lovett et al. 2005; Midgely et al. 2006). However, seasonal water relations
have only been studied among very few woody plant Species of South Africa (Miller et
al. 1983; M011 & Sommerville 1985; van der Heyden & Lewis 1989; Richardson &
Kruger 1990; Smith & Richardson 1990; J acobsen et al. 2007a). Additionally, published

data on cavitation resistance of woody Shrub Species from this region is lacking (however

170

see Jacobs et al. 2007 for data on four riparian species).

The woody, evergreen sclerophyllous shrubs that typify Mediterranean-type
climate regions appear to experience similar levels of water stress during the long
summer droughts that characterize the climate of these regions. This is supported by the
Similar range in and mean minimum seasonal water potential of plants in these regions
(Twmm; Martinez-Vilalta et al. 2002; Jacobsen et al. 2007a and 2007b). The shrubs of
these regions also display Similar ‘I’wmm to those reported for other arid and semi-arid
evergreen shrubland communities including species from the Great Basin Desert (Hacke
et al. 2000), the Mojave Desert (Chapter 3), the coastal sage scrub (Chapter 3), and the
Sonoran Desert (Pockman & Sperry 2000). Although a mean ‘Pwmin of approximately —4
to -5 MPa may represent a common physiological limit of these arid and semi-arid shrub
communities, it appears that species strategies for coping with this, level of water stress
vary greatly among these communities (Chapter 3).

The Mediterranean-type climate region of South Africa contains several plant
communities which differ in their average precipitation, topography, soil, etc., but which
often occur adjacent to one other in a patchwork across the broader landscape. Two such
communities are the fynbos and succulent karoo. Fynbos Shrub species occur in areas
that receive more rainfall than the succulent karoo and the shrub species are usually taller
than those which occur in the succulent karoo. Fynbos communities grade into succulent
karoo as one travels inland from the coast to areas of less precipitation. It is unknown if
shrub Species in these communities are utilizing similar xylem strategies in response to
protracted summer drought or if they are using different strategies and may be

differentially susceptible to climate change.

171

We examined vulnerability to cavitation of 15 Shrub species from South Africa at
an ecotone site between fynbos and succulent karoo vegetation communities. These data
were analyzed in tandem with previously reported ‘I’wmin data on these Shrub species in
order to examine their water use strategies. Knowledge of the cavitation resistance of
these Shrubs as it relates to ‘I’wmin may be useful in predicting species or communities that
are particularly sensitive to extreme water stress events in this region. Additionally, we
examined what anatomical traits are associated with increased cavitation resistance
among these Species. Lastly, data from these South African species were compared to
data from three semi-arid plant communities from North America in order to ascertain if
communities in these climatically similar regions are utilizing Similar strategies in
response to water stress, that is, if there is convergence in water stress tolerance among

shrub species and plant communities from different Mediterranean-type climate regions.

Materials and Methods

Xylem vulnerability to cavitation was measured in 15 species of evergreen sclerophyllous
shrubs located on Jonaskop in the Riviersonderend Mountain Range in the Western Cape
Province, South Africa (Table 7.1; see Jacobsen et al. 2007a for site and species
descriptions). Ten species were sampled from between 850 and 1020 m elevation and
typically receive around 420 mm of precipitation annually. Five species were sampled
from between 540 and 660 ft elevation and typically receive around 315 mm of
precipitation annually. This Site occurs across an ecotone with the 10 higher elevation
species occurring in fynbos vegetation while the 5 lower elevation species are more

Strongly associated with the succulent karoo vegetation community. These sites are

172

roughly comparable climactically to the chaparral and coastal sage Sites (approximately
460 mm of precipitation annual) and a Mojave Desert site (approximately 230 mm of
precipitation annually) of the California Mediterranean-type climate region and described
in J acobsen et al. (2007c). All Sites, both in South Africa and California, experience an
extended summer dry period and receive primarily winter rainfall as is typical of a
Mediterranean-type climate region.

Unbranched, straight stem segments approximately 6-8 mm in diameter and 30
cm long were collected in the ﬁeld during the early summer from 10 individuals per
species. Two Species were dioecious. For these Species stems were collected from 10
female individuals and 10 male individuals. Stems were trimmed underwater in Situ,
wrapped in moist paper towels, sealed in plastic bags, and shipped on ice to California
State University Bakersﬁeld, USA via international express shipping. Vulnerability to
cavitation was determined on stems as soon as they arrived and all stems were measured
within a week of being collected in the ﬁeld.

Stems were trimmed under water from both ends until a segment 4-8 mm in
diameter and 14 cm in length was obtained. Stems were connected to a tubing system
and ﬂushed for 1 h at 100 kPa and the maximum hydraulic conductivity (Khm) of stems
was measured gravimetrically (Sperry et al. 1988) using an analytical balance (CP124S,
Sartorius, Goettingen, Germany). Following determination of their Khmax, stems were
spun in a centrifuge (Sorvall RC-SC, Therrno Fisher Scientiﬁc, Waltham, MA, USA),
using a custom made rotor (Alder et al. 1997). Vulnerability to cavitation curves were
constructed by plotting the water potential (generated using the centrifuge) versus the

percent loss in hydraulic conductivity (PLC). For each stem, curves were ﬁt with a

173

second order polynomial model (J acobsen et al. 2007b). Cavitation resistance for each
species was estimated using the water potential at 50% loss in hydraulic conductivity
(W50) calculated from fatigue corrected curves using the conductivity following an initial
Spin of -0.25 MPa in place of Khmax (Hacke et al. 2000; Jacobsen et al. 2007c). Unpaired
t-tests were used to compare xylem traits of males and females of dioecious species
(Minitab v. 14.12, Minitab, Inc., State College, Pennsylvania, USA).

The xylem speciﬁc hydraulic conductivity (Ks) of stems was determined using the
methods described in J acobsen et al. (2007a). Xylem area (not including the pith) was
determined using a digital camera and image analysis software (Olympus SP-500UZ,
Olympus Imaging Corp., Center Valley, Pennsylvania, USA and Scion Image v. Beta
4.0.3, Scion Corp., Frederick, Maryland, USA). The Khmax was divided by the xylem area
to obtain xylem Speciﬁc conductivity (Ks).

Several anatomical and mechanical traits have been previously reported for all of
the species included in the present study (J acobsen et al. 2007a) except for the species
Erica vestita (see Table 7.2). These include the ﬁber associated traits of xylem density,
modulus of rupture (MOR), ﬁber lumen diameter, ﬁber wall thickness, and the
percentage ﬁber wall area per xylem cross sectional area, and the vessel associated traits
of vessel lumen diameter, vessel mechanical strength against implosion [(t/b)h2; Hacke et
al. 2001], and the percentage vessel area per xylem cross sectional area. We examined
which of these xylem traits were associated with T50. We also examined the relationship
between ‘I’so and ‘l’wmin and Ks. Correlations among ‘I’50 and these traits were examined
using both raw trait values and phylogenetic independent contrasts (PICs; Felsenstein

1985). Phylogenetic independent contrasts were run using the phylogeny reported in

174

J acobsen et al. (2007a) and COMPARE (Martins 2004). All interspeciﬁc comparisons
were analyzed using linear regression analyses (Minitab v. 14.12, Minitab, Inc.).

A principle components analysis was used to examine whether South African
Species were utilizing similar water stress tolerating strategies to those utilized by species
from Californian winter rainfall plant communities (Statview v.5.0.1, SAS Institute Inc.,
Cary, North Carolina, USA). Cavitation resistance (W50), Ks, xylem density, and
minimum seasonal water potential data (Twin) were included in the analyses for 28
species from California from previously published studies (J acobsen et al. 2007c,
Chapter 3). Data for these same four traits were included for 14 South African Species,
including ‘I’so and Ks from the present study and xylem density and Wm“ as reported in
J acobsen et al. (2007a). A MANOVA was used to examine whether the relationships
between these xylem traits differed among these communities and ANOVAS were used to

determine if communities’ multivariate components differed.

Results

Vulnerability to cavitation

Species varied in the Shape and magnitude of their vulnerability to cavitation curves,
displaying concave, convex, and linear shapes (Figure 7.1). In general, species displayed
very little cavitation fatigue, consistent with our sampling in early summer after the
growth of new xylem. Species displayed considerable variation in their resistance to
cavitation, with a range in water potentials at 50% loss in hydraulic conductivity (T50) of
-1.9 MPa (Searsia undulata) to -10.3 MPa (Passerina obtusifolia) (Figure 7.2). The

mean ‘I’so across Species was -4.5 :1: 1.5 MPa (Figure 7.2). Fynbos and succulent karoo

175

species did not signiﬁcantly differ in their resistance to cavitation (P = 0.277), although
the succulent karoo associated species displayed a broader range in cavitation resistances.

The males and females of the dioecious species Leucadendron salignum were
signiﬁcantly different in their cavitation resistance (P = 0.041), but they displayed similar
shapes to their vulnerability curves. The females were more resistant to cavitation than
the males, with an average ‘1’50 of -4.4 i 0.1 MPa for the females compared to -3.7 1 0.2
MPa for the males. In contrast, the males and females of the dioecious species L.

laureolum were not different in their cavitation resistance (P = 0.699).

Xylem anatomy and cavitation resistance

Across all species, cavitation resistance was correlated with anatomical traits of xylem
ﬁbers (Figure 7.3). Increased resistance to cavitation was associated with increased
xylem density (Figure 7.3 A; P = 0.007, r2 = 0.40), greater percentage ﬁber wall area per
cross sectional area (Figure 7.3 B; P = 0.001, r2 = 0.56), and increased stem mechanical
strength estimated by the modulus of rupture (Figure 7.3 C; MOR; P < 0.001, r2 = 0.79).
Fiber lumen diameter was also correlated with ‘1’50 (P = 0.023, r2 = 0.30; not Shown).
Fiber wall area and MOR remained correlated with ‘I’so when relationships were analyzed
using phylogenetic independent contrasts (PICs; P = 0.024, r2 = 0.33 and P = 0.029, r2 =
0.39, respectively); however, xylem density and ﬁber lumen diameter were not correlated
to ‘1’50 when PICS were used (P > 0.05). Fiber wall thickness was not correlated to ‘P50
when either raw traits or PICS were used (P > 0.05 for both; not shown). Thus, Species
with the greatest cavitation resistance have more ﬁber wall area per cross sectional xylem

area and have greater stem mechanical strength against breakage. Species with greater

176

cavitation resistance also tend to have increased xylem density than less resistant species,
but these traits are likely not evolutionarily linked and they are therefore likely not
functionally linked.

Cavitation resistance was also associated with vessel anatomical and functional
traits (Figures 7.3 and 7.4). Vessel lumen diameter (Figure 7.3 D; P < 0.001, r2 = 0.64),
theoretical vessel implosion resistance (the ratio of the vessel wall thickness to lumen
diameter [(t/b)h2]; Figure 7.3 E; P = 0.023, r2 = 0.30), and the percentage cross sectional
vessel area (Figure 7.3 F; P = 0.005, r2 = 0.42) were correlated with ‘I’so. Vessel lumen
diameter and percentage vessel area were also correlated with ‘I‘so when PICS were
analyzed (P =0.006, r2 = 0.45 and P = 0.030, r2 = 0.31, respectively); however, PICS of
(t/b)h2 and ‘I’so were not correlated (P > 0.05). Xylem Speciﬁc conductivity also was
correlated with ‘I’so when raw traits were analyzed (P = 0.020, r2 = 0.31), but not when
PICS were analyzed (P > 0.05; not shown). Thus, species with the greatest resistance to
cavitation have narrower vessel lumen diameters and less vessel area per cross section,
these combined traits likely result in more resistant species also displaying decreased
xylem efﬁciency (i.e. lower Ks). The lack of an evolutionary correlation between Ks and
Wm suggests that there may be changes occurring at the pit-level that uncouple changes in

these traits.

Water use “strategies”
Succulent karoo associated shrub species tend to experience lower seasonal water
potentials (Twin) than fynbos Shrub species, but are not signiﬁcantly different in their

cavitation resistance (0’50). Thus, these vegetation types appear to differ in their water

177

use strategies. Succulent karoo associated shrub species tend to fall above a 1:1 line of
‘P50 to ‘l’wmgn, suggesting that they would typically experience greater than 50% loss in
hydraulic conductivity annually (Figure 7.5). In contrast, fynbos shrub species tend to
fall below or on this 1:1 line suggesting they would typically experience 50% or less loss

in hydraulic conductivity annually (Figure 7.5).

Convergence among Mediterranean-type climate regions

Communities signiﬁcantly differed in the suites of xylem traits utilized by species (P <
0.001). Xylem traits were associated with two axes of variation. The ﬁrst principle
component (PCl) was associated with ‘I’wmin, xylem density, and Ks and explained 57% of
the variation among Species. Positive PClvalues are associated with higher ‘Pwmrn. lower
xylem density, and higher K.,. The second principle component (PC2) was associated
with ‘I’so and explained 20% of the variation among species. Positive PC2 values are
associated with lower cavitation resistance.

Fynbos and chaparral shrub species utilize similar suites of xylem traits and did
not differ in calculated values of either the ﬁrst or second components of a principle
components analysis (Figure 7.6; P > 0.05). Fynbos and chaparral species both tend to
fall in the lower right corner of this ﬁgure (Figure 7.6), consistent with a relatively safe
strategy of high cavitation resistance and comparatively low stress. The fynbos
“strategy” signiﬁcantly differed from the Mojave Desert Species in both PCI and PC2 (P
> 0.05 for both). Fynbos species did not differ from coastal sage in PCl (P > 0.05) but

did differ in values of PC2 (P = 0.006).

178

The succulent Karoo shrub species display widely variable strategies, but are most
closely associated with Mojave Desert species in PC] (Figure 7.7; P > 0.05 between the
Mojave Desert and succulent karoo) and with the chaparral and fynbos in PC2 (P > 0.05
for PC2 between the both the chaparral and fynbos compared to succulent karoo). These
species experience high water stress levels annually but are not very resistant to
cavitation relative compared to these water stress levels. Succulent karoo Species

differed from coastal sage species in values of both PCI and PC2 (P > 0.05 for both).

Discussion

Resistance to cavitation

Cavitation resistance varied broadly among 15 species from the Mediterranean-type
climate region of South Africa. Species displayed cavitation resistances (estimated as the
water potential at 50% loss in hydraulic conductivity; W50) ranging from -l.9 to -10.3
MPa and displayed as much variation within microsites as across the sampled ecotone.
Species displayed a mean cavitation resistance of -4.5 MPa which is not different from
that reported for angiosperms from other Mediterranean-type climate regions (Martinez-
Vilalta et al. 2002; Maherali et al. 2004; J acobsen et al. 2007b).

Cavitation resistance was correlated with various xylem ﬁber and vessel
anatomical and functional traits. Xylem density, percentage ﬁber wall area, and modulus
of rupture (MOR) were all correlated with cavitation resistance. Fiber wall area and
MOR were also correlated with ‘1’50 when data were analyzed taking into account the
evolutionary relationship among species (i.e. phylogenetic independent contrasts),

supporting a functional relationship among these traits. This is consistent with previous

179

studies that have found strong and phylogenetically independent correlations between
ﬁber traits and cavitation resistance (J acobsen et al. 2005; J acobsen et al. 2007b) and
between stem mechanical properties and cavitation resistance (J acobsen et al. 2005;

J acobsen et al. 2007b) in semi-arid Shrubs. These correlations suggest that xylem ﬁbers,
which largely determine xylem density and mechanical strength in angiosperms, may
play a role in cavitation resistance, perhaps through reinforcement of xylem vessel walls
against implosion (J acobsen et al. 2005). This points to a mechanical cost to increased
xylem cavitation resistance.

Vessel lumen diameter, vessel cross sectional area, and the theoretical implosion
threshold of vessels ([t/b]h2; Hacke et al. 2001a), were also correlated with cavitation
resistance. Decreased vessel lumen diameter was associated with increased cavitation
resistance and it may also be the driver for the relationship between (t/b)h2 and cavitation
resistance since this variable is partially dependent on lumen diameter (b). These vessel
traits increase the mechanical strength of vessels and, as with the ﬁber traits above, are
likely important in the resistance of vessel implosion in response to the extreme negative
pressures that develop in the xylem of arid and semi-arid shrubs. Smaller vessel lumen
diameters and reduced cross sectional vessel area both contributed to declined xylem
Speciﬁc conductivity (K5) in species with greater resistance to cavitation, leading to a
weak tradeoff between conductive efﬁciency and cavitation resistance. However, there is
no tradeoff between these traits when data are analyzed using phylogenetic independent
contrasts suggesting that this relationship may be due to community ﬁltering or selection

for some alternative trait, such as pit membrane area or Structure, rather than a direct

180

functional relationship between cavitation resistance and conductivity. However, there
may also be a conductivity efﬁciency cost to increased cavitation resistance.

Vessel and ﬁber anatomical traits may be useful in predictions of inter- or intra-
speciﬁc differences in cavitation resistance. For instance, Leucadendron salignum
females and males were found to differ in their cavitation resistance in the present study.
The sexes of this Species co-occur in the same microsites and experience Similar water
potentials suggesting that they may share similar resistances to cavitation; however, they
have previously been reported to vary in several xylem traits including Ks, vessel
diameter, vessel area, and ﬁber wall area (J acobsen et al. 2005). In contrast, the Ks,
vessel diameter, vessel area, and ﬁber wall area of females and males of Leucadendron
laureolum were not reported to differ and so it is not surprising that the sexes of this
Species are also not different in their resistance to cavitation.

Previous studies have examined the differences in water use between males and
females of dioecious Species. These studies have found that females often occur in more
mesic areas compared to males of the same species (Dawson & Bliss 1989; Dawson &
Ehleringer 1993) although females have also been reported to have a higher water use
efﬁciency than males in some Species (Correia & Diaz Barradas 2000). In the present
study, we found that females of the species Leucadendron salignum were more resistant
to cavitation than males of the same species. To our knowledge, this is the ﬁrst time that
a difference in cavitation resistance has been reported between the sexes of a dioecious
species. Additionally, the greater cavitation resistance of the females in this species
suggests that females may incur additional costs as carbon to xylem tissue to increase

cavitation resistance in order to maintain a steady water supply to developing fruit. This

181

is inconsistent with maternal investment hypotheses and may alter our understanding of
drivers and limits of sexual dimorphism in this genus (Bond & Midgley 1988; Bond &

Maze 1999).

Water use “strategies ” of fynbos and succulent karoo shrubs
The fynbos and succulent karoo Species included in the present study appear to be
utilizing differential Strategies for coping with summer water stress. The fynbos species
all experienced minimum seasonal water potentials that were the same or higher (less
negative) than their ‘I’so. This suggests that in a year of normal precipitation these species
will have dry season losses in hydraulic conductivity that are near or less than 50%. In
contrast, the succulent karoo species are not more resistant to cavitation than the fynbos
species, yet these species experience much more negative dry season water potentials. In
a typical year, these species are likely to reach higher percent losses in hydraulic
conductivity during the dry season, especially Searsia undulata and the Euclea Species.
The fynbos “strategy” appears Similar to that of other Mediterranean-type climate
region sclerophyllous shrublands including the California chaparral and mixed oak
forests of the Mediterranean Basin. Shrubs in these regions also typically reach water
potentials equivalent to 50% loss in hydraulic conductivity or less during the dry season
(Martinez-Vilalta et al. 2002; Jacobsen et al. 2007b and 2007c). Thus, in typical years
these species employ a relatively safe strategy consistent with their maintenance of full

canopies of leaves year round; however, this may be a risky strategy during extremely

dry years.

182

Evergreen shrubs in California and the Mediterranean Basin appear susceptible to
drought induced mortality during dry years (Lloret et al. 2004; Paddock 2006).
Additionally, individuals occurring at ecotones with drier vegetation communities may be
particularly susceptible as suggested by the high mortality observed among chaparral
species at a chaparral-desert ecotone during a drought year in California (Paddock 2006).
Shrubs in these communities may rely on avoidance of large declines in hydraulic
conductivity and most may not be able to adjust other traits, such as canopy area, in
response to declining water availability. Indeed, species that retain a nearly full canopy
often exhibit dieback, while co-occurring species that are able to facultatively thin their
canopy appear to survive in greater numbers (Pratt, personal communication).

The succulent karoo “strategy” appears most similar to that of desert shrubs which
also undergo high levels of embolism seasonally (Pockman & Sperry 2000; Chapter 3).
In drier areas, woody plants may be unable to avoid high levels of water stress and
concomitant losses in hydraulic conductivity and must therefore rely on traits other than
increased cavitation resistance, such as tight stomatal control or adjustment of leaf area
seasonally (Chapter 3). Succulent karoo shrub species may therefore be more able to
deal with annual rainfall variability than fynbos Species.

The coastal sage community of California is typiﬁed by facultatively deciduous
species which are sometimes referred to as “soft chaparral” because they are Similar in
form but lack the highly sclerophyllous leaves of the chaparral. We did not examine any
soft leaved Species from South Africa and there is little overlap between the coastal sage
and any of the studied sclerophyllous South African species examined in the present

study. This may be a separate water use “strategy” that is not utilized by species of the

183

fynbos or succulent karoo communities. However, there are some morphologically
similar plant communities in South Africa which may utilize a similar water use strategy

such as the coast Renosterveld.

Convergence among South African and Califomian plant communities

Morphologically and climactically similar plant communities from the Mediterranean-
type climate regions of South Africa and California appear to be convergent in the suites
of xylem traits utilized by species in relation to water stress. The plant communities of
the Mediterranean-type climate regions of South Africa and California have been
compared previously, resulting in mixed conclusions regarding plant convergence. Most
of these studies have focused on the dominant vegetation communities of these regions,
the fynbos and chaparral communities, and on plant structure and diversity rather than
physiological Strategies of plants (e. g. Cody & Mooney 1978; Barbour & Minnich 1990;
Keeley & Bond 1997). Limited comparisons have also been made between plants of the
succulent karoo and Mojave Desert (Esler & Rundel 1999).

Chaparral and fynbos communities, which are morphologically Similar (i.e. they
are woody, evergreen, sclerophyllous Shrubs) appear to converge in their water use
“strategy” as deﬁned by their cavitation resistance, minimum seasonal water potential,
xylem density, and hydraulic efﬁciency. The ﬁve Shrub species from the succulent karoo
included in the present study appear to be utilizing relatively divergent strategies in
regards to their xylem water use, although they share some overlap with sclerophyllous
Shrubs from the Mojave Desert consistent with these being drier and more variable

regions.

184

The apparent convergence in woody Shrub physiological strategies between these
climactically and morphologically similar plant communities suggests that these
communities may be similarly susceptible to climate change. The ability to compare
community and even species Speciﬁc strategies between these regions could provide
useful predictions for species and communities most likely to be affected by global
climate change. In addition, the ability to apply data measured in more thoroughly
studied Mediterranean-type climate regions and vegetation communities to those that
have been less studied could greatly enhance our ability to minimize the impact of

climate change on biodiversity in these regions.

185

Table 7.1. Species of evergreen shrubs located on J onaskop in the Riviersonderend

Mountain Range in the Western Cape Province, South Africa including species families
and the code used for each species in Figures 7.1, 7.2, 7.5, and 7.6.

 

Species Family Code
Fynbos

Aspalathus hirta E. Mey. Fabaceae Ah
Aspalathus pachyloba R. Dahlgren Fabaceae Ap
Cliffortia ruscifolia L. Rosaceae Cr
Erica plukenetti L. Ericaceae Ep
Erica vestita Thunb. Ericaceae Ev
Leucadendron laureolum (Lam.) Fourc. Females Proteaceae LIF
Leucadendron laureolum (Lam.) Fourc. Males Proteaceae LIM
Leucadendron salignum P.J. Bergius Females Proteaceae LsF
Leucadendron salignum P.J. Bergius Males Proteaceae LsM
Metalasia densa (Lam.) Karis Asteraceae Md
Nebelia Iaevis O. Kuntze Bruniaceae NI
Protea repens (L.) L. Proteaceae Pr
Succulent karoo

Euclea sp. Ebenaceae E
Passerina obtusifolia Thoday Thymelaeaceae Po
Pteronia fasciculata L.f. Asteraceae Pt
Pteronia paniculata Thunb. Asteraceae Pp
Searsia undulata (Jacq.) T.S. Yi, A.J. Miller & J. Wen1 Anacardiaceae Su

 

1 formerly Flhus undulata

186

Table 7.2. Xylem functional and anatomical traits for several xylem functional and
anatomical traits previously published in J acobsen et al. (2007a) and included in analyses
in the present study. See Chapter 6 for detailed methods and descriptions of data.

 

 

 

 

 

Species Xylem Density MOR 1pm," dh
Fjbos

Aspalathus pachyloba 570.5 1 31.0 279.2 1 12.2 -2.31 1 0.13 40.1 1 2.8
Aspalathus hirta 587.6 1 28.1 268.4 1 21.6 -2.48 1 0.10 26.4 1 1.8
Cliffortra ruscifolia 615.0 1 55.5 no data -2.89 1 0.15 31.1 1 1.3
Erica plukenetti 647.9 1 24.1 368.8 1 17.0 -4.20 1 0.30 26.6 1 0.9
Leucadendron laureolum (Females) 487.3 1 14.8 223.8 1 8.6 -2.06 1 0.11 32.0 1 1.6
Leucadendron laureolum (Males) 459.2 1 11.9 223.9 1 8.4 -1.84 1 0.04 33.5 1 0.5
Leucadendron salignum (Females) 518.6 1 15.9 262.1 1 21.8 -2.13 1 0.15 26.4 1 0.5
Leucadendrom salignum (Males) 536.1 1 18.1 253.7 1 14.1 -1.87 1 0.07 29.7 1 0.6
Metalasia densa 712.7 1 19.5 no data -3.37 1 0.16 23.5 1 0.9
Nebelia Iaevis 565.8 1 16.5 293.7 1 17.0 -3.68 1 0.13 21.2 1 0.3
Protea repens 579.2 1 17.4 225.1 1 4.7 -2.95 1 0.12 29.3 1 0.9
Succulent karoo

Euclea sp. 681.5 1 20.6 no data -4.88 1 0.20 39.0 1 1.6
Passerina obtusifolia 757.8 1 25.7 544.4 1 20.9 -5.94 1 0.79 21.5 1 0.9
Pteronia fasciculata 834.1 1 17.4 649.1 1 48.5 -10 18.0 1 0.8
Pteronia paniculata 860.0 1 23.3 583.9 1 36.4 -10 18.5 1 0.3
SearSIa undulata 764.0 1 15.5 267.1 1 19.1 -6.68 1 0.43 43.3 1 1.5

187

Table 7.2 (cont’d)

 

 

 

 

 

Fiber Lumen Fiber Wall Parenchyma Fiber Wall
(115).,2 Diameter Thickness (%) Vessel (%) (%)

0.021 1 0.003 6.19 1 0.61 3.57 1 0.15 13.6 1 0.7 15.5 1 1.5 55.8 1 2.8
0.030 1 0.002 5.13 1 0.38 3.65 1 0.19 13.4 1 0.8 15.0 1 2.2 59.5 1 2.4
0.031 1 0.004 5.69 1 0.37 4.34 1 0.38 4.5 1 1.1 11.6 1 0.9 70.4 1 3.0
0.048 1 0.003 5.18 1 0.14 3.66 1 0.27 4.7 1 0.2 13.8 1 1.0 67.3 1 1.1
0.019 1 0.002 5.95 1 0.41 3.76 1 0.13 7.4 1 2.1 18.2 1 1.2 59.9 1 1.3
0.019 1 0.002 6.28 1 0.28 3.42 1 0.07 6.3 1 0.9 18.7 1 1.6 57.8 1 1.2
0.026 1 0.001 6.51 1 0.33 3.23 1 0.04 8.3 1 1.6 9.1 1 0.6 61.8 1 1.4
0.021 1 0002 8.40 1 0.75 3.10 1 0.09 7.6 1 1.0 13.3 1 1.3 53.0 1 0.9
0.035 1 0.003 4.91 1 0.21 4.35 1 0.32 4.9 1 1.2 8.9 1 1.7 74.4 1 3.0
0.033 1 0.002 6.89 1 0.24 5.03 1 0.53 10.7 1 1.1 10.6 1 0.8 65.2 1 2.4
0023 1 0.001 6.63 1 0.25 3.54 1 0.21 9.7 1 1.7 16.9 1 1.1 56.3 1 1.5
0.051 1 0.004 3.45 1 0.26 3.50 1 0.14 9.3 1 0.8 11.4 1 1.0 70.8 1 2.6
0.129 1 0.013 4.34 1 0.32 3.75 1 0.19 3.9 1 0.7 8.6 1 1.5 75.8 1 1.8
0.241 1 0.024 3.02 1 0.04 3.40 1 0.10 2.4 1 0.3 9.9 1 1.4 79.3 1 1.3
019510.014 3.131010 3.161014 3.0104 11.4109 70111.0
0.040 1 0.003 6.31 1 0.27 3.05 1 0.20 10.6 1 1.5 14.6 1 1.5 55.3 1 2.5

188

Loss in Conductivity (%)

Figure 7.1. Vulnerability to cavitation curves for 15 evergreen shrub species from South
Africa depicting the percentage loss in hydraulic conductivity for a given decrease in
water potential generated using a customized rotor and centrifuge (see Methods for
details). Curves for monoecious species are shown with black ﬁlled circles, and for
dioecious species, curves from females are shown with grey triangles and for males with
open triangles. Species abbreviations are in black text for fynbos species and in grey
italics text for succulent karoo species. For key to species abbreviations, see Table 7.1.

 

 

 

 

 

 

 

60 --

20 --

“L A Females;
r2 = 0.98
- AMales;

. r2 1 0.98

 

 

  
 
 

:A Females;
r2 = 0.99
[A Males;

” . r2 |= 0.99

 

100 -

 

60 --
4o --
20 --

r

 

 

 

 

 

  

 

 

"r3 10.99.

 

-10

-8

-10 -8 -6 -4 -2 0
Water potential (MPa)

189

 

 

 

 

 

 

 

 

 

 

 

 

‘1’50 (MPa)

-10 1-

 

-12 _

 

 

-14

 

Figure 7.2. Cavitation resistance (W50) of 15 evergreen shrub species from South Africa,
estimated from fatigue-corrected vulnerability to cavitation curves (see Methods for
details). Bars represent species means 1 1 SE (monoecious species values are represent
as black bars, females from dioecious species as grey bars, and males from dioecious
species as open bars). Horizontal line indicates the across species mean cavitation
resistance of -4.5 MPa. Species abbreviations are in black text for fynbos species and in
grey text for succulent karoo species. For key to species abbreviations, see Table 7.1.

 

 

 

 

‘Pso (MP8)

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

60 70 80 90200300400500600700
Fiber Wall Area (%) MOR (N mm")

400 600 800
Xylem Density (kg m“)

 

 

12 l I
F. r = 0.42
- O . .

   

 

.2-

 

 

.4.

 

 

_6-

 

T50 (M Pa)

.8-

     

 

 

 

 

 

 

 

 

 

 

-10- - _ -
r2=.0.45 '
-12 i I l l i i i i i l i
10 15 20 25 30 35 0.0 0.1 0.2 0.3 8 10 12 14 16 18 20
Vessel Lumen Diameter (um) um)“2 Vessel area (%)

Figure 7.3. Xylem ﬁber and vessel anatomical traits as predictors of cavitation resistance
(‘1‘50) among 15 evergreen shrub species from South Africa. Xylem ﬁber associated traits
include xylem density (A), percentage ﬁber wall area per xylem cross sectional area (B),
and stem mechanical strength against breakage estimated by the modulus of rupture
(MOR) (C). Xylem vessel associated traits include vessel lumen diameter (D),
theoretical vessel implosion resistance [(t/b)h2] (E), and percentage vessel area per xylem
cross sectional area (F). Regressions of raw trait values are shown as ﬁlled circles and of
phylogenetic independent contrasts in insets as open circles (see Methods). Only
signiﬁcant regressions are shown.

191

 

Figure 7.4. Light micrographs of xylem longitudinal sections demonstrating some of the
xylem vessel anatomical differences among species. Passerina obtusifolia xylem (A)
displays the relatively narrow xylem vessels and thick vessel walls typical of very
resistant species. Leucadendron salignum male xylem (B) displays intermediate
cavitation resistance and has xylem vessel diameters and wall thickness typical of the
“average” species. Both micrographs were taken at the same magniﬁcation (lOOOx).

192

 

 

 

O I l l I ﬁ
Su E
- __ LI
2 ' a @E /%LIF/
E -4-+ / 12h" -
0- LSF
2 /// NI c.4189
V -6 -- / E _
O // Md
to P
9‘ '8 -i- p /// .—
/Pf/ Po j
‘10 "' /
/
/
I I I I I
I I l l 1

 

(MPa)

\Pwmin

Figure 7.5. Cavitation resistance (W50) plotted against minimum seasonal water potential
(Twin) for 15 species of evergreen shrubs from South Africa. Succulent karoo species
are represented by grey ﬁlled circles and italics text and fynbos species are represented
by black ﬁlled circles. Note, the ‘Pwmin values for the two Pteronia species (Pf and Pp)
shown are only approximate because they exceeded the limits of the pressure chamber
(‘I’Wﬁn < -10 MPa). The dashed line represents a 1:1 line. For key to species
abbreviations, see Table 7.1.

193

 

 

 

 

 

 

 

4
2 - -
N g 0
U 0
D.
2 _ @Fynbos
' v Succulent Karoo ‘ ~ - - — ’
(it Chaparral
{<32- Coastal Sage Scrub '29
'3.‘ Mojave Desert Scrub
-4 I I I I
-3 -2 -1 0 1 2 3

PC1

Figure 7.6. Relationships among species from South Africa to those from climatically
similar plant communities in California, USA as determined by principle components
analysis. The ﬁrst principle component (PC1) was associated with minimum seasonal
water potential (Tm), xylem density, and xylem speciﬁc conductivity (Ks) and the
second principle component (PC2) was associated with cavitation resistance (T50).
Positive PC1 values are associated with high seasonal ‘l’wmin, relatively high K, and low
xylem density. Positive values of PC2 are associated with low cavitation resistance (high
W50). Species from South Africa are shown as open triangles, with fynbos species as
upward pointing triangles and succulent karoo species as downward pointing triangles.
For key to South African species abbreviations, see Table 7.1. Communities included
from California include the chaparral (ﬁlled circles), the coastal sage scrub (open circles),
and the Mojave Desert scrub (ﬁlled triangles). See Chapter 3 for identiﬁcation of species
within the California plant communities.

194

CHAPTER EIGHT

CONCLUSION

Across arid communities, woody shrub species experience similar levels of water stress
and share several xylem traits associated with increased water stress tolerance. Species
that experience very low xylem water potentials seasonally have dense xylem and are
likely relying on mechanical reinforcement of both xylem vessel walls and the
surrounding ﬁber matrix for reinforcement against the threat of vessel implosion.
Additionally, there is a trend for species experiencing the lowest water potentials and
having the greatest resistance to cavitation to have decreased hydraulic efﬁciency
compared to less resistant species, suggesting that loss of conductivity efﬁciency may be
an additional cost of increased drought tolerance.

Species in arid communities also display species speciﬁc characteristics,
including differences in cavitation resistance and stomatal sensitivity to water stress
among three California arid communities. These community speciﬁc differences are
likely important in species response to biotic and abiotic differences among communities.
These community speciﬁc water use traits may also play a role in community assembly.
The trend for California aridland shrub communities (at the [3 level) to contain species
that are relatively closely related suggests that there are lineage speciﬁc functional traits
important for persistence in each community. Additionally, within communities (at the a
level) species tend to co-occur with other species utilizing similar xylem traits suggesting

that there may be microsite speciﬁc traits as well.

195

At the ecosystem level, comparable plant communities from the Mediterranean-
type climate regions of California and South Africa appear to be share many of the same
xylem structural and functional traits and to be utilizing similar water use strategies. This
suggests that these strategies may be common to winter rainfall aridland shrub
communities, even among species that are geographically and phylogenetically distant.

The apparent presence of community divergence and ecosystem convergence in
woody shrub physiological strategies between these aridlands shrub communities
suggests that these ecosystems and communities may be physiologically structured.
Future study of additional plant communities and ecosystems may enhance our
understanding of community assembly in arid shrublands and aridland ecosystem
functioning. Additionally, tests of physiological convergence among plant communities
may provide a use framework for understanding the relative roles of biotic and abiotic as

well as biogeographical inﬂuences on plant functional strategies.

196

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