Are small-scale overstory gaps effective in promotingthe development of regenerating oaks (Quercusithaburensis) in the forest understory?

Arnon Cooper • Yossi Moshe • Ela Zangi • Yagil Osem

Received: 29 December 2013 / Accepted: 9 June 2014� Springer Science+Business Media Dordrecht 2014

Abstract We investigated the effect of small-scale overstory gaps on the ecophysiology

and growth of Quercus ithaburensis saplings. The study aim was to characterize how

changes in daily exposure to direct beam radiation affect photosynthetic performance in the

short term and growth and biomass partitioning in the long term. Using individual net-

houses, the following treatments were applied: (a) Unshaded (daily irradiance = 100 %),

(b) shading net with no gap (Shade-daily irradiance = 6 %), (c) shading net with 1 h gap

allowing direct beam radiation (11:00 am–12:00 pm, Shade?1-irradiance = 20 %),

(d) shading net with 3 h gap (11:00 am–2:00 pm, Shade?3-irradiance = 44 %). The

experiment was performed in an irrigated field. We measured growth, biomass allocation,

leaf traits, daily courses of leaf gas exchange and water potential. Oak dry-weight

increased while height to dry-weight ratio and specific leaf area decreased with increasing

daily exposure to direct beam radiation. Leaf chlorophyll content was less affected. Higher

net carbon assimilation rates (A), stomatal conductance (gs) and A/gs were associated with

higher instantaneous photosynthetic photon flux density (PPFD) throughout the entire

experimental PPFD range. However, during gap-hours, while exposed to saturating radi-

ation levels of similar level (ca. 1,800 lmol photon m-2 s-1), A in the Shade?1 oaks was

about half that of the Shade?3 oaks and nearly one-third that of the Unshaded oaks.

Patterns of gs, intercellular CO2 (Ci) and quantum efficiency of photosystem II pointed

towards the possibility of a metabolic limitation. In conclusion, oaks benefited significantly

from small scale overstory gaps though their capacity to utilize transient saturating radi-

ation levels decreased with decreasing gap duration.

Keywords Photosynthesis � Stomatal conductance � Plant acclimation � Forest

management � Mediterranean

A. Cooper � Y. Moshe � E. Zangi � Y. Osem (&)Department of Natural Resources, Agricultural Research Organization, Volcani Center, P.O. Box 6,50250 Bet Dagan, Israele-mail: Yagil@agri.gov.il

A. CooperThe Faculty of Agriculture, Food and Environment, Hebrew University of Jerusalem, Rehovot, Israel

123

New ForestsDOI 10.1007/s11056-014-9441-9

Introduction

Quercus ithaburensis subsp. ithaburensis (Tabor oak) is a long lived, winter deciduous

oak, native to the East-Mediterranean including Israel (Zohary 1961). It is considered

drought resistant, thermophile and relatively fast growing (Dufour-Dror and Ertas 2004;

Grunzweig et al. 2008) and is therefore highly suitable for afforestation in dry Mediter-

ranean habitats. In Israel, native vegetation forms dominated by Q. ithaburensis are typ-

ically 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 current

populations are considered remnants of larger, more developed ancient forests. Recently,

foresters have become aware of the fact that this species is regenerating intensively in the

understory of mature pine plantations. This process is seen as an opportunity to manage

these monocultures towards the formation of pine-oak woodlands with increased diversity

and structural complexity (Ruiz-Benito et al. 2012; Sheffer 2012). However, the devel-

opment of oak recruits in the forest understory is very limited and knowledge with regard

to the adequate strategy through which this process could be enhanced while minimizing

impact on the current overstory canopy cover is lacking (Osem et al. 2008, 2009; Prevosto

et al. 2011). This study investigated the effect of small scale overstory gaps allowing

transient exposure to direct beam radiation on photosynthetic performance and growth

(herein after, function) of regenerating oaks in the forest understory.

Plant function in the forest understory is largely determined by light availability. Light-

related variability in understory species function may be the outcome of heterogeneity in

the total amount of incident light per day as well as in other characteristics related to the

diurnal pattern of light availability such as the magnitude, diurnal timing and duration of

daily peaks (Wayne and Bazzaz 1993; Leakey et al. 2003). Forest stand characteristics and

resulting canopy architecture govern the pattern by which light penetrates the overstory

layer becoming available to understory vegetation (Lieffers et al. 1999). Specifically

influential are overstory gaps which allow transient exposure of understory plants to direct

beam radiation (Wayne and Bazzaz 1993). Small-scale overstory gaps created by natural

disturbances are known as an important driver of forest succession (White et al. 1985;

Spies et al. 1990). Recently, as silvicultural strategies such as ‘‘close to nature silviculture’’

(Grassi et al. 2004) and ‘‘continuous cover forestry’’ (Gaulton and Malthus 2010) are

increasingly adopted, efforts are being made to develop guidelines for gap manipulations

with the aim of enhancing the natural regeneration, diversity and structural complexity of

managed forests (Lhotka 2013). Such guidelines should be based on intimate acquaintance

with the ecophysiology of understory focal species (Wayne and Bazzaz 1993; Morrissey

et al. 2010; Dey et al. 2012).

The capacity to tolerate low radiation levels on the one hand and utilize transient peak

radiation on the other hand is variable among species depending largely on their shade

tolerance strategy (Wayne and Bazzaz 1993; Humbert et al. 2007; Niinemets and Val-

ladares 2006). In Mediterranean water-limited forests questions related to shade tolerance

are even more complex as water and light limitations may occur simultaneously (Sabate

et al. 2002) requiring different and even contrasting resistance mechanisms (Smith and

Huston 1989). Moreover, variations in light regime resulting from differences in overstory

cover are usually confounded with variation in soil water availability and plant water

uptake (Maestre et al. 2003; Maestre and Cortina 2004). Therefore, studying light-related

function of understory species in Mediterranean forests requires that water aspects are

carefully being accounted for.

New Forests

123

In a recent observational study we have shown the importance of light availability in

limiting carbon assimilation and growth of Q. ithaburensis trees in the understory of East-

Mediterranean pine plantations (Cooper et al. 2014). Moreover, we have proposed small-

scale overstory gaps as a possible means to promote the development of understory oaks. In

this study we examined the effect of overstory gap treatments on the function of understory

oak saplings (Q. ithaburensis). We took an experimental approach in which oak saplings

were grown under specifically designed net-houses allowing transient exposure to direct

beam radiation of varying duration (i.e., varying gap duration) around midday time. To

eliminate possible water-related confounding effects the experiment was performed under

non-limiting soil water availability. We monitored daily courses of leaf-level gas exchange

chlorophyll fluorescence and water potential and measured growth, biomass allocation and

leaf traits in oak saplings receiving different gap treatments i.e., varying duration of daily

exposure to direct beam radiation. The study aim was to characterize how changes in daily

exposure to direct beam radiation affect photosynthetic performance in the short term and

growth and biomass partitioning in the long term. In our work we strive to contribute to the

development of guidelines for overstory manipulation in East-Mediterranean pine planta-

tions accommodating oak regeneration. Such guidelines may promote the gradual conver-

sion of these simply structured monocultures into mixed pine-oak woodlands.

Methods

Research site

The study was performed in an experimental field area near the village of Bet-Dagan

(UTM-E673010 N3541600). This area corresponds to the central seashore region of Israel.

Elevation is 35 m a.s.l. Climate is typical Eastern-Mediterranean with average annual

rainfall of 525 mm. Daily average temperature ranges between 7–17�C in the winter and

21–31�C in the summer. Daily average relative humidity ranges between 64 and 82 %.

Local soil is defined as brown–red sandy soil (Ravikovitch 1992).

Experimental setup

In the autumn (October) of 2006 acorns were collected from adult Q. ithaburensis trees

growing in the Sharon-Park nature reserve. Undamaged acorns of comparable size

(17–24 g each) were selected for the trial. They were kept in a cooler (4�C) until December

and then sown in the ground at 7 cm depth. Sowing spacing was 6 9 6 m. Germination

occurred, typically, in March and emerged seedlings were divided into four net-house

treatments (also referred to as ‘‘gap treatments’’): (1) Unshaded control, (2) neutral (black)

shading net (94 % shading) with no gap (hereafter–Shade), (3) neutral shading net with a

gap allowing 1 h of direct beam radiation (11:00 am–12:00 pm, Shade?1), (4) neutral

shading net with a gap allowing 3 h of direct beam radiation (11:00 am–2:00 pm,

Shade?3). The treatments were applied in 12 randomly arranged replicates (complete

randomized experimental design) with each seedling (48 seedlings in total, n = 12) treated

separately using individual cubic net-houses (1 9 1 9 1 m). Each net-house was elevated

15 cm above ground surface to allow air circulation (Wayne and Bazzaz 1993). Exposure

to direct beam radiation during midday was achieved by creating a perpendicular rect-

angular gap at the center of the south-facing net-house wall. The gap width determined the

duration of exposure to direct beam radiation. To avoid soil water limitation saplings were

New Forests

123

irrigated twice a day (6:00 am and 1:00 pm) throughout the entire experiment. The oaks

were grown under these conditions for 2.5 years. We measured their size (growth), above

ground biomass allocation, leaf traits, leaf-level gas exchange, chlorophyll fluorescence

and water potential as affected by the different gap treatments.

Parameters and measurements

Ecophysiology

Photosynthetic photon flux density (PPFD) was measured using LiCor PAR sensor (9901-

013 External Quantum Sensor). The PPFD measurements were conducted separately for

each sapling from 7:00 am to 5:00 pm at 2 h intervals. These measurements were taken on

clear sunny days during the third active growth season (spring–May). Instantaneous net

carbon assimilation rate (A), at the leaf-level, stomatal conductance (gs) and intercellular

carbon concentration (Ci) were measured in the 2 years old oak saplings, simultaneously,

using a portable gas exchange measuring system, LiCor-6400XT equipped with a 6400-40

Leaf Chamber Fluorometer (Li-Cor Lincoln Nebraska USA). These measurements were

conducted parallel to the PPFD measurements. Measurements taken during gap hours were

performed at least 15 min after exposure to direct beam radiation. Two young fully

developed healthy leaves were measured in each session for each sapling. Each mea-

surement 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 sensor. A constant CO2 concentration of 380 ppm was set. Leaf-level

A to gs ratio was calculated for each sapling in each measurement session (six sessions in

total) as a measurement of intrinsic water use efficiency (WUE) while quantum efficiency

of photosynthetic electron transport through photosystem II (UPSII) was used as a mea-

surement of photochemical efficiency. Maximal fluorescence values of light-adapted

leaves (Fm’) were obtained by saturating the leaf using a multiphase flash (Loriaux et al.

2006). The first phase consisted of a 7,000-lmol pulse for 300 ms followed by a 30 %

ramp for 300 ms and a second saturating flash of 7,000 lmol for 300 ms. In order to follow

the dynamics of leaf-level gas exchange during transient exposure to direct beam radiation

(treatments: Shade?1 and Shade?3) an intensive campaign was carried out taking mea-

surements of A, gs and Ci during the first hour following exposure at 15 min intervals. To

account for possible confounding microclimate effects, air temperature and relative

humidity were monitored continuously (day and night) inside and outside (reference area)

the net-houses. Day air temperatures and relative humidity were not affected by the net-

house treatments whereas night temperatures were slightly higher (up to 1�C) and the

relative humidity slightly lower (up to 5 %) in the net-houses than in the reference area.

Growth and morphology

In order to determine their growth all of the oak saplings were harvested 2.5 years after

germination (three growth seasons) and their above-ground dry weight was measured. Dry

weight was measured following 48 h of oven drying (60 �C). Canopy height to dry weight

ratio was used as a measure for above ground biomass allocation and specific leaf area

(SLA) and leaf chlorophyll content as leaf traits representing light-related acclimation. In

order to determine specific leaf area, 10 leaves were randomly sampled from each sapling

and photographed alongside a reference area of a known size. Leaf area to reference area

ratio was determined using Photoshop software and the real leaf area was calculated.

New Forests

123

Leaves were then oven dried and their dry weight was measured. Chlorophyll content was

measured via the soil plant analysis development (SPAD) value for each sapling in four

fully developed young healthy leaves using a chlorophyll meter (Minolta Spad-502, see

Markwell et al. 1995).

Oak water status

Oak water status was assessed by means of predawn twig water potential and midday stem

water potential measurements. These measurements were performed using a pressure

chamber (PMS Instrument Company, Oregon, USA). For each individual, three twigs

carrying fully developed healthy young leaves were measured. Twigs measured at midday

were sealed 2 hours prior to measurement in a plastic bag covered by aluminum foil to

allow balance with stem water potential and provide better assessment of the water status at

the whole plant level (Naor 2000). Water status measurements were conducted in three out

of the four treatments—Unshaded, Shade?3 and Shade.

Statistical analysis

One-way analysis of variance (ANOVA) was used to analyze variation among gap treatments

in oak growth, biomass allocation and leaf traits. Repeated measures two-way ANOVAs were

used to analyze the variation in PPFD, A, gs, Ci, UPSII, WUE and water status with respect to

the different gap treatments (Unshaded, Shade?3, Shade?1 and Shade) and time of day.

Assumptions for ANOVA were tested through the Levene and Bartlett tests for homogeneity

of variances and the Shapiro–Wilk test for normal distribution of error. Mathematical

transformations of data were used when necessary to correct deviations from normality and/

or homogeneity of variances. For post hoc comparisons the Tukey–Kramer test was used.

Results

PPFD

Photosynthetic photon flux density varied among the gap treatments and times of day in

accordance to the applied gap manipulation. In the Unshaded treatment it ranged during the

day between ca. 500 (7:00 am) to ca. 1,800 lmol photon m-2 s-1 (11:00 am–2:00 pm). In

the Shade?3 and Shade?1 treatments, during gap-hours (11:00 am–2:00 pm, and

11:00 am–12:00 pm, respectively), it was similar to the Unshaded treatment while during

no-gap-hours it was similar though slightly higher than the continuously shaded treatment

(Shade) (Fig. 1a; Table 1). Calculated integrated daily total PPFD (i.e. interpolation of

PPFD measurements taken every 2 h from 7:00 am to 5:00 pm) in the Shade?3, Shade?1

and Shade treatments was 44, 20 and 6 %, respectively, that of the Unshaded treatment.

PPFD during gap-hours accounted for 63 and 86 % of the integrated daily total PPFD in

the Shade?1 and Shade?3 treatments, respectively.

Growth and morphology

Above ground dry weight of 2.5 years old oak saplings was significantly different among

all gap treatments. In the Shade?3, Shade?1 and Shade treatments it was only 8, 2.5 and

New Forests

123

0.8 % that of the Unshaded control (Fig. 2a). Thus, oak above ground dry weight was

significantly positively affected by increasing duration of daily exposure to direct beam

radiation. The effect of gap treatments on above-ground biomass allocation as represented

through height to dry weight ratio was also highly significant with oaks in the Shade?3,

Shade?1 and Shade treatments exhibiting 20-fold, tenfold and fivefold greater height to

biomass ratio, respectively, compared to the Unshaded control (Fig. 2b). Similarly to

biomass allocation, SLA decreased significantly with increasing daily exposure to direct

beam radiation (Fig. 2c). Leaf chlorophyll content, however, was found to be less affected,

A (

µm

ol C

O2 m

-2 s

-1)

Ci (

pp

m)

ΦP

SII

Daily hourDaily hour

WU

E (

µm

ol C

O2 m

ol H

2O-1

)

0

5

10

15

20

25(b) Shade Shade+1

Shade+3 Unshaded

0

0.2

0.4

0.6

0.8

7:00 9:00 11:00 13:00 15:00 17:00

(e)

0

20

40

60

80

07:00 09:00 11:00 13:00 15:00 17:00

(f)

0

0.1

0.2

0.3

0.4(c)

0

100

200

300

400(d)

0

500

1000

1500

2000(a)

PP

FD

(µ

mo

l ph

oto

n m

-2 s

-1)

gs

(mo

l H2O

m-2

s-1

)

Fig. 1 Daily courses of a instantaneous photosynthetic photon flux density (PPFD) and of: b instantaneousnet carbon assimilation rate (A), c stomatal conductance (gs), d inter cellular carbon concentration (Ci),e quantum efficiency of photosystem II (UPSII) and, f intrinsic water use efficiency (WUE) of Quercusithaburensis saplings (2 years old) under constant shading (Shade), 1 h gap (11:00 am–12:00 pm,Shade?1), 3 h gap (11:00 am–2:00 pm, Shade?3) and control (Unshaded)

New Forests

123

with the Unshaded control differing significantly from the Shade?1 and Shade treatments

only (Fig. 2d).

Ecophysiology

There was considerable variation in A among treatments and hours of day including a

significant Treatment 9 Time interaction. The pattern of variation in A was generally

associated with the variation in instantaneous PPFD (Fig. 1b; Table 1). However, signif-

icant differences were observed among treatments during gap-hours while exposed to

saturating PPFD of similar level (ca.1,800 lmol photon m-2 s-1). During the first gap

hour under exposure to direct beam radiation, average A measured in the Shade?3 and

Shade?1 treatments was 85 and 36 % that measured in the Unshaded oaks, respectively

(Fig. 1b). At ca. 1:00 pm, still under direct beam radiation, A measured in the Shade?3

oaks was 68 % that measured in the Unshaded ones. Post-hoc comparisons revealed that

A during gap hours was significantly (P \ 0.05) lower in the Shade?1 (b) treatment than in

the Shade?3 (a) and the Unshaded (a) treatments among which no significant difference

was found (Table 2). When considering the variation in SLA among these treatments,

however, it became evident that the pattern of inter-treatment variation in net carbon

assimilation on leaf mass bases was different. Calculation of carbon assimilation rates on

Table 1 Two-way ANOVAs of the effect of gap treatments—constant shading (Shade), shading?1 h gap(11:00 am–12:00 pm, Shade?1), shading?3 h gap (11:00 am–2:00 pm, Shade?3) and control (Unsha-ded)—and times of day (7:00 am–5:00 pm) on instantaneous photosynthetic photon flux density (PPFD), netcarbon assimilation rate (A), stomatal conductance (gs), inter cellular carbon concentration (Ci), intrinsicwater use efficiency (WUE) and quantum efficiency of photosystem II (UPSII) of Quercus ithaburensissaplings (2 years old)

Variable df F P1

(a) PPFD Treatment 3 316.09 ****

Time 5 164.73 ****

R2 = 0.951 Treatment 9 Time 15 25.36 ****

(b) A Treatment 3 31.25 ****

Time 5 30.47 ****

R2 = 0.865 Treatment 9 Time 15 3.88 ****

(c) gs Treatment 3 25.15 ****

Time 5 20.16 ****

R2 = 0.872 Treatment 9 Time 15 4.62 ****

(d) Ci Treatment 3 63.38 ****

Time 5 30.29 ****

R2 = 0.777 Treatment 9 Time 15 4.16 ****

(e) WUE Treatment 3 47.96 ****

Time 5 21.18 ****

R2 = 0.737 Treatment 9 Time 15 3.86 ****

(f) : UPSII Treatment 3 49.05 ****

Time 5 125.69 ****

R2 = 0.923 Treatment 9 Time 15 29.89 ****

R2 values represent the ratio of explained variation by the whole model1 **** P \ 0.0001

New Forests

123

leaf mass bases revealed that in the Shade?3 oaks it was 15 % higher than in the Unshaded

oaks, while in the Shade?1 oaks it was still 37 % lower than in the Unshaded ones. In

Unshaded oaks gs varied during the day between 0.20 and 0.31 mol H2O m-2 s-1. The

variation among treatments and hours of day in gs followed the pattern observed for

A (Fig. 1c; Table 1). Post-hoc comparisons revealed that during gap hours gs was sig-

nificantly different among the Unshaded (a) Shade?3 (b) and Shade?1 (c) treatments

(Table 2). The Ci varied significantly among treatment and daily time with a significant

Treatment 9 Time interaction (Table 1). Lower Ci levels were generally associated with

higher instantaneous PPFD (Fig. 1d). Differently than A and gs, during gap-hours Ci was

similar among the Shade?1, Shade?3 and Unshaded treatments (Table 2). Similarly to Ci,

lower quantum efficiency of photosynthetic electron transport through photosystem II

(UPSII) was also associated with higher instantaneous PPFD (Fig. 1e). However, during

gap-hours, under similar PPFD UPSII was lowest in the Shade?1 (c) treatment followed

by Shade?3 (b) and highest in the Unshaded treatment (a) (Table 2). The intensive

measurements campaign, monitoring A, gs,Ci and WUE during 1 h since exposure in

15 min intervals, showed that 15 min at the most were required for both the gap treatments

to enrich their maximal A and stabilize (Fig. 3a; Table 3). Maximal A in the Shade?1 was

nearly half that in the Shade?3 and gs followed the same pattern described for A (Fig. 3b;

Table 3). The Ci decreased gradually with time while WUE increased gradually with no

significant difference found between the Shade?1 and Shade?3 treatments for both

parameters (Fig. 3c, d; Table 3). Looking beyond gap hours revealed that in both gap

a

ab

b

c0

1

2

3(b)

aa

abb

0

10

20

30

40

50

Shade Shade+1 Shade+3 Unshaded

(d)

d

c

b

a

1

10

100

1,000

10,000(a)

SP

AD

val

ue

Hei

gh

t to

dry

wei

gh

t (c

m g

-1)

Dry

wei

gh

t (g

)S

LA

(cm

2 g-1

)

cb

ab

a

0

50

100

150

200

Shade Shade+1 Shade+3 Unshaded

(c)

Fig. 2 The effect of gap treatments—constant shading, 1 h gap (11:00 am–12:00 pm, Shade?1), 3 h gap(11:00 am–2:00 pm, Shade?3) and control (Unshaded) on: a above ground dry weight (R2 = 0.9787,P \ 0.0001), b height to dry weight ratio (R2 = 0.948, P \ 0.0001), c specific leaf area (SLA, R2 = 0.891,P \ 0.0001) and d SPAD value (leaf chlorophyll content, R2 = 0.342, P \ 0.0001) of 2 years old Quercusithaburensis saplings

New Forests

123

treatments Ci as well as UPSII returned to pre-exposure values shortly after the oaks have

gone back into shade (Fig. 1d, e).

Water relations

Predawn twig water potential was high and similar among the gap treatments (Fig. 4).

However, midday stem water potential was significantly different among the treatments. It

decreased substantially with increasing daily exposure to direct beam radiation and asso-

ciated increase in stomatal conductance. The relatively strong decrease in stem water

potential observed in the Unshaded treatment during midday was not associated with

stomatal closure indicating no water stress (gs [ 0.3 mol H2O m-2 s-1, Flexas and

Medrano 2002). WUE followed the general daily pattern of PPFD. Accordingly, during

gap hours it was similar among the Shade?1, Shade?3 and Unshaded treatments (Fig. 1f;

Table 2).

Discussion

This research investigated the effect of small-scale overstory gaps (i.e. transient exposure

to direct beam radiation) on the Photosynthetic performance and growth (i.e. function) of

understory Q. ithaburensis saplings. The capacity of understory plants to utilize transient

exposure to direct beam radiation was previously shown to depend on the timing and

duration of exposure, making the relationship between gap size and oak function less

obvious (Volkova et al. 2009). The experimental setup presented in this study enabled an

examination of the extent to which oak saplings growing in the forest understory are able to

utilize small scale overstory gaps for enhanced growth. Additionally, it enabled an

investigation of the way by which oaks growing under different gap regimes acclimate to

the light conditions and assessment of the extent to which this acclimation determine oak

function. Looking at the general patterns of gas exchange throughout the entire experi-

mental setup higher A and gs levels and better WUE (A/gs) were found to be associated

with increased PPFD. The observed positive A to PPFD relationship indicates the inherent

capacity of Q. ithaburensis saplings to utilize increasing light availability throughout the

entire studied light availability range. In the absence of water limitation gs increased with

increasing light availability though this increase was controlled such that the increase in

instantaneous PPFD was associated with increasing WUE. Thus, oak saplings responded

positively to increasing light availability through increased A and better WUE. Corre-

spondingly, oak sapling growth (above ground size) was found to be positively affected by

increasing light availability and increased significantly with increasing duration of daily

exposure to direct beam radiation. This has resulted in oaks exposed to 1 and 3 h gaps

(daily PPFD = 20 and 44 % that of the Unshaded control, respectively) being threefold

and tenfold larger, respectively, compared to continuously shaded oaks (daily

PPFD = 6 %) but still 40-fold and 12-fold smaller, respectively, compared to Unshaded

oaks (daily PPFD = 100 %). The presented variations in leaf-level gas exchange and oak

size highlight Q. ithaburensis as a light demanding species (Sack 2004) and are in line with

a previous field observation of ours, in which the carbon assimilation rate, water use

efficiency, and size of Q. ithaburensis trees growing in the understory of pine plantations

were found strongly related to light availability as determined by the level of overstory

light interception (Cooper et al. 2014). Similarly to our findings Rodrıguez-Calcerrada

New Forests

123

et al. (2007) and Prevosto et al. (2011) reported enhanced growth of different Mediter-

ranean oak species with increased light availability in the understory of forest stands.

Addressing the question of acclimation, we compared the leaf-level ecophysiology

during exposure to direct beam radiation (gap) among oaks growing under the different gap

treatments. Despite similar instantaneous PPFD (ca. 1,800 lmol photon m-2 s-1),

A measured in the Shade?1 oaks was less than half that of the Shade?3 oaks and nearly

one-third that of the Unshaded oaks (6.67, 14.13 and 18.51 lmol CO2 m-2 s-1, respec-

tively). Thus, decreasing duration of daily exposure to direct beam radiation was associated

with reduced ability to utilize saturating radiation levels. Looking at the gs values, it may

have been inferred that the described inter-treatment variation in light utilization was the

outcome of stomatal limitation (Flexas and Medrano 2002; Gulıas et al. 2012). However,

this possibility was not supported by corresponding inter treatment variation in Ci levels

(i.e. lower Ci with lower gs, Cornic 2000; Flexas and Medrano 2002). Additionally, UPSII

during gap-hours was found significantly lower in the oak saplings growing under limited

daily exposure to direct beam radiation. These patterns may be the outcome of a metabolic

limitation (Teskey and Shrestha 1985). Yet, the possibility of stomatal constraints should

not be rejected. Interestingly, in both gap treatments UPSII returned to pre-exposure values

shortly after oaks have gone back into shade. This may indicate the development of

photoprotective mechanisms (Munne-Bosch and Alegre 2000). Our results are in line with

the photosynthetic tradeoff hypothesis, according to which a tradeoff exists between

photosynthetic performances at high versus low light availability (Wayne and Bazzaz

Table 2 Post-hoc comparisons between gap treatments—shading?1 h gap (11:00 am–12:00 pm,Shade?1), shading?3 h gap (11:00 am–2:00 pm, Shade?3) and Unshaded control, comparing net carbonassimilation rate (A), stomatal conductance (gs), inter cellular carbon concentration (Ci), intrinsic water useefficiency (WUE) and quantum efficiency of photosystem II (UPSII) of Quercus ithaburensis saplings(2 years old) during gap hours

Parameter Treatment Post-hoc (P \ 0.05)

(a) PPFD Unshaded a

Shaded?3 a

Shaded?1 a

(b) A Unshaded a

Shaded?3 a

Shaded?1 b

(c) gs Unshaded a

Shaded?3 b

Shaded?1 c

(d) Ci Unshaded a

Shaded?3 a

Shaded?1 a

(e) WUE Unshaded a

Shaded?3 a

Shaded?1 a

(f) UPSII Unshaded a

Shaded?3 b

Shaded?1 c

New Forests

123

A (

µm

ol C

O2 m

-2 s

-1)

gs

(mo

l H2O

m-2

s-1

)

Ci (

pp

m)

Time since exposure (h:min)

0

5

10

15

20(a)

0

0.05

0.1

0.15

0.2

0.25shade+3

shade+1

(b)

0

50

100

150

200

250

300

350

0:00 0:15 0:30 0:45 1:00

(c)

0

20

40

60

80

0:00 0:15 0:30 0:45 1:00

(d)

Time since exposure (h:min)

WU

E (

µm

ol C

O2 m

ol H

2O-1

)

Fig. 3 The effect of gap treatments—1 h gap (11:00 am–12:00 pm, Shade?1) and 3 h gap (11:00 am–2:00 pm, Shade?3)—and time since the beginning of gap (15 min. intervals up to 1 h) on: a instantaneousnet carbon assimilation rate (A), b stomatal conductance (gs) and c inter-cellular carbon concentration (Ci)of Quercus ithaburensis saplings (2 years old)

Table 3 Two-way ANOVAs of the effect of gap treatments—1 h gap (11:00 am–12:00 pm, Shade?1) and3 h gap (11:00 am–2:00 pm, Shade?3)—and time since the beginning of gap (15 min intervals up to 1 h)on instantaneous net carbon assimilation rate (A), stomatal conductance (gs), inter-cellular carbon con-centration (Ci) and intrinsic water use efficiency (WUE) of Quercus ithaburensis saplings (2 years old)

Variable F P1

(a) A Treatment 19.96 ****

Time 14.41 ***

R2 = 0.542 Treatment 9 Time 0.118 n.s

(b) gs Treatment 33.81 ****

Time 5.28 *

R2 = 0.565 Treatment 9 Time 0.26 n.s

(c) Ci Treatment 0.192 n.s

Time 12.82 **

R2 = 0.303 Treatment 9 Time 0.183 n.s

(d) WUE Treatment 0.03 n.s

Time 9.27 **

R2 = 0.236 Treatment 9 Time 0.157 n.s

1 * P \ 0.05, ** P \ 0.01 *** P \ 0.001, **** P \ 0.0001

New Forests

123

1993) due to differences in photosynthetic acclimation under contrasting daily light

regime. Correspondingly, decreasing gap duration (i.e. daily exposure to direct beam

radiation) is expected to be associated with reduced capacity of utilizing high PPFD levels.

Oak saplings growing under the different gap regimes differed significantly in traits

representing light related acclimation. However, the extent of variation differed among

traits, with canopy height to dry weight ratio showing the most pronounced variation while

chlorophyll content was only slightly affected. Higher canopy height to dry weight ratio is

known to represent a shade avoidance strategy (Monnier et al. 2013) though it may also

account for increased efficiency of light interception at the whole plant level (Givnish

1988). Light related phenotypic plasticity in SLA and chlorophyll content are also well-

known, both accounting for the potential rate of light utilization at the leaf-level (Puertolas

et al. 2008; Mallik et al. 2012; Guo et al. 2013). As mentioned earlier, the ability to utilize

saturating radiation levels as measured through A during gap-hours was significantly

reduced in oaks under decreasing gap size; that is, it was 85 and 36 % that of the Unshaded

oaks in the Shade?3 and Shade?1 treatments respectively. However, when considering

the variation in SLA among the gap treatments a different pattern emerged in which the

light utilization on leaf mass bases was higher by 15 % in the Shade?3 oaks than in the

unshaded ones, though it was still lower by 37 % in the Shade?1 oaks compared to the

Unshaded control. SLA plasticity is commonly thought to represent a tradeoff between the

investment in light utilization ability versus drought resistance (Knight and Ackerly 2003;

Ramırez-Valiente et al. 2010).

The results of this work have led us to the following conclusions:

• Quercus ithaburensis is a light-demanding species, vigorously increasing its growth

with increased duration of daily exposure to direct beam radiation.

• Oaks growing under different gap durations adjust through phenotypic plasticity in leaf

traits and biomass partitioning.

• Oaks receiving shorter daily exposure to direct beam radiation exhibit reduced capacity

of utilizing saturating radiation levels while oaks receiving prolonged exposure reveal a

synergistic effect combining higher availability of saturating radiation levels with a

better capacity of utilizing this radiation.

• A significant difference in the capacity to utilize saturating radiation levels develops

within the range of 1 h (irradiance = 20 %) to 3 h (irradiance = 44 %) daily exposure

a

aa

b

a

c-1.6

-1.2

-0.8

-0.4

0Predawn Midday

Shade

Shade+3

UnshadedT

wig

wat

er p

ote

nti

al (

MP

a)

Fig. 4 The effect of gaptreatments—constant shading(Shade), 3 h gap (11:00 am–2:00 pm, Shade?3) and control(Unshaded) on predawn andmidday twig water potential in2 years old Quercus ithaburensissaplings. R2 = 0.91, P \ 0.0001

New Forests

123

determining whether a leaf would develop into a ‘‘shade adopted leaf’’ or a ‘‘sun

adopted leaf’’.

In this study we focused on the effects of overstory gaps on understory oak function

through light regime, purely, leaving aside water related limitations. In a previous

observational field study on Q. ithaburensis trees growing in the understory of pine

plantations, we have shown the critical importance of water availability which varies

strongly both daily and seasonally (Cooper et al. 2014). However, spatial variation in light

availability in the forest understory was still found as the most important factor explaining

the variation in oak photosynthetic performance and growth. Integrating our understand-

ings from the current work with those of our previous observation, we propose that

overstory gaps exposing regenerated Q. ithaburensis saplings to direct beam radiation for a

few hours during morning time (7:00–11:00), in the spring season (April–May), is likely to

prove efficient in promoting oak growth in the understory of pine plantations. However, the

prescription of gap treatments optimizing understory oak growth and resource use effi-

ciency, on the one hand, while minimizing the impact on exiting pine canopy, on the other

hand, still requires further field investigation.

Acknowledgments Special thanks to: Jaime Kigel, Rinat Ovadia, Hedva and Max Cooper for theirvaluable assistance in this work. We thank: Asaf Tzur, Nitai Zeharia, Nurit Hibsher, Tom Fogel and EitanBney-Moshe for their help in the field measurements. The study was funded by The Israeli Forest Service(KKL).

References

Cooper A, Shapira O, Zaidan S, Moshe Y, Zangy E, Osem Y (2014) Oak restoration in water limited pineplantations: interactive effects of overstory light interception and water availability on understory oakperformance. Eur J For Res. doi:10.1007/s10342-014-0794-6

Cornic G (2000) Drought stress inhibits photosynthesis by decreasing stomatal aperture: not by affectingATP synthesis. Trends Plant Sci 5:187–188

Dey DC, Gardiner ES, Schweitzer CJ, Kabrick JM, Jacobs DF (2012) Underplanting to sustain futurestocking of oak (Quercus) in temperate deciduous forests. New For 43:955–978

Dufour-Dror JM, Ertas A (2004) Bioclimatic perspectives in the distribution of Quercus ithaburensis Decne.subspecies in Turkey and in the Levant. J Biogeogr 31:461–474

Flexas J, Medrano H (2002) Drought-inhibition of photosynthesis in C3 plants: stomatal and non-stomatallimitations revisited. Ann Bot 89:183–189

Gaulton R, Malthus TJ (2010) LiDAR mapping of canopy gaps in continuous cover forests: a comparison ofcanopy height model and point cloud based techniques. Int J Remote Sens 31:1193–1211

Givnish TJ (1988) Adaptation to sun and shade: a whole-plant perspective. Aust J Plant Physiol 15:63–92Grassi G, Minotta G, Tonon G, Bagnaresi U (2004) Dynamics of Norway spruce and silver fir natural

regeneration in a mixed stand under uneven-aged management. Can J For Res 34:141–149Grunzweig JM, Carmel Y, Sever N, McCreary DM, Flather CH (2008) Growth, resource storage, and

adaptation to drought in California and eastern Mediterranean oak seedlings. Can J For Res38:331–342

Gulıas J, Seddaiu G, Cifre J, Salis M, Ledda L (2012) Leaf and plant water use efficiency in cocksfoot andtall fescue accessions under differing soil water availability. Crop Sci 52:2321–2331

Guo X, Guo W, Luo Y, Tan X, Du N, Wang R (2013) Morphological and biomass characteristic acclimationof trident maple (Acer buergerianum Miq.) in response to light and water stress. Acta Physiol Plant35:1149–1159

Humbert L, Gagnon D, Kneeshaw D, Messier C (2007) A shade tolerance index for common understoryspecies of northeastern North America. Ecol Ind 7:195–207

Knight CA, Ackerly DD (2003) Evolution and plasticity of photosynthetic thermal tolerance, specific leafarea and leaf size: congeneric species from desert and coastal environments. New Phytol 160:337–347

Leakey ADB, Press MC, Scholes JD (2003) Patterns of dynamic irradiance affect the photosyntheticcapacity and growth of dipterocarp tree seedlings. Oecologia 135:184–193

New Forests

123

Lhotka JM (2013) Effect of gap size on mid-rotation stand structure and species composition in a naturallyregenerated mixed broadleaf forest. New Forest 44:311–325

Lieffers VJ, Messier C, Stadt KJ, Gendron F, Comeau PG (1999) Predicting and managing light in theunderstory of boreal forests. Can J For Res 29:796–811

Loriaux SD, Burns RA, Welles JM, McDermitt DK, Genty B (2006) Determination of maximal chlorophyllfluorescence using a multiphase single flash of sub-saturating intensity. American Society of PlantBiologists Annual Meeting, Boston MA, poster P13011. August 2006 http://abstracts.aspb.org/pb2006/public/P13/P13011.html

Maestre FT, Cortina J (2004) Are Pinus halepensis plantations useful as a restoration tool in semiaridMediterranean areas? For Ecol Manage 198:303–317

Maestre FT, Cortina J, Bautista S, Bellot J (2003) Does pinus halepensis facilitate the establishment ofshrubs under semiarid climate? For Ecol Manage 176:147–160

Mallik AU, Wang JR, Siegwart-Collier LS, Roberts BA (2012) Morphological and ecophysiologicalresponses of sheep laurel (Kalmia angustifolia L.) to shade. Forestry 85:513–522

Markwell J, Osterman JC, Mitchell JL (1995) Calibration of the Minolta SPAD-502 leaf chlorophyll meter.Photosynth Res 46:467–472

Monnier Y, Bousquet-Melou A, Vila B, Prevosto B, Fernandez C (2013) How nutrient availability influ-ences acclimation to shade of two (pioneer and late-successional) Mediterranean tree species? Eur JFor Res 132:325–333

Morrissey RC, Jacobs DF, Davis AS, Rathfon RA (2010) Survival and competitiveness of Quercus ru-bra regeneration associated with planting stocktype and harvest opening intensity. New For40:273–287

Munne-Bosch S, Alegre L (2000) The xanthophyll cycle is induced by light irrespective of water status infield-grown lavender (Lavandula stoechas) plants. Physiol Plant 108:147–151

Naor A (2000) Midday stem water potential as a plant water stress indicator for irrigation scheduling in fruittrees. Acta Hortic 537:447–454

Niinemets U, Valladares F (2006) Tolerance to shade, drought and waterlogging of temperate, Northernhemisphere trees and shrubs. Ecol Monogr 76:521–547

Osem Y, Ginsberg P, Tauber I, Atzmon N, Perevolotsky A (2008) Sustainable management of Mediter-ranean planted coniferous forests: an Israeli definition. J For 106:38–46

Osem Y, Zangy E, Bney-Moshe E, Moshe Y, Karni N, Nisan Y (2009) The potential of transforming simplestructured pine plantations into mixed Mediterranean forests through natural regeneration along arainfall gradient. For Ecol Manage 259:14–23

Prevosto B, Monnier Y, Ripert C, Fernandez C (2011) Can we use shelterwoods in Mediterranean pineforests to promote oak seedling development? For Ecol Manage 262:1426–1433

Puertolas J, Pardos M, Jimenez MD, Aranda I, Pardos JA (2008) Interactive responses of Quercus suber L.seedlings to light and mild water stress: effects on morphology and gas exchange traits. Ann For Sci65:611

Ramırez-Valiente JA, Sanchez-Gomez D, Aranda I, Valladares F (2010) Phenotypic plasticity and localadaptation in leaf ecophysiological traits of 13 contrasting cork oak populations under different wateravailabilities. Tree Physiol 30:618–627

Ravikovitch S (1992) The soils of Israel: formation, nature and properties. Hakibbuts Hamehuchad Publi-cation House, Israel

Rodrıguez-Calcerrada J, Pardos JA, Gil L, Aranda I (2007) Acclimation to light in seedlings of Quercuspetraea (Mattuschka) Liebl. and Quercus pyrenaica Willd. planted along a forest-edge gradient. Trees21:45–54

Ruiz-Benito P, Gomez-Aparicio L, Zavala MA (2012) Large-scale assessment of regeneration and diversityin Mediterranean planted pine forests along ecological gradients. Divers Distrib 18:1092–1106

Sabate S, Gracia CA, Sanchez A (2002) Likely effects of climate change on growth of Quercus ilex, Pinushalepensis, Pinus pinaster, Pinus sylvestris and Fagus sylvatica forests in the Mediterranean region.For Ecol Manage 162:23–37

Sack L (2004) Responses of temperate woody seedlings to shade and drought: do trade-offs limit potentialniche differentiation? Oikos 107:110–127

Sheffer E (2012) A review of the development of Mediterranean pine-oak ecosystems after land aban-donment and afforestation: are they novel ecosystems? Ann For Sci 69:429–443

Smith T, Huston M (1989) A theory of the spatial and temporal dynamics of plant communities. Vegetatio83:49–69

Spies TA, Franklin JF, Klopsch M (1990) Canopy gaps in douglas-fir forests of the cascade mountains. CanJ Forest Res 20:649–658

New Forests

123

Teskey RO, Shrestha RB (1985) Relationship between carbon dioxide, photosynthetic efficiency and shadetolerance. Physiol Plant 63:126–132

Volkova L, Bennett LT, Tausz M (2009) Effects of sudden exposure to high light levels on two tree fernspecies Dicksonia antarctica (Dicksoniaceae) and Cyathea australis (Cyatheaceae) acclimated todifferent light intensities. Aust J Bot 57:562–571

Wayne PM, Bazzaz FA (1993) Birch seedling responses to daily time courses of light in experimental forestgaps and shade-houses. Ecology 74:1500–1515

White PS, MacKenzie MD, Busing RT (1985) Natural disturbance and gap phase dynamics in southernAppalachian spruce-fir forests. Can J Forest Res 15:233–240

Zohary M (1961) On the oak species of Middle East. Bull Res Counc Isr Sect D Bot 4:161–186

New Forests

123