ORIGINAL PAPER

Oak restoration in water-limited pine plantations: interactiveeffects of overstory light interception and water availabilityon understory oak performance

Arnon Cooper • Or Shapira • Sohil Zaidan •

Yosi Moshe • Ela Zangy • Yagil Osem

Received: 10 September 2013 / Revised: 25 December 2013 / Accepted: 8 February 2014

� Springer-Verlag Berlin Heidelberg 2014

Abstract Oak regeneration within pine monocultures is

an opportunity to diversify forest structure. We examined

the relationships between overstory (Pinus brutia) light

interception and understory oak (Quercus ithaburensis)

performance in water-limited forests. The study was per-

formed in a mature pine plantation in Mediterranean Israel.

Twenty-year-old oaks differing in location with respect to

pine overstory and representing a gradient of light avail-

ability, such as open space (irradiance 100 %), interface

(17–77 %), and understory (14–23 %), were monitored.

Photosynthetic photon flux density (PPFD), leaf gas

exchange, and twig water potential (TWP) were measured

during the growth season under increasing drought stress.

Predawn TWP decreased sharply from early to late spring

and was positively related to irradiance during mid-spring

only. Predawn to midday TWP gradient was positively

related to irradiance mostly so during mid-spring. Daily

averages of stomatal conductance (gs), net carbon assimi-

lation rate (A), and transpiration rate (E) were highest in

early spring and decreased gradually toward late spring.

They were positively related to irradiance though this

relationship became less pronounced from early to late

spring. Oak height and stem basal area were positively

related to irradiance. A/gs ratio was positively related to

irradiance throughout the entire growth season. It increased

from early to mid-spring but decreased toward late spring.

A/PPFD ratio decreased from early to late spring showing a

negative relationship with irradiance. We concluded that

light availability was mainly responsible for spatial varia-

tion in oak performance and proposed that small-scale

overstory gaps aiming for direct sunlight exposure during

early spring should achieve maximum understory oak

performance with minimal pine removal.

Keywords Quercus ithaburensis � Pinus brutia �Photosynthesis � Stomatal conductance � Water-use

efficiency � Forest management � Mediterranean

Introduction

Converting simply structured monocultures into mixed

uneven-aged forests is a worldwide silvicultural challenge,

which requires intimate understanding of forest species and

their interactions. Natural oak regeneration in the under-

story of pine plantations provides an opportunity to manage

such systems toward the formation of multistory, pine-oak

woodlands with increased diversity and structural com-

plexity. However, knowledge regarding the best strategy

for managing this process is lacking (Prevosto et al. 2011).

Mature pine plantations in Israel inhabiting areas of native

oak regeneration offer a context for studying various sil-

vicultural aspects of this process.

Coniferous forests have been planted in Mediterranean

Israel since the 1920s. These forests were established as

simply structured monocultures dominated by Mediterra-

nean pine species, of which the most common ones are the

Communicated by C. Ammer.

A. Cooper � Y. Moshe � E. Zangy � Y. Osem (&)

Department of Natural Resources, Agricultural Research

Organization, Volcani Center, P.O. Box 6, 50250 Bet Dagan,

Israel

e-mail: yagil@agri.gov.il

A. Cooper � O. Shapira

The Faculty of Agriculture, Food and Environment, Hebrew

University of Jerusalem, Rehovot, Israel

S. Zaidan

Forestry Department KKL, Eshtaol, Israel

123

Eur J Forest Res

DOI 10.1007/s10342-014-0794-6

native Pinus halepensis Mill. and exotic Pinus brutia Ten.

Recently, foresters have made efforts to increase the

diversity and complexity of pine forests through planting,

direct seeding, and fostering natural regeneration of native

broad-leaved tree species within these forests (Osem et al.

2009). This study investigated the overstory–understory

interaction within plantations of mature pine—P. brutia—

inhabiting areas of native oak—Quercus ithaburensis—

regeneration.

Q. ithaburensis. subsp. ithaburensis (Tabor oak) is a

long-lived, deciduous oak, native to the eastern Mediter-

ranean including Israel. It is considered drought-resistant,

thermophile, and relatively fast-growing. In Israel, native

vegetation farms dominated by Q. ithaburensis are typi-

cally sparse woodlands that occur mainly in lowlands (up

to 500 m a.s.l) of the northern part of the country. This

species has been widely exploited in the past, and its cur-

rent populations are considered remnants of larger more

developed ancient forests. P. brutia (Cyprus pine) is native

to the northeastern Mediterranean, not including Israel.

This species which is specifically suitable for afforestation

in degraded arid environments has been extensively plan-

ted in Israel for the past 50 years. Some of these pine

forests have been established over degraded oak woodlands

and now include regenerating oaks as their understory

forest layer.

The establishment and development of forest understory

vegetation is most often determined by light availability.

The amount of photosynthetically active radiation (PAR)

penetrating the overstory presents the availability of the

light resource to the understory vegetation. However, other

characteristics of the light regime such as the range and

distribution of PAR intensity may affect the proportion of

the available PAR practically exploited by the understory

vegetation (Wayne and Bazzaz 1993). These light regime

characteristics vary depending on overstory interception

patterns (Lieffers et al. 1999). Moreover, acclimation of

plant and leaf photochemistry under different light envi-

ronments may further complicate light availability–plant

performance relationships (Parelle et al. 2006).

In Mediterranean forests, light constraints co-occur with

water scarcity (Rodrıguez-Calcerrada et al. 2007a; Prevo-

sto et al. 2011) and the relative importance of these two

factors in limiting understory vegetation performance may

vary depending on season, location (Prevosto et al. 2011;

Holmgren et al. 2012), and ontogeny (Ammer et al. 2008).

In contrast to the light resource, the way by which water

availability is effected by overstory cover is not straight-

forward. In Mediterranean P. halepensis forests, for

example, reported effects of pine cover on understory water

regime are inconsistent, varying among climatic regions,

season, canopy cover, soil characteristics, and depth

(Maestre et al. 2003; Bellot et al. 2004; Prevosto et al.

2011).

The complex light–water interplay occurring in the

understory of Mediterranean pine forests makes it hard to

prescribe simple silvicultural guidelines to promote

understory growth. Moreover, overstory treatments may

vary in the way they affect different understory species,

depending on species traits (Rodrıguez-Calcerrada et al.

2008; Holmgren et al. 2012). Particularly important are

traits related to shade tolerance and drought resistance

(Erpon et al. 1993; Rodrıguez-Calcerrada et al. 2007b,

2008). Mechanisms of shade tolerance may differ and even

be inversely related to those of drought resistance (Smith

and Huston 1989; Pardos et al. 2005). Nevertheless, plant

species growing in the understory of Mediterranean forests

often need to cope, simultaneously, with both stress types.

Thus, they are likely to present complex behavior patterns

with respect to variation in overstory cover and related

variation in light and water regime (van Hees 1997; Aranda

et al. 2005).

Several studies have focused directly on the perfor-

mance of oak species in forest understory. While some oak

species have shown better performance with increasing

light availability (Teskey and Shrestha 1985; Dey and

Parker 1997; Prevosto et al. 2011), others have shown

equal or even better performance under some shading

(Ziegenhagen and Kausch 1995; Cardillo and Bernal

2006). Some studies have demonstrated the capacity of oak

species to survive under shading (Rentch et al. 2003) and to

respond vigorously to release from shading (Ziegenhagen

and Kausch 1995).

The current research examined the relationship between

the extent of light interception by the pine overstory and

the performance of 20-year-old Q. ithaburensis trees

growing in the understory of water-limited mature P. brutia

plantation.

The specific aims were as follows:

1. To examine the relationship between light availability

and oak performance.

2. To examine the way light availability interacts with

water availability in determining oak performance.

We addressed these questions by taking an observational

approach in which the light availability, water availability,

and leaf gas exchange were monitored in understory oaks

growing in different locations with respect to pine over-

story cover and representing a gradient of light availability.

Measurements were executed repeatedly during the growth

season, representing a temporal gradient of increasing

drought stress. Our goal was to contribute to the develop-

ment of forest management strategies for enhancing oak

seedling performance established in the pine understory

Eur J Forest Res

123

and achieving a gradual conversion of simply structured

monocultures into complex mixed forests.

Methods

Research site

The study was performed in the Metzer Forest located in

northwestern part of the Shomron region of Israel (UTM-

690950E 3591870N). The forest (60 ha) consists mainly of

mature pine monocultures planted during the 1960s. The

climate is typical east Mediterranean with an average

annual rainfall of about 600 mm concentrated mainly

between December and March. The drought season is long,

typically about 6 months with no rain. Daily maximum

temperatures increase during this time and peak during

July–August at about 36–40 �C. Local soils are brown

mountain rendzines that developed on soft to semi-hard

chalk. The native vegetation in this region ranges from

dwarf shrublands to sparse woodlands with Q. ithaburensis

as the dominant tree species.

Experiment structure

The study was carried out in 2009 in a mature (45 year old)

P. brutia plantation. In 1988–1989, acorns of Q. ithaburensis

were sown in the understory of this plantation as part of an

experimental oak seeding campaign. The acorns were sown

in proximity to pine stumps (trees that were cut in a previous

thinning) at a constant direction (north) and distance (ca.

50 cm) to enable their identification as seeded oaks. Ten

years later (1999), a wildfire broke out, consuming some

parts of the plantation. According to forest inventory data,

pine density and stem basal area in the studied plantation,

prior to the fire, were ca. 300–350 tree ha-1 and

12–14 m2 ha-1, respectively. Following the fire, areas in

which pine crowns were burnt were salvage-logged. The

remaining unburnt area was left as is, with no subsequent

silvicultural intervention. This has created a situation in

which oaks that had been growing under similar overstory

conditions for the 10 years prior to the fire were now exposed

to variable overstory light interception levels, depending on

their location with respect to logged and non-logged areas.

Based on personal communication with the local forester, at

the time of the salvage logging, all of the seeded oaks were

very small (\40 cm in height). Some of the oaks, specifically

those in the cleared area, were injured by the fire but survived

it. This local situation presented a unique opportunity to

investigate the effect of various light interception levels on

the performance of understory oaks with similar age and

history. The observation was conducted 10 years after the

fire (2009) on the seeded 20-year-old oaks. Three zones were

identified with respect to the pine overstory, they are as

follows: (1) open space—unshaded areas more than 15 m

away from the margins of the pine overstory. These areas

were salvage-logged following the 1999 fire and became

unshaded; (2) understory—shaded areas more than 15 m

away from the overstory canopy margins toward the inside

of the forest; and (3) interface—along the margins of the pine

overstory canopy—including up to 5 m from the outer pine

stem line (northeast) toward both the open space and

understory (Fig. 1). During the study period, stand tree

density (overstory pines) in the non-logged areas was typi-

cally 300 tree ha-1, leaf area index (LAI) was 5.5 m2 m-2,

stem basal area was 14–16 m2 ha-1, and average tree height

16 m. Ground vegetation cover in the understory and stem

line was nearly nonexistent. In the interface and open space,

it was more developed, mainly composed of annual herba-

ceous vegetation with some dwarf shrub cover (ca. 20 %).

Oaks, positioned at least 12 m apart, were selected randomly

in each of the three predefined zones. This has created a

stratified random sampling design that represents a gradient

of overstory interception occurring from the open space (6

oaks), through the interface (18 oaks), and toward the

understory (6 oaks). Each oak was monitored for (a) daily

photosynthetic photon flux density (PPFD), (b) leaf level gas

exchange, and (c) water status. Measurements were taken

three times at various stages of the growth season: early

season (April 13), mid-season (May 22), and late season

(June 30). This period represents the first 3 months of the

Fig. 1 The observational setup in the Metzer Forest 2009. Oaks from

three zones—open space (6 oaks), interface (18 oaks), and understory

(6 oaks)—were assigned randomly representing an overstory light

interception gradient

Eur J Forest Res

123

rainless season during which soil water content decreases

sharply and air temperature and radiation intensity increase.

In order to investigate the variation in oak growth, the size of

all monitored oaks was measured once.

Parameters and measurements

Light availability

PPFD (lmol photon m-2 s-1) was measured using Li-

6400XT (Li-Cor Lincoln Nebraska USA). These mea-

surements were taken throughout the growth season: early

season, mid-season, and late season, on clear sunny days.

PPFD was monitored for each oak every 2 h from 7:00 am

to 17:00 pm. Daily average PPFD, calculated separately

for each oak (herein after irradiance), was used as the basic

measure for light availability. Irradiance varied moderately

by season and increased consistently from the understory

(irradiance = 14–23 %), through the interface (17–77 %),

and toward the open space (100 %). Air temperature and

relative humidity were not affected by irradiance. Daily

ranges (7:00 am to 17:00 pm) of air temperature were

18–33, 24–34, and 26–43 �C while the ranges of relative

humidity were 25–47, 28–46, and 16–48 % in early, mid-,

and late season, respectively.

Oak water status

Oak water status was assessed by means of predawn and

midday (solar noon) twig water potential (TWP) measure-

ments. These measurements were taken throughout the

growth season using a pressure chamber (PMS Instrument

Company, Oregon, USA). For each oak, three twigs carrying

fully developed healthy young leaves were measured. Twigs

measured at midday were sealed 2 h prior to measurement in

a plastic bag covered with aluminum foil to allow balance

with stem water potential and provide better assessment of

the water status at the whole plant level (Naor 2000).

Oak size and leaf gas exchange

Two measurements were used for oak size: tree height and

stem basal area at ground level. Instantaneous gas exchange

measurements at the leaf level scale were taken using Li-

6400XT (Li-Cor Lincoln Nebraska USA) parallel to the

PPFD measurements. Each oak was monitored throughout

the growth season for net carbon assimilation rate (A),

transpiration rate (E), stomatal conductance (gs), and inter-

cellular carbon concentration (Ci). One young, fully devel-

oped, healthy leaf was measured in each session of the day

for each tree. Leaves selected for measurements were sun

leaves, facing the direction of the sun at measurement time.

Measurement was taken ca. one minute after attachment

when steady state was achieved. Light level inside the leaf

chamber was maintained equal to the outdoor PPFD by the

LI–6400 external quantum light sensor. A constant CO2

concentration of 380 ppm was set. Instantaneous measure-

ments taken throughout the day (7:00 am to 5:00 pm) were

used to extract daily averages for each oak.

Water-use efficiency and A-to-PPFD ratio

The ratio between A and gs was used to calculate intrinsic

water-use efficiency (WUE) of the oaks leaves. The ratio

between A and PPFD (A/PPFD) was calculated as a measure of

leaf level light-use efficiency. Daily averages of WUE and A/

PPFD were calculated for each oak in each of the three sea-

sons. Calculations of these averages were weighted by gs and

PPFD, respectively. In addition, we calculated the ratio

between daily E and daily leaf water potential gradient (pre-

dawn–midday, hereinafter—E/WPG). This was used as a

measure for hydraulic sufficiency in the soil–plant continuum.

Statistical analysis

Relationships between light availability and oak size, leaf

level gas exchange, and water status were examined, at the

single tree level, via linear regression analyses. Common

transformations (e.g., log x and log y) were used in order to

explore alternative relationship patterns. Repeated-mea-

sures analyses of covariance were used in order to analyze

the interactive effect of season (nominal) and light avail-

ability (continuous) on gas exchange and water status of

oaks. Assumptions of homogeneity of variances and nor-

mal distribution of error were tested through the Levene

and the Shapiro–Wilk tests, respectively. Mathematical

transformations of data were used when necessary.

Results

Water relations

Measurements of predawn and midday TWP revealed a

significant decrease in oak water status along the growth

season. Predawn TWP was found to be positively related to

irradiance (i.e., became less negative with increasing irra-

diance) though this relationship was clearly evident only in

mid-season (Table 1a; Fig. 2a). Midday TWP, however,

presented an interactive pattern in which it was negatively

related to irradiance in early and mid-season but not

affected by irradiance in late season (Table 1b; Fig. 2b).

Looking at the predawn to midday TWP gradient, we found

that it was positively affected by irradiance (i.e., larger

gradient with increasing irradiance) mostly in mid-season

Eur J Forest Res

123

and more moderately so in the early and late seasons

(Table 1c; Fig. 2c).

Carbon assimilation and growth

Daily average A increased linearly with increasing irradi-

ance and decreased from early to late season, i.e., it was

typically lower by 30–35 and 70–80 % in mid- and late

season, respectively, than in early season (Table 1d;

Fig. 2d). Irradiance 9 season interaction was found to be

significant, indicating that the positive effect of irradiance

has gradually diminished from early to late season. Pattern

of daily average E was similar to that of A with one dif-

ference—A was significantly reduced from mid- to late

season while E was hardly changed during that period

(Table 1e; Fig. 2e). Oak size increased substantially with

irradiance. Spatial variation in oak height was found to be

linearly related to irradiance ranging, typically, from 30 cm

in the understory to 350 cm in the open space (Fig. 3a).

Stem basal area was found to be exponentially related to

irradiance ranging from 0.25 to 88 cm2, respectively

(Fig. 3b). Irradiance–oak size relationships improved

slightly when size parameters were plotted against irradi-

ance taken exclusively from early season (data not shown).

Similar patterns were found by plotting oak size against

daily average A (data not shown).

Stomatal conductance and carbon assimilation

efficiency

Daily average gs of the oaks leaves was positively related to

irradiance and decreased strongly from early to late season

(Table 1f; Fig. 2f). The gs of open space oaks during midday

varied between 0.21, 0.12–0.10, and 0.06–0.02 mol

H2O m-2 s-1 in early, mid-, and late season, respectively.

Intrinsic WUE recorded in the oaks’ leaves increased sig-

nificantly with irradiance. An interesting pattern of seasonal

effect was found in which WUE was highest in mid-season

and lower in both early and late seasons (Table 1g; Fig. 2g).

Season 9 irradiance interaction was significant indicating

that the PPFD–WUE relationship became less pronounced in

late season. The pattern of A/PPFD was different than that of

WUE. It decreased sharply from early to late season and was

negatively related to irradiance (Table 1h; Fig. 2h). When

looking at daily average intercellular carbon concentration

(Ci), an interactive pattern emerged in which Ci was nega-

tively related to irradiance in early and late seasons but was

not related to irradiance during late season. In general, Ci was

lowest in mid-season and higher during early and late sea-

sons (Table 1i; Fig. 2i). Looking at the ratio between daily

average E versus predawn to midday water potential gradient

(E/WPG) revealed that this ratio decreased significantly

from early to late season. However, no significant effect of

irradiance was found for this index (Table 1j).

Discussion

Light availability and oak performance

Light availability varied considerably among oaks located

throughout the open space–understory continuum. This

Table 1 Repeated-measures analyses of covariance of the effect of

irradiance (continuous variable) and season (April 13, May 22, and

June 30) on (a) predawn twig water potential (TWP), (b) midday

TWP, (c) predawn to midday TWP gradient (WPG), (d) net carbon

assimilation rate (A), (e) transpiration rate (E), (f) stomatal conduc-

tance (gs), (g) intrinsic water-use efficiency (WUE), (h) A/PPFD,

(i) intercellular carbon concentration (Ci), and (j) E/WPG of 20-year-

old oak (Quercus ithaburensis) leaves in Metzer Forest 2009

Variable df F P

(a) Predawn twig water

potential (TWP)

Season 2 120.8 ****

R2 = 0.84 Irradiance 1 8.02 *

(b) Midday TWP Season 2 162.63 ****

R2 = 0.90 Irradiance 1 5.64 *

Season 9 Irradiance 2 4.32 *

(c) Predawn to midday

TWP gradient

Season 2 15.12 ****

R2 = 0.54 Irradiance 1 26.47 ****

(d) Net carbon

assimilation rate (A)

Season 2 65.65 ****

R2 = 0.77 Irradiance 1 85.93 ****

Season 9 Irradiance 2 6.86 **

(e) Transpiration rate (E) Season 2 36.06 ****

R2 = 0.69 Irradiance 1 67.75 ****

Season 9 Irradiance 2 8.78 ***

(f) Stomatal conductance

(gs)

Season 2 91.43 ****

R2 = 0.75 Irradiance 1 34.22 ****

(g) Intrinsic water-use

efficiency WUE

Season 2 15.7 ****

R2 = 0.68 Irradiance 1 44.93 ****

Season 9 Irradiance 2 3.69 *

(h) A/PPFD Season 2 63.08 ****

R2 = 0.78 Irradiance 1 49.75 ****

(i) Intercellular carbon

concentration (Ci)

Season 2 15.86 ****

R2 = 0.70 Irradiance 1 56.14 ****

Season 9 Irradiance 2 11.66 ****

(j) Daily average E/WPG Season 2 14.51 ****

R2 = 0.49 Irradiance 1 2.63 n.s.

* P \ 0.05, ** P \ 0.01, *** P \ 0.001, **** P \ 0.0001, n.s. not

significant

Eur J Forest Res

123

a

c

b

Eur J Forest Res

123

was in accordance with the level of light interception by

the pine overstory. Oak size as represented by height and

stem basal area of 20-year-old individuals had a clear

positive relationship with irradiance. This positive rela-

tionship was also manifested through the A–PPFD rela-

tionship indicating an overriding importance of light

availability as a limiting factor for Q. ithaburensis growth

in the understory of Mediterranean pine forests. Similarly,

Rodrıguez-Calcerrada et al. (2007b) and Prevosto et al.

(2011) reported enhanced growth of different Mediterra-

nean oak species with increased canopy openness (higher

irradiance) in pine forest stands. Our results demonstrate

the capability of Q. ithaburensis to respond vigorously to

release from shading following 10 years under substantial

shading (irradiance \20 % relative to open space).

The importance of water availability

In Mediterranean forests, water availability is known to

play an important role in determining vegetation perfor-

mance. Accordingly, the oaks’ A decreased significantly

from early to late season, throughout the entire light

availability range, along with decreasing soil water avail-

ability as indicated by the predawn TWP. The gs during

midday hours was observed exclusively in unshaded oaks

(open space) as a surrogate for the drought stress level

experienced by the oaks (Flexas and Medrano 2002). These

measurements indicated no drought stress in early season,

moderate drought stress in mid-season, and severe to very

severe drought stress in late season. Correspondingly, daily

average A under comparable irradiance was typically 35

and 80 % lower in mid- and late seasons, respectively, than

in early season. Similarly to A, E has also decreased along

the season though unlike A, this decrease was clearly

apparent only from early to mid-season. Thus, the inter-

seasonal variation in E was the outcome of both stomatal

adjustment (Flexas and Medrano 2002) as well as variation

in atmospheric pressure deficit (VPD) resulting mainly

from increasing air temperature along the growth season. In

contrast to seasonal effect, the relationship between irra-

diance and water availability is non-trivial as it involves a

series of processes related to overstory cover including rain

interception, evaporation, and transpiration (Raz-Yaseef

et al. 2012). Interestingly, in the monitored system, the

variation in oak predawn TWP along the light availability

gradient was relatively minor and clearly observed only in

mid-season during which daily average A was already

b Fig. 2 Relationship between daily average irradiance and a predawn

twig water potential (TWP), b midday TWP, c predawn to midday

TWP gradient (WPG), d net carbon assimilation rate (A), e transpi-

ration rate (E), f stomatal conductance (gs), g intrinsic water-use

efficiency (WUE), h A/PPFD, i intercellular carbon concentration

(Ci), j E/predawn to midday water potential gradient (E/WPG),

measured in early season (April 13), mid-season (May 22), and

late season (June 30) in 20-year-old oak (Quercus ithaburensis)

leaves in Metzer Forest 2009. a Filled black circle Early season

(y = 1E-05x - 0.3, R2 = 0.005, P = 0.78); filled blue circle mid-

season (y = 0.0002x - 0.87, R2 = 0.3, P \ 0.05); filled yellow circle

late season (y = 0.0004x - 1.64, R2 = 0.15, P = 0.11). b Filled black

circle Early season (y = -0.0003x - 0.99, R2 = 0.24, P \ 0.05);

filled blue circle mid-season (y = -0.0005x - 1.21, R2 = 0.5,

P \ 0.01); filled yellow circle late season (y = 6E-05x - 2.88,

R2 = 0.005, P = 0.78). c Filled black circle Early season

(y = 0.0003x ? 0.7, R2 = 0.25, P \ 0.05); filled blue circle mid-

season (y = 0.0007x ? 0.34, R2 = 0.67, P \ 0.0001); filled yellow

circle late season (y = 0.0004x ? 1.24, R2 = 0.11, P = 0.17).

d Filled black circle Early season (y = 0.01x ? 1.80, R2 = 0.88,

P \ 0.0001); filled blue circle mid-season (y = 0.005x ? 1.98,

R2 = 0.77, P \ 0.0001); filled yellow circle late season

(y = 0.002x ? 1.18, R2 = 0.38, P \ 0.001). e Filled black circle

Early season (y = 0.003x ? 1.55, R2 = 0.69, P \ 0.0001); filled blue

circle mid-season (y = 0.001x ? 1.14, R2 = 0.46, P \ 0.0001); filled

yellow circle late season (y = 0.001x ? 1.14, R2 = 0.30, P \ 0.01).

f Filled black circle Early season (y = 0.05ln(x) - 0.17, R2 = 0.64,

P \ 0.0001); filled blue circle mid-season (y = 0.02ln(x) - 0.06,

R2 = 0.29, P \ 0.01); filled yellow circle late season

(y = 0.01ln(x) - 0.02, R2 = 0.32, P \ 0.01). g Filled black circle

Early season (y = 15.86ln(x) - 43.84, R2 = 0.76, P \ 0.0001); filled

blue circle mid-season (y = 13.77ln(x) - 13.71, R2 = 0.55,

P \ 0.0001); filled yellow circle late season (y = 9.32ln(x) - 0.33,

R2 = 0.24, P \ 0.01). h Filled black circle Early season

(y = 0.021e-5E-04x, R2 = 0.27, P \ 0.01); filled blue circle mid-

season (y = 0.016e-8E-04x, R2 = 0.41, P \ 0.0001); filled yellow

circle late season (y = 0.008e-0.001x, R2 = 0.47, P \ 0.0001). i Filled

black circle Early season (y = -29.17ln(x) ? 456.91, R2 = 0.81,

P \ 0.0001); filled blue circle mid-season (y = -26.31ln(x) ? 412.24,

R2 = 0.64, P \ 0.0001); filled yellow circle late season (y =

-7.85ln(x) ? 324.47, R2 = 0.09, P = 0.11). (Color figure online)

0

100

200

300

400

0 500 1000 1500

a0

50

100

150

0 300 600 900 1200 1500

b

Hei

ght (

cm)

Irradiance (µmol photon m-2s-1)Irradiance (µmol photon m-2s-1)

Stem

bas

al a

rea

(cm

2)

Fig. 3 Relationship between

daily average irradiance and

a height, b stem basal area

(b) of 20-year-old oaks

(Quercus ithaburensis) growing

in Metzer Forest 2009.

a y = 0.30x - 19.58,

R2 = 0.85, P \ 0.0001,

b y = 0.39e0.005x, R2 = 0.81,

P \ 0.0001

Eur J Forest Res

123

much reduced (i.e., by ca. 35 %). Oaks’ midday TWP,

however, decreased significantly with irradiance, especially

during early and mid-season. This should be attributed to

E, which increased with irradiance with this relationship

becoming less steep from early to late season. Our results

are partially in line with the findings of Rodrıguez-Cal-

cerrada et al. (2008) in Spain and Prevosto et al. (2011) in

Southern France who reported for different Mediterranean

oak species improved water status of seedlings with

increased pine canopy openness. This was despite similar

or even lower soil water contents recorded in the more

opened stands and was explained, in both studies, by better

root development in seedlings growing under higher light

availability. The relatively minor variation in predawn

TWP observed in the current study may have been the

outcome of (1) oak age (20 years), which enabled the

development of deep roots in both the open space and

understory, and (2) the time elapsed since pine overstory

removal (10 years), which allowed the development of a

ground vegetation layer compensating for the lower pine

cover in terms of competition for water (Simonin et al.

2007). It may be concluded that variation in soil water

availability may have contributed, to some extent, to the

observed spatial variation in oak performance. However,

this effect was minor relative to the direct influence of light

availability.

Water-use and carbon assimilation efficiency

The spatial variation in intrinsic WUE, as observed in

the current study, could have resulted from differences in

irradiance and related A (Sanches and Valio 2008;

Medrano et al. 2012), stomatal adjustment (Gulıas et al.

2012), or metabolic efficiency (Teskey and Shrestha

1985). In early season when oak water status was

favorable and similar throughout the light availability

gradient, the observed decrease in WUE from the open

space toward the understory is most likely attributable

directly to the variation in irradiance. Assuming constant

gs, light limitation is expected to result in decreased

A and, consequently, lower WUE. However, gs was not

constant, but rather decreased gradually with decreasing

irradiance. Nevertheless, the lower WUE associated with

decreasing irradiance indicated that A was still more

limited by light availability than by gs. This was also

manifested through the intercellular carbon concentration

(Ci), which increased significantly with decreasing irra-

diance (Flexas and Medrano 2002). It may, thus, be

concluded that in early season under favorable water

conditions, light limitation resulted in decreased WUE

since stomatal adjustment was more strongly aimed at

maximizing A than optimizing WUE. In mid-season,

however, as water limitation became important (i.e.,

moderate drought stress), gs decreased strongly

throughout the entire light availability gradient and the

WUE increased significantly despite a parallel decline in

A. In this case, stomatal closure was associated with a

decrease in Ci indicating that during mid-season, A was

more limited by gs (Cornic 2000; Flexas and Medrano

2002). In late season, as soil water became critically

scarce (i.e., severe to very severe drought stress) and gs

was further decreased, WUE became lower throughout

the entire light availability gradient and similar to that

observed in early season. However, in contrast to the

early season, the decrease in gs in the late season was

associated with an increase in Ci indicating some degree

of metabolic (Flexas and Medrano 2002) and/or other

non-stomatal limitation (Aranda et al. 2012). Thus, WUE

fluctuated among seasons following shifts in mechanism

limiting A. Nevertheless, the positive relationship

between WUE and irradiance persisted throughout the

entire growth season indicating that water was more

efficiently used by the open space than by the understory

oaks, consistently. This was despite the water availability

being slightly lower in the understory than in the open

space. Unlike WUE, A/PPFD was found to be negatively

related to irradiance and decreased consistently along the

growth season with decreasing water availability. Higher

A/PPFD in the understory than in the open space may be

attributed to both lower proportion of saturating PPFD

levels (Gomez et al. 2012) as well as to better exploita-

tion of low PPFD levels through plant acclimation (Val-

ladares et al. 2005) in the former than in the latter.

Practical implications

Understory Q. ithaburensis trees, whether seeded or nat-

urally established, provide a basis for transforming simply

structured Mediterranean pine plantations into more

complex pine-oak woodlands. This process can be pro-

moted through release thinning that will increase light

availability to target oaks. Release thinning should be

applied in a way that will optimize oak performance with

minimal pine cover loss. According to our findings, small-

scale gaps in the pine overstory allowing direct sunlight

to target oaks in early to mid-spring (April–May) and

during morning to midday hours should enable ideal

exploitation of the light and water resources by understory

oaks. This is enabled by bringing together favorable water

conditions (higher soil water content and lower VPD) on

the one hand and high light availability on the other hand.

To achieve that, gaps should be opened east to southeast

with respect to target oaks with the optimal distance

determined according to overstory height and the course

of sun zenith angle.

Eur J Forest Res

123

Conclusions

We propose the following conclusions:

1. Q. ithaburensis is capable of responding vigorously in

growth following release from shading after more than

10 years under substantial shading by pine overstory.

2. In the understory of Mediterranean pine forests, Q.

ithaburensis performance is strongly limited by light

availability. The light limitation is specifically crucial

in the early growth season when soil water availability

is adequate.

3. Soil water availability decreases sharply along the

growth season reaching severe to very severe drought

stress by late spring–early summer. It gradually

replaces light availability as the main limiting factor

for oak performance.

4. The effect of pine overstory on water availability for

understory oaks is complex and case-sensitive with only

a slight negative trend found in this study. However, the

effect of pine overstory on the WUE of understory oaks

was found to be consistently negative under both

favorable as well as stressful seasonal water conditions.

5. Release thinning of pine overstory aiming for direct

sunlight exposure of understory target oaks in early to

mid-spring and during morning to midday hours is

proposed as a preferable strategy. It should achieve

higher oak performance for less pine removal, thus

enhancing the conversion of pine monocultures into

mixed pine-oak woodlands in Mediterranean water-

limited environments.

The results of this study shed light on key ecophysio-

logical processes and their relationships with light and

water conditions in the forest understory. The study pro-

vides new insights, which may help foresters to better

manage the conversion of simply structured pine plantation

into complex pine-oak woodlands in water-limited envi-

ronments. We strongly encourage the performance of well-

designed manipulative trials to further test pine overstory

gap patterns and their effects on the performance of

understory oaks.

Acknowledgments Special thanks to Rinat Ovadia, Hedva, and

Max Cooper for their valuable assistance in this work. We thank Asaf

Tzur, Nitai Zeharia, Nurit Hibsher, Tom Fogel, and Eitan Bney-

Moshe for their help in the field measurements. The study was funded

by The Israeli Forest Service (KKL).

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