Directory UMM :Data Elmu:jurnal:T:Tree Physiology:vol17.1997:

Tree Physiology 17, 241--250
© 1997 Heron Publishing----Victoria, Canada

Geographical variation in water relations, hydraulic architecture and
terpene composition of Aleppo pine seedlings from Italian provenances
ROBERTO TOGNETTI, MARCO MICHELOZZI and ALESSIO GIOVANNELLI
Istituto Miglioramento Genetico delle Piante Forestali, Consiglio Nazionale delle Ricerche, via Atto Vannucci 13, I 50134, Firenze, Italy

Received February 8, 1996

Summary Ecotypic variations in leaf conductance, soil-toleaf hydraulic conductance, components of tissue water potential, hydraulic architecture parameters and xylem embolism
were examined in greenhouse-grown two-year-old Aleppo pine
(Pinus halepensis Mill.) seedlings from six origins representing the geographic range of the species in Italy. Cortical
resin composition of the seedlings was also determined. Measurements were made on well-watered seedlings and on seedlings subjected to recurring severe drought. Drought-stressed
seedlings had lower mean leaf conductances, transpiration
rates and soil-to-leaf hydraulic conductances than well-watered seedlings. They also exhibited more negative osmotic
potentials, higher relative water deficit at incipient plasmolysis,
but a similar maximum modulus of elasticity. Drought-stressed
seedlings showed a higher degree of xylem embolism, a lower
Huber value, lower leaf specific conductivity and lower specific conductivity than well-watered seedlings.
Drought-stressed seedlings of provenances from more xeric

habitats (Tremiti, Porto Pino and Mottola) had greater leaf
conductances, transpiration rates and soil-to-leaf hydraulic
conductances than drought-stressed seedlings of provenances
from more mesic habitats (Imperia, Otricoli and Vico del
Gargano). They also showed higher osmotic adjustment and a
lower degree of xylem embolism. Among provenances, there
were no significant differences in hydraulic architecture parameters in response to the drought treatment; however, Tremiti and Porto Pino seedlings displayed smaller
drought-induced reductions in specific conductivity and leaf
specific conductivity, respectively, than seedlings from other
provenances. These differences suggest that seedlings from
xeric provenances, especially Tremiti, have greater resistance
to desiccation than seedlings from mesic provenances. No
clear association was found between terpene variability and
the other traits investigated, although terpene composition was
related to the geographical distribution of the provenances. We
conclude that the drought-tolerance responses of Tremiti make
it a more suitable provenance than the others for establishment
on sites prone to severe soil water deficits.

Keywords: drought, ecotypic variation, embolism, monoterpene.

Introduction
Aleppo pine (Pinus halepensis Mill.) grows in parts of southern Europe, Asia Minor and northern Africa, adjacent to the
Mediterranean Sea (Mirov 1967). The native range of Aleppo
pine includes a wide range of forest sites throughout the
Mediterranean, especially dry habitats (Nahal 1981). Aleppo
pine populations are often disjunct, resulting in prolonged
isolation and complex geographic patterns of genetic variation
(Schiller et al. 1986).
The species is selected for afforestation because of its high
drought tolerance. The major components of drought resistance, including stomatal response to drought, soil-to-leaf hydraulic conductance, osmotic potential, relative water deficit at
incipient plasmolysis, maximum modulus of elasticity, loss of
hydraulic conductivity and hydraulic architecture, are known
to vary among tree species (Abrams 1988, Braatne et al. 1992,
Cochard 1992, Wang et al. 1992, Jackson et al. 1995). However, there are few data on intraspecific variation in the major
components of drought resistance in woody species (Bongarten and Teskey 1986, Abrams et al. 1990, Shumway et al.
1991, Borghetti et al. 1993), although variation in stem and leaf
morphology, seed physiology, phenological stages and growth
have been reported among Aleppo pine populations raised
from different seed sources (Eccher et al. 1982, Falusi et al.

1983, Calamassi 1986, Weinstein 1989, Schiller and Brunori
1992). We examined several aspects of drought resistance in
Aleppo pine seedlings from six provenances representing the
spectrum of soil water conditions in Italy. Specifically, we
investigated variability in the major components of drought
resistance in well-watered seedlings and in seedlings preconditioned with recurring drought.
Adaption of species to geographic variation in the environment often depends on genetic variation among seed sources.
For example, in loblolly pine, genetic variation is closely
related with the habitat from which plants originate (Bongarten and Teskey 1986). In the present study, we used terpenes
as biochemical markers of genetic variability among provenances to determine if variation in the major components of
drought resistance is associated with genetic variation. Terpenes have been widely used in chemosystematic studies to
characterize species, determine provenances and identify

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TOGNETTI, MICHELOZZI AND GIOVANNELLI

clones, because they are strongly inherited and little influenced
by environmental factors (Baradat and Yazdani 1988, Hanover
1992, Adams et al. 1993, Lang 1994, Baradat et al. 1996).

Terpenes also offer the opportunity to select trees for resistance
to pests or diseases because they are involved in the defense
mechanisms of plants (Michelozzi et al. 1990, Stone and
Bacon 1994, Michelozzi et al. 1995, Raffa and Smalley 1995).

Materials and methods
Plant material and growth conditions
The experiment was conducted on two-year-old seedlings of
Aleppo pine from six geographical origins (Table 1) that were
chosen to represent the natural geographic range of this species
in Italy (Figure 1). In 1991, seeds were collected from mature
trees in natural stands of each provenance (at least 30 trees per
stand were sampled) and sown in a forest nursery at Pisa, Italy,
in March 1992. The following year, seedlings were moved to
the experimental nursery of the Institute of Silviculture, University of Florence, Italy, and transplanted to 2.5-liter plastic
pots filled with a mixture of sandy-loam soil and peat. The
seedlings were watered daily and fertilized at the beginning of
the growing season with Osmocote, a commercial slow-release
fertilizer (18,18,18, N,P,K).
In October 1993, 100 plants (total of all provenances) were

selected for dimensional uniformity (average height and root
collar diameter were 32.25 ± 5.19 cm (SE) and 0.51 ± 0.11 cm,
respectively) and moved to a greenhouse. The day/night temperature in the greenhouse was maintained at 27--30/22-25 °C, but relative humidity and photoperiod were not
regulated. The seedlings were watered every other day, but no
fertilizer was applied in order to simulate the nutrient-poor soil
conditions of Aleppo pine natural forests. After a 5-month
acclimation period in the greenhouse, the seedlings from each
seed source were divided into two groups and the treatments
applied. One group was watered every other day (well-watered
seedlings), whereas the other group was exposed to recurring
cycles of drought by watering only when predawn water potentials reached about −3 MPa (drought-stressed seedlings).
The drought-stressed seedlings had completed six drought
cycles (corresponding roughly to the dry season in the Medi-

Figure 1. The six sampled Italian provenances of Aleppo pine.

terranean climate where Aleppo pine grows) when the measurements were made in June 1994.
Transpiration, leaf conductance and soil-to-leaf hydraulic
conductance
Transpiration (E) and leaf conductance (gs) were measured

under steady-state conditions (high soil water content and
equal evaporative demands). Before measurements, each seedling was watered and placed in the dark for 12 h (until 0800 h).
Eight seedlings from each seed source × drought treatment
combination were randomly sampled. Because photosynthetically active radiation reached a maximum of about 1300 µmol
m −2 s −1 (midday, 1100--1400 h), at least two shoots (upper
canopy) were sampled on each seedling at a time with a
steady-state porometer and a conifer foliage cuvette (LI-1600,
Li-Cor Inc., Lincoln, NE). Precautions were taken to avoid
large differences between external environmental conditions
and those inside the cuvette. Leaf conductance and transpiration were expressed in molar units, taking into account temperature and atmospheric pressure changes due to altitude. We

Table 1. Geographical origin and habitat characteristics of the studied Aleppo pine provenances listed in order of the amount of rainfall.
Seed
source

Latitude
(N)

Longitude
(E)

Altitude1
(m)

Temperature2
(°C)

Rainfall3
(mm)

Soil
type

V. Gargano
Otricoli
Imperia
Mottola
Tremiti
Porto Pino

41° 54′
42° 24′
43° 54′
40° 32′
42° 07′
38° 58′

16° 00′
12° 38′
8° 03′
17° 02′
15° 30′
8° 37′

225
400
150
10
60
5

15.5
13.0
15.0
17.0
17.5
18.0

848
830
750
445
440
430

Brown Soil
Terra Rossa
Rendzina
Sandstone
Terra Rossa

Lithosol

1
2
3

Above sea level.
Mean annual temperature.
Total annual rainfall.

GEOGRAPHICAL VARIATION IN ALEPPO PINE

determined all-sided leaf area as h (2πr + 6r) (Bongarten and
Teskey 1986) for two-needle fascicles, where h = needle length
and r = average fascicle radius.
For each seedling, soil-to-leaf hydraulic conductance (gL)
was estimed as Ohm’s law analogy (assuming predawn water
potential is an estimate of the soil potential) by means of the
following equation (Koide et al. 1989):
g L = E/(Ψ p−Ψx),

(1)

where Ψp = shoot xylem predawn water potential and Ψx =
minimum shoot xylem water potential, both measured with a
pressure chamber (PMS Instruments Co., Corvallis, OR).
Minimum shoot xylem water potential was measured as E
reached its maximum at about midday.
Pressure--volume curves
Components of tissue water potential were measured by the
drying method (Talbot et al. 1975). The apical shoots were
severed from the seedlings under water and allowed to resaturate in a covered container in distilled water for approximately
12 h in the dark. Before taking measurements, the excised
shoots were recut under water above the level to which they
had been submerged during the rehydration period. Then, the
shoots were weighed and immediately placed in a pressure
chamber to determine their initial xylem water potentials. The
shoots were left to desiccate by free transpiration on the laboratory bench at room temperature. The shoots were then periodically reweighed and measured for xylem water potential as
they dried until xylem water potentials reached −5 MPa, well
below the turgor loss point. For each xylem water potential,
two fresh weight measurements were obtained, one immediately preceding and one immediately following the xylem
water potential determination, and averaged. Shoot dry
weights were subsequently determined after drying for 48 h at
70 °C. Pressure--volume data were analyzed as described by
Schulte and Hinckley (1985). Pressure--volume curves defined
the osmotic potential at saturation (Ψπo), the osmotic potential
at incipient plasmolysis (Ψπp), the relative water deficit at
incipient plasmolysis (RWDp) and the maximum modulus of
elasticity (ε max).
Hydraulic architecture
Hydraulic conductivity was measured before and after removing air embolisms as described by Sperry et al. (1988). After
steady-state treatment, the stem of each seedling was cut under
water and then, while still submerged, recut to avoid further
embolism. Both ends of the stem section (5--10 cm long) were
fitted with rubber gaskets and trimmed in distilled water. The
perfusing solution was 10 mM oxalic acid in distilled water
(pH 1.8) to minimize microbial occlusions of xylem vessels.
The perfusing solution was degassed by agitating under vacuum for 60 min, and then introduced into an air-free plastic ball
enclosed in a compressed gas tank. The solution, passing
through a 0.2 µm inline filter (POLYCAP-36AS, Arbor Technologies Inc., Ann Arbor, MI), perfused the samples under a
constant pressure gradient maintained by a pressure regulator.

243

Stopcocks allowed selective influx for measuring the initial
conductivity (K i) on one sample at a time under a pressure
gradient of 9--10 kPa. Maximum conductivity (K m) was determined by pressurizing the solution through all the segments at
150 kPa for 60--90 min. The permeating solution flowed from
the pressurizing reservoir across the samples to a container on
an analytical balance linked to a computer that was programmed to make the calculations. Measurements of hydraulic
conductivity were recorded every 30 s and calculated by averaging ten readings after steady-state had been achieved.
Embolism causing per cent loss of hydraulic conductivity
(K l) was assessed from:
Kl = 100(Km−Ki)/Km .

(2)

Specific hydraulic conductivity (Ks), as a measure of the
porosity of the xylem on a cross-sectional area basis, was
calculated from:
Ks = K i /A w ,

(3)

where Aw is the cross-sectional area of xylem tissue.
Leaf specific hydraulic conductivity (LSC), providing information about the hydraulic efficiency of seedling stems on a
leaf dry weight basis, was derived from:
LSC = K i /D L ,

(4)

where DL is the dry weight of whole foliage fed by the stem.
The Huber value (HV), which provides information about
the investment in stem tissue per distal foliage, was computed
as the conducting cross-sectional area of the stem divided by
the weight of oven-dried leaves:
HV = Aw /D L .

(5)

Terpene composition
One-year-old cortical samples for oleoresin analysis were collected, as described by Squillace (1976), from seedlings growing in an experimental plantation near Florence. The seedlings
were from the same seed lots and of the same age and origin
as the seedlings used for the physiological analyses. The total
number of seedlings sampled was 160, with 25 to 30 seedlings
per provenance. The sampling was carried out on a single day
in autumn 1994. Samples were taken from the same position
on each plant. Samples of approximately 1 g fresh weight per
tree were shredded and placed in glass vials, sealed with Teflon
septums and crimped with aluminum caps. The vials were
stored at −20 °C until analyzed. The cortex of each seedling
was sampled and analyzed by gas chromatography with a
Perkin-Elmer 8500 gas chromatograph (Perkin-Elmer Co.,
Norwalk, CO). The gas chromatograph was equipped with a
flame ionization detector and a Perkin-Elmer HS-101 automatic headspace sampler, and fitted with a 30-m-long and 0.25mm-diameter (i.d.) fused silica capillary column coated with
DB-WAX (J & W Scientific, Folson, CA). Samples were
conditioned for 60 min at 50 °C and analyzed with helium as

244

TOGNETTI, MICHELOZZI AND GIOVANNELLI

the carrier gas at a flow rate of 1 ml min −1, an injector temperature of 130 °C and a detector temperature of 230 °C. The
column oven was maintained at 50 °C isothermal for 3 min
after injection and then increased in 3 °C increments to 170 °C,
which were held constant for 5 min. Terpenes were identified
by comparison of their retention times with those of standards
under the same conditions.
Statistical analysis
Data were subjected to analysis of variance and Duncan’s
multiple range test with P < 0.05, using individual seedlings as
observations.
Ten monoterpenes and one sesquiterpene (β-caryophyllene)
were present in sufficient quantities to be considered in the
statistical analysis. The amount of each monoterpene was
expressed as a percentage of total monoterpenes, whereas the
β-caryophyllene concentration was expressed as a percentage
of total terpenes. Percentages of various components were
transformed to arcsin-square root functions on the plot mean
basis to fulfil the normality assumption. The transformed plot
means were used for analysis of variance and discriminant
function analysis.

Table 2. Leaf transpiration rate (E), leaf conductance (gs) and soil-toleaf hydraulic conductance (gL) for well-watered and drought-stressed
seedlings of Aleppo pine. Means ± SE (n = 8; at least two shoots per
plant were sampled concurrently). Statistically significant seed source
differences (P < 0.05) within a treatment are indicated by different
letters. Within seed sources, the difference between treatments is
significant in all cases (P < 0.05).
Seed
source

E
gs
(mmol m −2 s −1) (mol m −2 s −1)

Well-watered treatment
V. Gargano
5.06 ± 0.30 a
Otricoli
4.66 ± 0.33 a
Imperia
4.67 ± 0.37 a
Mottola
4.83 ± 0.31 a
Tremiti
5.06 ± 0.54 a
Porto Pino
4.97 ± 0.19 a
Means

4.88 ± 0.15

Drought treatment
V. Gargano
1.42 ± 0.21 a
Otricoli
0.96 ± 0.28 a
Imperia
1.20 ± 0.27 a
Mottola
1.75 ± 0.35 ab
Tremiti
1.67 ± 0.23 ab
Porto Pino
2.43 ± 0.51 b
Means

1.57 ± 0.13

gL (mmol m −2
s −1 MPa −1)

0.29 ± 0.03 a
0.22 ± 0.02 a
0.26 ± 0.03 a
0.26 ± 0.03 a
0.28 ± 0.02 a
0.27 ± 0.02 a

3.76 ± 0.13 a
4.07 ± 0.40 a
3.82 ± 0.29 a
4.02 ± 0.38 a
4.07 ± 0.33 a
3.75 ± 0.21 a

0.27 ± 0.01

3.91 ± 0.12

0.12 ± 0.01 a
0.09 ± 0.01 a
0.09 ± 0.01 a
0.15 ± 0.02 ab
0.14 ± 0.01 ab
0.21 ± 0.02 b

2.11 ± 0.28 b
1.13 ± 0.18 a
1.76 ± 0.26 ab
1.89 ± 0.19 ab
2.59 ± 0.38 b
2.63 ± 0.37 b

0.14 ± 0.00

2.01 ± 0.12

Results
Transpiration, leaf conductance and soil-to-leaf hydraulic
conductance
Taking all provenances together, values of E and gs were more
than twice as large for well-watered seedlings (4.88 and 0.27
mol m −2 s −1, respectively) as for drought-stressed seedlings
(1.57 and 0.06 mol m −2 s −1, respectively) (P < 0.05) (Table 2).
There were also significant differences in E and gs between
drought-stressed seedlings and well-watered seedlings of the
same seed origin. Seed source differences in E and gs were not
significant among well-watered seedlings. Among droughtstressed seedlings, those of xeric origins (Tremiti, Mottola and
Porto Pino) displayed higher E and gs than seedlings from
mesic origins (Imperia, Otricoli and Vico del Gargano).
Among the xeric provenances, seedlings originating from the
southernmost provenance, Porto Pino, showed the smallest
drought-induced reductions in E and gs.
For all provenances combined, well-watered seedlings had
significantly greater gL than drought-stressed seedlings (3.91
versus 2.01 mmol m −2 s −1 MPa −1) (P < 0.05) (Table 2) as a
result of lower E in the drought-stressed seedlings. There were
also significant differences in gL between drought-stressed
seedlings and well-watered seedlings of the same seed origin.
Water potential gradients were similar in seedlings of both
treatments because xylem water potentials were lower in
drought-stressed seedlings than in well-watered seedlings. Although seed source differences in gL were not significant
among the well-watered seedlings, differences were detected
among seed sources in the drought treatment. Among provenances, seedlings of the Porto Pino provenance showed the
smallest drought-induced reductions in gL.

Pressure--volume curves
For all provenances combined, drought-stressed seedlings differed significantly (P < 0.05) from well-watered seedlings in
Ψπp (−2.33 versus −2.51 MPa) and RWDp (25 versus 28%)
(Table 3), whereas treatment differences in Ψπo were small
(P = 0.05) (−1.66 versus −1.74 MPa), and there were no significant treatment effects on ε max (14.56 versus 14.70 MPa).
Provenance differences in the measured parameters were
detected in both well-watered and drought-stressed seedlings
(Table 3). Among provenances, seedlings from the interior and
mesic seed source Otricoli showed the highest Ψπo, Ψπp and
ε max and the lowest RWDp. No differences in Ψπp were found
between well-watered and drought-treated seedlings from the
Otricoli and Mottola seed sources, and no differences in RWDp
were detected between well-watered and drought-stressed
seedlings from the Otricoli, Tremiti and Mottola seed sources.
However, none of these traits showed a clear geographic pattern, although the insular and xeric provenances (Tremiti and
Porto Pino) displayed an opposite tendency from the mesic
seed sources (Imperia, Otricoli and Vico del Gargano). Among
provenances, drought-stressed seedlings of the Tremiti provenance displayed the greatest osmotic adjustment at saturation
(0.15 MPa). The treatments affected Ψπo and ε max of seedlings
from each provenance similarly.
Hydraulic architecture
For all provenances combined, well-watered seedlings differed
significantly (P < 0.05) from drought-stressed seedlings in Ks
(37.24 × 10 −4 versus 12.76 × 10 −4 kg m −1 MPa −1 s −1), LSC

GEOGRAPHICAL VARIATION IN ALEPPO PINE

245

Table 3. Shoot tissue water relations for well-watered and drought-stressed seedlings of Aleppo pine. Means ± SE (n = 8). Statistically significant
seed source differences (P < 0.05) within a treatment are indicated by different letters. Significant differences between treatments are indicated by
asterisks: * = P = 0.05; ** = P < 0.05.
Seed
source

Ψπο1
(MPa)

Ψπp2
(MPa)

RWDp3
(%)

εmax4
(MPa)

Well-watered treatment
V. Gargano
Otricoli
Imperia
Mottola
Tremiti
Porto Pino

−1.63 ± 0.04 a
−1.46 ± 0.04 c
−1.69 ± 0.04 ab
−1.66 ± 0.03 ab
−1.78 ± 0.04 b
−1.76 ± 0.05 b

−2.30 ± 0.05 a**
−2.02 ± 0.08 c
−2.35 ± 0.05 ab**
−2.29 ± 0.07 a
−2.55 ± 0.08 b**
−2.45 ± 0.09 ab**

24.7 ± 0.5 a**
21.5 ± 0.7 b
24.4 ± 1.0 a**
25.3 ± 0.7 ac
27.1 ± 0.8 c
25.2 ± 0.5 ac**

14.71 ± 0.57 a
17.18 ± 0.33 b
14.04 ± 0.65 a
14.44 ± 0.46 a
13.11 ± 0.37 a
13.90 ± 1.12 a

Means

−1.66 ± 0.02*

−2.33 ± 0.03**

24.7 ± 0.3**

14.56 ± 0.26

Drought treatment
V. Gargano
Otricoli
Imperia
Mottola
Tremiti
Porto Pino

−1.71 ± 0.04 a
−1.52 ± 0.05 b
−1.73 ± 0.05 a
−1.72 ± 0.07 a
−1.93 ± 0.07 c
−1.85 ± 0.05 ac

−2.52 ± 0.07 a**
−2.12 ± 0.04 b
−2.53 ± 0.05 a**
−2.44 ± 0.04 a
−2.75 ± 0.07 c**
−2.70 ± 0.05 c**

27.8 ± 0.9 a**
23.1 ± 1.1 c
28.8 ± 0.2 ab**
27.4 ± 1.0 a
31.7 ± 1.1 b
29.3 ± 0.8 ab**

14.71 ± 0.86 a
17.57 ± 0.71 b
14.50 ± 0.81 a
14.35 ± 0.85 a
12.92 ± 1.16 a
14.12 ± 0.61 a

Means

−1.74 ± 0.02*

−2.51 ± 0.02**

28.0 ± 0.4**

14.70 ± 0.70

1
2
3
4

Ψπο = osmotic potential at saturation.
Ψπp = osmotic potential at incipient plasmolysis.
RWDp = relative water deficit at incipient plasmolysis.
ε max = maximum modulus of elasticity.

(11.54 × 10 −4 versus 2.87 × 10 −4 kg m −1 MPa −1 s −1), HV
(32.30 × 10 −4 versus 22.66 × 10 −4 m2 kg −1) and Kl (8.32
versus 55.21%) (Table 4).
No seed source differences were detected among seedlings
in either treatment for Ks and LSC (Table 4), although Otricoli
seedlings usually had the lowest Ks and LSC values, and the
Tremiti and Porto Pino seedlings displayed smaller droughtinduced reductions in specific conductivity and leaf specific
conductivity, respectively, than seedlings from other provenances. Seed source differences in HV were present only in
well-watered trees, whereas provenance differences in Kl were
detected only in drought-stressed seedlings. Among provenances, seedlings from insular and xeric seed sources (Tremiti
and Porto Pino) were the least embolized, whereas seedlings
from internal and mesic seed source (Otricoli) were the most
embolized.
Monoterpene composition
Among the terpenes, α-pinene (40.70%), β-myrcene (31.04%)
and ∆-3-carene (19.70%) were the major constituents, whereas
β-pinene, an unknown compound and β-caryophyllene were
minor constituents, respectively with 4.10, 1.92 and 1.46%
(Table 5). None of the other components detected represented
more than 1% of the total terpene fraction of cortical oleoresin.
There were highly significant differences among the provenances for all of the compounds (Table 6). Among provenances, seedlings of the southernmost provenances (Tremiti,
Vico del Gargano, Mottola and Porto Pino) contained higher
proportions of α-pinene, limonene and β-caryophyllene,

whereas a large number of seedlings from the Imperia and
Otricoli provenances had high amounts of β-myrcene.
Duncan’s test indicated clear discrimination among provenances for many compounds (Table 7). The positions of the six
seed sources on the plane of the first two canonical axes
suggest four groupings, corresponding to the pooled southeastern provenances (Tremiti, Vico del Gargano and Mottola) and
the other individually separated provenances (Figure 2).

Discussion
Regardless of origin, seedlings repeatedly exposed to drought
had lower leaf conductances and rates of transpiration than
well-watered seedlings. Because all measurements were recorded under steady-state conditions of high xylem pressure
potential, the differences in E and gs (and in components of
water potential and hydraulic architecture parameters) between well-watered and drought-stressed seedlings reflect
physiological or morphological responses to soil water availability during the drought treatment, rather than subsequently
when measurements were made (Seiler and Johnson 1985,
Bongarten and Teskey 1986, Teskey et al. 1987). Reduced
stomatal aperture in response to drought is consistent with the
hypothesis that complete stomatal closure is not the optimal
response to drought and that limited embolism allows a maximization of gas exchange (Jones and Sutherland 1991).
Differences in transpiration rates among drought-stressed
seedlings from the various provenances provide evidence that,
in Aleppo pine, drought resistance increased from mesic to

246

TOGNETTI, MICHELOZZI AND GIOVANNELLI

Table 4. Stem hydraulic architecture and loss of hydraulic conductivity for well-watered and drought-stressed seedlings of Aleppo pine. Means ±
SE (n = 8). Statistically significant seed source differences (P < 0.05) within treatments are indicated by different letters. An asterisk indicates
significant differences (P < 0.05) between well-watered and drought treatment means.
Seed
source

Specific conductivity
(Ks)
(10 −4 kg m −1 MPa −1 s −1)

Leaf specific
conductivity (LSC)
(10 −4 m MPa −1 s −1)

Huber
value
(10 −4 m2 kg −1)

Loss of hydraulic
conductivity
(Kl) (%)

Well-watered treatment
V. Gargano
Otricoli
Imperia
Mottola
Tremiti
Porto Pino

45.97 ± 3.27 a*
34.40 ± 7.81 a*
48.49 ± 4.69 a*
36.84 ± 5.02 a*
31.19 ± 10.99 a
27.46 ± 7.28 a

11.24 ± 1.75 a*
9.49 ± 1.67 a*
15.35 ± 2.11 a*
13.50 ± 1.43 a*
13.43 ± 5.77 a
6.21 ± 1.07 a

24.63 ± 2.41 a
28.96 ± 1.60 a*
31.62 ± 2.56 ab*
38.78 ± 6.43 ab
44.36 ± 7.79 b*
25.44 ± 4.06 a

8.08 ± 0.81 a*
8.83 ± 0.43 a*
8.78 ± 0.68 a*
7.84 ± 0.71 a*
7.63 ± 0.97 a*
8.74 ± 0.73 a*

Means

37.24 ± 2.94*

11.54 ± 1.18*

32.30 ± 2.20*

8.32 ± 0.28*

Drought treatment
V. Gargano
Otricoli
Imperia
Mottola
Tremiti
Porto Pino

14.10 ± 6.65 a*
6.83 ± 3.91 a*
12.29 ± 4.99 a*
11.12 ± 6.47 a*
19.98 ± 7.11 a
12.25 ± 5.69 a

4.33 ± 2.05 a*
1.50 ± 0.90 a*
2.89 ± 1.23 a*
2.14 ± 1.23 a*
4.06 ± 1.35 a
2.32 ± 1.02 a

28.17 ± 3.46 a
21.63 ± 1.58 a*
22.85 ± 1.53 a*
23.21 ± 5.44 a
21.31 ± 4.39 a*
18.78 ± 2.01 a

56.08 ± 0.76 ac*
63.56 ± 2.98 b*
58.23 ± 1.47 ab*
54.91 ± 3.39 ac*
49.22 ± 0.92 c*
49.42 ± 3.18 c*

Means

12.76 ± 2.41*

2.87 ± 0.55*

22.66 ± 1.39*

55.21 ± 0.97*

Table 5. Average terpene composition (%) of cortical oleoresin from seedlings of different Aleppo pine provenances. The amount of each
monoterpene is expressed as a percentage of total monoterpenes, whereas the β-caryophyllene concentration is expressed as a percentage of total
terpenes.
Seed source α-Pinene1 Camphene β-Pinene Sabinene ∆-3-Carene β-Myrcene Limonene Cineole γ-Terpinene Unknown β-Caryophyllene
V. Gargano
Otricoli
Imperia
Mottola
Tremiti
Porto Pino

50.67
30.52
36.17
42.62
46.36
37.20

0.71
0.49
0.40
0.82
0.42
0.83

4.12
4.14
3.86
4.16
4.01
4.25

0.45
0.30
0.24
0.44
0.29
0.23

24.74
18.65
21.34
20.87
18.10
17.53

15.07
42.22
35.09
27.55
27.86
35.91

1.30
0.37
0.29
0.67
0.43
1.32

0.45
0.99
0.25
0.53
0.45
0.51

0.27
0.31
0.15
0.31
0.16
0.32

2.09
1.93
1.89
1.95
1.81
1.86

2.05
1.23
0.90
1.79
1.55
1.28

Means

40.70

0.60

4.10

0.32

19.70

31.04

0.72

0.55

0.26

1.92

1.46

1

Compounds are listed in order of elution.

Table 6. Results of analyses of variance (F tests) for transformed relative proportions of terpene in seedlings of different Aleppo pine provenances.
Source of
variation

α-Pinene Camphene β-Pinene Sabinene ∆-3-Carene β-Myrcene Limonene Cineole γ-Terpinene Unknown β-Caryophyllene

Among
563.171
provenances
Within
provenances
1

39.89

11.081

0.911

6.661

89.991

1.16

0.12

1.65

9.15

1149.801
71.35

23.671

25.021

5.081

1.05

22.041

6.89

0.58

1.55

0.25

1.72

Significant at P < 0.01.

xeric sites of origin. Drought-stressed seedlings of provenances originating from regions of severe summer drought
(Tremiti, Mottola and Porto Pino) had higher leaf conductances and transpiration rates than seedlings originating from
seed sources from wetter locations (Imperia, Otricoli and Vico

del Gargano), indicating that seedlings of xeric provenances
may be better able to adjust their osmotic potentials. Among
provenances, seedlings of the Porto Pino provenance showed
the smallest drought-induced reductions in leaf conductance
and transpiration rate. Because of the threshold-type relation-

GEOGRAPHICAL VARIATION IN ALEPPO PINE

247

Table 7. Terpenes differing significantly (P < 0.05 ) in content between pairs of Aleppo pine provenances according to Duncan’s test.
Provenance

Imperia

Porto Pino

Mottola

Tremiti

V. Gargano

Otricoli

β-pinene
∆-3-carene
cineole
γ-terpinene
β-caryophyllene

α-pinene
camphene
limonene
cineole

α-pinene
camphene
cineole
β-caryophyllene

α-pinene
β-myrcene
cineole
γ-terpinene
β-caryophyllene

α-pinene
camphene
∆-3-carene
β-myrcene
limonene
cineole
γ-terpinene
unknown
β-caryophyllene

camphene
β-pinene
∆-3-carene
limonene
cineole
γ-terpinene

α-pinene
camphene
β-pinene
sabinene
cineole
γ-terpinene

α-pinene
β-pinene
∆-3-carene
cineole

α-pinene
camphene
β-pinene
sabinene
∆-3-carene
β-myrcene
limonene
cineole
γ-terpinene
unknown
β-caryophyllene

sabinene
∆-3-carene
β-myrcene
β-caryophyllene

α-pinene
camphene
β-pinene
sabinene
γ-terpinene

α-pinene
sabinene
∆-3-carene
β-myrcene
unknown
β-caryophyllene

camphene
∆-3-carene
γ-terpinene

∆-3-carene
β-myrcene
unknown

Imperia

Porto Pino

Mottola

Tremiti

ship between leaf conductance and net photosynthesis in conifers (Teskey et al. 1986), photosynthetic capacity may be
sacrificed as a result of reduced leaf conductance particularly
in mesic seed sources. However, the well-watered seedlings
did not show any geographical discrimination attributable to
climate.
The soil-to-leaf hydraulic conductance measurements
showed that, following recovery from drought, droughtstressed seedlings had lower rates of water movement from
roots to leaves than well-watered seedlings. In whole or in part,
this difference must reflect the observed difference between
the treatments in leaf conductance. The reduction in leaf conductance caused by drought-stress may have been caused by
cavitation in water conducting tracheids leading to a decrease
in hydraulic conductance of roots, stem or leaves (Sperry and
Tyree 1988). Among provenances, the greatest reduction in

camphene
∆-3-carene
β-myrcene
limonene
γ-terpinene
unknown
β-caryophyllene

soil-to-leaf hydraulic conductance caused by drought stress
was in Otricoli seedlings.
Although the drought treatment had little effect on osmotic
potential at saturation, drought-stressed seedlings had lower
osmotic potentials and relative water deficits at incipient plasmolysis than well-watered seedlings (cf. Seiler and Johnson
1985, Bongarten and Teskey 1986), indicating that recurring
droughts resulted in a persistent alteration of the osmotic
potential of Aleppo pine seedlings. Well-watered seedlings had
low osmotic potentials, indicating that Aleppo pine seedlings
have intrinsically low osmotic potentials. Although osmotic
potentials declined in drought-stressed seedlings, elastic
modulus remained constant. Similar behavior has been reported in other conifers, e.g., Tsuga heterophylla (Raf.) Sarg.
by Kandico et al. (1980). Because stomatal activity is closely
related to turgor maintenance, turgor and turgor-related proc-

248

TOGNETTI, MICHELOZZI AND GIOVANNELLI

Figure 2. Scatter diagram of Aleppo pine provenance centroids in the
plane of the first two canonical functions.

esses may be maintained at lower shoot xylem water potentials
in drought-stressed Aleppo pine seedlings than in well-watered
seedlings as a result of decreased osmotic potentials (Kramer
1983).
It is unclear whether osmotic adjustment delays stomatal
closure during drought (Abrams 1988). Among provenances,
drought-stressed Otricoli seedlings had the highest osmotic
potentials and the lowest leaf conductances and rates of transpiration, suggesting that gas exchange may be partially limited by a lack of osmotic adjustment. On the other hand, each
provenance may have an inherent relative gas exchange capacity under drought conditions. Of the provenances studied,
Tremiti, and to a lesser extent Porto Pino, seedlings displayed
the greatest degree of drought tolerance, as evidenced by
greater osmotic adjustment at saturation (0.15 MPa).
Relative water deficits at incipient plasmolysis differed
among the provenances. In drought-stressed seedlings of
mesic or xeric genotypes, higher or lower values of osmotic
potential and maximum modulus of elasticity contributed to a
lower or higher relative water deficit at incipient plasmolysis,
respectively. In severely drought-stressed seedlings of Otricoli
provenance, inelastic cell walls might increase water extraction from dry soil by producing a steeper water potential
gradient within the plant (Hinckley et al. 1983, Meinzer et al.
1986). If the low relative water deficit at incipient plasmolysis
indicates a greater sensitivity to tissue desiccation in seedlings
of the Otricoli provenance than in more xeric provenances,
then a high modulus of elasticity might help these plants
maintain a high leaf water content.
Seedlings responded to drought by producing less xylem
tissue in the stem as indicated by decreases in Huber value, leaf
specific conductivity and specific conductivity. However, in
the most xeric Tremiti and Porto Pino provenances, the drought
treatment did not significantly decrease specific conductivity
and leaf specific conductivity, respectively, suggesting that

high hydraulic permeability and efficiency are associated with
resistance to cavitation, because seedlings of these two provenances were less embolized than seedlings of the other provenances. In contrast, Cochard (1992) found that Cedrus
atlantica (Endl.) Carr. had a high permeability but a low
vulnerability to xylem embolism.
Drought caused a marked reduction in Huber values of
Tremiti seedlings, perhaps indicating a drought-induced increase in allocation of biomass to leaves and roots. Trees from
xeric environments often allocate a larger portion of dry matter
to roots than trees from mesic environments. Cuccui et al.
(1996), who studied 1-year-old seedlings from the same provenances, found that Porto Pino seedlings had the lowest height
increments and height/diameter ratios and that Otricoli seedlings had the highest height increments and height/diameter
ratios and also the largest root collar diameters. We found that
drought increased Huber values of Vico del Gargano seedlings.
Huber values may be positively related to leaf specific conductivity, because both parameters are related to the amount of
foliage sustained by the stem.
Drought-stressed seedlings showed a more than 50% loss of
hydraulic conductivity and negligible nocturnal refilling (Borghetti et al. 1989, Jackson et al. 1995). This high loss may be
explained by the combined effects of recurring drought and
high concentrations of dissolved carbon dioxide in the xylem
sap, because measurements were made during the growth
period when the transpiration stream is especially prone to
cavitation (Peña and Grace 1986). Recurring drought may also
have caused irreversible sealing of bordered pits (Sperry and
Tyree 1990). Conifers have been found to refill tracheids
within a few days after rewatering in several studies, but not in
others (Peña and Grace 1986, Borghetti et al. 1991, Sobrado et
al. 1992, Jackson et al. 1995). Sperry and Tyree (1990) suggest
that conifers lack the ability to refill cavitated tracheids because they cannot generate a positive xylem pressure. Wellwatered seedlings showed a low percentage loss of hydraulic
conductivity in the range of native and structural embolisms
(Tyree and Ewers 1991), with no differences among genotypes. Differences in percent loss of hydraulic conductivity
among drought-stressed seedlings were consistent with climatic differences among seed sources and with the pattern of
reductions in transpiration rates. Variations in stem diameters,
tracheid sizes and pit membrane flexibility, which are known
to vary along geographical gradients, could account for the
genotype differences (Tyree et al. 1984, Sperry and Tyree
1990, Cochard 1992, Borghetti et al. 1993, Jackson et al.
1995). For example, the lower growth rate of seedlings of xeric
seed sources may have permitted a relatively higher flexibility
of the margo’s strands (Cochard 1992).
There was no clear relationship between terpene variability
and the other traits investigated; however, a weak correlation
was found between terpene variability and physiological parameters of seedlings originating from seed sources from xeric
habitats. The proportions of α-pinene, β-myrcene, limonene
and the sesquiterpene β-caryophyllene showed a tendency for
clinal patterns with the geographical distribution of the provenances. This trend was less evident when climate rather than

GEOGRAPHICAL VARIATION IN ALEPPO PINE

latitude of origin was considered. Adaption to local environmental conditions might be important in determining provenance genetic structure, and the observed variation in our study
material could be interpreted as ecotypic variation. However,
a significant role of geographical isolation in influencing the
observed pattern of genetic variation cannot be ruled out.
Discriminant analysis confirmed that southeastern seed
sources (Tremiti, Vico del Gargano and Mottola) are closely
related, whereas the other seed sources are distinct from each
other (cf. Schiller et al. 1986, Baradat et al. 1989, Baradat et
al. 1996). Seedlings of the southeastern provenances (Tremiti,
Vico del Gargano and Mottola) had lower amounts of β-myrcene and larger amounts of limonene than seedlings of the
nothern provenances (Imperia and Otricoli), whereas seedlings
of the Porto Pino provenance had higher amounts of both
monoterpenes. In Aleppo pine, both of these monoterpenes are
associated with susceptibility to attack by Matsucoccus
josephi (Bodenh.) Harpaz (Homoptera: Matsucoccidae)
(Schiller and Grunwald 1987, Mendel and Schiller 1993). The
provenances with lower amounts of β-myrcene and higher
amounts of limonene have reduced susceptibility to the pest
(Schiller and Grunwald 1987). However, Schiller and Grunwald (1987) found that other terpenes, which were not detected
in the trees we sampled, are also related to increased injury by
this phytophagous insect.
In conclusion, although we found geographic variations in
Aleppo pine seedlings along a latitudinal pattern, as revealed
by terpene markers, seed source differences in the examined
physiological traits were minor compared to the effects of the
drought treatment. Many of the drought-induced physiological
differences were consistent with the geographic location of the
seed sources, particularly when seedlings from Otricoli (mesic
extreme of the species’ range in Italy) were compared with
seedings from Tremiti and Porto Pino (xeric extremes of the
species’ range in Italy). These drought-induced traits may
result in greater resistance to desiccation in seedlings of xeric
provenances than in seedlings of mesic provenances.

Acknowledgments
We thank C. Boggi for her kind assistance in the laboratory. We are
indebted to A. Tani, A. Maltoni and A. Pierguidi (Institute of Silviculture, University of Florence, Italy) for assisting in seedling establishment and maintenance, and for encouraging the research. We also
thank A.E. Squillace and J.D. Johnson (School of Forest Resources
and Conservation, University of Florida, USA) for helpful discussion
and comments on the manuscript.

References
Abrams, M.D. 1988. Sources of variation in osmotic potentials with
special reference to North American tree species. For. Sci. 34:1030-1046.
Abrams, M.D., M.E. Kubiske and K.C. Steiner. 1990. Drought adaptations and responses in five genotypes of Fraxinus pennsylvanica
Marsh.: photosynthesis, water relations and leaf morphology. Tree
Physiol. 6:305--315.

249

Adams, R.P., T. Demeke and H.A. Abulfatith. 1993. RAPD DNA
fingerprints and terpenoids: clues to past migrations of Juniperus in
Arabia and east Africa. Theor. Appl. Genet. 87:22--26.
Baradat, Ph. and R. Yazdani. 1988. Genetic expression for monoterpenes in clones of Pinus sylvestris grown on different sites. Scand.
J. For. Res. 3:25--36.
Baradat, Ph., M. Michelozzi and M. Lambardi. 1989. Terpene composition in four Italian provenances of Aleppo pine (Pinus halepensis
Mill.). J. Genet. Breed. 43:195--200.
Baradat, Ph., M. Michelozzi, R. Tognetti, M.L. Khouja and A. Khaldi.
1996. Geographical variation of Pinus halepensis Mill. In Population Genetics and Genetic Conservation of Forest Trees. Eds. Ph.
Baradat, W.T. Adams and G. Müller-Starck. SPB Academic Publishing, Amsterdam, pp 141--158.
Bongarten, B.C. and R.O. Teskey. 1986. Water relations of loblolly
pine seedlings from diverse geographic origins. Tree Physiol.
1:265--276.
Borghetti, M., A. Raschi and J. Grace. 1989. Ultrasound emission after
cycles of water stress in Picea abies. Tree Physiol. 5:229--237.
Borghetti, M., W.R.N. Edwards, J. Grace, P.J. Jarvis and A. Raschi.
1991. The refilling of embolised xylem in Pinus sylvestris L. Plant
Cell Environ. 14:357--369.
Borghetti, M., S. Leonardi, A. Raschi, D. Snyderman and R. Tognetti.
1993. Ecotypic variation of xylem embolism, phenological traits,
growth parameters and allozyme characteristics in Fagus sylvatica.
Funct. Ecol. 7:713--720.
Braatne, J.H., T.M. Hinckley and R.F. Stettler. 1992. Influence of soil
water on the physiological and morphological components of plant
water balance in Populus trichocarpa, Populus deltoides and their
F1 hybrids. Tree Physiol. 11:325--339.
Calamassi, R. 1986. Characterisation de quelques provenances de
Pinus halepensis sur la base de la structure anatomique et morphologique des aguilles. Ann. Sci. For. 43:281--289.
Cochard, H. 1992. Vulnerability of several conifers to air embolism.
Tree Physiol. 11:73--83.
Cuccui, I., A. Maltoni and A. Tani. 1996. Indagini su semi e semenzali
di provenienze Italiane di Pinus halepensis Mill. Monti e Boschi.
5:55--62.
Eccher, A., E. Fusaro and F. Righi. 1982. Primi risultati di prove a
dimora sui pini Mediterranei della ‘‘sezione halepensis,’’ con particolare riferimento a Pinus eldarica Medw. Cellulosa e Carta 33:3-30.
Falusi, M., R. Calamassi and A. Tocci. 1983. Sensitivity of seed
germination and seedling root growth to moisture stress in four
provenances of Pinus halepensis Mill. Silvae Genet. 32:4--9.
Hanover, J.W. 1992. Applications of terpene analysis in forest genetics. New For. 6:159--178.
Hinckley, T.M., F. Duhme, A.R. Hinckley and H. Richter. 1983.
Drought relations of shrub species: assessment of the mechanisms
of drought resistance. Oecologia 59:344--350.
Jackson, G.E., J. Irvine and J. Grace. 1995. Xylem cavitation in Scots
pine and Sitka spruce saplings during water stress. Tree Physiol.
15:783--790.
Jones, H.G. and R.A. Sutherland. 1991. Stomatal control of xylem
embolism. Plant Cell Environ. 14:607--612.
Kandico, R.A., T. Timmis and J. Warral. 1980. Pressure--volume
curves of shoots and roots of normal and drought conditioned
western hemlock seedlings. Can. J. For. Res. 10:10--16.
Koide, T.R., R.H. Robichaux, S.R. Morse and L.M. Smith. 1989. Plant
water status, hydraulic resistance and capacitance. In Plant Physiological Ecology. Eds. R.W. Pearcy, J. Ehrlinger, H.A. Mooney and
P.W. Rundel. Chapman and Hall, London, pp 161--183.

250

TOGNETTI, MICHELOZZI AND GIOVANNELLI

Kramer, R.J. 1983. Water Relations of Plants. Academic Press, New
York, 489 p.
Lang, K.J. 1994. Abies alba Mill.: differentiation of provenances and
provenance groups by the monoterpene patterns in the cortex resin
of twigs. Biochem. System. Ecol. 22:53--63.
Meinzer, F., P.W. Rundel, M.R. Sharifi and E.T. Nilson. 1986. Turgor
and osmotic relations of the desert shrub Larrea tridentata. Plant
Cell Environ. 9:467--475.
Mendel, Z. and G. Schiller. 1993. Biogeography of Matsucoccus
josephi Bodenheimer et Harpaz in Crete and mainland Greece. Ann.
Sci. For. 50:383--388.
Michelozzi, M., A.E. Squillace and T.L. White. 1990. Monoterpene
composition and fusiform rust resistance in slash pine. For. Sci.
36:470--475.
Michelozzi, M., T.L. White, A.E. Squillace and W.J. Lowe. 1995.
Monoterpene composition and fusiform rust resistance in slash and
loblolly pines. Can. J. For. Res. 25:193--197.
Mirov, N.T. 1967. The genus Pinus. Ronald Press, New York, 602 p.
Nahal, I. 1981. The Mediterranean climate from a biological viewpoint. In Ecosystems of the World. Ed. F. Di Castri. Elsevier,
Amsterdam, pp 63--86.
Peña, J. and J. Grace. 1986. Water relations and ultrasound emissions
of Pinus sylvestris before, during and after a period of water stress.
New Phytol. 103:515--524.
Raffa, K.F. and E.B. Smalley. 1995. Interaction of pre-attack and
induced monoterpene concentrations in host conifer defense against
bark beetle-fungal complexes. Oecologia 102:285--295.
Schiller, G. and C. Grunwald. 1987. Resin monoterpene in range wide
provenance trials of Pinus halepensis Mill. in Israel. Silvae Genet.
36:109--114.
Schiller, G. and A. Brunori. 1992. Aleppo pine (Pinus halepensis
Mill.) in Umbria (Italy) and its relation to native Israeli populations.
Isr. J. Bot. 41:123--127.
Schiller, G., M.T. Conkle and C. Grunwald. 1986. Local differentiation among Mediterranean populations of Aleppo pine in their
isoenzymes. Silvae Genet. 35:11--19.
Schulte, P.J. and T.M. Hinckley. 1985. A comparison of pressure--volume curve data analysis techniques. J. Exp. Bot. 36:1590--1602.
Seiler, J.R. and J.D. Johnson. 1985. Photosynthesis and transpiration
of loblolly pine seedlings as influenced by moisture-stress conditioning. For. Sci. 31:742--749.

Shumway, D.L., K.C. Steiner and M.D. Abrams. 1991. Effects of
drought stress on hydraulic architecture of seedlings from five
populations of green ash. Can. J. Bot. 69:2158--2164.
Sobrado, M.A., J. Grace and P.G. Jarvis. 1992. The limits of xylem
embolism recovery in Pinus sylvestris L. Plant Cell Environ.
43:831--836.
Sperry, J.S. and M.T. Tyree. 1988. Mechanism of water-stress-induced
xylem embolism. Plant Physiol. 88:581--587.
Sperry, J.S. and M.T. Tyree. 1990. Water-stress-induced xylem embolism in three species of conifers. Plant Cell Environ. 13:427--436.
Sperry, J.S., J.R. Donnelly and M.T. Tyree. 1988. A method for
measuring hydraulic conductivity and embolism in xylem. Plant
Cell Environ. 11:35--40.
Squillace, A.E. 1976. Analyses of monoterpenes of conifers by gasliquid chromatography. In Modern Methods in Forest Genetics. Ed.
J.P. Miksche. Springer-Verlag, Berlin, pp 120--157.
Stone, C. and P.E. Bacon. 1994. Relationship among moisture stress,
insect herbivory, foliar cineole and the growth of river red gum
Eucalyptus camaldulensis. J. Appl. Ecol. 31:604--612.
Talbot, A.J.B., M.T. Tyree and J. Dainty. 1975. Some notes concerning
the measurement of water potentials of leaf tissue with specific
reference to Tsuga canadensis and Picea abies. Can. J. Bot.
53:784--788.
Teskey, R.O., J.A. Fites, L.J. Samuelson and B.C. Bongarten. 1986.
Stomatal and nonstomatal limitations to net photosynthesis in Pinus
taeda L. under different environmental conditions. Tree Physiol.
2:131--142.
Teskey, R.O., B.C. Bongarten, B.M. Cregg, P.M. Dougherty and T.C.
Hennessey. 1987. Physiology and genetics of tree growth response
to moisture and temperature stress: an examination of the characteristics of loblolly pine (Pinus taeda L.). Tree Physiol. 3:41--61.
Tyree, M.T. and F.W. Ewers. 1991. The hydraulic architecture of trees
and other woody plants. New Phytol. 119:345--360.
Tyree, M.T., M.A. Dixon, E.L. Tyree and R. Johnson. 1984. Ultrasonic
acoustic emissions from the sapwood of cedar and hemlock: an
examination of three hypotheses regarding cavitations. Plant
Physiol. 75:988--992.
Wang, J., N.E. Ives and M.J. Lechowicz. 1992. The relation of foliar
phenology to xylem embolism in trees. Funct. Ecol. 6:469--475.
Weinstein, A. 1989. Geographical variation and phenology of Pinus
halepensis, P. brutia and P. eldarica in Israel. For. Ecol. Manage.
27:99--108.