Ackerly2004 Water Deficit

Ecological Monographs, 74(1), 2004, pp.
2544
q 2004 by the Ecological Society of America
FUNCTIONAL STRATEGIES OF CHAPARRAL SHRUBS IN RELATION TO

SEASONAL WATER DEFICIT AND DISTURBANCE
DAVID ACKERLY1
Department of Biological Sciences, 371 Serra Mall, Stanford University, Stanford, California 94305 USA
Abstract. The study of interspecific variation in plant ecological strategies has revealed
suites of traits associated with leaf life span and with maximum levels of water deficit
(measured as leaf water potentials). Here, the relationship between these sets of traits was
examined in a study of 20 co-occurring chaparral shrubs that vary in leaf habit, rooting
depth, and regeneration strategies. Leaf life span (LLS) and minimum seasonal water potentials (cmin) were not significantly correlated, suggesting that they are associated with
independent aspects of functional variation. Multiple regression analyses of a large suite
of physiological, functional, and phenological attributes in relation to these two anchor
traits supported this view. Short LLS was significantly associated with high specific leaf
area, high carbon assimilation and leaf nitrogen (per mass), early onset of growth, and a
multistemmed, short stature growth form. This suite of traits was also associated with
opportunistic regeneration following physical disturbance. Area-based gas exchange was
not tightly linked to LLS. Low cmin (i.e., greater water deficit) was associated with high
wood density, small vessel diameters, thin twigs, low leaf area : sapwood area ratios, and
early onset of leaf abscission. Among the evergreen species, this suite of traits was most
characteristic of post-fire seeders, which depend on high drought tolerance for post-fire
regeneration of seedlings. Plant stature was the only trait associated with both the LLS
axis and the cmin axis of functional variation. A two-dimensional strategy space, approximately defined by LLS and cmin, can be used to distinguish contrasting strategies of drought
tolerance vs. avoidance, and alternative modes of regeneration following fire and other
disturbance. This conceptual scheme illustrates the strength of a trait-based approach to
defining plant strategies in relation to resource availability and disturbance.
Key words: chaparral; drought avoidance; drought tolerance; ecological strategy; ecosystem,
mediterranean-type; fire ecology; leaf habit; leaf life span; photosynthesis; specific leaf area; water
potential; wood density.
INTRODUCTION
whether these suites of traits covary or whether they

are orthogonal and potentially reflect independent dimensions of variation in ecological strategies. A prominent exception are studies suggesting that functional
strategies associated with regeneration (seedling attributes) are decoupled from strategies of persistence (attributes of mature plants; Shipley et al. 1989, Grime
et al. 1997).
Quantitative tests for independent suites of traits rely
on the absence of correlation (where low r 2 values are
more important than significance levels) and they may
thus be seen as negative results of little interest. But
if the traits have been carefully chosen and appropriately measured, lack of correlation provides valuable
insights into major axes of phenotypic variation. These
axes may define independent dimensions of niche partitioning related to coexistence (Loehle 2000), orthogonal axes defining major functional strategies (Westoby
et al. 2002), and independent axes of evolutionary
change (e.g., Ackerly and Donoghue 1998). Robust
tests for multiple suites of traits are challenging, as
they require consideration of many species and many
traits (e.g., Grime et al. 1988), and they will be
strengthened by testing explicit hypotheses of ecological differentiation among coexisting species.
A central goal of comparative ecology is to understand the diversity of physiological, functional, and life
history strategies among co-occurring species, and the
implications for potential niche differentiation and coexistence. In terrestrial plants, a great deal of progress
has been made in identifying major axes of ecological
strategy variation and the underlying adaptive tradeoffs between the traits (Westoby et al. 2002). Important
examples include the suites of traits associated with
leaf life span and photosynthesis (Mooney and Dunn
1970, Reich et al. 1997), successional status (Bazzaz
1979), hydraulic architecture and drought tolerance
(Tyree et al. 1994, Pockman and Sperry 2000), seed
size and regeneration strategies (Leishman et al. 2000),
plant stature, life history, and allocation (Enquist et al.
1998, Niklas and Enquist 2002), leaf size and canopy
architecture (Ackerly and Donoghue 1998), and overall
stress tolerance (Chapin et al. 1993). In contrast,
few multivariate studies have been conducted to test
Manuscript received 10 February 2003; accepted 23 February
2003 (originally submitted 13 March 2002). Corresponding Editor: M. J. Lechowicz.
1 E-mail: dackerly@stanford.edu
25
DAVID ACKERLY
26
Mediterranean-type ecosystems (MTE) provide an

excellent opportunity to examine suites of traits related
to carbon assimilation and water availability in the context of diverse regeneration strategies. Studies of the
comparative ecology of woody plants in MTE have
focused on three factors: (1) evergreen vs. deciduous
leaf habit, (2) rooting depth and drought tolerance, and
(3) post-fire regeneration strategies. In each case, there
has been considerable research on the physiological
traits associated with contrasting strategies, but there
have been few broad attempts to integrate these three
areas. In addition, the role of opportunistic regeneration
following non-fire disturbance (e.g., canopy openings,
soil disturbance) may be an important aspect of vegetation dynamics in MTE, but it has received little attention (Zedler 1982). The objective of this paper is to
integrate comparative ecophysiology and regeneration
ecology of woody plants of the California chaparral,
illustrating the importance of considering both correlated and independent suites of functional traits to evaluate the ecological strategies of coexisting species.
Chaparral ecophysiology
Woody plant communities of MTE, especially in California, Chile, and the Mediterranean Basin, are characterized by a mix of evergreen and deciduous species
(i.e., long and short leaf life span). Evergreen species
generally exhibit lower leaf nutrient concentrations,
photosynthetic rates per unit mass, and specific leaf
area (leaf area:mass ratio), compared to coexisting deciduous taxa (Mooney and Dunn 1970, Miller et al.
1981). The tough, evergreen leaves of MTE shrubs
(sclerophylls; Schimper 1903) have long been considered a classic case of convergent evolution, though
the relative importance of low water vs. low nutrient
availability favoring sclerophylly continues to be debated (see Lamont et al. 2002). The evergreen and deciduous habits reflect trade-offs between high instantaneous and daily rates of carbon gain and water loss
vs. a prolonged duration of carbon gain at lower rates,
amortizing the investment in leaf tissue over a longer
time period and enhancing long-term photosynthetic
nitrogen use efficiency (Small 1972, Gray 1983). Within chaparral communities, evergreen and deciduous
species may occupy contrasting microsites on topographic gradients (Parsons 1976, Meentemeyer et al.
2001, Ackerly et al. 2002), and exhibit differing regeneration requirements in relation to disturbance.
Variation in rooting depth and seasonal access to
water represents a second critical axis of differentiation
among chaparral plants (Burk 1978, Miller and Poole
1979, Dodd et al. 1984, Davis and Mooney 1986b,
Goulden 1996, Redtfeldt and Davis 1996, Davis et al.
1998). During summer drought, deep-rooted taxa may
continue transpiring and photosynthesizing at high
rates, taking advantage of warm temperatures and high
light, but they presumably incur a high cost of root
production at the whole plant level. In several species,
Ecological Monographs
Vol. 74, No. 1
rooting depths of 4 m or more have been recorded in

excavation studies, and root:shoot ratios are high (Hellmers et al. 1955, Kummerow et al. 1977). Species with
shallow roots can allocate more to aboveground
growth, and are the first to take advantage of autumn
rains, but must reduce transpiration in summer (through
deciduousness or stomatal closure) and/or have extremely high tolerance of water deficit in xylem and
leaves. Studies of water relations and hydraulic architecture have increasingly focused on the minimum water potential experienced through the annual cycle as
a comparative measure of maximum water deficit at
the leaf level (Tyree et al. 1994, Pockman and Sperry
2000). Minimum seasonal water potential (cmin) integrates the effects of spatial and temporal soil water
profiles, rooting depth, foliar phenology, and diurnal
water potential dynamics due to transpiration and hydraulic supply. Across several ecosystems, there is a
significant positive correlation among species between
cmin and both hydraulic conductivity and xylem drought
tolerance, measured as the water potential at which
embolism causes substantial drops (e.g., 50% or 75%)
in conductivity (Pockman and Sperry 2000). Due in
part to the role of vessel diameters and cell wall dimensions, there are weak trade-offs between conductivity and xylem resistance to embolism (safety vs.
efficiency; Tyree et al. 1994, Pockman and Sperry
2000), and evidence of a positive relationship between
wood density and xylem resistance (Hacke et al. 2001).
This set of relationships points to a correlated suite of
traits associated with minimum water potentials, hydraulics, and xylem drought tolerance. Comparisons of
selected chaparral taxa suggested that the deciduous
leaf strategy was associated with shallow roots and a
seasonal strategy of drought avoidance, while evergreens were deeper rooted and physiologically active
through the dry season (e.g., Mooney 1982). However,
shallow roots are observed in both evergreen and deciduous taxa and some aspects of water relations may
be quite similar in the two groups (see Poole and Miller
1975, Gill and Mahall 1986, Kolb and Davis 1994).
No previous study has examined a large group of coexisting species to assess potential relationships between the suites of traits associated with leaf life span
and minimum water potentials.
Disturbance and regeneration

Regeneration ecology in MTE has focused on the
role of fire. The small stature and high flammability of
the vegetation, combined with extreme drought conditions, promote stand-replacing crown fires (Bond and
van Wilgen 1996, Keeley et al. 1999). Three primary
strategies of post-fire regeneration are recognized in
the shrubs of California chaparral, reflecting the role
of resprouting and establishment from seed (Keeley
1991, 1998; see also Noble and Slatyer 1980, Gill
1981): (1) obligate sprouters resprout from the root
crown, but their seeds are generally heat sensitive and
February 2004
FUNCTIONAL STRATEGIES OF CHAPARRAL SHRUBS
only germinate below the canopy during fire-free intervals (e.g., Quercus, Heteromeles); (2) seedersprouters or facultative seeders exhibit post-fire
seed germination from a soil seed bank, and are also
able to resprout (e.g., Adenostoma, Rhus); and (3) obligate seeders are unable to resprout vegetatively, and
depend entirely on fire-stimulated seed germination
from soil or canopy (i.e., serotinous) seed banks (e.g.,
some Ceanothus, Arctostaphylos, and Pinus). The obligate seeders exhibit high rates of seedling establishment after fire (Keeley and Zedler 1978, Thomas and
Davis 1989) and studies in Australia have also reported
high aboveground growth and shoot:root ratios, rapid
attainment of reproductive age, and high fecundity
(Bell et al. 1984, Enright and Lamont 1989, Pate et al.
1990, Bell and Pate 1996, Enright and Goldblum 1999).
These traits contribute to offset the demographic effects
of adult mortality and short life span (Keeley and Zedler 1978, Hilbert 1987, Bond and van Wilgen 1996).
This strategy has led to the evolution of shallow rooting
and a high degree of physiological drought tolerance,
including high resistance to xylem cavitation (Davis
1989, Davis et al. 1999). At the other extreme, the
obligate sprouters face the least water deficit as seedlings since they germinate in the interval between fires,
and they rely more on a deep-rooted drought avoidance
strategy. Thus, the post-fire regeneration strategies are
linked to a suite of hydraulic traits related to rooting
depth, at least among the evergreen taxa (Davis et al.
1998, Keeley 1998).
The role of smaller scale canopy and soil disturbance, such as those caused by human impacts, landslips, animal disturbance, or gap creation due to disease, drought, or other non-fire causes, has received
little attention in MTE (see Zedler 1982). In California,
summer deciduous species characteristic of the xeric
coastal scrub community (Westman 1981) are frequently observed regenerating in disturbed sites in the chaparral (after fire or non-fire disturbance) (Zedler 1981,
Keeley 2000). The short leaf life span and rapid growth
rates of these deciduous taxa are characteristic of early
successional species in general (Bazzaz 1979, Reich et
al. 1997), and contrast with the attributes of post-fire
seeders. An understanding of the role of disturbance
in MTE and other fire-prone systems needs to consider
both small-scale and large-scale disturbance, and the
functional characteristics of species that regenerate following these events. In this paper, I use the term opportunistic regeneration (and opportunists) to refer
to species that germinate and establish in open sites or
disturbed soil following fire and/or non-fire disturbance. This is analogous to the familiar pioneer or early
successional designations used in old-field and forest
ecology, but these terms may fail to distinguish responses to different types of disturbance in MTE.
Objective
The objective of this study was to assess functional,
physiological, and phenological traits in a large number
27
of co-occurring species from a California chaparral

community, in relation to strategies of regeneration following disturbance. The central questions of this analysis are the following. (1) Are leaf life span (LLS) and
minimum seasonal water potentials (cmin) correlated in
this community? (2) If not, are they associated with
independent axes of variation in correlated functional
traits? (3) How are these potential axes of functional
variation related to strategies of regeneration following
fire or other disturbance? For statistical analyses, LLS
and cmin have been selected as anchor traits, due to
their central role in the literature and their clear functional interpretation. This is not meant to suggest that
these traits have a developmental, functional, or evolutionary primacy, or that they are the cause of variation in other attributes. Functional strategies depend
on covariation in multiple traits expressed in an ecological context, and comparative data alone cannot determine if one or more traits have a primary role in the
discrimination of these strategies.
METHODS
Site
The study was conducted from 1998 to 2001 at the
Jasper Ridge Biological Preserve (JRBP), San Mateo
County, California, USA (37.48 N, 122.258 W), located
in the mediterranean climate zone of coastal California
(see Plate 1). The Jasper Ridge Biological Preserve is
located at ;150 m above sea level, with mean summer
temperature (AprilSeptember) of 17.88C, mean hottest
month (July) of 20.18C, mean winter temperature (OctoberMarch) of 11.38C, and mean coldest month (January) of 9.18C. Freezing occurs occasionally from late
November to early March (1642 times/yr; 1997
2001). Total annual precipitation averages 654 mm
(19752001), with a severe dry season of ;5 mo (May
September; precipitation ,15 mm/mo). The physiological and phenological data for this study were obtained during the growing seasons of 1998 and 1999.
Total annual rainfall for water years 1998 and 1999 (1
October of previous year to 30 September of current
year) was 1324 mm and 760 mm, respectively. The
1998 precipitation was approximately twice the longterm average, reflecting both heavy El Nino winter
rains and continued precipitation through late May (N.
Chiariello, unpublished data).
Chaparral at JRBP occurs on undulating topography
with a predominance of north-facing and south-facing
aspects, and slopes between 58 and 308 (see Ackerly et
al. 2002). Soils are derived from basaltic greenstones
(serpentine areas were not included in this study; see
Davis and Mooney 1985). There have been no wildfires
at JRBP in at least 100 years. Analysis of past fire
history, based on charcoal records in redwood stumps,
suggests a relatively short fire return interval of ,10
yr in the understory of adjacent oak woodland (S. Stephens, personal communication), but the fire history
DAVID ACKERLY
28
Vol. 74, No. 1
PLATE 1. Chaparral shrub species of the Jasper Ridge Biological Preserve, San Mateo Co., California. (Upper left) Mixed
species chaparral, with Adenostoma fasciculatum in flower on left and right, and Arctostaphylos tomentosa in middle. Upper
right) flushing of new leaves in Arbutus mensiezii. (Lower left) Eriodicyton californicum. (Lower right) Ribes californicum.
Photo credits: K. A. Preston, upper left; D. D. Ackerly, upper right and bottom.
of the chaparral is unknown. Though chaparral extends

to southern Oregon, it is most extensive in the mountains of southern California where a longer dry season
and foehn winds from the desert promote frequent fire
(Keeley et al. 1999). In this context, the chaparral at
JRBP may be somewhat unusual, as it experiences a
milder climate due to proximity to San Francisco Bay,
higher rainfall, and currently a prolonged interval free
of fire. In addition, human activity over 150 years (primarily trail and road building) has enhanced the role
of non-fire disturbance, relative to the natural chaparral disturbance regime. Although these factors may
alter composition, relative abundance, and local distributions of species in this community, there is no
apparent reason why they would affect trait correlations
and ecological strategies that reflect long-term outcomes of trait evolution and assembly of the chaparral
flora.
Species and plant selection

Relative abundance and distribution of woody plants
in the chaparral were assessed in a previous study based
on a set of transects placed through undisturbed vegetation on north-facing and south-facing slopes (Ackerly et al. 2002), as well as surveys of vegetation along
trails and roads. Based on these surveys, a total of 20
species were chosen for this comparative study (Table
1; species are referred to by generic names, except for
Ceanothus and Rhamnus, which each had two species
in the study; nomenclature follows Hickman 1993).
The 20 selected species include all dominant woody
plants (excluding vines) as well as a variety of less
common species representing a range of ecological
strategies. Chaparral species present at JRBP but excluded from this study included: Artemisia californica
(its growth form made our physiological and phenological measurements impractical); Quercus agrifolia
(primarily a tree in the oak woodland); Quercus durata
(only on serpentine); and Garrya elliptica, Oemleria
cerasiformis, Pickeringia montana, Ribes malvaceum,
and Solanum umbelliferum (low abundance). Cistus
creticus and Pistacia atlantica have been recorded, but
no woody alien species are common or invasive in the
chaparral community.
February 2004
29
TABLE 1. Species included in this study, and values of the two anchor traits used for multiple regression analysis: leaf life
span and midday water potentials.
Phenology
Species
Adenostoma fasciculatum Hook &

Arn.
Arbutus menziesii Pursh
Arctostaphylos tomentosa (Pursh)
Lindley var. crustacea (Eastw.)
P. Wells
Baccharis pilularis DC.
Ceanothus cuneatus (Hook.) Nutt.
Ceanothus oliganthus Nutt. var.
sorediatus (Hook. & Arn.)
Hoover
Cercocarpus betuloides Torrey &
A. Gray
Dirca occidentalis A. Gray
Eriodictyon californicum (Hook.
& Arn.) Torrey
Heteromeles arbutifolia (Lindley)
Romer
Holodiscus discolor (Pursh) Maxim.
Lepechinia calycina (Benth.)
Epling
Lotus scoparius (Nutt.) Opley
Mimulus aurantiacus Curtis
Prunus ilicifolia (Nutt.) Walp.
Rhamnus californica Eschsch.
Rhamnus crocea Nutt.
Ribes californicum Hook. & Arn.
Sambucus mexicana C. Presl
Toxicodendron diversiloba (Torrey
& A. Gray) E. Greene
Family
Code
Leaf
habit
Leaf life
span (mo)
Midday c
June
(MPa)
August
(MPa)
Regeneration
Rosaceae
Af
18\
22.5
23.7
Sd
Ericaceae
Ericaceae
Am
At
E
E
14.7
22.0
21.3
22.1
22.3
23.4
Sp
Sd
Asteraceae
Rhamnaceae
Rhamnaceae
Bp
Cc
Co
E
E
E
8.9
14.4
10.7
22.3
23.1
22.9
23.4
25.1
23.7
Op
Sd
Sd
Rosaceae
Cb
11.4
22.3
23.8
?#
Thymelaeaceae
Hydrophyllaceae
Do
Ec
D
E
4.0
9.0
23.6
21.4
N/A
21.5
Sp
Op
Rosaceae
Ha
22.5
22.1
22.3
Sp
Rosaceae
Hd
4.5
22.2
N/A
Op
Lamiaceae
Lc
4.1
23.2
N/A
Op
Fabaceae
Scrophulariaceae
Rosaceae
Rhamnaceae
Rhamnaceae
Grossulariaceae
Caprifoliaceae
Anacardiaceae
Ls
Ma
Pi
Rc
Rr
Ri
Sm
Td
D
E
E
E
E
D
D
D
2.0
7.3
16.0
14.8
13.2
3.2
4.0
4.1
22.4
22.5
22.1
21.5
22.8
21.6
21.1
20.57
N/A
24.2
22.1
21.8
24.4
N/A
21.2
20.64
Op
Op
Sp
Sp
Sp
Op
Op
Op
Notes: Minimum seasonal water potentials (cmin) were based on late summer (August) values for evergreens and for
Sambucus and Toxicodendron, and based on early summer (June) values for remaining deciduous species. N/A means not
applicable.
Nomenclature follows Hickman (1993).
Leaf habit: D 5 deciduous, E 5 evergreen.
Regeneration: Sd 5 post-fire seeder, Sp 5 post-fire obligate sprouter, Op 5 opportunistic regeneration following disturbance (see Introduction: Disturbance and regeneration).
\ Data for Adenostoma from Jow et al. (1980); others were measured in this study.
The only obligate seeder.
# Uncertain; see Methods: Regeneration strategies.
The only winter deciduous species that loses its leaves after summer drought.
The majority of data were collected on a set of 10

individuals per species (the primary plants). These
individuals were located along trails and roads, and
were distributed across the range of microhabitats representative of the species; individuals were dispersed
as much as possible across different locations to minimize similarity among replicates due to local microsite
effects. All individuals were located using GPS with
differential correction, and positioned on the JRBP GIS
base map. A GIS digital elevation model was used to
estimate potential diurnal insolation (PDI) for each
plant, based on slope, aspect, and local topography (Hetrick et al. 1993). Mean insolation values for each species, based on distributions along random transects,
were obtained in a previous study as an index of microhabitat segregation along the north-facing to southfacing exposure gradient (Ackerly et al. 2002). Mean
insolation values for the locations of the primary plants

in this study were significantly correlated with corresponding means from the transect study (r2 5 0.48, P
, 0.002, N 5 18; Arbutus and Arctostaphylos were not
encountered in the transects). This result indicates that
our primary plants were sampled appropriately with
respect to the microhabitat distributions of the species
on the exposure gradient. Prunus ilicifolia and Heteromeles arbutifolia exhibit particularly broad distributions along the insolation gradient (Ackerly et al.
2002), and for these two species 20 individuals were
selected for the sample of primary plants, located
across a broad range of high and low insolation microsites.
Regeneration strategies
Species were assigned to one of three regeneration
strategies; post-fire seeder, post-fire obligate sprouter,
Vol. 74, No. 1
DAVID ACKERLY
30
or opportunist (Table 1). Nine of the evergreen species were easily assigned to one of the two post-fire
groups based on prior studies (see Keeley 1987, 1991,
1992b); there was only one obligate seeder (Ceanothus
cuneatus) so this group was not treated separately here.
Dirca occidentalis, a deciduous species endemic to the
San Francisco Bay Area, was also considered an obligate sprouter based on its sprouting capacity (J. Kriewall, unpublished data) and observations of seed germination in the understory of intact chaparral (W. Cornwell, unpublished data). The remaining species include
the six other deciduous taxa and several evergreens
with relatively short-lived leaves (e.g., Mimulus, Baccharis, Eriodictyon). Field observations and literature
review support the classification of nine of these species as post-disturbance opportunists that regenerate
following fire or non-fire disturbance. Some of these
taxa represent minor elements of the chaparral vegetation and they are generally observed in disturbed sites
(roadsides, animal trails, landslips). In a survey at
JRBP, we found a clear preference for establishment
along trail and road sides in several deciduous species
(e.g., Lotus, Lepechinia, Toxicodendron) and short LLS
evergreens (e.g., Baccharis, Mimulus, Eriodictyon; C.
Phillips and D. Ackerly, unpublished data). Seed germination biology also suggests a general disturbance
strategy. In some species, germination is triggered by
fluctuating light or temperatures (e.g., Baccharis, Ribes; Young and Young 1992), and in others germination
has been observed following non-fire disturbance (e.g.,
Eriodictyon, Holodiscus, Toxicodendron; USDA 2002,
available online).2 In contrast, seed germination of the
post-fire seeders is generally triggered by heat, smoke,
and other factors directly related to fire (Keeley 1987,
Young and Young 1992, Keeley and Bond 1997).
The life history of one species is enigmatic. Cercocarpus betuloides lacks seed dormancy but has effective wind-assisted dispersal. It can colonize postfire environments by dispersal from off site and seed
rain from lightly burned trees (USDA 2002, available
online; see footnote 2), and has also been recorded in
unburned, abandoned agricultural sites (Keeley 1992 a).
It can also persist by vigorous sprouting under a range
of fire regimes. These characteristics combine features
of all three of the major groups considered here.
Trait selection
A large number of traits were selected related to gas
exchange, functional morphology, water relations, phenology, and microhabitat distribution (Table 2). Traits
were chosen based on their relevance to gas exchange,
growth, and regeneration strategies, and based on feasibility for measurement in a large number of individuals and species. The complete data set of species
means, standard errors, and sample sizes is available
online (see the Supplement).
2
URL: ^http://www.fs.fed.us/database/feis/&
Ecophysiology
Water potentials.Predawn (cpd) and midday
(13:0015:00, cmd) water potentials were obtained in
early (28 June1 July) and late (2327 August) summer, 1999, for six of the primary plants of each species
(Plant Water Status Console 3005, Soil Moisture, Goleta, California, USA). Because individuals were widely dispersed, cpd provides an integrated measure of soil
water availability due to microsite, soil structure, soil
water profiles, and root depth and distribution (assuming equilibrium between leaf and soil; see Donovan et
al. 2001). The June measurements were conducted to
compare evergreen and deciduous taxa before the latter
lost their leaves. Minimum water potential (cmin) was
estimated using late summer cmd for evergreen taxa,
and Sambucus and Toxicodendron (which do not shed
leaves until late summer or fall), and using early summer cmd for the remaining deciduous species.
Gas exchange and leaf nitrogen.Light-saturated
photosynthesis and conductance were measured on two
recently expanded, mature leaves on each of six primary plants per species (between 23 June and 9 July
1998). This period in early summer would normally be
too late for photosynthesis measurements on the deciduous species, but due to the high rainfall in 1998,
the plants maintained functioning canopies later than
usual (personal observations). Measurements were obtained with a LI-COR 6400 Portable Photosynthesis
System (LI-COR, Lincoln, Nebraska, USA), and a clear
chamber top for ambient light. Measurements were
made at PAR . 1000 mmolm22s21, and median (5th,
95th percentiles) air temperature of 24.8 8C (23.58C,
25.78C), CO2 concentration of 361 ppm (331 ppm, 376
ppm), and relative humidity of 56% (38%, 73%).
Leaves were sampled for determination of leaf area (LICOR 3000 Leaf Area Meter, LI-COR, Lincoln, Nebraska, USA) and dried for .48 hr at 708C for determination of dry mass; specific leaf area (SLA) was
calculated as area/mass, excluding the petiole. Leaf nitrogen (Nm) and phosphorous (Pm) were determined
with a continuous flow autoanalyser (Alpkem, College
Park, Texas, USA) after Kjeldahl digestion. Photosynthesis (5 assimilation) and leaf nitrogen content were
considered on both an area and mass basis (Aa, Am, Na,
Nm), while transpiration (E) and conductance (g) were
evaluated on an area basis only. Instantaneous photosynthetic nitrogen use efficiency (PNUE) was calculated as Am/Nm, and water use efficiency (WUE) was
calculated as Aa/g (g was used rather than E to eliminate
the effect of vapor pressure deficit differences among
sites and measurement days).
Functional morphology
Leaf and twig dimensions.Five twigs per species
(except Toxicodendron) collected from different individuals were sampled in summer 2000 for the following
variables: twig cross-sectional area, leaf-bearing twig
February 2004
TABLE 2.
31
Summary of traits used in this study.

Species means
minimum,
maximum
No.
species
MJm22d21
N/A
18
cpd
cmd
cpd
cmd
cmin
MPa
MPa
MPa
MPa
MPa
115
119
89
85
115
20
20
15
15
20
LLS
SLA
Am
Nm
Pm
Aa
g
E
Na
PNUE
mo
mm2/mg
nmolg21s21
mg/g
mg/g
mmolm22s21
mmolm22s21
mmolm22s21
g/m2
mmolmg21s21
229
245
246
239
235
247
239
239
234
233
20
20
20
20
20
20
20
20
20
20
1.99, 22.5
3.55, 17.6
51.3, 228
10.4, 26.4
1.08, 2.24
7.38, 25
0.14, 0.56
1.64, 8.42
1.35, 4.17
3.22, 11.1
WUE
mmol/mmol
239
20
36.2, 88.9
Leaf and twig morphology

Twig cross-sectional area
Twig length
Leaf number
Internode length
Effective leaf area
Inflorescence length
Annual leaf production
Annual twig extension
Leaf angle, July
TXA
TwLng
LfNm
IntLng
EffAr
InfLng
LfProd
TExt
LfAng
mm2
mm
97
97
97
97
97
71
205
195
194
20
19
19
19
19
20
19
19
20
1.37, 18.5
44.2, 271
4.96, 129
4.83, 46.5
0.79, 2135
6.56, 126
2.43, 29
6.16, 195
10.8, 57.7
Wood and xylem

Wood density
Leaf area:sapwood area
Vessel diameter
WdDn
LA/SA
VsDm
mg/mm3
m2/m2
mm
log
95
102
62
20
20
20
0.33, 0.80
2.17, 82.4
6.93, 21.7
Canopy architecture
Canopy height\
Crown diameter
Number of stems
STATURE
SPREAD
StNm
m
m
log
log
log
220
220
220
20
20
20
0.75, 4.75
1.24, 2.54
1.5, 10
Seed size
Seed mass
SdSz
mg
log
159
20
0.04, 401
Phenology
Month peak leaf flush#
Duration of leaf flush#
First leaf drop
Onset
Dur
LfDr
month
months
month
185
185
229
19
19
19
1.7, 6.6
1, 7.8
1, 6.1
Group, trait
Code
Distribution
Insolation distribution
PDI
Water potentials (c)

Predawn c, June
Midday c, June
Predawn c, August
Midday c, August
Minimum seasonal c
Gas exchange and leaf function
Leaf life span
Specific leaf area
Assimilation/mass
Nitrogen/mass
Phosphorous/mass
Assimilation/area
Conductance
Transpiration
Nitrogen/area
Photosynthetic nitrogen
use efficiency (Am/Nm)
Photosynthetic water use
efficiency (Aa/g)
Transformation
Units
mm
mm2
mm
mm
degrees
log
sq rt
log
log
log
sq rt
log
log
log
0.5, 16.6
23.02,
23.57,
24.30,
25.14,
25.14,
20.24
20.57
20.38
20.64
20.64
Traits were transformed as necessary to meet the assumption of normality of residuals.

N 5 total number of individual measurements across all species.
Evergreen taxa plus Sambucus and Toxicodendron.
\ Canopy height values are shown for reference. A composite measure of stature, including crown size and basal area, was
used in multiple regression and principal components analysis.
Normalized for crown height in analysis of covariance (see Methods: Functional morphology).
# Month and duration of leaf flushing shown for reference; composite measures of the onset and duration of growth were
used for multiple regression and principal components analysis. See phenology methods in the Appendix.
Values refer to calendar month.
length, leaf number (including leaves on fascicles in

Adenostoma), internode length, effective leaf area (inscribed circle), and inflorescence length (for Dirca this
was obtained from Hickman 1993). Stem cross-sectional area for Toxicodendron was obtained from twigs
sampled for water potentials and the other data were

missing.
In July 1999, leaf angles relative to horizontal were
measured on two randomly selected leaves per plant
for 519 of the primary plants of each species. Data
32
Vol. 74, No. 1
DAVID ACKERLY
were obtained from all species, though some deciduous

taxa had begun to lose leaves, which may have biased
the measurements obtained on remaining leaves.
Wood and xylem attributes.Wood density of first
year twigs with pith removed was determined in an
independent sample from the same species at this site
(W. Cornwell and D. Ackerly, unpublished data). Fresh
volume was determined by immersion in a narrow graduated cylinder. Dry mass was determined after oven
drying for at least 48 hours at 808C. Wood density was
calculated as dry mass/fresh volume.
Vessel diameters and leaf area : sapwood area ratios
were determined for deciduous species in June and evergreen species in August, using the shoots collected
for measurement of water potentials (see Methods:
Ecophysiology: Water potentials). After pressure
bombing, the area of all leaves on the shoot was determined. A small segment was then removed from the
base of the twig, and several thin sections were sliced
from the end for anatomical study. Cross-sectional area
was measured in two perpendicular directions. Thin
sections were examined by light microscope to determine sapwood area, and the ratio of total distal leaf
area:sapwood area (inverse of Huber value) was calculated. Sections were digitally photographed at 20 3
or 403 magnification, and the diameters of 20 randomly sampled vessels in three sections per species
were measured with image analysis software (Scion
Image 4.02, Scion, Frederick, Maryland, USA). Hydraulic mean vessel diameter was calculated as 2(Sr 4/
N)1/4 (r 5 vessel radius, N 5 number of vessels measured on a section), following the Hagen-Poiseuille relationship that conductivity is proportional to the fourth
power of conduit radius. The alternate equation provided by Sperry et al. (1994), 2(Sr 5/Sr 4), gives almost
identical results for species means. We did not examine
xylem macerations or conduct staining experiments to
distinguish active vessel elements from inactive elements and tracheids. In addition, vessel diameters are
generally smaller in first year twigs than in older wood
(Gartner 1995). As a result, our mean vessel diameters
were considerably smaller than those reported in the
literature for chaparral taxa (Carlquist and Hoekman
1985). Measurements of older stems (K. A. Preston,
unpublished data) were fairly close to published data,
suggesting that twig age is the primary explanation for
this discrepancy. Relative ranking of species was comparable to published comparisons, and in a recent study
we also found a significant correlation between our
vessel diameter data and direct measurements of hydraulic conductivity (R. Bhaskar, K. A. Preston, D.
Schwilk, and D. D. Ackerly, unpublished data). This
supports the use of these values for analysis of trait
correlations, though the absolute values may be underestimates of actual vessel diameters for hydraulically active elements.
Canopy dimensions.Stature and canopy dimensions were measured for the 10 primary plants of each
species. On each plant the following measurements

were obtained: plant height; projected crown diameter
in the longest dimension and its perpendicular; height
of the lowest leaf; number of stems at 10% of height;
diameter of each stem at 10% of height (Ackerly and
Donoghue 1998). From these values, several derived
values were calculated: crown area and volume (based
on the formula for area of an ellipse and volume of an
ellipsoid, respectively); maximum and mean stem diameter; basal area; and the ratio of crown diameter to
height, as a measure of relative lateral spread vs. vertical stature.
Canopy dimensions were reduced to three variables
to minimize autocorrelation (see Appendix): STATURE, based on principal components analysis (PCA)
scores for height, crown area, crown volume, maximum
stem diameter, mean stem diameter, and basal area;
SPREAD, a measure of canopy breadth based on analysis of covariance of log (crown diameter) vs. species
with log (height) as covariate; and log (number of
stems) as a measure of shrub vs. tree growth form.
Seed size.Samples of .10 mature seeds per plant
were collected from 212 individuals per species for
determination of mean fresh seed mass (fleshy fruits
and other dispersal structures were removed prior to
weighing). For Prunus, only eight mature seeds could
be obtained due to rapid consumption by birds. For two
species, mature seeds could not be collected at JRBP,
and seed mass was obtained from published values (Adenostoma fasciculatum, Keeley 1991; Arbutus menziesii, Burns and Honkala 1990).
Phenology
In December 1998, two shoots per plant on the 10
primary plants of each species were marked to examine
the phenology of vegetative growth and reproduction.
Shoots selected for study were in relatively exposed
positions in the crown. Shoots were censused once per
month (at approximately mid month) until December
1999. At the first census, the base of the shoot was
permanently marked as a reference point for length
measurement. For deciduous species, the following
traits were measured at each census: shoot length (from
base to apex); number of leaves produced in the current
month; and number of leaves surviving from each previous months cohort. For evergreen species, transition
points between cohorts of the current and previous
year(s) were marked based on morphological characteristics (e.g., bud scale scars) and preliminary measurements from the previous growing season. At each
census during 1999, shoot length, the total number of
leaves produced in 1999, and the number of leaves
surviving from each previous years cohort were recorded. For deciduous species, leaf life span (LLS) was
calculated as the mean for all leaves produced in 1999,
based on the repeated censuses of the number of leaves
remaining in each months cohort. For evergreen species, LLS was calculated as the mean for all leaves that
February 2004
33
were lost during 1999, based on the month in which

they were dropped and the annual cohort to which they
belonged, and using the month of peak leaf production
as the average month of birth for all leaves. The growth
form of Adenostoma made our phenological methods
prohibitively time consuming, so no data were included
in this analysis (LLS was obtained from Jow et al.
1980).
The following six variables were derived from these
data (see details in Appendix): (1) vegetative onset
(Onset), a composite measure of the timing of initial
and peak vegetative growth (timing of peak leaf production is reported in Table 2); (2) vegetative duration
(Dur), based on the number of months during which
leaf production and twig extension were observed (leaf
production is reported in Table 2); (3) month of first
leaf drop, a measure of the onset of abscission, which
is of interest in relation to summer drought; (4) leaf
life span; (5) total number of leaves produced; and (6)
total twig extension per shoot.
of normality of residuals (Table 2). One extreme low

outlier for wood density (Dirca) was removed for regression analysis (see Fig. 2E, F). For multiple regression, the P values for significant results are indicated in the summary figure (Fig. 3), and are not stated
in the Results section. Finally, a descriptive multivariate analysis was conducted using principal components analysis, focusing on the first two axes due to
the small number of species (20) relative to traits (33).
A Varimax rotation resulted in imperceptible changes
in orientation of the first two axes (results not shown),
so the original loadings from the PCA were used. Trait
loadings were used to assess patterns of covarying
traits, and the distribution of species in the PCA space
was examined in relation to strategies of regeneration
and response to water deficit. Analyses were conducted
with Data Desk 6 (Data Description, Ithaca, New York,
USA).
Statistical analysis
Interspecific variation in functional traits
Thirty three morphological, phenological, and physiological traits (all continuous variables) were measured for all or most of the 20 species (Table 2). The
final data matrix was 98.3% complete (669 of 680 entries), and all but two variables (PDI and SPREAD)
were measured with intraspecific replication to allow
tests of significant differences among species.
Tests for the independence of LLS and cmin, and for
distinct suites of correlated traits, were conducted in
three steps. First, I selected these two parameters as
anchor traits representing the hypothesized strategy
axes, and the correlation between LLS and cmin was
examined to test whether they were independent across
species. These traits were chosen based on prior studies
demonstrating that they are associated with the functional strategies of interest in this community. This
does not reflect a belief that they are physiologically
independent or causal of other attributes (as in a path
analysis model), or that they are intrinsically more important in a functional context. This approach simply
provides a useful statistical approach to explore independent trait correlations in a large multivariate data
set, given explicit a priori hypotheses, while reducing
the problem of multiple comparisons (e.g., compared
to tests of all pairwise trait correlations; see Schwilk
and Ackerly 2001). Minimum water potentials ( cmin)
were based on midday values (cmd, measured in early
afternoon), representing the maximum water deficit experienced by the leaves and xylem (Pockman and Sperry 2000).
Second, multiple regression was used to test whether
each of the other traits was significantly related to one
or both of these two anchors independently. Multiple
regression analyses were conducted for the full set of
20 species and separately for the 13 evergreens. Traits
were transformed as necessary to meet the assumption
There were highly significant differences among species for all measured traits (P # 0.0001 for all but one
trait). The percentage of total variation among individuals associated with interspecific differences was
.50% for 23 of the 33 traits, and .90% for four traits
(seed size, leaf size, inflorescence length, and leaf life
span; results not shown).
RESULTS
Leaf life span and minimum seasonal water potential

Early summer predawn water potential (cpd) ranged
from 20.2 MPa to 23.0 MPa across all 20 species, and
midday water potential (cmd) ranged from 20.6 MPa
to 23.6 MPa. Predawn water potentials and midday
water potentials were tightly linked (Fig. 1A), indicating that relative access to soil water was the primary
factor influencing variation in minimum daily water
potentials. For the 13 evergreens, cpd and cmd values
from early and late summer were strongly correlated
(R 5 0.84 and 0.89, respectively), and the late summer
values averaged 1.1 MPa and 1.0 MPa lower, respectively. Species with more negative water potentials exhibited greater decline from early to late summer, as
expected due to drying of shallow or exposed soils (Fig.
1B).
Mean leaf life span (LLS) varied from 2.0 mo to 4.5
mo in deciduous species (Lotus and Holodiscus, respectively) and 7.2 mo to 22.4 mo among evergreens
(Mimulus and Heteromeles, respectively; Fig. 1C). Five
of the 13 evergreens had LLS of ,1 yr, indicating that
the evergreen habit was maintained by seasonal replacement of one or more leaf cohorts. The differences
in LLS between deciduous and evergreen species were
highly significant (t test, P # 0.001).
There were no significant correlations between log
LLS and early summer cpd (R 5 0.21 and R 5 0.24,
for all 20 species and for the 13 evergreens, respec-
34
DAVID ACKERLY
Vol. 74, No. 1
FIG. 1. Scatter plots of (A) early summer predawn vs. midday leaf water potentials (c); (B) early summer vs. late summer
midday c; (C) leaf life span vs. early summer midday c; (D) leaf life span vs. minimum seasonal c (based on late summer
midday c for evergreens, Sambucus, and Toxicodendron, and early summer midday c for remaining deciduous taxa). Open
circles represent deciduous species; solid circles represent evergreen species. NS indicates nonsignificance (P . 0.05).
tively) or early summer cmd (R 5 20.04 and R 5 0.09,

N 5 20 and 13, respectively; Fig. 1C). There was a
non-significant negative trend between LLS and cmin
(R 5 20.35, P 5 0.14; Fig. 1D), and a barely significant
difference in cmin between deciduous and evergreen
species (ANOVA, P 5 0.048). Comparison of early
summer vs. seasonal minimum data (Fig. 1C vs. 1D)
demonstrates that this trend is due to the decline in cmd
exhibited by evergreen species during the summer
drought, not to differences in rooting position or diurnal water loss associated with LLS. The lack of a
strong relationship between LLS and cmin supports their
selection as independent attributes for multiple regression analysis.
Ecophysiology and functional morphology

Photosynthesis and leaf function.Across all 20
species Am, SLA, Nm, and PNUE (see Table 2 for codes
used in this section) declined significantly with LLS,
and were significantly lower in evergreen than decid-
uous species (Figs. 2A, 3). Nitrogen/area (Na ) was

higher in evergreens, and showed a weak positive relationship with LLS. Assimilation/area ( Aa ), g, E, and
WUE were not significantly different between deciduous and evergreen species and were not associated
with LLS or cmin. Assimilation/area and g were strongly
correlated with each other (R 5 0.83, P # 0.0001).
Among the 13 evergreens, Am and PNUE declined significantly with LLS (Fig. 2A). The correlation between
PNUE and WUE was negative but not significant (R
5 20.23 for all 20 species and R 5 20.21 for the 13
evergreens; cf., Field et al. 1983).
Leaf and twig dimensions.Internode length decreased significantly with LLS, and was greater in deciduous than in evergreen taxa (P 5 0.02). Twig diameter and inflorescence length increased and leaf angle decreased (more horizontal) with increasing (less
negative) cmin. For the evergreens, leaf size increased
with cmin (larger leaves in species with lower water
deficit; Fig. 3B).
February 2004
35
FIG. 2. Scatter plots of selected traits in relation to leaf life span (LLS, left) and minimum seasonal leaf water potential
(cmin, right). Lines indicate regression analyses for individual factors, when significant, and R values are pairwise correlation
coefficients. Analyses discussed in Results: Ecophysiology and functional morphology and shown in Fig. 3 were based on
multiple regression with respect to both LLS and cmin. (A, B) Assimilation/mass (total r2 of multiple regression model 5
0.52); (C, D) month of peak leaf production (r2 5 0.53); (E, F) wood density (r2 5 0.23 with Dirca removed, shown by
3); (G, H) hydraulic mean vessel diameter (r2 5 0.51); and (I, J) leaf area:sapwood area ratios (r2 5 0.32). Open circles
represent deciduous species; solid circles represent evergreen species.
Wood and xylem.Wood density (measured on sapwood of twigs from current year) was not significantly
different between evergreen and deciduous species. In
multiple regression, wood density decreased with cmin
and was not significantly associated with LLS (one
outlier, Dirca, was removed for this analysis; Fig. 2E,

F). Hydraulic mean vessel diameter was higher in deciduous than in evergreen species (but not significantly
associated with LLS in multiple regression) and increased with cmin (Fig. 2G, H). Leaf area:sapwood area
36
DAVID ACKERLY
Vol. 74, No. 1
FIG. 3. Summary of significant results of multiple regression for all traits (Table 2) vs. the two anchor traits: leaf life
span and minimum seasonal water potential (cmin). (A) Results for all 20 species. Wood density regression on cmin is only
significant when Dirca is removed. (B) Results for 13 evergreen species (see Table 1). Only traits with significant effects of
one or both factors are shown. Solid lines: positive effect; dashed lines: negative effect; thin lines: P # 0.05; heavy lines:
P # 0.01. Symbols by trait names indicate traits associated with leaf life span only (open circles), with cmin only (solid
circles), or with both (gray circles).
February 2004
ratios (inverse of Huber ratio) increased with cmin (Fig.

2I, J). Among the 13 evergreen species, wood density
decreased and both vessel diameters and leaf area:sapwood area ratios increased with cmin.
Canopy dimensions and seed size.Plant stature
(composite variable based on height, canopy diameter,
individual stem diameter, and basal area) increased
with LLS across all 20 species. For the evergreens,
canopy spread and number of stems declined with cmin,
and spread increased with LLS. Seed size increased
with LLS among the evergreens.
Phenology
The onset of vegetative growth was significantly later in species with longer LLS, and was later in evergreen than in deciduous species (P , 0.01; Fig. 2C).
In the evergreen species, the duration of vegetative
growth declined with LLS. Across all species, the initiation of leaf drop was significantly later as cmin increased (i.e., in species with lower water deficit).
Summary of trait variation

Fig. 3 summarizes these results, showing significant
effects of the multiple regression of each trait on LLS
and cmin (anchor traits), for all 20 species and separately for the 13 evergreens. Traits are arranged to
show those associated only with LLS (gas exchange,
phenology, seed size), only with cmin (vessel diameter,
leaf angle, leaf size, leaf area:xylem area, wood density), or with both (canopy spread, stem number). Results were similar for individual regression on each
anchor trait or multiple regression on both, demonstrating that these traits are independently linked to
LLS and cmin.
Principal components analysis

The first two axes of a principal components analysis
(PCA) explained 22.6% and 19.3% of the variance in
the 33 traits (the third axis explained only 12%). The
top 10 traits loading on the first axis were primarily
related to water potentials and xylem characteristics (in
descending order, indicating the trait values associated
with positive scores on the axis; Fig. 4A): low leaf
area:sapwood area ratios, more negative cmin, high
wood density, low specific leaf area, small vessel diameter, high canopy spread, high Na, high leaf numbers,
small leaf size, more negative cpd. The traits loading
on the second axis were associated with leaf life span
and gas exchange (in descending order): low Am, low
PNUE, long LLS, low stomatal conductance, low transpiration rate, short twigs, low Aa, short internode
lengths, late onset of growth, and large leaf size. Leaf
life span and cmin, the two anchor traits in this paper,
loaded primarily on the second and first axes, respectively, though LLS was also weakly associated with
axis 1. As a result, the vectors for these two traits were
obliquely angled but not strictly orthogonal (Fig. 4A),
reflecting their weak but nonsignificant negative as-
37
sociation. The position of the species in the PCA plot

(Fig. 4B) reflected clear distinctions among the three
strategies of regeneration (with the exception of one
post-fire sprouter, Rhamnus crocea, which occurred
within the post-fire seeder group). The two evergreen
post-fire groups fall in the upper half (positive values
of axis 2), corresponding to long leaf life span, but
they are differentiated along the first axis reflecting
differences in maximum water deficit. The opportunist
group falls in the lower half, corresponding to short
leaf life span, and is broadly distributed along the
orthogonal c min axis. Cercocarpus, which was not assigned to any group, was located at the edge of the
opportunist group near Baccharis (see Methods: Regeneration strategies).
DISCUSSION
The comparative ecology of chaparral and other
mediterranean climate vegetation has played a critical
role in the development of plant physiological ecology.
Much of the early work in this area focused on the
costs and benefits of evergreen vs. deciduous leaves,
followed by studies on rooting depth and water relations, and the functional ecology of post-fire regeneration. The objective of this paper was to assess a large
number of physiological and functional traits to integrate these three areas of inquiry in the context of a
single community of co-occurring species.
Suites of traits associated with leaf life span and

minimum seasonal water potential
The traits linked to leaf life span (LLS) and to minimum seasonal water potential (cmin) in this study are
largely consistent with previous studies in chaparral
and other ecosystems (e.g., Pockman and Sperry 2000,
Westoby et al. 2002). One notable outcome of this study
is the contrasting results for area-based vs. mass-based
assimilation (A) and nitrogen (N) concentrations. Areabased assimilation (Aa) was not correlated with LLS
and not significantly different between deciduous and
evergreen species (see Damesin et al. 1998). In addition, Na was negatively correlated with SLA (R 5
20.73, P 5 0.0003), and Aa was positively associated
with both Na (P 5 0.016) and stomatal conductance (g,
P # 0.0001) in multiple regression. These results are
consistent with recent studies showing that reduced
specific leaf area and increased Na enhance water use
efficiency in arid environments (Cunningham et al.
1999, Wright et al. 2001; see also Givnish 1979).
Broader studies across multiple habitats have not observed such a dramatic shift in area-based vs. massbased patterns in relation to LLS (Reich et al. 1999),
so these patterns may reflect the particularly important
role of water limitation in semiarid to arid environments.
It is also important to note that the evergreendeciduous distinction reflects a continuum of variation in
LLS and associated physiological traits. Deciduousness
38
DAVID ACKERLY
Vol. 74, No. 1
FIG. 4. Position of (A) traits and (B) species on first two axes of principal components analysis for all traits included in
this study (trait abbreviations follow Table 2 codes; species follow Table 1 codes). In panel B, lines are drawn around groups
of species with different post-disturbance regeneration strategies (see Methods: Regeneration strategies). Bold font indicates
evergreen species; plain font, deciduous species.
is an important phenological trait in strongly seasonal

environments, but there is as much variation in LLS
among the evergreens as there is between the two
groups in this community. In addition, five species had
mean LLS of ,1 yr and were evergreen due to a prolonged period of leaf production from early spring into
summer (negative correlation of LLS with growth duration, Fig. 3B; see Kikuzawa 1991, Ackerly 1996). A
February 2004
similar pattern occurs in the coastal sage species Salvia

mellifera, which has short leaf life span (and is often
considered drought deciduous), but actually maintains
some leaf area throughout the year due to sustained
production of new leaves on subcanopy shoots through
the dry season (Gill and Mahall 1986).
Minimum seasonal water potentials (cmin) were
strongly correlated with predawn water potentials, indicating that effective rooting depth (relative to the
water profile) was the primary source of variation
among species. Across all 20 species, those with less
negative (5 higher) cmin had larger vessels, lower wood
density, more horizontal leaves, thicker twigs, longer
inflorescences, higher leaf area:sapwood area ratios,
and later onset of leaf drop. In the evergreens, higher
cmin was also associated with larger leaf sizes, narrower
crowns, and fewer stems (more tree-like growth form,
rather than multistemmed shrubs). We did not assess
xylem resistance to embolism, but published correlations with wood density (Hacke et al. 2001) suggest
that this measure of drought tolerance would also be
associated with this suite of traits, at least in evergreens
(see Pockman and Sperry 2000). The results for leaf
size of evergreens are also noteworthy, as the significance of leaf size variation within communities is still
poorly understood (Givnish 1987, Grubb 2002, Westoby et al. 2002). Across broad climatic gradients, leaf
size is associated with water availability, as predicted
on functional grounds in relation to energy balance and
water use efficiency (Hamann 1979, Dolph and Dilcher
1980, Givnish 1984, Fonseca et al. 2000). Here, the
relationships of twig diameter, inflorescence size, and
leaf size with cmin indicate that the leaf size traits are
linked to variation in water deficit. A subsequent study
found that small leaf size enhanced water use efficiency
in the evergreens, apparently due to reduced leafair
temperature differentials (R. Bhaskar, unpublished
data), and the other traits may be indirectly associated
due to allometric linkages (see Ackerly and Donoghue
1998, Herrera 2002).
Ecophysiology, drought tolerance, and regeneration

The relationship between LLS and cmin in this community was weakly negative (though not perfectly orthogonal), reflecting an absence of deciduous species
that experience the most extreme leaf water deficit, and
of evergreens with extremely deep roots (Fig. 1D). The
former combination probably does not exist due to sensitivity of xylem and leaves of deciduous plants to water deficit (e.g., Nilsen and Muller 1981, Kolb and Davis 1994). The deep-rooted evergreen strategy may be
represented by Quercus spp. (Goulden 1996), but we
do not have comparable data to determine exactly
where these species would fall. Distinct suites of traits
were associated with the two anchor traits (Fig. 3).
The overall distribution of the 33 traits in the principal
components analysis (PCA) space does not suggest that
all the traits cluster neatly into two discrete suites.
39
FIG. 5. Conceptual diagram relating (A) strategies of

avoidance and tolerance of tissue water deficit and (B) strategies of regeneration following disturbance, in a two-dimensional space defined by suites of traits related to leaf life span
and minimum seasonal leaf water potentials. See Discussion:
Ecophysiology, drought tolerance, and regeneration.
However, the traits in these two groups do have the

strongest combined loadings on the first two PCA axes
(based on distance from the origin, Fig. 4A). So the
multivariate analysis does support the selection of the
two anchor traits as key attributes to differentiate functional strategies among these species. Based on these
results, I propose a conceptual model integrating plant
strategies in chaparral related to seasonal water deficit
and disturbance. The strategy space is defined by axes
related to LLS and cmin, and their associated suites of
traits (Fig. 5). These anchors are used to identify the
two dimensions, but the axes reflect overall covariation
40
DAVID ACKERLY
in the respective suites of correlated traits. The strategy

space is based on an almost 908 clockwise rotation of
the PCA space, such that the deciduousevergreen axis
is aligned horizontally, and the water deficit axis vertically (Fig. 5). Higher values of cmin are at the top (as
in Fig. 1), corresponding to greater access to water
(deeper roots or establishment in moist microsites).
The various combinations of LLS and maximum water deficit correspond to recognized strategies for dealing with seasonal water availability (Levitt 1980).
Plants that experience high (less negative) minimum
water potentials avoid drought either through deep
roots or establishment in wet microsites, representing
a morphological or habitat-based strategy of avoidance
of tissue water deficits. Summer deciduous plants with
shallow roots, or living in very dry sites, have a phenological strategy for avoidance of tissue water deficits,
as they drop their leaves in early summer in response
to decreasing water potentials and avoid the worst of
the summer drought (Nilsen and Muller 1981).
Physiological drought tolerance is restricted to the
combination of shallow roots and long leaf life span,
leading to very low leaf water potentials in leaves that
persist through the dry season. Some of these species
maintain leaf turgor and gas exchange during the dry
season through shifts in osmotic potential and the bulk
modulus of elasticity (e.g., Quercus, Heteromeles; Davis and Mooney 1986a; D. Ackerly, unpublished data).
In other cases, evergreen species with very shallow
roots may not be capable of sufficiently large osmotic
adjustments to maintain turgor through the summer
(e.g., Ceanothus; Saruwatari and Davis 1989; D. Ackerly, unpublished data). In this situation, the functional
advantage of evergreenness, and high drought tolerance
of xylem is presumably the capacity for rapid utilization of autumn rains for increased carbon gain, without
waiting for the production of a new cohort of leaves,
and amortization of leaf construction costs over two or
more growing seasons. In this study, late summer physiological activity was not evaluated, so it is not possible
to generalize about other functional traits that may be
associated with these different forms of drought tolerance.
Contrasting strategies of regeneration following disturbance (post-fire seeders, post-fire sprouters, and opportunists) are also differentiated in this two-dimensional trait space (Fig. 5B, and see Fig. 4B). Among
evergreens, the discrimination of post-fire seeders vs.
sprouters along the cmin axis reflects the contrasts in
rooting depth and drought tolerance previously recognized in these groups (Davis 1989, Groom and Lamont 1995, Davis et al. 1998, 1999). The physiology
of the opportunist species (short leaf life span, high
specific leaf area, high photosynthetic rates, prolonged
growing season) parallels the constellation of traits associated with early successional strategies in mesic forests (Bazzaz 1979). These traits promote rapid growth
to stay above competitors or complete the life cycle
Vol. 74, No. 1
before repeated disturbance. The variation among opportunists in maximum water deficit deserves further
consideration. It may reflect differing tolerance to low
water availability during establishment, such that species that are deep rooted as adults (e.g., Sambucus,
Eriodictyon) are restricted to relatively moist microsites for seedling establishment, or to unusually wet
years. Shallow-rooted deciduous species (e.g., Lotus,
Lepechinia) may be more successful in dry and exposed
microsites, in dry years, or in frequently disturbed sites,
as they can reach reproductive maturity at a small size.
These species do have smaller vessels and denser wood
than their deeper rooted deciduous counterparts. This
suggests a strategy intermediate between drought tolerance and avoidance, as they avoid the late summer
drought by dropping leaves but they may have greater
tolerance of the early summer drought experienced at
the end of their growing season (Fig. 5).
The central importance of fire as a disturbance factor
in chaparral is clear, but small-scale soil and canopy
disturbances have received less attention (Zedler 1982).
In the absence of fire, especially for long periods of
time, mature shrubs may die from drought, herbivory,
or disease, opening up possibilities for gap-dependent
regeneration. Landslips, animal activity, and human
disturbance (trails, roads, development) also cause soil
disturbance and create canopy openings of various sizes. These canopy gaps may result in a localized flush
of belowground resources, as well as light availability
that can be utilized by fast-growing species. Canopy
openings may also play a significant role in recruitment
of juveniles of the obligate sprouting species, which
establish under the canopy during fire free intervals,
analogous to the process of advance regeneration in
forests (see Keeley 1992b). At our study site, the history of human disturbance may have increased the
abundance of opportunist species, especially along trail
and road edges. However, these species (and others
such as Artemisia californica) occur widely in chaparral, suggesting an important role of non-fire disturbance in the evolution of chaparral communities and
the life histories of the constituent species.
In terms of the physiological ecology of succession,
the opportunists and the post-fire obligate sprouters
parallel the early vs. late successional strategies, respectively, of temperate and tropical forests. In contrast, the post-fire seeders present a novel functional
group. In the PCA (Fig. 4), this group is intermediate
between the opportunist and post-fire sprouters on axis
2, but they are at the extreme along axis 1. They have
small seeds and high Aa, like the opportunists, but long
leaf life span and low Am, like the post-fire sprouters,
and they have the highest wood density of the three
groups. This represents a unique combination of early
successional and stress tolerant traits reflecting the
post-fire environment of mediterranean communities,
where seedlings and resprouts experience intense
drought in the first summer following fire.
February 2004
Collectively, these observations suggest that two distinct modes of post-disturbance regeneration should be
recognized in the chaparral, a specialized fire-dependent strategy, and an opportunistic post-disturbance
strategy, including fire as well as small-scale physical
disturbance of the soil and/or canopy. It is well established that disturbances of different frequency and severity have critical effects on community structure and
dynamics. In temperate and tropical forests there is also
evidence of distinct sets of colonizing species depending on disturbance severity (Frelich and Reich 1999,
Loehle 2000). However, the species that colonize very
large disturbances (e.g., Populus in temperate forests,
Miconia in the tropics) and smaller tree-fall gaps (e.g.,
Betula, Cecropia, respectively) are all characteristic of
the early-successional group in terms of their physiological attributes. The post-fire specialists in the chaparral, combining stress tolerance and early-successional traits, may be unique to semiarid, fire-prone ecosystems and it would be interesting to search for analogous groups in other ecosystems that combine severe
disturbance and highly seasonal nutrient or water availability.
CONCLUSIONS
The development of plant ecological strategy
schemes, like many exercises in classification, has proceeded simultaneously from top-down and bottomup approaches. Top-down approaches have identified
critical aspects of the environment which are believed
to influence plant function and life history, such as
disturbance and regeneration (Bazzaz 1979, 1984,
Grime 1979, Tilman 1988), the unique environments
created by resource limitation at different spatial and
temporal scales (Grubb 1998), and overall variation in
resource availability and abiotic stress (Grime 1979,
Chapin et al. 1993). Bottom-up approaches have started
from a consideration of the critical plant traits influencing growth and regeneration (e.g., carbon gain, seed
size), and searched for suites of covarying traits that
define major axes of variation (Grime et al. 1997, Reich
et al. 1997). Westoby et al. (2002) have summarized
research in this area, highlighting four more or less
independent axes of plant strategy variation anchored
by leaf life span, seed size, leaf size, and plant stature.
Recently, there has been a renewed interest in plant
hydraulic strategies and the ecological implications of
xylem anatomy and physiology (Pockman and Sperry
2000, Sperry 2000). These studies have suggested a
fifth important axis of interspecific variation related to
minimum seasonal water potentials, and trade-offs between hydraulic conductivity and resistance to embolism at low water potentials (Tyree et al. 1994).
As discussed in this paper, the ecological significance
of these suites of traits depends on their relationships
with one another. In particular, the observation that
functionally important suites of traits are independent
of one another, in terms of their relationships in a set
41
of coexisting species, may indicate that they represent

independent axes of niche differentiation. To understand the broader implications of these results, it would
be useful to examine the generality of the relationships
between different suites of traits within and between
communities. Traits that are uncorrelated in this set of
chaparral species may collapse into a single axis of
functional variation in other communities, or they may
covary at very large scales along climatic gradients but
remain relatively independent within local communities. For example, early successional species are often
described as possessing both small seed size and high
specific leaf area and photosynthetic rates, and in some
communities this is reflected in a direct correlation between these traits (e.g., Reich et al. 1998). On the other
hand, in the chaparral species studied here these traits
are not significantly correlated, as small seed size is
found in both the opportunists and the post-fire seeders,
so there is no overall relationship with leaf function.
Similarly, leaf size and specific leaf area both tend to
decline along gradients of nutrient and water availability, leading to positive correlations of the two traits
on large geographic gradients (Fonseca et al. 2000).
However, within individual communities the relationship between the two may be negative, insignificant (as
in this study), or positive depending on the most important factors influencing leaf function in a given site
(see Niinemets and Kalevi 1994, Shipley 1995, Grubb
1998, Ackerly et al. 2002).
Conceptual discussion of ecological strategies is enhanced by collapsing species functional diversity into
discrete groups (e.g., functional types). Unfortunately,
a focus on functional group classifications often leads
to debate about whether or not the groups are distinct and real, and to conflicts between different
classification schemes (Grace 1991). As an alternative,
we may wish to identify the major dimensions of variation in plant strategies with reference to a relatively
small number of measurable traits, and examine the
distribution of species in the multidimensional space
defined by these axes (Westoby 1998, Loehle 2000,
Westoby et al. 2002; Diaz et al., unpublished manuscript). Such an approach may help to resolve conflicting or disparate views of plant strategies by focusing
on relationships among the underlying species traits.
Dividing the multidimensional space into discrete
groups (e.g., Fig. 5) is useful for synthesis and communication, but it is essential to remember that there
may be few discontinuities in the distributions of functional traits underlying this ecological diversity.
ACKNOWLEDGMENTS
I am deeply indebted to Kathleen Starmer, who managed
and conducted much of the data collection for this study;
without her assistance it would not have been possible. Will
Cornwell generously contributed data on wood density. I also
thank N. P. R. Anten, B. Bennett, S. Colfer, C. L. Phillips,
K. A. Preston, C. A. Knight, B. Lazarus, S. Allison, R. Starmer, V. Yovovich, and P. Yelton for assistance with data col-
42
DAVID ACKERLY
lection and analysis. Discussions with T. M. Aide, S. Davis,

P. Grubb, J. Keeley, J. Kriewall, H. A. Mooney, C. Peterson,
and M. Westoby contributed greatly to this paper. I thank R.
Bhaskar, W. K. Cornwell, M. J. Lechowicz, K. A. Preston,
and D. Schwilk for comments on the manuscript. Funding
was provided by a Terman Fellowship from Stanford University, and NSF grant 0078301.
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Young, J. A., and C. G. Young. 1992. Seeds of woody plants
in North America. Dioscorides Press, Portland, Oregon,
USA.
Zedler, P. H. 1981. Vegetation change in chaparral and desert
communities in San Diego County, California. Pages 406
430 in D. C. West, H. H. Shugart, and D. B. Botkin, editors.
Forest succession: concepts and application. Springer-Verlag, New York, New York, USA.
Zedler, P. H. 1982. Plant demography and chaparral management in southern California. Pages 123127 in C. E.
Conrad and W. C. Oechel, editors. Proceedings of the symposium on dynamics and management of mediterraneantype ecosystems; 2226 June 1981; San Diego, California.
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APPENDIX
Additional details on data analysis are available in ESAs Electronic Data Archive: Ecological Archives M074-001-A1.
SUPPLEMENT
Comparative data on functional traits of chaparral shrubs are available in ESAs Electronic Data Archive: Ecological
Archives M074-001-S1.

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Ecological Monographs, 74(1), 2004, pp.

FUNCTIONAL STRATEGIES OF CHAPARRAL SHRUBS IN RELATION TO

whether these suites of traits covary or whether they

Mediterranean-type ecosystems (MTE) provide an

rooting depths of 4 m or more have been recorded in

Disturbance and regeneration

FUNCTIONAL STRATEGIES OF CHAPARRAL SHRUBS

of co-occurring species from a California chaparral

of the chaparral is unknown. Though chaparral extends

Species and plant selection

FUNCTIONAL STRATEGIES OF CHAPARRAL SHRUBS

Adenostoma fasciculatum Hook &

The majority of data were collected on a set of 10

insolation values for the locations of the primary plants

FUNCTIONAL STRATEGIES OF CHAPARRAL SHRUBS

Summary of traits used in this study.

Leaf and twig morphology

Wood and xylem

Water potentials (c)

Traits were transformed as necessary to meet the assumption of normality of residuals.

length, leaf number (including leaves on fascicles in

sampled for water potentials and the other data were

were obtained from all species, though some deciduous

species. On each plant the following measurements

FUNCTIONAL STRATEGIES OF CHAPARRAL SHRUBS

were lost during 1999, based on the month in which

of normality of residuals (Table 2). One extreme low

Interspecific variation in functional traits

Leaf life span and minimum seasonal water potential

tively) or early summer cmd (R 5 20.04 and R 5 0.09,

Ecophysiology and functional morphology

uous species (Figs. 2A, 3). Nitrogen/area (Na ) was

FUNCTIONAL STRATEGIES OF CHAPARRAL SHRUBS

outlier, Dirca, was removed for this analysis; Fig. 2E,

FUNCTIONAL STRATEGIES OF CHAPARRAL SHRUBS

ratios (inverse of Huber ratio) increased with cmin (Fig.

Summary of trait variation

Principal components analysis

sociation. The position of the species in the PCA plot

Suites of traits associated with leaf life span and

is an important phenological trait in strongly seasonal

FUNCTIONAL STRATEGIES OF CHAPARRAL SHRUBS

similar pattern occurs in the coastal sage species Salvia

Ecophysiology, drought tolerance, and regeneration

FIG. 5. Conceptual diagram relating (A) strategies of

However, the traits in these two groups do have the

in the respective suites of correlated traits. The strategy

FUNCTIONAL STRATEGIES OF CHAPARRAL SHRUBS

of coexisting species, may indicate that they represent

lection and analysis. Discussions with T. M. Aide, S. Davis,

FUNCTIONAL STRATEGIES OF CHAPARRAL SHRUBS

vegetation. Second edition. Cambridge University Press,

resprouters species of mediterranean-type ecosystems of

Sperry, J. S., K. L. Nichols, J. E. Sullivan, and S. E. Eastlack.

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