Patterns of tree dieback in Queensland, Australia: The importance of drought stress and the role of resistance to cavitation

Article (PDF Available)inOecologia 139(2):190-8 · May 2004with128 Reads
DOI: 10.1007/s00442-004-1503-9 · Source: PubMed
Abstract
During the extreme 1992-1997 El Niño drought event, widespread stem mortality, or tree "dieback", of both mature and juvenile eucalypts occurred within the tropical savannas of northeast Australia. Most of the dieback occurred in individuals of the ironbark species complex ( Eucalyptus crebra- E. xanthoclada) while individuals of the bloodwood species Corymbia erythrophloia, exhibited significantly less stem mortality. Indicative of greater water stress, predawn and midday xylem water potentials of ironbark adults and saplings were significantly more negative than predawn values of bloodwoods. The very negative xylem water potentials in ironbarks suggest that stem mortality in both adult and juvenile ironbarks results from drought-induced embolism and that ironbarks perhaps have a shallower and less extensive root system than bloodwoods. Although predawn and midday water potentials for ironbark adults and saplings were similar, a census of mature and juvenile ironbark trees indicated that mortality was higher in adult trees. Cavitation vulnerability curves indicated that ironbark saplings may be better buffered against cavitation than adult trees. If they possess smaller root systems, saplings are more likely than adults to experience low xylem water potentials, even in non-drought years. Xylem conduits produced in adult trees during periods of normal rainfall, although perhaps more efficient in water conduction, may be more vulnerable to cavitation during infrequent severe droughts.
Oecologia (2004) 139: 190198
DOI 10.1007/s00442-004-1503-9
ECOPHYSIOLOGY
Kevin J. Rice
.
Steven L. Matzner
.
William Byer
.
Joel R. Brown
Patterns of tree dieback in Queensland, Australia: the importance
of drought stress and the role of resistance to cavitation
Received: 14 April 2003 / Accepted: 14 January 2004 / Published online: 6 February 2004
# Springer-Verlag 2004
Abstract During the extreme 19921997 El Niño drought
event, widespread stem mortality, or tree dieback,of
both mature and juvenile eucalypts occurred within the
tropical savannas of northeast Australia. Most of the
dieback occurred in individuals of the ironbark species
complex (Eucalyptus crebra E. xanthoclada) while
individuals of the bloodwood species Corymbia ery-
throphloia, exhibited significantly less stem mortality.
Indicative of greater water stress, predawn and midday
xylem water potentials of ironbark adults and saplings
were significantly more negative than predawn values of
bloodwoods. The very negative xylem water potentials in
ironbarks suggest that stem mortality in both adult and
juvenile ironbarks results from drought-induced embolism
and that ironbarks perhaps have a shallower and less
extensive root system than bloodwoods. Although pre-
dawn and midday water potentials for ironbark adults and
saplings were similar, a census of mature and juvenile
ironbark trees indicated that mortality was higher in adult
trees. Cavitation vulnerability curves indicated that
ironbark saplings may be better buffered against cavitation
than adult trees. If they possess smaller root systems,
saplings are more likely than adults to experience low
xylem water potentials, even in non-drought years. Xylem
conduits produced in adult trees during periods of normal
rainfall, although perhaps more efficient in water conduc-
tion, may be more vulnerable to cavitation during
infrequent severe droughts.
Keywords Xylem cavitation
.
Drought stress
.
Eucalyptus
.
Hydraulic conductance
.
Water relations
Introduction
Forest dieback is a recurring phenomenon that has been
reported from a variety of woodland and forest commu-
nities in many parts of the world (Mueller-Dombois 1986;
Auclair 1993; Tafangenyasha 1997; Nepstad et al. 1999).
Dieback is characterized by rapid defoliation and progres-
sive stem mortality in overstory trees and has been
attributed to a wide range of potential causes (Landsberg
and Wylie 1983; Pook and Forrester 1984; Mueller-
Dombois 1990). In Australia, tree or eucalypt dieback
occurs in a number of woodland and savanna habitats
throughout the continent (Old et al. 1981; Kirkpatrick and
Marks 1985). Although dieback events in the late
nineteenth and early twentieth century were primarily in
southern locations on the continent, diebacks occurring
within Australia in the last 50 years are now more
widespread (Kile 1981). Using scientific records and
historical accounts, the occurrence of dieback has been
related to the severe droughts Australia has experienced
periodically during the last 150 years (Fensham and
Holman 1999). These El Niño drought events have had a
significant effect on Australian savanna structure and
composition (Newell 1998; Weste et al. 2002) as well as
the fauna associated with these habitats (Newell 1997;
Ford et al. 2001). Some researchers have questioned the
primary role of drought as the factor initiating dieback
(Podger 1981; Landsberg 1985). However, the most
widely accepted view is that drought stress causes dieback
directly by inducing cavitation (Auclair 1993) and also
renders the tree more susceptible to insect attack (Lowman
and Heatwole 1992) and pathogens (Old et al. 1990).
K. J. Rice (*)
Department of Agronomy and Range Science and Center for
Population Biology, University of California,
Davis, CA 95616, USA
e-mail: kjrice@ucdavis.edu
Fax: +1-530-7524361
S. L. Matzner
Department of Biology, Augustana College,
Sioux Falls, SD 57197, USA
W. Byer
Davies Laboratory, CSIRO,
4814 Aitkenvale, Queensland, Australia
J. R. Brown
Jornada Experimental Range, New Mexico State University,
P.O. Box 30003 Las Cruces, NM 88003, USA
Australian eucalypt species differ significantly in sus-
ceptibility to dieback on both regional and local scales
(Old et al. 1981; Martin et al. 2001). Interspecific
differences in dieback are well documented; however
there has been less study of the ecophysiological
mechanisms underlying these differences (Auclair 1993;
McFarlane and Adams 1998; Fensham and Holman 1999;
Burgess et al. 2001).
During the El Niño event from 1992 to 1997, northeast
Australia experienced a severe drought; analyses of
regional patterns of soil moisture deficit indicated that
the drought in northern Queensland was the most severe
on record (Fensham and Holman 1999). This period of
drought in northern Queensland was accompanied by
widespread tree dieback in a variety of savanna woodlands
and a survey conducted by Fensham and Holman (1999)at
the end of the drought demonstrated strong differences in
rates of dieback among tree species. In part these
interspecific differences were explained by variation in
geology and soil characteristics that presumably influences
water availability. However, the factors responsible for
interspecific differences in dieback within a site were less
clear and the authors noted that further study is needed to
determine how variation in drought tolerance may affect
local patterns of dieback.
During the middle of the drought in November 1995,
our initial observations of tree dieback at two field stations
located in northern Queensland revealed a large amount of
stem mortality in adults and saplings of the dominant
overstory tree species. Our preliminary survey also
suggested that there were interspecific differences in
dieback at both sites. In particular, ironbark eucalypts at
both sites appeared much more susceptible to dieback than
bloodwood eucalypts.
To better understand the causes underlying these
apparent differences in dieback, we conducted a study
that combined field surveys of stem mortality with
ecophysiological measurements of drought stress and
cavitation resistance. In particular we were interested in:
(1) documenting whether there were differences in stem
mortality among species and among age classes within a
species, and (2) exploring the possibility that these
differences were related to differences in drought stress
or drought tolerance, or both.
Materials and methods
Two field stations in north Queensland, Australia were used for stem
mortality surveys and water relations studies. Both the Hillgrove
Station site (19°40S, 145°45E) and the Cardigan Station site (20°
11S, 146°43E) are characterized by a sub-humid climate; precip-
itation is highly seasonal with most rainfall (approx. 80%) occurring
from December to April. The Hillgrove site receives an average
rainfall of 535 mm. Although long term rainfall records for Cardigan
are not available, annual rainfall at nearby Ravenswood (20°06S,
146°53E) averages 684 mm (McIvor and Gardener 1991). During
the period of our study, northern Queensland was undergoing the
most severe drought ever recorded (Fensham and Holman 1999); the
average annual precipitation from 1992 to 1996 was 42% and 40%
below the long-term average at Hillgrove and Cardigan, respec-
tively. The soil at the Hillgrove site is a clay loam (Ustic Paleagid)
derived from basalt parent material and is slightly more fertile than
the soil at the Cardigan site (McIvor and Gardener 1995). Soil at the
Cardigan site is a sandy clay loam (Typic Rhodustalf) derived from
granodiorite parent material. Tree density within the open woodland
at Hillgrove is 64 trees per hectare. Using tree distribution data and
nomenclature from Henderson (1997), the overstory is dominated by
red-barked bloodwood, Corymbia erythrophloia and a species
complex of two closely related narrow leaf ironbark species
Eucalyptus crebra and E. xanthoclada (hereafter referred to as the
E. crebra complex). An understory of warm season, perennial
grasses consists primarily of Heteropogon contortus, Chrysopogon
fallax, and Bothriochloa ewartiana (McIvor et al. 1991). C.
erythrophloia and the E. crebra complex are also the dominant
overstory species at Cardigan with a tree density of 127 trees per
hectare. Understory composition is similar to that at Hillgrove with
perennial grasses that include H. contortus, C. fallax, B. ewartiana,
and Sehima nervosum (McIvor and Gardener 1991).
To quantify patterns of stem mortality, a series of four 100 m belt
transects were established at 200 m intervals from an initial random
point located within relatively continuous woodland stands at each
site. Within each 20 m wide belt transect, the number of saplings and
adults exhibiting total stem dieback (i.e. no stems with leaves) were
recorded; trees with partial stem dieback were noted but included in
the totals. Saplings were defined as plants with a stem diameter
between 1 and 5 cm at a height of 1 m and adults were defined as
plants with a diameter greater than 5 cm at a height of 1 m.
Seedlings (i.e. plants less than 1 cm stem diameter at 1 m height)
were rare at both sites and were not recorded. At Cardigan the total
number of bloodwood plants counted was 320 adults and 536
saplings and the number of ironbark plants counted was 382 adults
and 608 saplings. At Hillgrove the number of bloodwood plants
counted was 85 adults and 156 saplings while for ironbark the totals
were 305 adults and 472 saplings.
During the initial survey of stem dieback, eight adult trees and
eight saplings of the ironbark and bloodwood species at each site
were selected in a stratified random procedure and tagged. For each
of the tagged plants, stem xylem pressure was measured in
November 1995 and September 1996 using a Scholander pressure
chamber (PMS Instruments, Corvallis, Ore., USA). Replicate shoot
tips from each of the tagged plants were measured at predawn
(02000500 hours) and at midday (12001400 hours). Shoots were
placed in plastic bags and measured within 5 min of collection to
minimize water loss (Turner 1987). Because of some mortality, the
number of plants measured in 1996 was slightly less than in 1995.
Following a series of rainstorms in March 1997, predawn and
midday measurements were made on surviving tagged plants at the
Hillgrove site to examine patterns of xylem pressure at the end of the
drought.
Native embolism and vulnerability measurements were taken in
September 1996 for ironbark and bloodwood plants at both sites on
a random subset of at least five tagged trees and saplings used in
xylem pressure measurements. At Hillgrove the sample size for
ironbark was increased to seven adults and saplings. Stem material,
estimated at no more than 2 years old, was collected in early
morning and transported to the laboratory in plastic bags containing
moist paper towels to minimize water loss. From each branch, stem
segments approximately 20 cm long and 0.5 cm in diameter were
cut underwater with a razor blade to prevent the introduction of
additional embolisms. Stem length and diameter were measured. To
measure native embolism (i.e. xylem embolism associated with in
situ cavitation), stems were fitted to tubing attached to a hydraulic
head of 0.003 MPa. Using a filtered (0.22 µm) 0.5% sodium
hypochlorite perfusion solution that retards microbial growth
(Matzner et al. 2001), this hydraulic head induced flow through
the stem segment. Stem exudate was collected and weighed to
determine an initial flow rate (k
hi
). The initial flow rate was used to
calculate native embolism (see below).
To construct vulnerability curves for the collected stem samples,
the air-injection procedure was used (Salleo et al. 1992; Sperry and
Saliendra 1994). After measurement of the initial flow rate (k
hi
),
stems were then flushed for 15 min at 0.1 MPa to refill any
191
embolized vessels and the maximum flow rate (k
hf
) was measured.
After conductivity was measured on the flushed stems (i.e. k
hf
), stem
segments were sealed in a double-ended pressure sleeve. Forcing air
into the xylem vessels as pressure was increased within the sleeve
induced xylem cavitation. The amount of cavitation was estimated
by measuring hydraulic conductivity in stem segments exposed to
pressures of 0.0, 0.5, 1.5, 4.0 and 8.0 MPa. Because xylem in
ironbarks and bloodwoods is diffuse porous (Penfold 1961) and
stem material represented 2 years of growth, we used hydraulic
conductivity at 0.5 MPa as a measure of maximum conductivity. In
stems older than 1 year, degraded xylem elements may refill rapidly
with flushing thus artificially increasing maximum conductivity
rates. In turn, because they cavitate rapidly, these aged xylem
elements may give a false indication of high vulnerability (J.S.
Sperry, personal communication). For this reason conductivity was
expressed as a percentage of the conductance measured at 0.5 MPa.
Setting maximum conductance at 0.5 MPa is also justified by the
fact that our field measurements of xylem pressure potentials were
rarely less negative than 0.5 MPa even during the wet season (K.
Rice and W. Byer, unpublished data). Use of the conductivity
measured at 0.5 MPa as a maximum did not change the overall
shape of the vulnerability curves but it did increase the pressures
resulting in 50% conductivity loss by 0.5 0.7 MPa. As a measure of
native embolism, conductivity for k
hi
was expressed as a percentage
of the conductance measured at 0.5 MPa. To check on the
consistency of these vulnerability curves with field observations,
values of native embolism and their associated midday xylem
pressures were compared to rates of conductivity predicted by the
vulnerability curves.
Nominal logistic regression (JMP Statistical Program, SAS, Cary,
N.C.) was used to analyze both the main and interactive effects of
site (Hillgrove vs Cardigan), species (ironbark vs bloodwood) and
age class (adult vs sapling) on frequency of stem mortality. Main
and interactive effects of site, species and age class on predawn
xylem pressure were examined separately for the November 1995
and September 1996 samples as a three-way factorial ANOVA using
the general linear model procedure (SAS, Cary, N.C.). Because
predawn xylem pressure was highly correlated with midday xylem
pressure for all data sets (P <0.001; Pearsons r >0.90), statistical
analyses were conducted only on predawn data. A two-way factorial
analysis of predawn measurements taken at the Hillgrove site in
March 1997 examined species and age class effects only. To reduce
heterogeneity of variance among treatments, predawn xylem
pressure data were transformed to natural logarithms. Effects of
site, species and age class on cavitation vulnerability were analyzed
using repeated-measures ANOVA within the SAS general linear
model procedure. The within-subject effect was the level of applied
pressure while successive hydraulic conductance measurements on
Fig. 1 Variation in average predawn and midday xylem pressures
between saplings and adults of bloodwoods and ironbarks at A
Cardigan and B Hillgrove in 1995 and C Cardigan and D Hillgrove
in 1996. Error bars represent ±1 SE. Diurnal recovery is represented
by the percent change between midday and predawn xylem
pressures
192
single stems represented the repeated factor. Interactive effects of
site, species and age class on vulnerability curves were tested by the
within-subject by between-subject interaction terms. Hydraulic
conductivity data conformed to assumptions of parametric analysis
and so were not transformed. Vulnerability curves were created by
fitting second order polynomial regressions to the data.
Results
Stem mortality
Stem mortality was significantly higher in ironbark than in
bloodwood (Wald χ
2
=145.31, P < 0.0001); the size of this
difference in stem mortality between species was sig-
nificantly dependent on site (Wald χ
2
=7.76, P =0.0054).
At Cardigan there was 4.3% stem mortality in bloodwood
(C. erythrophloia) and 45.2% incidence of stem mortality
in ironbark (E. crebra complex). At Hillgrove, bloodwood
stem mortality was again low (4.1%) while stem mortality
in ironbark at this site was 21.5%. This reduction in
ironbark stem mortality at Hillgrove might reflect site
differences, differences between populations in the
ironbark species complex, or both. A significant species
by age class interaction in the analysis (Wald χ
2
=9.31,
P =0.0023) indicates that differences in stem mortality
between adult trees and saplings varied between blood-
wood and ironbark. In bloodwood there was very little
difference in incidence of stem mortality between adults
(3.2%) and saplings (4.9%). In contrast, stem mortality
was higher in ironbark adults (46.1%) than in saplings
(27.5%). A lack of a three-way interaction between site,
species and age class (P =0.82) indicates that greater stem
mortality in adult ironbarks was found at both sites.
Xylem pressure (November 1995)
Analysis of predawn xylem pressure measurements taken
in 1995 indicate that there were strong differences between
bloodwood and ironbark (F =216.74, P < 0.0001) and that
these differences were dependent on site (F =19.33, P
=0.0002; Fig. 1A, B). Averaged across adults and saplings,
ironbarks at Cardigan had much more negative predawn
xylem pressures (mean ±1 SE =2.17±0.07 MPa) than
bloodwoods (1.03±0.10 MPa). This difference was even
more pronounced at Hillgrove where the average predawn
xylem pressure for ironbark was 3.92±0.26 MPa com-
pared to 1.01±0.14 MPa for bloodwood. As noted
previously for stem mortality, significant differences in
ironbark xylem pressures between Cardigan and Hillgrove
may reflect site differences, differences between ironbark
populations, or both. A significant site by age class
interaction (F =8.37, P =0.0080) indicates that for both
bloodwoods and ironbarks, adult predawn xylem pressure
at Cardigan was slightly less negative (1.48±0.22 MPa)
than predawn values for saplings (1.72±0.23 MPa). In
contrast, at Hillgrove the opposite was true; Hillgrove
saplings exhibited less negative average predawn pres-
sures (2.56±0.54 MPa) than Hillgrove adults (2.74
±0.64 MPa).
Xylem pressure (September 1996)
Unlike the results for 1995, there were no significant
interactive effects between site and species or site and age
class on predawn xylem pressure (Fig. 1C, D). There were
significant site differences in predawn pressure (F =7.74,
P =0.010) such that the Cardigan site, with an average
predawn pressure of 3.41±0.53 MPa, appeared to be
more water-limited than the Hillgrove site (2.94
±0.45 MPa). There was also a very strong species effect
(F =318.6, P <0.0001) in that predawn xylem pressures of
the ironbark species complex (averaged across sites and
age class) were more negative (4.89±0.17 MPa) than
those measured for bloodwood (1.23±0.13 MPa).
Xylem pressure (Hillgrove, March 1997)
Taken after a series of storms that signaled the end of the
drought, analysis of xylem pressure measurements at
Hillgrove indicated a strong interactive effect of species
and age class (F =7.12, P =0.017; Fig. 2). Predawn values
were high and similar for bloodwood adults (0.51
±0.07 MPa) and saplings (0.64±0.08 MPa) while
predawn pressures in ironbark saplings (2.58
±0.20 MPa) were much more negative than those
measured for ironbark adults (1.04±0.08 MPa).
In sum, during the dry season in 1995 and 1996 neither
bloodwood adults nor saplings appeared to be significantly
water limited at either site. In contrast, both predawn and
midday xylem pressures measured in the ironbark saplings
and adult trees suggested extreme water-limitation and
exposure to significant drought stress. At the end of the
Fig. 2 Variation in average predawn and midday xylem pressures
between saplings and adults of bloodwoods and ironbarks at the
Hillgrove site at the end of the drought in 1997. Error bars represent
±1 SE. Diurnal recovery is represented by the percent change
between midday and predawn xylem pressures
193
drought, measurements at Hillgrove in March 1997
indicate that, with significant precipitation, xylem pres-
sures in both adult and sapling ironbarks became less
negative. However, adult ironbarks at Hillgrove appear to
recover more rapidly than saplings and their xylem
pressures approached those measured for bloodwood
adults and saplings.
Cavitation vulnerability
Repeated measures analysis of vulnerability curves for
plant material collected in September 1996 from both
Cardigan (Fig. 3) and Hillgrove (Fig. 4) indicated that
bloodwoods were potentially more vulnerable to cavitation
than ironbarks (F =31.07, P <0.0001) and that vulnera-
bility was similar for sapling and adult bloodwoods. In
contrast, a significant age class difference in vulnerability
was apparent for ironbarks (F =9.18, P =0.0045); saplings
appeared to be more resistant to cavitation than adults.
Native embolism in stems collected in September 1996
was expressed as the percent loss of conductivity relative
to maximum conductivity at 0.5 MPa (Table 1). Although
losses of conductivity were less severe than predicted by
the vulnerability curves, there was a strong correlation
(r =0.97; P <0.001) between predicted and measured
values.
Fig. 3 The relationship between stem hydraulic conductance
(expressed as a percentage of maximum conductance) and applied
pressure (MPa) for adult and saplings of A E. erythrophloia and B
E. crebra complex at the Cardigan field site. Curves were fitted
using a second-order polynomial and each point represents the
average SE) of at least five individuals
Fig. 4 The relationship between stem hydraulic conductance
(expressed as a percentage of maximum conductance) and applied
pressure (MPa) for adult and saplings of A E. erythrophloia and B
E. crebra complex at the Hillgrove field site. Curves were fitted
using a second-order polynomial and each point represents the
average SE) of at least five individuals
Table 1 Native embolism of
stems collected in September
1996. Embolism is expressed as
percent loss of conductivity
(mean ± SE) relative to maxi-
mum stem conductivity at
0.5 MPa
Bloodwood (C. erythrofloia) Ironbark ( E. crebraE. xanthoclada)
Cardigan site
Adult plants 37.6% ±6.4 76.7% ±5.4
Saplings 60.1% ±8.2 68.8% ±7.5
Hillgrove site
Adult plants 40.8% ±3.5 69.8% ±6.9
Saplings 34.6% ±7.6 47.6% ±8.9
194
Discussion
Patterns of stem mortality
From our survey of stem mortality at both sites, it is clear
that there were strong differences among tree species in
susceptibility to dieback. In particular, the ironbark
populations at both sites exhibited much higher rates of
dieback than bloodwood populations. This differential
susceptibility among eucalypts to dieback has been
observed before in Queensland as well as other locations
in Australia (Old et al. 1981). Similar to our findings,
previous studies in woodlands in Queensland have
identified the ironbarks such as E. crebra as species that
are likely to exhibit dieback (Wylie and Bevege 1981). A
large-scale survey of dieback in the same area of
Queensland as our study indicated that individuals in the
E. crebra ironbark species complex were especially
susceptible to dieback during the 1990s drought while
C. erythrophloia populations exhibited little stem mortal-
ity (Fensham and Holman 1999). In comparisons among
species that occur in different habitats, site differences in
geology, soil depth and soil type have often been
suggested as factors causing interspecific differences in
dieback (Pook et al. 1967; Fensham and Holman 1999).
Although Fensham and Holman (1999) identified some
differences between canopy and sub-canopy species, there
is a poorer understanding of the causes of species
differences in dieback within a single site (Landsberg
and Wylie 1983). Suggestions that species may differ in
their rooting depth, tolerance of water stress, or suscep-
tibility to cavitation have remained somewhat speculative
in the absence of direct measurements of plant xylem
pressures and cavitation resistance (Auclair 1993). Perhaps
because it is rarely measured, age class differences in
dieback similar to what we found for the ironbarks has
been rarely reported. Pook and Forrester (1984) found that
dieback was generally greater in younger age classes and
they attributed it to higher water stress caused by smaller
root systems in saplings and seedlings. Fensham and
Holman (1999) found that of 21 common overstory
species examined for age class differences in dieback, only
in the E. crebra complex was dieback higher in adult trees;
for the other species there was no significant difference
among age classes. They offered no direct explanation for
this age class difference in populations of the E. crebra
complex and they argued that local patterns of dieback are
probably a complex interaction of local rainfall, soil
characteristics and competition. Although their results
corroborate our findings for lower sapling dieback in
ironbarks, the fact that they found it rarely in their species
survey suggests that this pattern may be the exception
rather than the rule.
Xylem pressure and stem mortality
It has been noted repeatedly that in situ measurements of
water relations of trees undergoing dieback could help to
determine the importance of drought-induced cavitation
relative to other potential causative factors such as insect
herbivores and pathogens (Old et al. 1981; Auclair 1993).
Our measurements of both predawn and midday xylem
pressures provide substantial evidence that differences in
stem mortality between bloodwood and ironbark species
are related to pronounced species differences in water
relations. The ironbarks experienced negative midday
xylem pressures that would seem likely to initiate
significant amounts of stem cavitation. Water stress in
ironbarks was especially pronounced in September 1996
when both midday and predawn xylem pressures at
Hillgrove and Cardigan were consistently more negative
than 4.0 MPa and 5.0 MPa, respectively. Relative
differences between predawn and midday xylem pressure
potentials provide additional evidence for greater water
stress in ironbarks; small relative differences between
predawn and midday values in ironbarks suggest low rates
of diurnal recovery. Significant cavitation resulting from
these very low xylem pressures is supported by our
measures of native embolism that indicate substantial
losses of conductivity in both adult and sapling ironbarks.
The pronounced differences between bloodwoods and
ironbarks in predawn xylem pressures suggest greater soil
water availability for bloodwoods. Use of predawn xylem
potential as an index of soil water potential is based on the
assumption that during the night the plant comes into
equilibrium with the wettest soil water potential
available to a plants root system (Ritchie and Hinckley
1975; Richter 1997). Although there is current controversy
as to the whether the assumption of predawn equilibrium
is always justified (Sellin 1999; Donovan et al. 2001),
nighttime transpiration has not been reported for these
species so the use of these measurements to characterize
general differences in soil moisture availability seems
valid. It seems unlikely that localized habitat differences in
soil moisture are responsible for higher predawn xylem
pressures in bloodwood because we conducted our
measurements in stands that were mixtures of bloodwood
and ironbark individuals. A more likely explanation for
higher moisture availability in bloodwood is a difference
in rooting structure, in particular, rooting depth. Although
we did not excavate root systems of either species, field
observations of exposed roots systems along streams and
road cuts suggested that the root systems in bloodwoods
are characterized by a deep tap-root structure while the
root system in ironbarks are dominated by a series of
shallower, lateral roots. These observations coupled with
our xylem pressure measurements suggest that during
severe droughts the bloodwood tap root system allows
access to water deep in the soil profile and thus reduces
water stress and embolism.
Given the prevailing assumption that drought stress and
resulting cavitation are primary factors underlying dieback
(Auclair 1993), measurements of the water status of trees
undergoing dieback have been surprisingly few. By
comparing predawn and midday xylem pressures, Lands-
berg and Wylie (1983) found trees undergoing dieback had
different diurnal patterns of soil water deficit development.
195
Although there were no differences in predawn xylem
pressures, trees expressing dieback exhibited more nega-
tive midday water potentials than healthy trees. Interest-
ingly, a later study by Landsberg (1985), where she
measured predawn xylem pressure alone, did not demon-
strate a relationship between xylem pressure and proba-
bility of stem mortality during a severe drought in 1983.
She suggested that previous droughts may have induced
changes in root-shoot allocation that buffered trees against
effects of the 1983 drought. To monitor the water status of
woodland eucalypts during a 1965 drought in New South
Wales, Pook (1981) measured the water content of foliage
as an index of leaf water potential. Although not analyzed
statistically, for two species (E. rossii and E. macro-
rhyncha) there was a trend of lower leaf water potential in
trees undergoing dieback. Unfortunately, leaf water po-
tential data for E. polyanthemos, a species that did not
experience significant dieback, were not collected so an
interspecific comparison relating susceptibility to dieback
and water status was not possible.
By the end of the drought in 1997, xylem pressures in
adult ironbarks had recovered from their extremely
negative values of 1996 and were comparable to those
measured in bloodwood sapling and adults. This rapid
recovery underscores the hydraulic resilience of these
species and the potential importance of recovery from
embolism as an adaptation to drought stress (Tyree and
Sperry 1989). Xylem pressures in ironbark saplings were
also much higher than measured in 1996 but they were still
significantly lower than in ironbark adults. A shallower
and less extensive root system in the ironbark saplings
may be responsible for these persistently lower xylem
pressures. By measuring xylem pressures at the end of the
drought we hoped to characterize the water status of the
plants under more normal climatic conditions. Our
measurements after the 1990s drought suggest that greater
water stress relative to adults may be the normal and more
modal condition for ironbark saplings. This suggestion
that drought is a more chronic condition for juveniles is
similar to what has been found previously for other woody
species in dry habitats (Griffin 1973; Pook and Forrester
1984; Sperry and Saliendra 1994).
Cavitation resistance and stem mortality
Analyses of vulnerability curves in bloodwoods and
ironbarks clearly indicate that lower stem mortality in
bloodwoods is not the result of greater resistance to
cavitation. Bloodwood adults and saplings were signifi-
cantly more vulnerable to cavitation than ironbark adults
and saplings. Averaged for adults and saplings, the 50%
loss in conductance points for bloodwoods at Cardigan
and Hillgrove were 1.6 MPa and 1.8 MPa respectively;
the corresponding values for ironbarks were significantly
lower at 2.3 MPa and 2.7 MPa, respectively. Taken
together, the vulnerability curves, xylem pressure data,
relatively low rates of native embolism, and field
observations on rooting depth suggest a drought avoidance
strategy in bloodwood that reduces incidence of dieback in
both saplings and adults. In contrast, ironbarks appear to
employ a drought tolerance strategy with higher resistance
to cavitation and an apparent ability for rapid recovery
from embolism. Similar results were found in a study on
the relationship between cavitation resistance and rooting
depth in Great Basin desert shrubs (Sperry and Hacke
2002). Deep-rooted phreatophytic species experienced less
water stress and were more vulnerable to cavitation while
drought deciduous species had shallower root systems and
exhibited greater resistance to cavitation.
The importance of variation in cavitation resistance in
preventing dieback during the drought is especially
apparent in the comparison of stem mortality between
age classes in ironbark. Lower rates of stem mortality in
ironbark saplings were not due to reduced water stress
because adult and sapling ironbarks experienced similarly
negative predawn and midday xylem pressures. Rather,
significantly higher resistance in ironbark saplings to
cavitation may be the difference between age classes that
reduces dieback during severe drought. The higher rate of
native embolism that we measured in adult ironbarks
relative to saplings provides field evidence of the potential
adaptive importance of increased resistance to cavitation.
Although adult and sapling ironbark xylem pressures did
not differ significantly during the drought, sapling
predawn and midday xylem pressures were more negative
than in adults after the drought ended in 1997. This would
suggest that root systems in saplings are shallower and that
under non-drought conditions saplings experience lower
soil water availability than adults. Higher vulnerability to
drought stress in juvenile plants is often assumed, but there
is little evidence available to determine whether the
increased resistance to cavitation we observed in ironbark
saplings is a general response. Greater cavitation resis-
tance in seedlings was found in Betula occidentalis
(Sperry and Saliendra 1994). No differences were detected
in native xylem pressures between Betula adults and
juveniles but the authors suggested that increased vulner-
ability to drought might select for greater cavitation
resistance in shallow-rooted juveniles. A study on intra-
specific variation in cavitation resistance in live oak
(Quercus wislizenii) found slight differences in resistance
between saplings and adults (Matzner et al. 2001).
Although oak sapling xylem pressures were not measured
in this study, the authors noted that juveniles of the
congener Q. douglasii experience lower predawn xylem
values than adults and suggested that such differences may
also occur in Q. wislizenii.
Higher rates of stem mortality in ironbark adults than in
saplings was unexpected because we assumed that the
larger root system in adults would reduce water stress and
thus rates of cavitation and embolism. If reduced stem
mortality in ironbark saplings results from higher resis-
tance to cavitation, this difference in embolism among
ironbark age classes may be an example of the presumed
trade-off between efficiency of conductance and resistance
to cavitation (Tyree and Sperry 1989; Tyree et al. 1994;
Sperry 1995). A potential example of this trade-off was
196
provided by a study of intraspecific variation in stem death
and cavitation resistance in Populus trichocarpa (Sparks
and Black 1999). Populations from more mesic sites
exhibited poor stomatal control, low resistance to cavita-
tion, and higher rates of stem mortality. The authors
argued that this apparently maladaptive condition might be
explained by a trade-off between cavitation resistance and
maximizing plant conductance. Although data on stomatal
behavior is currently not available for ironbarks, it is
possible that tighter stomatal control in ironbark saplings
may be another mechanism (in addition to changes in
cavitation resistance) that reduces stem mortality in
saplings relative to adults. Additional evidence for this
trade-off comes from a recent comparative study that
examined conduit wall strength and cavitation resistance
across a wide range of conifer and angiosperm species
(Hacke et al. 2001). Wood density and conduit wall
reinforcement were found to be positively related to
cavitation resistance. Reductions in conductivity and
growth rate accompany increases in wood density (Enquist
et al. 1999) and thus indicate a cost to cavitation
resistance.
Under normal climatic conditions in these dry woodland
habitats, ironbark saplings might be expected to produce
xylem more resistant to cavitation because their presum-
ably smaller and shallower root system exposes them to
frequent periods of reduced soil water availability. Several
studies have shown that environmentally induced changes
in cavitation resistance can occur. Particularly relevant to
our study are the results from Alder et al. (1996) who
reported an increase in root cavitation resistance in Acer
grandidentatum individuals at the drier end of a soil
moisture gradient. Other studies have demonstrated that
environmental variation in light levels (Cochard et al.
1999) and nutrient availability (Harvey and van den
Driessche 1997) can also induce changes in cavitation
resistance.
In contrast to saplings, because their more extensive
root system reduces water stress, adult ironbarks would be
expected to produce xylem that is more efficient at
conduction and less resistant to cavitation. If severe
droughts occur with a low enough frequency, this may be a
viable strategy because in most years adults will not
experience xylem pressures negative enough to initiate
significant cavitation. However, in extreme drought years
when both adults and saplings experience similarly
negative xylem pressures, this strategy may result in the
adults being more vulnerable than juveniles to cavitation.
In a sense, the typically more water-limited environment
of juveniles may induce a conservative cavitation resis-
tance strategy that pre-adapts saplings for survival
during extreme drought. These results suggest that a better
understanding of tradeoffs in xylem conduction efficiency
and cavitation resistance might benefit from more detailed
comparisons of adult and juvenile water relations.
Acknowledgements We would like to thank Andrew Ash and
Tony Grice for providing logistic support for this research. We also
acknowledge the helpful comments of Jim Richards, Todd Dawson,
and two anonymous reviewers. K.R. was supported in part by a
Visiting Scientist grant from the Cooperative Research Centre for
the Sustainable Development of Tropical Savannas.
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198
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