H!

{

 

”Will

i

—
—
=
—
—
—
—
—
*
_
—
—
=

 

u. .-\4II

LIDHHH 1
Michigan State
University

 

 

This is to certify that the
thesis entitled

ADULT MORTALITY OF CHAPARRAL SHRUBS
FOLLOWING SEVERE DROUGHT

presented by

WILLIAM ALBERTSON STEBBINS PADDOCK III

has been accepted towards fulfillment
of the requirements for the

Master of Science degree in Plant Biology

 

 

«4% L

 

Major Professor’s Signature
‘I/ i 0 / o 6

Date

MSU is an Affirmative Action/Equal Opportunity Institution

- -,.-.-.-.-—.-.—.-.- .. -

PLACE IN RETURN BOX to remove this checkout from your record.
To AVOID FINES return on or before date due.
MAY BE RECALLED with earlier due date if requested.

 

DATE DUE DATE DUE DATE DUE

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

2/05 plelRC/DaleDue.indd-p.1

 

ADULT MORTALITY OF CHAPARRAL SHRUBS
FOLLOWING SEVERE DROUGHT

By

William Albertson Stebbins Paddock III

A Thesis

Submitted to
Michigan State University
in partial fulfillment of the requirements
for the degree of

MASTER OF SCIENCE
Department of Plant Biology

2006

ABSTRACT

ADULT MORTALITY OF CHAPARRAL SHRUBS
FOLLOWING SEVERE DROUGHT

By
William Albertson Stebbins Paddock llI

While drought is an annual event in Chaparral systems, adult mortality of the
woody shrubs is extremely rare. We examined a Chaparral shrub community that was at
an ecotone with a desert system and that had experienced widespread dieback following a
severe 5-year drought. The initial aim of the study was to quantify patterns of dieback,
detect whole plant mortality, and make comparisons of dieback among seven co-
dominant evergreen sclerophyllous species. Since mortality did occur, and varied
dramatically among species, we attempted to relate the mortality to post fire regeneration
strategy and to various physiological parameters such as xylem resistance to cavitation,
specific leaf area, predawn and midday xylem pressure potential and leaf stomatal
conductance, and transpiration rate. As expected, no general relationship between water
stress and mortality was observed. Contrary to predictions, mortality was significantly
higher in the two nonsprouting species, which had the most cavitation-resistant xylem
and lowest specific leaf area. An explanation for the surprising relationship between
mortality and water stress resistance is offered, based on rooting depth. Deep rooted
species appear to avoid water stress, possibly by accessing deep water resources available
even during the prolonged drought. Shallow rooted species (with roots < 1 m deep) are
denied this resource so they must tolerate water stress during annual summer droughts.
They were apparently unable to do so during the severe 4-year drought from 1998 to

2002.

DEDICATION

This work is dedicated to everyone that made it possible, from friends and family
to colleagues and mentors. I am fortunate to have been surrounded by so many great
people. Most of all I dedicate this to my wife, Carrie Tansy, who makes so much

possible for me.

iii

ACKNOWLEDGMENTS

I would first like to acknowledge my committee-- Dr. Frank Ewers, Dr. Peter
Murphy, and Dr. Carolyn Malmstrom-- for their guidance and assistance. I would like to
give special mention to Dr. Frank Ewers for doing everything a graduate advisor should
do for a student, but usually much more.

I would like to acknowledge Dr. Steve Davis, Dr. Brandon Pratt, and Anna
Jacobsen for helping me gain an understanding of the Chaparral system by sharing their
time, expertise, lab equipment, and lab space. Also, I thank Dr. Steve Davis and wife
Janet for sharing their home during my time working in California.

I would like to acknowledge Kate Kramer and others at the USDA Forest Service
in the San Bemardino National Forest who proved to be a valuable local resource and
were generous with time and resources.

I would like to acknowledge the accommodations and lab space made available
by the University of California reserve system, specifically James Reserve and Deep
Canyon Reserve.

I would also like to acknowledge MSU undergraduate Evin Jerkins for help in the
field on very early mornings and very hot afternoons.

Finally, I would like to acknowledge the generous funding provided for my work
by NSF grants 0131247 (awarded to Frank Ewers) and 130870 (awarded to Steven
Davis), by the Department of Plant Biology at Michigan State University through Paul
Taylor Travel Funds, and by the California Native Plant Society through the Educational

Research Grant Award.

iv

TABLE OF CONTENTS

LIST OF TABLES ........................................................................................................... vi
LIST OF FIGURES ........................................................................................................ vii
INTRODUCTION ............................................................................................................. 1
The Chaparral ................................................................................................................. 1
The Stuajz Site .................................................................................................................. 6
Research Objectives ........................................................................................................ 7
Hypotheses ...................................................................................................................... 7
MATERIALS AND METHODS ..................................................................................... 9
The Study Site .................................................................................................................. 9
Quantifiing Dieback ....................................................................................................... 9
Xylem Vulnerability to Cavitation ................................................................................ 11
Specific Leaf Area ......................................................................................................... 13
Xylem Pressure Potential .............................................................................................. 14
Transpiration Rates and Stomatal Conductance .......................................................... 15
Characterization of the Drought Period ....................................................................... 17
RESULTS ........................................................................................................................ 18
Dieback ......................................................................................................................... l 8
Xylem vulnerability ....................................................................................................... 19
Specific Leaf Area ......................................................................................................... 19
Xylem pressure potential ............................................................................................... 19
Transpiration Rates ...................................................................................................... 21
Precipitation Data ........................................................................................................ 21
DISCUSSION .................................................................................................................. 23
Species Eflects ............................................................................................................... 23
Site Eflects ..................................................................................................................... 29
Morphology ................................................................................................................... 30
Future implications ....................................................................................................... 31
FUTURE DIRECTIONS ................................................................................................ 34
LITERATURE CITED ................................................... Error! Bookmark not defined.

LIST OF TABLES

Table 1. Location, elevation, slope, and aspect of 7 sampling sites. Sites are listed in
order of increasing distance from the desert ecotone. Refer to Figure 1 for a map of
locations. Species are listed (see table 2 below for abbreviations) from left to right in
general order of occurrence on sites with increasing distance from the desert ecotone.
Species numbers indicate the quantity of individuals captured in the mortality survey.
Less than 60 individuals are listed in some sites if some woody species were sampled but
were too rare to be included in statistical analyses. .......................................................... 36

Table 2. A list of the seven species of woody shrubs co-dominant in the study
community. Abbreviations (Ab.) are given as they are used in figures. Authorities are
according to the Jepson Manual (Hickman, 1993). Life history strategy refers to
regeneration mode after fire or other disturbance that removes above-ground biomass. 36

vi

LIST OF FIGURES

Figure 1. Location of Study Site in Riverside County, CA, USA. The inset shows the
location of the seven sites used for sample collection. See Table 1 for latitude and
longitude of each site ........................................................................................................ 37

Figure 2. Specialized centrifuge rotor designed to exert tension on the xylem water
column. Plastic cups at each end of each stem segment keep the ends submerged in
deionized water while the rotor spins ............................................................................... 38

Figure 3. Vulnerability curves for 6 species showing mean i SE percent loss of
conductivity. The point where each curve intersects the horizontal dotted line represents
the pressure potential inducing 50% loss in conductivity (W50). Solid points represent
high mortality species. Open points represent low mortality species. Abbreviations as in
Table 2 .............................................................................................................................. 39

Figure 4. Measures of dieback recorded in 2003. Figure a shows mean :t SE dieback

score for seven species (scale of 1-no dead foliage, to 5-all foliage dead). A and B denote
significantly different dieback (p<0.0001). Figure b shows the frequency of death within
each of the 7 species. Abbreviations as in Table 2 .......................................................... 40

Figure 5. Comparison of physiological measures for the 7 species. Figures a + b
represent water stress resistance; Figures c-f represent water stress experienced. Bars
represent means :1: SE for the seven co-dominant species (abbreviations as in Table 2).
Letters adjacent to bars denote significantly different groups (p<0.05). Closed bars
indicate high-mortality species, open bars represent low-mortality species ..................... 41

Figure 6. Lines indicate a 7 year rolling average of annual rainfall for the area
surrounding the study site. Solid lines represent the 2 individual rain stations nearest to
the study site (Anza in grey; Deep Canyon in black). Dashed lines represent the climate
division in which each station is located (South Coast Drainage Climate Division in grey;
Southeast Basin Climate Division in black). Original data from NCAA (2005) ............ 42

vii

INTRODUCTION

The observation of widespread adult mortality in a community of Chaparral shrubs is
a rare event. A recent observation of such an event by Stephen D. Davis (Pepperdine
University, pers. comm, 2003), following a prolonged severe drought, provided a special
opportunity to observe and measure plant responses to water limitation. Most Chaparral
communities experience annual summer drought punctuated by winter rain; however, the
particular community we studied was at an ecotone with desert communities and thus
appears to have been particularly responsive to regional decreases in precipitation. In this
study, we looked for physiological characteristics that may relate to patterns in the

mortality of the woody shrubs in the community.

The Chaparral

“Chaparral” refers to the evergreen sclerophyllous shrub vegetation found in
southwestern North America. The Chaparral is the most extensive vegetation type in
California, dominating the foothills from the Sierra Nevada to the Pacific Ocean
(Wieslander and Gleason, 1954). These shrublands form a nearly continuous cover of
shrubs, ofien of similar height (i.e., 1.5-2.0 m) and with intertwining branches (Hanes,
1995).

While physiognomy is relatively consistent throughout the region, there is a great
amount of species diversity. More than 100 evergreen shrub species are found in the
Chaparral, only some of which are widespread in distribution (Keeley and Keeley, 1988;

Keeley, 2000). Local communities typically have multiple co-occurring species. There

are several factors that are known to affect local species composition, including moisture,
elevation, latitude, slope, aspect, fire history, and substrate (Hanes, 1995; Keeley, 2000).

The climate in this region is a key factor in the ecology of the Chaparral. The
Chaparral occurs in a region of Mediterranean-type climate with cool, moist winters and
hot, dry summers. In the winter (November to April) the Chaparral receives limited
rainfall (i.e., 200-1000 mm), which often falls in a few intense storms (Miller and Hajek
1981). Because winter rainfall typically occurs irregularly, there may be prolonged dry
periods even in the wet season (Keeley, 2000). There is usually no rain in the summers,
creating extremely dry conditions and resulting in annual drought. Hot, dry winds in the
late summer and early autumn add to the severity of the drought stress of the shrubs
(Hanes, 1995). The dry conditions of the vegetation in the summer, and the density of
shrubs which create large areas of contiguous fuel, provide ideal conditions for
propagation of wild fire.

Fire frequency in the Chaparral averages about once every 20 to 30 years,
although historically fire may have occurred less frequently (Keeley, 2000). Human
activity is the primary cause of present-day wildfires (Keeley, 2000); historically,
lightning strikes were the natural sources of fire ignition in the region. Chaparral fires
typically kill all aboveground biomass. The rate of shrub recovery varies with patterns of
precipitation, elevation, slope, aspect, and degree of coastal influence (Keeley and
Keeley, 1981; Hanes, 1995). Communities tend to return rapidly to their pre-fire
composition, illustrating the resilience of Chaparral to fire disturbance (Keeley, 1986;

Keeley, 2000).

Chaparral species are often categorized by life history strategy according to their
post fire regeneration method. After fire, some species resprout from a basal root burl
(i.e., “sprouters”). The seeds of these species are typically short-lived and germinate
readily with adequate moisture, but are killed in the intense heat of a fire. Thus, these
species fail to establish seedlings after a fire but persist at a site because individuals
survive fire events (Keeley, 1997; Keeley, 2000). Other species recruit from seed
following fire (i.e., “non-sprouters”) (Keeley and Keeley, 1988; Keeley, 2000). These
species are dependent on the fire disturbance to establish seedlings; recruitment is almost
non-existent in the absence of fire. Individuals do not survive fire events but species
persist at a site because of the existence of a long-lived seed bank (Keeley, 1977; Parker
and Kelly, 1989). Germination of these species is triggered by intense heat or by
chemical stimulus from charred wood or smoke (Keeley, 2000). A third, intermediate,
life history type has been termed “facultative sprouter” (Keeley and Keeley, 1988;
Keeley, 2000). These species use a combination of both sprouting and seed germination.
These species produce fire-resistant seeds but also have the capacity to resprout from a
basal burl (Keeley, 1986).

These patterns of post-fire regeneration result in what Hanes (1971) termed
“autosuccession” because with time a post-fire chaparral stand essentially regenerates
itself with much the same composition that was present pre-fire. The succession pattern
in the chaparral after fire is unusual compared to most plant communities; following fire
disturbance, the chaparral community does not return entirely to earlier seral stages
(Hanes, 1971). Although some of the same individual plants are present following fire,

other species may be present only temporarily following fire in the chaparral. In the first

year after fire, there is an abundant growth of herbaceous and suffrutescent vegetation,
often comprised of annuals. Many of these species are short lived, and by the third or
fourth year woody shrubs commonly dominate the site (Keeley, 2000). Further, many
shrub species are present on recently burned sites but are not found in mature chaparral
stands. These pioneer species may dominate burned sites several years after a fire, but
will die out gradually as the stand ages (Hanes, 1995). Hanes refers to the great bulk of
California chaparral as being in some stage of secondary succession; an apparently
mature, stable community is actually part of a cycle between stand regeneration from
seed and resprouts punctuated by destruction due to episodic fire. 1

From a biogeographical perspective, it is interesting to note that the dominant
woody genera of the California chaparral (i.e., Adenostoma, Arctostaphylos, C eanothus,
Heteromeles, and Rhus) are absent from other regions having a similar Mediterranean-
type climate (Hanes, 1995). Axelrod (1958) concluded that the entire California
chaparral evolved in place. Keeley (2000) and Axelrod (1989) reviewed the evolutionary
history of the chaparral shrub community and described several key environmental
factors driving the evolution of the system including topography, drought, edaphic
factors, and fire. While both sprouting and non-sprouting species are successful in
chaparral in the present day, according to Wells (1969) the sprouting strategy is ancestral
while the nonsprouting strategy is the derived trait. Axelrod (1989) proposed that fire
was important in driving speciation in the nonsprouting species, which are common in the
genera Arctostaphylos and C eanothus.

In addition to evolutionary implications, post fire regeneration strategy appears to

have associations with certain morphological characteristics. Sprouters (i.e., those that

regenerate from a root burl) tend to be more deeply rooted, whereas the non-sprouting
species tend to have more shallow root systems (Hellmers et al., 1955). Conversely, the
leaves of all chaparral shrubs are generally sclerophyllous, meaning “hard-leaved”
(Schimper, 1903), and having low specific leaf area (F ahn and Cutler, 1992).
Furthermore, many additional xeromorphic traits are seen in various chaparral species,
including sunken stomata, waxy cuticle, resistance to xylem cavitation, and dense xylem
(Krause and Kummerow, 1977; Blake-Jacobson, 1985; Langan et al., 1997; Ackerly et
aL,2002)

One final feature of chaparral vegetation is that, outside of fire events, adult
mortality is uncommon. In an extensive study of chaparral succession Hanes (1971)
sampled chaparral sites with costal and desert exposure in the San Gabriel and San
Bemardino mountains. Hanes reported the percentage of individuals that were dead, in
coastal stands of 4 age classes. Stands growing for 2-8, 9-21, 22-40, and over 40 years
since fire contained dead individuals representing 14%, 8%, 15%, and over 25% of the
communities, respectively. Hanes reported that while the desert communities were less
dense than the costal chaparral, desert stands contained smaller proportions of dead
individuals than similarly aged coastal chaparral. Compared to the rate of mortality in
adults, the regular summer drought in chaparral causes widespread mortality in seedlings.
Frazer and Davis (1988) reported mortality rates of 99.9% and 46% in Malosma laurina
and Ceanothus megacarpus, respectively, during the first summer drought after
germination. However, while there is evidence of drought-induced branch dieback in
adults (Davis et al., 2002); we are unaware of documentation of widespread whole-plant

mortality in adult chaparral shrubs following drought.

The Study Site

This study involved a community of chaparral shrubs located in Riverside
County, CA, near Pinyon Pines (Figure 1). The soils throughout the site are of the Trigo
family with rock outcrops common. The Trigo family soils are “loamy, mixed, nonacid,
thermic, shallow Typic Xerothents” (USDA, 2006). The site is particularly usefirl for
the study of water stress because it is located at the dry edge of the local chaparral range.
The area has been described by Hanes (1995) as desert chaparral. This indicates that the
plants are at the edge of their physiological tolerance for water stress. For chaparral
communities throughout California, the majority of rainfall occurs in the winter and is
limited, averaging from 200 to 1000 mm annually (Miller and Hajek, 1981). From 1963
to 2003, the average annual rainfall at our study site was 236mm, which is near the

lowest known for chaparral systems (NOAA, 2005).

Severe Drought

Based upon data collected at two weather stations in close proximity to the study
site, the area experienced a severe multiyear drought beginning in 1998. During this
time, drought was occurring throughout the southwestern United States. From 1998 to
2002 the average annual rainfall at the study site was only 103mm (N OAA, 2005). The
drought culminated during the 2001-2002 rainy season when only 73mm of rain fell
(N 0AA, 2005). No drought of this duration and magnitude had occurred in the previous
30 years (NOAA, 2005). This drought was followed by the rare observation of
widespread dieback in the adult shrubs around the study site, providing a special

opportunity to observe species differences in adult mortality.

Research Objectives

Our first objective was to quantify dieback and determine if adults were
experiencing whole plant mortality. We wanted to determine: 1) if plants were only
experiencing partial dieback of branches or if whole individuals were being killed
following the drought event, 2) if the frequency of dieback was different among the co-
dominant shrub species of the area, and 3) if certain physiological parameters associated
with water stress resistance, namely xylem vulnerability to cavitation and specific leaf
area, were associated with the patterns of mortality among species.

Our second objective was to determine if the life history strategy of these species
was related to the extent of drought-induced dieback experienced. Since differences in
water stress resistance have been associated with post fire regeneration strategy, we were
interested in determining if there was an association between life history strategy and the
dieback observed.

Our third objective was to determine if particular measures of water stress were
associated with the patterns of mortality among species. We used xylem pressure
potential, stomatal conductance, and transpiration rates to characterize the water stress

that species were experiencing.

Hypotheses

Based on the widespread occurrence and severe nature of the dieback we initially
observed, we hypothesized that we would find whole plant death for some individuals in
the community. We predicted that there would be species differences in this drought

induced mortality based on water stress resistance. We reasoned that species with low

xylem vulnerability (i.e., high resistance) to cavitation and low specific leaf area (i.e.,
thick leathery leaves) should be more resistant to water stress and should thus exhibit low
mortality.

Furthermore, we predicted that there would be differences in species’ mortality
based on life history type; nonsprouting chaparral species tend to be more resistant to
water stress (Davis, 1989) and thus should experience less dieback and mortality
following drought.

Finally, we predicted that the water stress that species experienced might be a
poor predictor of mortality following extreme drought since some species are known to
be more resistant to water stress (e.g., can tolerate more negative xylem pressure

potentials) than others (Blake-Jacobson, 1985).

MATERIALS AND METHODS

The Study Site

The widespread shrub mortality in this community was first recognized by
Stephen D. Davis (Pepperdine University, pers. com., 2003). Seven sites were selected
within the community to capture the variation in slope, aspect, and altitude of the area.
All data were collected from a community of chaparral shrubs of about 4000 ha located
in the San Bemardino National Forest in Riverside County, CA, USA, located north of
Santa Rosa Mountain along State Route 74 (N33°35’ W116°27’), near Pinyon Pines
(Figure l). The community is bounded by desert to the north and east, by forest to the
south and west, and is interspersed with Pinyon-Juniper woodland. Elevations of the

study sites ranged from 1100 m in the northeast to 1600 m in the southwest.

Quantifying Dieback

The community was sampled between April of 2003 and September of 2004. To
quantify differences in dieback among all woody species present, seven sites (Table 1)
were chosen to represent the diversity in both community composition and environmental
factors such as slope and aspect (Figure 1). Sixty plants were selected within each site
using a modified wandering quarter method (Catana, Jr., 1963). This method provides an
objective way to select plants and allows estimation of population density. At each site a
30 m base transect was set out perpendicular to the slope of the site. A 90° angle was
described using compass bearings so that the apex of the angle fell on the 0 m point of the

base transect and the bisector of the angle was pointing up the slope, perpendicular to the

base. The closest plant within this 90° angle was selected for data collection; this plant
was then used as the apex of the next 90° angle within which the next closest plant would
be selected. This process was used to select 15 plants. A total of four such wandering
transects was used at each site beginning at 0 m, 10 m, 20 m, and 30 m along the base
transect. This sampling identified seven co-dominant shrub species, which are listed in
Table 2.

Each plant was identified to species; height and two perpendicular crown
diameters were measured. The two crown diameters were used to calculate the crown
area by estimating it as an ellipse. The distance between the center of each plant and the
previous one was recorded and used to estimate density. Finally, each plant was given a
dieback score. Recently dead foliage could be distinguished from long-dead plants
because, like most chaparral shrubs, these species have tough, sclerophyllous foliage
which remains on the stems for a prolonged period after death. Dieback was assessed
visually on a scale from one to five. A value of one indicated that the plant had
essentially no dead foliage on the branches whereas a five indicated that the plant had
essentially no live foliage (and typically much dead foliage).

Differences in dieback among species were determined with pairwise
comparisons using Cochran-Mantel-Haenszel Statistics, controlling for differences
among sites. Within each species logistic regression was used to determine if plant
height, crown size, or distance from adjacent plants were correlated with mortality (i.e., a
score of 5). Forward selection was used to determine which parameters contributed
significantly to the logistic regression.

After the rainy season of 2003-2004, during which the 5-year drought eased

10

somewhat, we returned to the site in June 2004 to determine if the plants that had
previously scored 5 (i.e., no living foliage) were able to recover and produce any
functional photosynthetic tissue. A sub-sample of individuals that had been scored 5 was
located using GPS and markers lefi at the site in 2003. Once located, each plant was

scored for dieback again and a photograph was taken.

Xylem Vulnerability to Cavitation

To assess the vulnerability of the xylem to cavitation for each species, stem
segments were collected from healthy individuals at the site in August of 2003. A single
stem was taken from each individual sampled. Because it was not possible to locate all
seven species in one location, stems were collected from sites 4 and 7 (Figure 1). At site
4, samples of Bernardia incana, Quercus cornelius-mulleri, Rhus ovata, and
Arctostaphylos glauca were collected. At site 7, samples of Adenostoma fascieulatum.
Adenostoma sparsifolium, and Ceanothus greggii were collected. Six stem samples of
each species were collected and analyzed. Samples were free of side branches and
foliage and were selected to be as straight as possible. Each sample came from a stem
that supplied living foliage to indicate that the xylem was conductive. The presence of
conductive xylem was later verified by a lack of discolored xylem tissue in the samples.

To avoid the introduction of air embolisms into the xylem of the desired segment,
shoots approximately 2 m in length were cut from each plant and double-bagged in heavy
plastic bags with moist paper towel to prevent desiccation during transport. In the
laboratory the branches were cut to the desired length underwater in preparation for

vulnerability analysis by the centrifuge method (Alder et al., 1997). For most species 140

11

mm segments were used. In the case of C. greggii. it was necessary to use 271 mm
segments. The xylem of this species is very resistant to cavitation and the centrifuge is
capable of subjecting longer stems to greater tensions. In all cases the stem segments
used were 5-8 mm in diameter. After cutting the samples to the desired length, the ends
of each segment were shaved smooth with a razor blade to remove any obstruction to the
flow of water.

Rubber gaskets were placed on the ends of each stem sample and the samples
were then installed in a tubing manifold. The xylem was flushed with a 0.01 M solution
of HCl, which had been degassed and filtered to 0.1 pm, at a pressure of 100 kPa for at
least 1 h to remove any native embolisms. Following flushing, each stem was placed in
another tubing manifold to measure hydraulic conductivity (kh=mass flow rate per
pressure gradient, in m4mPa’ls") (Pockman and Sperry, 2000). Gravity was used to
create a pressure of approximately 2 kPa (4 kPa for A. glauca and A. sparsifolium) on one
side of the stern sample, which was sufficiently small to avoid displacing embolisms
during conductivity measurement. The mass of water leaving the other side of the
sample was measured on an electronic balance for a period of 60 s and an average flow
rate was calculated. In addition, flow rates were measured with the stem in the apparatus,
but before and after pressure was applied, so any background flow could be eliminated
from the measure of flow through the sample (Stiller and Sperry, 1999).

After the initial measurement of hydraulic conductivity the stems were spun in a
centrifuge to exert tension on the water column in the xylem. The stems were placed in a
specialized rotor that allowed the cut ends of the stems to be submerged in water as the

tension was applied (Figure 2). By controlling the speed of rotation the tension on the

12

xylem water can be carefully controlled (Alder et al., 1997). Initially the stems were
subjected to a tension of -0.5 MPa. Any xylem vessels that cavitate at this very low
tension have likely experienced cavitation fatigue and thus would never be conductive in
vivo (Hacke et al., 2001).Therefore, the hydraulic conductivity measured after the stem
had experienced -O.5 MPa was used as the maximum hydraulic conductivity and any loss
in conductivity was divided by that maximum to determine percent loss in conductivity
(PLC).

Each stem was subjected to alternating cycles of conductivity measurement and
centrifuge treatment through a series of increasing tensions. A vulnerability curve was
constructed for each stern by curvilinear regression of PLC as a function of tension
exerted by the centrifuge. These curves illustrate the cavitation vulnerability of the
xylem over a wide range of xylem tensions. A curve representing the means of each
species is shown in Figure 3.

The tension which caused 50% loss in conductivity (8’50) was determined for each
sample by interpolating the regression curve. Comparison of Wm was performed with
ANOVA using log transformed data and Tukey’s test for means separations to control

experimentwise error.

Specific Leaf Area

In June of 2004, leaves were collected from 12 individuals of each species. As
discussed above, it was not possible to locate all seven species in one location; therefore,
stems were collected from sites 4 and 7 (Figure 1). At site 4, samples of B. incana, Q.

cornelius-mulleri, R. ovata, and A. glauca were collected. Adenostomafasciculatum, A.

13

sparsifolium, and C. greggii were collected from site 7. Leaves were collected from the
same individuals used for vulnerability analysis and from additional plants to achieve a
total of 12 plants per species. All individuals used had mortality scores between 1 and 3.
For the broad leaved species 3 leaves were collected. However, due to the small leaf size
of A. fasciculatum and A. sparsifolium, 15 leaves were collected from each plant. All
leaves collected met the following conditions: had expanded in the previous year, from
sunlit branches, with no senescence, no physical damage, and no apparent disease.

The leaves were cut from the plants, placed in zip closure bags, and immediately
placed in a cooler. The leaves were stored for less than 48 hours before being processed.
In the lab, the petioles were removed and fresh mass was recorded. Then a LI-3100 Leaf
Area Meter (Li-Cor, Inc.) was used to determine the projected area of the leaves. The
leaves were dried at 80°C for several 24 hour periods until a repeatable mass was
obtained for each sample.

As an estimate of sclerophylly, specific leaf area (SLA) was calculated according
to the following equation

SL A = fresh pr0jected leaf area

 

(1)

dry mass
ANOVA was performed on logo transformed data and Tukey’s test was used to

control experimentwise error (p <0.050) for means separations.

Xylem Pressure Potential
In June of 2004, and again in August of the same year, leaves were collected for
measurement of xylem pressure potential from the same individuals used to measure

SLA. Again, 12 individuals from each species were measured each sampling period.

14

One sample from each plant was collected predawn (before 6am). A second was
collected midday (typically 1pm-3pm). The samples were cut, placed in a small zip
closure bag, and placed in a cooler for 1-2 h at which time water potential was measured
with a pressure chamber (Scholander et al., 1965).

The samples collected at midday in August were used to characterize minimum
seasonal pressure potential. Repeated Measures AN OVA was performed and Tukey’s
test was used to control experimentwise error (p <0.0001) for means separations.

Repeated Measures ANOVA showed no significant difference between predawn
water potentials from June to August (p>0.05); therefore, the predawn data were
aggregated for analysis. The predawn data are used as an estimation of soil water
potential in the soil surrounding the plant’s roots (Slatyer, 1967). Repeated Measures
ANOVA was performed and Tukey’s test was used to control experimentwise error (p

<0.0001) for means separations.

Transpiration Rates and Stomatal Conductance

In August of 2004 an LI-1600 Steady State Porometer (Li-Cor, Inc., Lincoln,
Nebraska) was used to measure transpiration rates and stomatal conductance. The
measurements were made at the end of the dry season because this is the time when the
greatest variance among species occurs. Measurements were made according to the Li-
Cor instruction manual (Li-Cor, 1989); however, the leaf temperature was also measured,
with an infrared thermometer, so that measurements of transpiration rate could be
corrected for true leaf temperature (Pearcy et al., 1991). Two different aperture caps

were needed because of the different leaf morphologies among the seven species. For Q.

15

cornelius-mulleri, R. ovata, and A. glauca the 1600-06 Small Aperture (0.66 cmz, Li-Cor,
Inc.) was used. For B. incana, A. fasciculatum. A. sparsifolium, and C. greggii the 1600-
07 Cylindrical Chamber (Li-Cor, Inc.) was used.

While using the small aperture, readings were taken from the top and bottom of
each leaf sampled because the aperture only measures transpiration on one side of a leaf;
these two sub samples were combined for analysis as one sample to make them
comparable to measurements taken with the cylindrical chamber. Two leaves per
individual were sampled. The porometer was set to 0.65 cm2 and the readings were later

corrected for the true aperture of 0.66 cm2 with the following calculation

g _ g x 0.65 cm2 (2)
corrected measured 0. 66 cm 2
with gcorrecte d equal to corrected stomatal conductance, and gmeasured equal to

measured stomatal conductance.

While using the cylindrical chamber, all surfaces of the several leaves on a single
branchlet contributed to the transpiration measured for each sample. Two samples were
measured for each individual. After measurement with the porometer the branchlet was
collected and stored in a zip-closure bag and immediately placed in a cooler. Back in the
lab the leaves were cut from their petioles and projected area for all leaves of each sample
was measured with a Li-3100 leaf area meter (Li-Cor, Inc.). This projected area was
doubled since the cylindrical chamber measures transpiration from both the top and
bottom surfaces of leaves. During measurement the porometer was set to use a leaf area
of 1 cm2 so the actual leaf area (i.e., 2 x projected area) was used to correct measurements

using the following equation

16

2

__ X 1 cm (3)
g corrected — g measured 2 2
x A 1 cm
with g equal to corrected stomatal conductance, g equal to measured
corrected measured

stomatal conductance, and A 1 equal to projected leaf area.

For measurements made both with the small aperture and the cylindrical chamber
transpiration rate was further adjusted for temperature. Any differences in temperature
inside and outside the cuvette make the measured transpiration (inside the cuvette)
different from the native transpiration rate (outside the cuvette); Pearcy et al. (1991)
described the calculations which can correct for this source of error.

For both stomatal conductance and transpiration rates AN OVA was performed on
logm transformed data and Tukey’s test was used to control experimentwise error (p

<0.050) for means separations.

Characterization of the Drought Period

Climatic Data were collected from the National Climatic Data Center’s (N CDC)
on-line database located at http://www.ncdc.noaa.gov/oa/ncdc.html (NOAA, 2005). The
primary data used were from two data collection stations: Anza and Deep Canyon. These
stations are located to the east (Anza 33°33'N/ 116°40'W) and west (Deep Canyon

33°39'N/ 116°23'W) of the study site.

17

RESULTS

Dieback

Seven species were observed in sufficient quantities to allow analysis of the
dieback scores: A. fasciculatum, A. glauca, A. sparsifolium, B. incana, C. greggii, Q.
cornelius-mulleri, and R. ovata (Table 2). Two species, C. greggii and A. glauca. had
significantly higher dieback than all other species, but did not differ from each other
(p=0.5296). The five remaining species also did not differ from each other (p=0.3208);
thus the seven species could be divided into low- and high-dieback groups, which
differed at p<0.0001 (Figure 4a).

Logistic regression of the mortality of A. glauca showed a small but significant
negative correlation (p=0.0150) with crown area: as crown area increased, dieback tended
to decrease. A similar relationship was observed for C. greggii (p=0.0277). This
relationship was only significant in the two species with high mortality; neither height
nor distance to adjacent plants were significantly correlated with mortality for any species
(p>0.05 for all comparisons).

Verification of mortality in 2004 showed that the vast majority of plants with
100% death of foliage in 2003 (score of 5) were completely dead. Ninety individuals that
were given a dieback score of 5 in 2003 were verified; only one was observed to have
any living foliage in 2004. This was an A. glauca individual. Since it is clear that a score
of 5 represented mortality, the two groups of species described above will hereafter be

referred to as the “low-mortality” and “hi gh-mortality” groups. Percentages of mortality

18

observed in 2003 were 66% and 75% for C. greggii and A. glauca, respectively. In the

low mortality group percentages ranged from 0% to 15% (Figure 4b).

Xylem vulnerability

In general, the high-mortality species tended to have xylem that is relatively
cavitation resistant. Arctostaphylos glauca and C. greggii had more negative mean
pressure potentials resulting in 50% loss of conductivity (9’50) than the low-mortality
species (Figure 5a). However, not all of the differences were statistically significant.
Arctostaphylos glauca did have xylem that was significantly more cavitation-resistant
than that of all low-mortality species (p=0.003) with the exception of A. fasciculatum (p=
0.138). The two species with the most vulnerable xylem were Q. cornelius-mulleri and
R. ovata; both were in the low-mortality group. The remaining species had xylem of

intermediate vulnerability (Figure 5a).

Specific Leaf Area

Specific leaf area (SLA) was generally higher in the low-mortality group. The
SLA was significantly higher for all low-mortality species than high-mortality species
(p<0.005) with one exception: R. ovata (low mortality) had a SLA not different (p=1.00)

from A. glauca (high mortality) (Figure 5b).

Xylem pressure potential

Predawn xylem pressure potential was used to characterize functional rooting

depth based on the assumption that the soil-plant continuum approaches water potential

19'

equilibrium during nighttime stomatal closure (Slatyer, 1967). Predawn pressure
potential divided the seven species into three significantly different groups. The group
with the least negative predawn pressure potentials included R. ovata, A. sparsifolium, Q.
cornelius-mulleri, and A. glauca. All these species experienced low-mortality except A.
glauca. The intermediate group consisted of two low-mortality species, A. fasciculatum
and B. incana. C eanothus greggii had significantly more negative predawn pressure
potential than all other species. Pairwise comparisons within all groups resulted in
p>0.36, but between all groups p<0.001. The two high-mortality species were at opposite
ends of the range of predawn pressure potentials observed, thus there was no apparent
relationship between predawn water potential and mortality (Figure 5c).

Minimum seasonal pressure potential, measured in 2004 at the end of the dry
season at midday, was used to estimate the maximum water stress experienced by each
species. Rhus ovata had a mean minimum seasonal pressure potential of -2.30 MPa
which was significantly less negative than all other species (p<0.0001). The remaining
six species fell into two significantly different groups. Those with intermediate minimum
seasonal pressure potentials included one high-mortality species, A. glauca, and two low-
mortality species, A. sparsifolium and Q. cornelius-mulleri which were not significantly
different from each other QFI). Another group of three species formed a group that had
the most negative minimum seasonal pressure potentials but were not significantly
different from each other (p>0.76); this group included two low-mortality species, A.
fasciculatum and B. incana, and one high-mortality species, C. greggii. There was no
overall relationship observed between minimum seasonal pressure potential and mortality

(Figure 5d).

20

Stomatal Conductance

One species, C. greggii, had a lower mean stomatal conductance than all other
species Q)<0.001) based upon measurements made in August of 2004. Ceanothus greggii
is in the high-mortality group. The other high-mortality species, A. glauca, was not
significantly different from the three low-mortality species with the highest stomatal
conductances, R. ovata, Q. cornelius-mulleri, and B. incana (p>0.051). The two
remaining species (both having low mortality) had intermediate stomatal conductance
and were significantly different than either high-mortality species (p<0.001). Thus, no

relationship between mortality and stomatal conductance was observed (Figure 5e).

Transpiration Rates
The pattern of transpiration rates among species was similar to the pattern in

stomatal conductance. Ceanothus greggii, a high-mortality species, had a lower mean
transpiration rate than all other species (p<0.001) with the exception of one low-mortality
species, A. sparsifolium (p= 0.089). The other high-mortality species, A. glauca, was not
significantly different from the three low-mortality species with the highest transpiration
rates, R. ovata, Q. cornelius-mulleri, and B. incana (p>0.114). The remaining species, A.
fasciculatum (low mortality), had an intermediate mean transpiration rate significantly
different than either hi gh-mortality species (p<0.001). Thus, no relationship between

mortality and transpiration rate was observed (Figure 5f).

Precipitation Data

The data files we obtained from the NCDC contained monthly precipitation for

21

Anza, Deep Canyon, and for each climatic division in which the stations are located.
Anza is located in the South Coast Drainage Climate Division while Deep Canyon is in
the Southeast Basin Climate Division (NOAA, 2001). The study site is located on the
border of two of these areas.

Due to the westerly movement of weather systems in the region and the decrease
in elevation from west to east, the Anza station generally receives more precipitation than
the study site while Deep Canyon generally receives less. Therefore, the precipitation at
the study site was estimated as the arithmetic mean of precipitation at the two stations.

Annual precipitation was calculated by summing monthly precipitation from July
of one year to June of the next. This is most biologically relevant because this includes
all of the rain from one wet season within one data point. Rolling averages were
calculated to smooth variation in annual precipitation in Figure 6; the arithmetic mean of
7 years, including a given year and the 6 previous years, were used.

From 1963 to 2003, the average annual rainfall at the site was estimated to be 236
mm. The average annual rainfall for the 5 year period from 1998 to 2003 was estimated
as only 103 mm. This is less than 44% of the site’s average. During the year from July
2002 to June 2003 it is estimated that only 73 mm of rain (31% of average) fell on the
study site (Figure 6). During the year from July 2003 to June 2004 the drought eased

some; it is estimated that 143 mm of rain fell on the site.

22

DISCUSSION

Species Eflects

Mortality of adult shrubs did occur, and it was more frequent among some species
than others, but the pattern was opposite to that we had expected; the highest proportions
of mortality were observed in the species that exhibited the greatest resistance to xylem
cavitation (lowest 9’50) and the greatest sclerophylly (lowest SLA). This resulted in a
relationship between life history type and mortality that was opposite to our prediction as
well. The nonsprouting species had higher proportions of mortality than the sprouting
species. Finally, we correctly predicted that the water stress experienced by the various
species would not be a good predictor of dieback or mortality, but the relationship
between life history strategy and the water stress experienced was not as expected.

Since it was expected that species with low ‘1’50 and low SLA should be resistant
to water stress, we predicted that these species would experience less mortality during the
drought. Sclerophylly has classically been considered a measure of water stress tolerance
(Schimper, 1903; Oppenheimer, 1960; F ahn and Cutler, 1992). Also, species with high
resistance to cavitation are less likely to have their water conduction compromised during
water limitation (Tyree and Sperry, 1989; Pockman and Sperry, 2000). Species with low
SLA are considered to be more conservative in water use (Oppenheimer, 1960; Fahn and
Cutler, 1992). Since more xeric sites tend to contain species with low xylem
vulnerability (Davis et al., 1999; Kolb and Sperry, 1999; Pockman and Sperry, 2000) and
more sclerophyllous leaves (Ackerly et al., 2002) it has generally been assumed that these

traits are advantageous for drought survival.

23

Species with more vulnerable xylem should be the first to experience cavitation
and eventually catastrophic failure of water conduction (Tyree and Sperry, 1989; Hacke
and Sperry, 2001). Species with more sclerophyllous leaves should be more resistant to
desiccation (F ahn and Cutler, 1992). Our conclusion that more resistant species were less
successful at surviving drought conditions suggests that water stress resistance alone
cannot predict success during a prolonged and severe drought. Specifically, the stress a
species experiences must be known to make predictions about the extent of dysfunction
caused. Since the data show that the more resistant species were actually more likely to
experience dieback and mortality it seems that co-occurring species were not
experiencing water stress in the same way.

Our quantification of water stress showed much variability and, as expected, little
relationship between water stress and mortality. One reason to expect differences in water
stress among species would be if different water stress coping strategies were being
utilized by each species. The various strategies for resisting water stress have been
reviewed thoroughly by Oppenheimer ( 1960) and later by Fahn and Cutler (1992). For
woody shrubs, the two available strategies are: l) to avoid tissue dehydration and 2) to
tolerate tissue dehydration (Fahn and Cutler, 1992). These strategies have characterized
by suites of characteristics that enable species to either avoid or tolerate water limitation
(Oppenheimer, 1960; F ahn and Cutler, 1992).

Reviews of xerophytism by Oppenheimer (1960) and Fahn and Cutler (1992)
have listed of dozens of strategies for success in xeric environments. One method of
avoiding tissue dehydration is to have deep roots with large root mass relative to shoot

mass, thus reducing the need to conserve water (Fahn and Cutler, 1992). Oppenheimer

24

(1960) asserts that since these species “spend much water” they should not be considered
xerophytes at all because they survive in arid environments by accessing ground water
available year-round. He points out that these species have few anatomical,
morphological, or physiological characters typically associated with xerophytes. Davis
(1989) also described this suite of characteristics, suited for avoidance of tissue
dehydration, in resprouting chaparral species. This avoidance strategy is plausible at this
site given that measurements of ground water depth from wells less than five km from the
study site show ground water to fluctuates between 6 m and 15 m below the surface
(California Department of Water Resources, 2006). Considering rooting depths observed
in some chaparral species by Hellmers et a1. (1955) and Thomas and Davis (1989) it is
reasonable to hypothesize that species could be accessing ground water.

Alternatively, species that resist water limitation by tolerating tissue dehydration
have relatively shallow roots; therefore, these species utilize xeromorphic adaptations
such as reduction in leaf area per mass (i.e. low SLA) and reduced stomatal conductance
(Fahn and Cutler, 1992). Davis (1989) described this suite of characteristics as being
associated with the nonsprouting chaparral species. Davis (1989) further suggests that
there are species in the chaparral that have an intermediate strategy (e. g. A. fasciculatum)
with intermediate rooting depth and intermediate stomatal conductances.

Another strategy to avoid tissue dehydration is the succulent habit as
characterized by members of the Cactaceae, Agavaceae, and Euphorbiaceae families
(Oppenheimer, 1960; F ahn and Cutler, 1992). This strategy is not found in chaparral but
is found in desert communities adjacent to the study site. This strategy is particularly

effective when rain is especially unpredictable and scarce (Oppenheimer, 1960).

25

The species examined in this study seem to represent a continuum from drought
evading to drought tolerating. Rooting depth may be the primary characteristic that
allows us to predict which strategies species will employ. Rhus ovata and Q. Cornelius-
mulleri are perhaps the most avoidance oriented species of the group. Both are likely to
be very deep rooted and so apparently can have higher transpiration and still experience
high xylem pressure potentials, thus they do not require highly resistant xylem to survive
the extreme drought. We are not aware of any published data from root excavation of
these species but closely related congeners of each have been observed to be some of the
deepest rooted species ever excavated in the chaparral (Hellmers et al., 1955; Thomas
and Davis, 1989). Regarding stomatal conductance and transpiration, our data show that
these two species had values among the highest, but they both maintained xylem pressure
potentials that were among the least negative. Since Poole and Miller (1975) showed that
stomatal closure occurred quickly in R. ovata, before xylem pressure potentials reach low
values (i.e., -3 MPa), the relatively high conductance and transpiration rates maintained
in the individuals we sampled is firrther evidence that the plants were not water stressed.
The fact that these plants did not experience great stress at the end of the summer drought
in 2004 suggests that the plants would not need highly resistant xylem in order to be
successful during drought. Therefore, it is not surprising that R. ovata and Q. Cornelius-
mulleri had the most vulnerable xylem but were still among the group of species with
extremely low dieback and mortality. In the case of R. ovata it has also been
demonstrated that the species has very low minimum transpiration rates; when
individuals are water stressed they are particularly effective at minimizing water loss

(Pratt et al., 2005).

26

Adenostoma sparsifolium appears to be next on the continuum from drought
avoidance to drought tolerance. Hanes (1965) measured the rooting depth of A.
sparsifolium and its congener A. fasciculatum to be just over 2 m deep. However,
physiological evidence collected from co-occurring individuals of the two species
suggests that A. sparsifolium has deeper roots than A. fasciculatum (Redtfeldt and Davis,
1996). Since A. sparsifolium has more shallow roots than R. ovata or Q. Cornelius-
mulleri it is advantageous for the species to reduce stomatal conductance and conserve
water. In this way A. sparszfolium can maintain xylem pressure potentials similar to
those of the two deep rooted species and can survive severe drought even with fairly
vulnerable xylem.

Further along the continuum from drought avoidance to drought tolerance is A.
fasciculatum. Two studies have excavated roots of this species. When Hellmers et al.
(1955) excavated roots of A. fasciculatum they found roots penetrating rock 8 meters
below the surface. At another location, Hanes (1965) measured the rooting depth of A.
fasciculatum to be just over 2 m deep. Direct measures of rooting depth are few in
number and therefore somewhat anecdotal, but as stated above, physiological evidence
suggests that this species has shallower roots than A. sparsifolium (Redtfeldt and Davis,
1996). Since we measured similar transpiration rates in the two species we would expect
A. fasciculatum to experience lower xylem pressure potentials. This too was observed in
the present study. Adenostomafasciculatum was still able to survive the extreme drought
because, compared to all the other low-mortality species, it has the most cavitation

resistant xylem.

27

Since A. glauca is a much shallower rooted species [less than 1 m deep (Hellmers
et al., 1955), or 0.3 m deep (Miller and Ng, 2005)] it has less access to deeper water
resources and is likely to experience low xylem pressure potentials during drought. This
did not seem to be the case when we measured minimum seasonal xylem pressure
potential at the end of the summer of 2004. At this time A. glauca maintained high
stomatal conductance while also keeping xylem pressure potential high. Poole and Miller
(1975) also observed that A. glauca maintains high conductance even while xylem
pressure potential gets quite low (i.e., to -5.5 MPa). Our xylem vulnerability curves
(Figure 3) show that this potential is not sufficient to cause much dysfunction in water
conduction. However, since the species has shallow roots, the situation must have been
different following the prolonged and severe drought from 1998 to 2003. During such a
dry time it appears that even though A. glauca had the most cavitation resistant xylem of
all species, there was not enough water available at such shallow soil depths, thus it
experienced a high frequency of mortality following the drought.

Like A. glauca, C. greggii is a shallow rooted species with roots growing less that
1 m deep (Hellmers et al., 1955; Miller and Ng, 2005). Lateral root growth is much less
than A. glauca (Hellmers et al., 1955; Kummerow et al., 1977). It too has less access to
water resources during drought; however, our data suggest that it compensates for this
with low stomatal conductance. Poole and Miller (1975) demonstrated that C. greggii
only reduced stomatal conductance when experiencing very low xylem pressure
potentials. This is consistent with our observation that C. greggii experienced the lowest
pressure potentials of all species in August of 2004. This species appeared to be the most

water stressed of all 7 co-dominant shrubs at the study site; it is not surprising that, even

28

though its xylem is resistant, it failed to function adequately during the prolonged
drought.

The fact that the seven co-existing species are utilizing different strategies along
the continuum from drought avoidance to drought tolerance suggests all of the strategies
are successful in this water-limited system. Hacke et al. (2000) described a similar
variety of strategies used by species in the Great Basin desert of Utah. On the other hand,
the extreme drought that occurred from 1998 to 2003 shows that drought avoidance may
be more effective when conditions get very dry. It appears that during this extreme event
the tolerance of A. glauca and C. greggii was surpassed by the water stress they
experienced, likely inducing catastrophic dysfunction of the xylem (Tyree and Sperry,

1989; Tyree and Ewers, 1991; Rood et al., 2000; Davis et al., 2002).

Site Effects

As was noted above, there was little clear relationship to measures of stress
experienced by a species and mortality thereof. However, there appears to be a
relationship between the four measures of drought stress and the site where the
physiological data was collected. As stated above, it was not possible to locate all seven
species at one site; therefore, physiological data was collected fi'om individuals at sites 4
and 7. Inspection of the data shows that the plants at site 7 appear to have been more
water stressed at the end of the 2004 dry season than the plants at site 4. Figure 6 shows
that B. incana, Q. cornelius-mulleri, R. ovata, and A. glauca which occur at site 4 all had
greater mean stomatal conductance and transpiration rates than the species at site 7, A.

fasciculatum, A. sparsifolium, and C. greggii. In almost all cases these differences were

29

significant, with the exception of R. ovata which was not different from two of the
species at site 7. A similar pattern is seen in xylem pressure potential, but the differences
between site 4 and 7 are less distinct (figure 6c and 6d).

It appears that site differences are best correlate with our measures of water stress.
It is know that soil moisture can have dramatic effects on transpiration rates (Pereira and
Chaves, 1993). Therefore, it is likely that there were differences in water availability at
site 4 and site 7. Still, it was surprising that site 7 contained the more stressed species
because appears to be the more mesic site; it is farther from the desert and has more
dense vegetation. It may be that in dry years the denser vegetation results in more

transpirational water loss from the soil.

Morphology

The inverse relationship between crown size and mortality in the two high-
mortality species is intriguing. One explanation for this pattern could be microsite
differences. An individual growing in a dry microsite would be more water limited,
resulting in reduced size (Stocker, 1960). Although increased root allocation can be a
response to drought (Stocker, 1960), root: shoot biomass allocation appears to be
relatively consistent within a species (Miller and Ng, 2005) so we would expect smaller
individuals to have shorter, perhaps shallower, roots than conspecific neighbors. Thus,
the higher mortality of small individuals could be due to small-crown individuals having

more shallow roots and/or to the smaller individuals occurring at drier microsites.

30

Future implications

It is notable that, although the site where this morality was observed has
experienced drought in recent years, the western United States has been wetter in this
century than it has been historically (Smith et al., 2001 ). The western United States has
also increased in temperature by 2-5°C this century (Smith et al., 2001). Smith et al.
(2001) examine two climate models, the Hadley and Canadian models, and make a
number of predictions for the next century: temperature is likely to increase by 8-11°C;
precipitation will likely increase (although the Canadian model suggests some chance
that the area will be drier); and there will likely be more extremes of wet and dry years.
The fact that the mortality observed in this study follows a five year dry period suggests
that the predictability of rainfall may be of particular importance to chaparral species.

For plants living in water-limited environments changes in temperature and

precipitation will have important implications for survival and recruitment. If the Hadley
model is correct, species that can take advantage of increased moisture may out-compete
the species that are currently present. If the Canadian model is correct and the area does
become drier, drought adaptations will be increasingly important for survival. Our data
suggests that the strategy plants use to cope with water limitation in the chaparral system
may affect their success as the climate changes.

Based on these climate models, it is possible, if not likely, that the climate in the
CA chaparral will become drier, and it is likely that rainfall will become more
unpredictable (Smith et al., 2001). Our results allow us to make several predictions for
chaparral systems at ecotones with more xeric ecosystems, assuming climate change fits

the predictions of the models (Smith et al., 2001). First of all, there will be effects on

31

species composition. Drought-tolerating, nonsprouting species will likely experience
widespread mortality and potentially be lost from these communities. Secondly,
seedlings of the drought-avoiding, sprouting species, which have more vulnerable xylem
and less sclerophyllous foliage, have a high frequency of mortality when water limited
(Davis, 1989). Therefore, recruitment will be very difficult, even for sprouting species.
The mortality in drought-tolerating, nonsprouting species and lack of recruitment in
drought-avoiding, sprouting species could result in desertification of chaparral stands that
grow at ecotones with desert communities.

However, if rainfall increases and occurs with the annual regularity that is typical
of the chaparral then our data would lead us to predict the opposite trend. With the
absence of drought-induced mortality there would be no regression of chaparral stands.
In addition, increased rainfall would support recruitment of sprouting species during fire
free periods and non-sprouting species afier fire events. The increased rainfall would
likely allow chaparral species to recruit in areas currently dominated by desert
communities.

In addition to the ecological effects there is evolutionary significance to the
patterns of mortality we observed. Of the various regeneration strategies, sprouting is
considered a relictual trait present in ancestors, which evolved in different ecosystems
(Wells, 1969). Nonsprouting is considered to be the derived trait in the chaparral
community and an adaptation to the frequent fire events in chaparral stands (Wells,
1969). Nonsprouters are most successful at recruiting new individuals after fire (Keeley
and Zedler, 1978). However, since both climate models predict that rainfall is likely to

be more unpredictable, severe drought events may become as frequent as fire events; if

32

this occurs, our data suggest that sprouting species may have a strong survival advantage.
Severe drought events would result in mortality in nonsprouters as reduced fire frequency
restricts recruitment in those species since they require fire for germination. The
reduced rainfall predicted by the Canadian model would reinforce this trend since
drought conditions would reduce the density of individuals in chaparral communities,
reducing the extensive spread of fire. On the contrary, if the Hadley model is correct the
increased moisture would result in denser chaparral vegetation and improved fire
propagation. It is interesting to note that in desert communities fire is not important in
driving community structure (Brown and Minnich, 1986). If increased moisture results in
more dense vegetation thus increasing the propagation of fire in areas of desert then fire
could contribute to the replacement of desert with chaparral communities.

As global climate change continues, the southwestern United States will likely
provide many opportunities to examine the effects on plant ecology and biogeography.
Prior to this study, subleathal effects of drought have been reported in woody plant
communities (Parsons et al., 1981; Rood et al., 2000; Davis et al., 2002) but there has
been no documentation of widespread drought-induced mortality in chaparral
communities. However, as communities respond to the changing climate and species
distributions shift, it is likely that widespread mortality will be observed at ecotones and
we will be provided with many opportunities to learn more about the survival value of

strategies for success in the water-limited chaparral system.

33

FUTURE DIRECTIONS

The dramatic difference in mortality between deep rooted and shallow rooted
species suggests several promising directions for research. Since there has been little
direct measurement of rooting depth it would be valuable to excavate plants to learn more
about variation in rooting habit both within and among species. It is also true that our
real interest is not the depth of roots but rather in their ability to access water resources.
If, as Oppenheimer (1960) suggests, extremely deep rooted species like R. ovata and Q.
cornelius-mulleri are accessing ground water, then stable isotope analysis, which
characterizes active rooting depth (Ehleringer and Dawson, 1992), should be very
effective at differentiating water resources used by deep rooted and shallow rooted
species. For example, Williams and Ehleringer (2000) examined hybrid Quercus plants
and identified individuals that avoided drought by accessing deep water sources. If the
active rooting depths of the species in this system are congruent with rooting depths
estimated from excavations, it would provide verification of the patterns of tolerance and
avoidance proposed above.

There would also be value in expanding the suite of anatomical and physiological
characteristics associated with mortality in the current study by making additional
measures on plants in this community. We demonstrated that high xylem resistance to
cavitation and low specific leaf area, both commonly associated with drought adaptation
(Oppenheimer, 1960; Fahn and Cutler, 1992), were associated with high mortality
following severe drought. Measuring xylem parameters such as specific conductivity,

hydraulic mean vessel diameter, vessel implosion resistance, xylem density, and the

34

mechanical strength of stems would likely elucidate additional patterns since each has
been associated with water stress resistance (Wagner et al., 1998; Hacke and Sperry,
2001; Martinez-Vilalta and Pinol, 2002; Jacobsen et al., 2005).

Finally, the sampling methods used here did not thoroughly address ecological
factors that likely influenced the incidence of mortality in this community. Species
identity was clearly very important in determining which individuals experienced
mortality. However, ecological factors such as slope inclination, slope aspect, elevation,
and various microsite differences almost certainly influenced mortality as well. Trends in
global climate predict even drier times to come for the southwestern United States
(Sheppard et al., 2002). If widespread mortality reoccurs it will be important to
characterize ecological patterns of mortality using classical ecological methods on the

local scale and remote sensing techniques to characterize patterns on the landscape scale.

35

TABLES

Table 1. Location, elevation, slope, and aspect of 7 sampling sites. Sites are listed in
order of increasing distance from the desert ecotone. Refer to Figure l for a map of
locations. Species are listed (see table 2 below for abbreviations) from left to right in
general order of occurrence on sites with increasing distance from the desert
ecotone. Species numbers indicate the quantity of individuals captured in the
mortality survey. Less than 60 individuals are listed in some sites if some woody
species were sampled but were too rare to be included in statistical analyses.

 

Site Lat; Lon Elevation Slope Aspect Species
(deg N; W) (m) (deg) (deg) Bi Ag Ro (go Cg As Af
3 33.604;116.422 1103 12 108 28 22 4
1 33.587;116.437 1339 30 250 48 2 7

4 33.592;116.444 1265 07 168 22 5 4 21

5 33568;] 16.444 1453 26 020 2 2 5 41 10

2 33.577;116.460 1259 06 035 2 7 46 5
6 33.565;116.477 1502 30 008 2 4 53 l

7 33.549;116.508 1591 11 225 13 18 29

 

Table 2. A list of the seven species of woody shrubs co-dominant in the study
community. Abbreviations (Ab.) are defined. Authorities are according to the
Jepson Manual (Hickman, 1993). Life history strategy refers to regeneration mode
after fire or other disturbance that removes above-ground biomass.

 

 

Species Ab. Family Life history strategy

A denostoma fasciculatum Hook. & Am. Af Rosaceae (Sggzlétsiplggfi)

Rhus ovata S. Watson Ro Anacardiaceae Eggnugigfd Juhren, 195 1)
Adenostoma sparsifolium Torrey As Rosaceae (sagginlggfi)

Sprouting

Quercus corneltus-mullert K. Nixon & K. Steele Qc Fagaceae (Nixon, 2002)

Bernardia incana C. Morton Bi Euphorbiaceae unknown

Nonsprouting
(Keeley and Zedler, 1978)

Nonsprouting
(Keeley, 1977)

C eanothus greggii A. Gray Cg Rhamnaceae

Arctostaphylos glauca Lindley Ag Ericaceae

 

36

FIGURES

    

 

V

r I l
9‘ Site 3
o 3:;-
Q ’0
fl

4
a Pin nP’nes .
0 yo 1
j 0 O T U1 Site

_

 

 

 

 

Figure 1. Location of Study Site in Riverside County, CA, USA. The inset shows the
location of the seven sites used for sample collection. See Table 1 for latitude and
longitude of each site.

37

Figure 2. Specialized centrifuge rotor designed to exert tension on the xylem water
column. Plastic cups at each end of each stem segment keep the ends submerged in
deionized water while the rotor spins.

 

 

Ro
Qc
As
Af

120 r

100-

ODOD<04

Ag

 

Percent Loss of Conductivity (%)

 

 

 

l l l l l l

 

-14 -12 -10 -8 -6 -4 -2 0
Xylem Pressure Potential (MPa)

Figure 3. Vulnerability curves for 6 species showing mean 3: SE percent loss of
conductivity. The point where each curve intersects the horizontal dotted line represents
the pressure potential inducing 50% loss in conductivity (W50). Solid points represent

high mortality species. Open points represent low mortality species. Abbreviations as in
Table 2.

39

 

 

 

Dieback Score
is»
l

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

A TA
A TA I .1.
2* T
.L .L
1
8° n
e§6o
E“ “
a5
32
E540*
'59..
.59
H'o'
°4=
$320"
0 T If I 1
Af Ro As Qc Bi Cg Ag
Species

Figure 4. Measures of dieback recorded in 2003. Figure a shows mean i: SE dieback
score for seven species (scale of l-no dead foliage, to 5-all foliage dead). A and B denote
significantly different dieback (p<0.0001). Figure b shows the frequency of death within
each of the 7 species. Abbreviations as in Table 2.

40

Pressure Potential Inducing
50% Loss of Conductivity (MPa)

Predawn Xylem Pressure

Stomatal Conductance

(mmol m'2 s'l)

Potential (MPa)

.'..
e

L.
A

G

 

 

l-I
N

 

 

 

 

 

G

I
N

L

 

Ah

 

 

 

 

 

 

 

 

 

36o

 

'5’

b

N
6

t—n
e
a

 

 

 

 

 

 

 

AfRo As Qc Bi Cg Ag
II! It ill Ill

Species

Area (cm2 g‘l)
N u a
e 9

Specific Leaf
c

10'

G

a L t'o

Mrnrmum Seasonal Xylem
Pressure Potential (MPa)
do

 

0|
9

Ma

 

 

 

 

 

 

 

 

 

 

 

 

>

 

 

 

 

 

 

 

 

 

 

 

 

 

 

~10
1.8
1.6
g I
g : 1.4
a in 1.2 '
.2 '7' 1 0
a E '
-a 'g 0.8
g g 0.6
E- 0.4
0.2
0.0

[‘1

 

 

 

 

   

 

 

Af Ro As Qc Bi Cg Ag

*

*

Species

1'

Figure 5. Comparison of physiological measures for the 7 species. Figures a + b

represent water stress resistance; Figures c-f represent water stress experienced. Bars
represent means t SE for the seven co-dominant species (abbreviations as in Table 2).

Letters adjacent to bars denote significantly different groups (p<0.05). Closed bars

indicate high-mortality species, open bars represent low-mortality species. * Denotes

species for which physiological data was collected at site 4; such data for the other
species was collected at site 7.

41

600

 

500

400

’f l

300 l

Annual Rainfall (mm)

200 *

100

 

 

 

 

1965 1975 1985 1995 2005
Year

Figure 6. Lines indicate a 7 year rolling average of annual rainfall for the area

surrounding the study site. Solid lines represent the 2 individual rain stations nearest to
the study site (Anza in grey; Deep Canyon in black). Dashed lines represent the climate
division in which each station is located (South Coast Drainage Climate Division in grey;
Southeast Basin Climate Division in black). Original data from NCAA (2005).

42

LITERATURE CITED

ACKERLY, D., C. A. KNIGHT, S. B. WEISS, K. P. BARTON, AND K. P. STARMER.
2002. Leaf size, specific leaf area, and microhabitat distribution of chaparral woody

plants: contrasting patterns in species level and community level analysis. Oecologia 130:
449-457.

ALDER, N., W. T. POCKMAN, J. S. SPERRY, AND S. NUISMER. 1997. Use of
centrifugal force in the study of xylem cavitation. Joum_al of Experimentgl Botaml 48:
665-674.

AXELROD, D. I. 1958. Evolution of the Madro-Tertiary geoflora. Botanical Review 24:
433-509.

----- 1989. Age and origin of chaparral. In S. C. Keeley [ed.], The California Chaparral:
paradigms reexamined, 7-19. natural History Museum of Los Angeles County, Los
Angeles.

BLAKE-JACOBSON, M. E. 1985. Stomatal conductance and water relations of shrubs
growing at the chaparral-desert ecotone in California and Arizona. In J. D. Tenhunen, F.
M. Catarino, O. L. Lange, and W. C. Oechel [eds.], Plant Responses to Stress, vol. 15,
223-245. Springer-Verlag, Berlin.

BROWN, D. E. AND R. A. MINNICH. 1986. Fire and changes in creosote bush scrub of
the western Sonoran Desert, California. American Midland Naturalist 116: 411-422.

CALIFORNIA DEPARTMENT OF WATER RESOURCES. Groundwater well data for
California. https://wd1.water.ca.gov. 2006.

CATANA, A. J ., JR. 1963. The wandering quarter method of estimating population
density. Ecology 44: 349-360.

DAVIS, S. D. 1989. Patterns in mixed chaparral stands: Differential water status and
seedling survival during summer drought. In S. C. Keeley [ed.], The California
Chaparral: Paradigms Reexamined 97-105. Natural History Museum of Los Angeles
County, Los Angeles.

DAVIS, S. D., F. W. EWERS, J. S. SPERRY, K. A. PORTWOOD, M. C. CROCKER,
AND G. C. ADAMS. 2002. Shoot dieback during prolonged drought in C eanothus
(Rhamnaceae) chaparral of California: a possible case of hydraulic failure. American
Journgl of Botgnv 89: 820-828.

DAVIS, S. D., F. W. EWERS, J. WOOD, J. J. REEVES, AND K. J. KOLB. 1999.
Differential susceptibility to xylem cavitation among three pairs of Ceanothus species in
the Transverse Mountain Ranges of southern California. Ecoscience 6: 180-186.

43

EHLERINGER, J. R. AND T. E. DAWSON. 1992. Water-uptake by plants - perspectives
from stable isotope composition. Plant Cell and Environment 15: 1073-1082.

F AHN, A. AND D. F. CUTLER 1992. Xerophytes. Gebriider Bomtraeger, Berlin.

FRAZER, J. M. AND S. D. DAVIS. 1988. Differential survival of chaparral seedlings
during the lst summer drought after wildfire. Oecologip 76: 215-221.

HACKE, U. G. AND J. S. SPERRY. 2001. Functional and ecological xylem anatomy.
Perspectives in Plant Ecology, Evolutionfi and Systematics 4: 97-115.

HACKE, U. G., J. S. SPERRY, AND J. PITTERMAN. 2000. Drought experience and
cavitation resistance in six shrubs from the Great Basin, Utah. Basic and Applied
Ecology 1:31-41.

HACKE, U. G., V. STILLER, J. S. SPERRY, J. PITTERMANN, AND K. A.
MCCULLOH. 2001. Cavitation fatigue. Embolism and refilling cycles can weaken the
cavitation resistance of xylem. flant Physiology 125: 779-786.

HANES, T. L. 1965. Ecological studies on two closely related chaparral shrubs in
southern California. Ecologicfldonogpaphs 35: 213-235.

----- . 1971. Succession after fire in the chaparral of southern California. Ecological
Monographs 41: 27-52.

----- 1995. California chaparral. In M. G. Barbour and J. Major [eds.], Terrestrial
vegetation of California. New expanded edition, 417-469. California Native Plant
Society, Davis, California.

HELLMERS, H., J. S. HORTON, G. JUl—IREN, AND J. OKEEFE. 1955. Root systems
of some chaparral plants in southern California. Ecology 36: 667-678.

HICKMAN, J. C. 1993. The Jepson manual: Higher plants of California. University of
California Press, Berkeley and Los Angeles, California.

JACOBSEN, A. L., F. W. EWERS, R. B. PRATT, W. A. PADDOCK, AND S. D.
DAVIS. 2005. Do xylem fibers affect vessel cavitation resistance? Plant Physiology 139:
546-556.

KEELEY, J. E. 1977. Seed production, seed populations in soil, and seedling production
afier fire for two congeneric pairs of sprouting and nonsprouting chaparral shrubs.
Ecologv 58: 820-829.

----- 1986. Resilience of Mediterranean shrub communities to fire. In B. Dell, A. J. M.

Hopkins, and B. B. Lamont [eds], Resilience in mediterranean-type ecosystems, 95-112.
Junk, Dordrecht.

44

----- . 1997. Seed longevity of non-fire recruiting chaparral shrubs. Four seasons 10: 36-
4;.

----- 2000. Chaparral. In M. G. Barbour and W. D. Billings [eds], North American
terrestrial vegetation, 203-253. Cambridge University Press, Cambridge.

KEELEY, J. E. AND S. C. KEELEY. 1981. Postfire regeneration of California chaparral.
American Journal of Botanv 68: 524-530.

----- 1988. Chaparral. In M. G. Barbour and W. D. Billings [eds], North American
terrestrial vegetation. 165-207. Cambridge University Press, Cambridge, United
Kingdom.

KEELEY, J. E. AND P. H. ZEDLER. 1978. Reproduction of Chaparral Shrubs After Fire
- Comparison of Sprouting and Seeding Strategies. American Midland Naturalist 99: 142-
161.

KOLB, K. J. AND J. S. SPERRY. 1999. Differences in drought adaptation between
subspecies of sagebrush (Artemisia tridentata). Ecology 80: 23 73-23 84.

KRAUSE, D. AND J. KUMMEROW. 1977. Xeromorphic structure and soil moisture in
chaparral. Oecologia Plantarum 12: 133-148.

KUMMEROW, J., D. KRAUSE, AND W. JOW. 1977. Root systems of chaparral shrubs.
Oecologia 29: 163-177.

LANGAN, S. J ., F. W. EWERS, AND S. D. DAVIS. 1997. Xylem dysfunction caused by
water stress and freezing in two species of co-occurring chaparral shrubs. Plant Cell and
Environment 20: 425-43 7.

 

Ll-COR, I. Li-1600 Steady State Porometer Instruction Manual. [6]. 1989.

MARTINEZ-VILALTA, J. AND J. PINOL. 2002. Drought-induced mortality and
hydraulic architecture in pine populations of the NE Iberian Peninsula. Forest Ecology
and Management 161: 247-256.

MILLER, P. C. AND E. HAJEK 1981. Resource availability and environmental
characteristics of Mediterranean type ecosystems. In P. C. Miller [ed.], Resource use by
chaparral and matorral. A comparison of vegetation function in two Mediterranean type
ecosystems, vol. 39, 17-41. Springer-Verlag, New York.

MILLER, P. C. AND E. NG. 2005. Root: shoot biomass ratios in shrubs in southern
California and central Chile. Madrono 24: 215-223.

NIXON, K. C. The oak (Quercus) biodiversity of California and adjacent regions. USDA
Forest Service Technical Report PSW-GTR-184, 3-20. 2002.

45

NOAA. Location US Climate Divisions.
http://www.cdc.noaa.gov/usclimate/map.html#Califomia. 2001. NCAA-Cooperative
lnstitutefor Research in Environmental Science, Climate Diagnostic Center.

----- . National Climatic Data Center. http://www.ncdc.noaa.gov/oa/ncdc.html. 2005.

OPPENHEIMER, H. R. Adaptation to drought: Xerophytism. Plant water relationships in
arid and semi-arid conditions. Reviews of Research, UNESCO, Arid Zone Research.
[15], 105-138. 1960.

PARKER, V. T. AND V. R. KELLY 1989. Seed banks in California chaparral and other
Mediterranean climate shrublands. In M. A. Leck, V. T. Parker, and R. L. Simpson [eds],
Ecology of soil seed banks, 231-255. Academic Press, New York.

PARSONS, D. J., P. W. RUNDEL, R. P. HEDLUND, AND G. A. BAKER. 1981.
Survival of severe drought by a non-sprouting chaparral shrub. American Journal of
Botany 68: 973-979.

PEARCY, R. W., E. D. SCHULZE, AND R. ZIMMERMANN 1991. Measurement of
transpiration and leaf conductance. In R. W. Pearcy, J. R. Ehleringer, H. A. Mooney, and

P. W. Rundel [eds], Plant physiological ecology: Field methods and instrumentation,
137-160. Chapman and Hall, London.

PEREIRA, J. S. AND M. M. CHAVES 1993. Plant water deficits in Mediterranean
ecosystems. In J. A. C. Smith and H. Griffiths [eds], Water Deficits: plant responses
from cell to community, 237-251. BIOS Scientific Publishers Limited, Oxford.

POCKMAN, W. T. AND J. S. SPERRY. 2000. Vulnerability to xylem cavitation and the
distribution of Sonoran Desert vegetation. American Journal of Botany 87: 1287-1299.

POOLE, D. K. AND P. C. MILLER. 1975. Water relations of selected species of
chaparral and coastal sage communities. Ecology 56: 1118-1128.

PRATT, R. B., F. W. EWERS, M. C. LAWSON, A. L. JACOBSEN, M. M. BREDIGER,
AND S. D. DAVIS. 2005. Mechanisms for tolerating freeze-thaw stress of two evergreen

chaparral species: Rhus ovata and Malosma laurina (Anacardiaceae). American Journal
ofBotanY 92: 1102-1113.

REDTFELDT, R. A. AND S. D. DAVIS. 1996. Physiological and morphological
evidence of niche segregation between two co-occurring species of Adenostoma in
California Chaparral. Ecoscience 3: 290-296.

ROOD, S. B., S. PATINO, AND K. COOMBS. 2000. Branch sacrifice: cavitation-
associated drought adaptation of riparian cottonwoods. Trees - Structure and Function 14:
248-257.

SCHIMPER, A. F. W. 1903. Plant geography on a physiological basis. Clarendon Press,
Oxford.

46

SCHOLANDER, P. F ., H. T. HAMMEL, E. D. BRADSTREET, AND E. A.
HEMMINGSEN. 1965. Sap pressure in vascular plants. Science 148: 339-346.

SHEPPARD, P. R., A. C. COMRIE, G. D. PACKIN, K. ANGERSBACH, AND M. K.
HUGHES. 2002. The climate of the US Southwest. C lim_ate Research 21: 219-238.

SLATYER, R. O. 1967. Plant-water relationships. Academic Press, London.

SMITH, J. B., R. RICHELS, AND B. MILLER 2001. Potential consequences of climate
variability and change for the western United States. In J. Melillo, A. Janetos, and T. Karl
[eds], Climate change impacts on the United States: The potential consequences of
climate variability and change, 219-245. Cambridge University Press, Cambridge.

STILLER, V. AND J. S. SPERRY. 1999. Canny's compensating pressure theory fails a
test. American Journal of Botany 86: 1082-1086.

STOCKER, 0. Physiological and morphological changes in plants due to water
deficiency. Plant water relationships in arid and semi-arid conditions. Reviews of
Research, UNESCO, Arid Zone Research. [15], 93-97. 1960.

STONE, E. C. AND G. JUHREN. 1951. The effect of fire on the germination of the seed
of Rhus ovata Wats. American Joum_al of Botany 38: 368-372.

THOMAS, C. M. AND S. D. DAVIS. 1989. Recovery patterns of three chaparral shrub
species after wildfire. Oecologia 80: 309-320.

TYREE, M. T. AND F. W. EWERS. 1991. Tansley Review No. 34: The hydraulic
architecture of trees and other woody plants. New Phytologist 119: 345-360.

TYREE, M. T. AND J. S. SPERRY. 1989. Vulnerability of xylem to cavitation and
embolism. Annu_al Review of Plant Physiology and Plant Molecular Biology40: 19-38.

USDA. Natural Resources Conservation Service. Soil information for California, San
Bemadino Nation Forest Area (CA 777). https://soildatamart.nrcs.usda.gov. 2006.

WAGNER, K. R., F. W. EWERS, AND S. D. DAVIS. 1998. Tradeoffs between
hydraulic efficiency and mechanical strength in the stems of four co-occurring species of
chaparral shrubs. Oecologia 117: 53-62.

WELLS, P. V. 1969. Relation between mode of reproduction and extent of speciation in
woody genera of California chaparral. Evolution 23: 264-&.

WIESLANDER, A. E. AND C. H. GLEASON. Major brushland areas of the Coastal
Ranges and Sierra Cascades Foothills in California. 15. 1954.

WILLIAMS, D. G. AND J. R. EHLERINGER. 2000. Carbon isotope discrimination and
water relations of oak hybrid populations in southwestern Utah. Western North American
Mturalist 60: 121-129.

47

TE UNIVERSITY

lllllllllllllllllllllllllllllll

3 1293 02736 8665