Ecophysiological Competence of Populus alba L., Fraxinus angustifolia Vahl., and Crataegus monogyna Jacq. Used in Plantations for the Recovery of Riparian Vegetation

Ecophysiological Competence of Populus alba L., Fraxinusangustifolia Vahl., and Crataegus monogyna Jacq. Used inPlantations for the Recovery of Riparian Vegetation

Jose A. Manzanera Æ Maria F. Martınez-Chacon

Published online: 12 September 2007

� Springer Science+Business Media, LLC 2007

Abstract In many semi-arid environments of Mediterra-

nean ecosystems, white poplar (Populus alba L.) is the

dominant riparian tree and has been used to recover

degraded areas, together with other native species, such as

ash (Fraxinus angustifolia Vahl.) and hawthorn (Crataegus

monogyna Jacq.). We addressed three main objectives: (1)

to gain an improved understanding of some specific rela-

tionships between environmental parameters and leaf-level

physiological factors in these riparian forest species, (2) to

compare the leaf-level physiology of these riparian species

to each other, and (3) to compare leaf-level responses

within native riparian plots to adjacent restoration plots, in

order to evaluate the competence of the plants used for the

recovery of those degraded areas. We found significant

differences in physiological performance between mature

and young white poplars in the natural stand and among

planted species. The net assimilation and transpiration

rates, diameter, and height of white poplar plants were

superior to those of ash and hawthorn. Ash and hawthorn

showed higher water use efficiency than white poplar.

White poplar also showed higher levels of stomatal con-

ductance, behaving as a fast-growing, water-consuming

species with a more active gas exchange and ecophysio-

logical competence than the other species used for

restoration purposes. In the restoration zones, the planted

white poplars had higher rates of net assimilation and water

use efficiency than the mature trees in the natural stand. We

propose the use of white poplar for the rapid restoration of

riparian vegetation in semi-arid Mediterranean environ-

ments. Ash and hawthorn can also play a role as

accompanying species for the purpose of biodiversity.

Keywords Floodplain vegetation � Gas exchange �Hawthorn � Narrow-leaf ash � White poplar

Introduction

Some attention has been given to how floodplain tree

species are physiologically adapted to tolerate periodic

flooding (Pereira and Kozlowski 1977), but there has been

comparatively little research on the physiological differ-

ences between tree species in riparian areas (Horton and

others 2001a,b). It has been suggested that floodplain trees

maintain high-carbon assimilation and growth rates under

conditions that cause drought-induced growth reduction in

upland trees (Foster 1992, Hart and Disalvo 2005). Nev-

ertheless, because of their phreatophytic nature, many

riparian trees are thought to lack physiological adaptations

to drought. In many semi-arid Mediterranean-climate

regions, riparian ecosystems receive irregular annual pre-

cipitations and may suffer from streamflow variations;

therefore, some riparian species may be more water-stres-

sed in these conditions than those from mesic ecosystems

(Smith and others 1998). Snyder and Williams (2000)

observed that transpiration by riparian vegetation from

semi-arid regions depended on the species–environment

interaction. In cottonwood (Populus fremontii Wats.), the

maximum transpiration rates occurred when temperature

and vapor pressure deficit were highest, but transpiration

J. A. Manzanera (&)

Technical University of Madrid (UPM), Research Group for

Sustainable Management, E.T.S.I. Montes, Ciudad Universitaria

s.n., 28040 Madrid, Spain

e-mail: [email protected]

M. F. Martınez-Chacon

Instituto Madrileno de Investigacion y Desarrollo Rural Agrario

(IMIDRA), Carretera Nacional 2, Km 38, 28800 Alcala de

Henares, Madrid, Spain

123

Environmental Management (2007) 40:902–912

DOI 10.1007/s00267-007-9016-z

decreased in parallel with the radiation input on cloudy

days, while the behavior of willow (Salix goodingii Ball)

was slightly different (Schaeffer and others 2000). These

results suggest the relationship between leaf-level physi-

ology of floodplain tree species and environmental factors,

such as light and vapor pressure gradient, influence their

ecological role in riparian areas. Leaf-level gas exchange

parameters vary among species and can therefore be used

as indicators of the floodplain species response to changes

in the riparian ecosystem and as predictors of plant

behavior in restoration activities.

We hypothesize that gas exchange parameters at the

leaf level could be good indicators of the capacity of

acclimation of plantations with woody species for the

restoration of riparian areas. We therefore address three

main objectives: (1) to gain an improved understanding

of some specific relationships between environmental

parameters (e.g., photosynthetic photon flux density and

water vapor pressure gradient) and three key leaf-level

physiological factors, net assimilation, stomatal conduc-

tance to water vapor, and water use efficiency in riparian

forest species, (2) to compare leaf-level physiology of

three important riparian species to each other, and (3) to

compare leaf-level responses within native riparian plots

to adjacent restoration plots, as indicators of the eco-

physiological competence of woody species to restore the

natural vegetation of riparian forests under a Mediterra-

nean climate.

Materials and Methods

The study was conducted in a floodplain of the Henares

river, a government protected space near the industrialized

area of Alcala de Henares (Madrid, Spain), located at

40�020 N, 3�360 W and at 588 m elevation. Prior to the

establishment of the protected area, all vegetation was

cleared over 26 ha for the installation of quarries. Resto-

ration activities conducted in these disturbed areas included

the establishment of plantations of native species such as

white poplar (Populus alba L.), narrow-leaved ash (Frax-

inus angustifolia Vahl.), and hawthorn (Crataegus

monogyna Jacq.), a fast-growing, thorny deciduous native

shrub, tolerant of wet soils and frequently present along

water streams. Natural riparian forests have been preserved

close to these restored areas, consisting of mature white

poplar stands accompanied by elm (Ulmus minor Mill.) and

alternating with patches of natural regeneration dominated

by young white poplars. The soil is alluvial, well-drained,

with sandy-gravel subsoil derived from deposits from the

nearby river. Meteorological data were recorded in a pre-

viously established local weather station, located within the

study site. Mean annual precipitation was 800 mm and

mean annual temperature was 14� C for the 2-year period

from 2002–2003 (Fig. 1), with a broad range of daily

temperatures between –8.9� C and 39.7� C during the same

period.

The plantations were established in 1994 and 1999.

The study area was divided into three zones, corre-

sponding to a zone of natural vegetation (zone A),

consisting of alternating patches of both mature and

young white poplars, and two plantation zones, one

planted in 1994 (9-years old during the study, zone B)

and one planted in 1999 (4-years old during the study,

zone C). One 25 m · 25 m square plot was randomly

installed in each zone, and 10 plants of each species/type

(defined later) were selected within each plot for the

measurements. Plant establishment after planting was

guaranteed by supplemental water to each tree by drip

irrigation for 4 h every 2 weeks during the summer

months for the first 3 years after planting.

Gas exchange parameters were measured in natural

light, which ranged from 26 to 2640 lmol m–2 s–1 during

measurements, with a portable LCI (ADC Bioscientific

Ltd.) gas analyzer. These measurements were performed

on clear days on four fully developed leaves, each located

at the apex of four lateral branches, oriented north, south,

east, and west in the crown of each plant. Net assimilation

(A, lmol CO2 m–2 s–1), transpiration rate (E, mmol water

vapor m–2 s–1), stomatal conductance to water vapor (gs,

mmol water vapor m–2 s–1), and photosynthetic photon flux

Fig. 1 Mean temperature (T� C) and monthly precipitation (mm)

distributions for the study period (2002–2003) in the Henares

floodplain

Environmental Management (2007) 40:902–912 903

123

density (PPFD, lmol m–2 s–1) were recorded. Water use

efficiency (WUE, the ratio of A to E), intrinsic water use

efficiency (IWUE, the ratio of A to gs), and leaf -to-air

water vapor pressure gradient (VPG, kPa) were calculated

using the recorded data. Physiological measurements were

initiated 9 years after the first plantation was established,

during the period from August 2002 to August 2003. The

following experiments were designed (Table 1):

Experiment 1: Specific Relationships Between

Environmental Parameters and Leaf-Level

Physiological Factors

Daily Variation in Leaf Gas Exchange in Poplars in the

Natural Stand During Early Summer

During June and July 2003, two age classes (mature and

juvenile) of white poplars from the natural zone were

compared by recording gas exchange parameters, i.e., A, E,

and gs, in 10 mature and 10 young poplars every 2 h, in

four periods: from 8 to 10 h, from 10 to 12 h, from 12 to 14

h, and from 14 to 16 h, solar time, 1 day per month.

Seasonal Variation in Leaf Gas Exchange in Poplars in the

Natural Stand at Midday

Leaf gas exchange parameters (i.e., A, E, and gs) were

recorded at midday in monthly measurements taken from

both 10 mature and 10 young poplars in the natural zone, 1

day per month in August, September, and October 2002,

and in June and July 2003.

Experiment 2: Leaf-Level Physiology of White Poplar,

Ash, and Hawthorn

Comparison of Gas Exchange Characteristics Among

Species in Plantations During the Summer Period

In both plantations (zones B and C), white poplar, ash, and

hawthorn were compared by measuring leaf gas exchange

parameters, A, E, and gs, in 10 plants per species per zone

in four periods: from 8 to 10 h, from 10 to 12 h, from 12 to

14 h, and from 14 to 16 h, solar time, 1 day per month,

from June to August 2003.

Comparison of Annual Variations in Leaf Gas Exchange

Between Planted Species

The same leaf gas exchange parameters, A, E, and gs, were

recorded 1 day per month at midday in measurements taken

from the three species planted in both plantation zones, by

sampling from 6 plants (in August, September, and October

2002) to 10 plants (in June, July, and August 2003) per

species and zone.

Experiment 3: Leaf-level Responses Within Native

Riparian Plot Versus Adjacent Restoration Plots

Mature poplar trees from the natural zone (A) and poplar

plants from both plantation zones (B and C) were compared

to determine gas exchange measurements 1 day per month,

from June to August 2003. Ten plants per zone were mea-

sured in four periods per day: from 8 to 10 h, from 10 to 12 h,

from 12 to 14 h, and from 14 to 16 h, solar time.

Table 1 Experimental design of the present study and period of measurement of each experiment

Experiment August

2002

Sept.

2002

October

2002

June

2003

July

2003

August

2003

1: specific relationships between environmental

parameters and leaf-level physiology

1a: Daily variation in leaf gas exchange in

natural poplars during early summer

* *

1b: Seasonal variation in leaf gas exchange in

natural poplars at midday

* * * * *

2: leaf-level physiology of white poplar, ash, and hawthorn

2a: Gas-exchange characteristics among planted

species during summer period

* * *

2b: Annual variations in leaf gas exchange

between planted species

* * * * * *

3: leaf-level responses within native riparian

plot vs. adjacent restoration plots

* * *

904 Environmental Management (2007) 40:902–912

123

Statistical Analysis

For all mean comparisons, multifactorial ANOVA (Stat-

graphics Plus 5.1) was used with PPFD as a covariate to

adjust gas exchange characteristics to the same PPFD. This

parameter ranged from 26 to 2640 lmol m–2 s–1 in natural

conditions. The multiple range test of the least significant

difference (LSD) at the 0.05 level was used to discriminate

means. The ANOVA model is:

Yijkl ¼ l þ ai þ bj þ vk þ abij þ avik þ bvjk þ abvijk

þ dPPFDijkl þ eijkl

where Yijkl is the leaf gas exchange variable, l is the mean

of the experiment, ai is the species or plant type, bj is the

zone, vk is the time period (month or hour, depending on

the experiment), abij, avik, bvjk, and abvijk are the inter-

actions, d is the regression coefficient of the covariate, and

eijkl is the experiment error.

After statistical analysis, they were grouped into two

sunlit (east and south) and two shaded (north and west)

leaves per plant. Responses of leaf gas exchange were also

related to environmental variables (PPFD and VPG) by

boundary-line analysis, and regression models were fitted

to the higher part (top 1%) of the data (Chambers and

others 1985, Cheeseman and Lexa 1996). The model of

best fit was selected and the adjusted r2 statistic was cal-

culated for each model. Assimilation versus PPFD curves

of the planted species in June and July 2003 were fitted to

the rectangular hyperbola model for canopy carbon

assimilation (Landsberg and Gower 1997):

A ¼ Uc � PPFD � Amax

Uc � PPFD þ Amax

where the apparent maximum quantum efficiency (Uc) is

given by the initial slope of the A versus PPFD curve and

Amax is the photon-saturated assimilation rate. Conductance

to water vapor versus VPG curves of the planted species in

June and July 2003 were fitted to a polynomial regression

model.

Results




Daily Variation in Leaf Gas Exchange in Poplars in the

Natural Stand During Early Summer

A typical summer pattern of daily variation in the gas

exchange of white poplar is shown in Fig. 2. At dawn, no

data were recorded because there were no sunlit leaves, or

they were out of reach. Net assimilation reached the

maximum early in the morning and progressively des-

cended, showing midday depression (Fig. 2a). The same

behavior was observed for transpiration, conductance to

water vapor, and water use efficiency (Fig. 2b–d).

No significant differences in A were found between

young and mature poplars (p = 0.58). Both transpiration

Fig. 2 Daily variation in (a) net assimilation rate (A, lmol CO2 m–2

s–1), (b) transpiration (E, mmol m–2 s–1), (c) conductance of water

vapor (gs, mmol m–2 s–1), and (d) water use efficiency (WUE) in

mature white poplar trees (mature) and in young plants (young) of the

same species in the natural stand of the Henares river bank during

early summer (June and July 2003). Vertical bars denote 95% least

significant difference (LSD) intervals. Means of one treatment not

overlapped by the vertical bars of other treatments are statistically

different at the 0.05 level


123

and conductance were higher in the mature trees than in the

young regenerating poplars (p \ 0.001 for E and

p = 0.0002 for gs). In the afternoon (14 to 16 h), transpi-

ration of the mature trees dropped rapidly (Fig. 2b), as the

conductance reached its minimum value. In addition, WUE

and IWUE were greater in the young than in the mature

trees (p \ 0.001 for WUE and p = 0.0013 for IWUE).

Seasonal Variation in Leaf Gas Exchange in Poplars in the

Natural Stand at Midday

In the natural stand, the net assimilation rate of sunlit

leaves of poplars varied seasonally, increasing from June to

July, whereas the A rate of shaded leaves was relatively

constant throughout the year. Net assimilation diminished

in August and reached its maximum in September. In

October, assimilation dropped again prior to leaf fall

(Fig. 3a). In this experiment, mature trees showed greater

transpiration rates than regenerating plants in June and July

(p \ 0.05), whereas there were no significant differences in

August, September, and October (p [ 0.05; Fig. 3b).

Significant differences occurred in water vapor con-

ductance among poplar age groups, month period, and leaf

types, but not due to the interactions among these factors.

Young poplars showed lower conductance rates than

mature trees (p = 0.007). Conductance peaked in Septem-

ber and October (Fig. 3c).

Young poplars had greater WUE and IWUE than mature

trees (p = 0.002 for WUE and p = 0.0003 for IWUE). The

maximum WUE was obtained in September, whereas

IWUE was highest in June and July, and also in August for

the juvenile poplars (Fig. 3d).


Ash, and Hawthorn

Comparison of Gas Exchange Characteristics Among

Species in Plantations During the Summer Period

Survival rate of the plantations was high for all the species

used for the restoration of the Henares floodplain: 91.3% for

white poplar, 97.8% for ash, and 87% for hawthorn. White

poplar showed a higher growth in diameter and height than

ash and hawthorn (Table 2). White poplar plants in the

second plantation (1999, zone C) reached similar sizes to

those of ash plants established in 1994 (zone B). Differences

were found in net assimilation among the three species. A

was significantly higher for poplar trees in June and July

(p \ 0.05), whereas in August ash had higher A than the

others (p \ 0.05; Fig. 4a). The maximum net assimilation

rate was obtained in July for all species. The fitted

rectangular hyperbola model for canopy carbon assimilation

(Landsberg and Gower 1997) explained a high percentage of

variability in all three species (between 83.08 and 89.41%,

Table 3). Figure 5a shows typical A versus PPFD boundary-

line curves for all three species. Ash showed the highest

estimated Uc and Amax and hawthorn had the lowest esti-

mated values of both parameters (Table 3).

Transpiration rate increased as the summer advanced,

with differences among species. While poplar transpired

more in June than the other species (p \ 0.05), ash showed

a significantly higher transpiration rate in August

(p \ 0.05; Fig. 4b). The water vapor conductance of white

poplar was superior to that of the other species (p \ 0.001);

Fig. 3 Seasonal variation in (a) net assimilation rate (A, lmol CO2

m–2 s–1) in white poplar leaves exposed to sunlight (L) or shade (S),

and (b) transpiration (E, mmol m–2 s–1), (c) conductance to water

vapor (gs, mmol m–2 s–1), and (d) intrinsic water use efficiency

(IWUE) in mature trees and young regenerate of white poplar in the

natural stand, during the annual period from August 2002 to July

2003. Vertical bars denote 95% least significant difference (LSD)

intervals. Means of one treatment not overlapped by the vertical bars

of other treatments are statistically different at the 0.05 level


123

the trend for all species was a progressive increase from

June to July and stabilization from July to August (Fig. 4c).

Boundary-line analysis showed a good association between

gs and VPG (Fig. 5b), with r2 values between 87.38 and

94.55 % for the polynomial regression models of all three

species (Table 4). Statistically significant differences were

also found between the net assimilation rates of both

plantation zones. Four-year-old ash and hawthorn plants

(zone C) assimilated at a higher rate than nine-year-olds

(zone B; p \ 0.05). In contrast, there were no differences

between poplars between plantations (p [ 0.05; Fig. 4d).

Comparison of Annual Variations in Leaf Gas Exchange

Between Planted Species

Both ash and white poplar showed a higher assimilation

rate than hawthorn. This difference was significant in July,

August, and September (p \ 0.05), although not in June

and October (p [ 0.05; Fig. 6a). Poplar, ash, and hawthorn

showed similar A rates in August 2002 and August 2003

(Fig. 6a). However, the transpiration rate of all three spe-

cies was significantly greater in August 2003 than in

August 2002 (Fig. 6b). Transpiration reached its maximum

in August and July and was lower in September (Fig. 6b),

when poplar had the highest assimilation rate.

Differences between plants in the two restoration zones

were also found. Four-year-old ash and hawthorn plants

had higher assimilation (p \ 0.05; Fig. 7a), transpiration

(p \ 0.05; Fig. 7b), and conductance rates (p \ 0.05;

Fig. 7c) than 9-year-old plants. In the case of white poplar,

significant differences were found for carbon assimilation,

transpiration, and conductance, which were higher in the

group of older plants (p \ 0.05; Fig. 7a–c). Both ash and

hawthorn had higher WUE values than poplar, especially

for older plants (p \ 0.05). The same occurred for the

IWUE parameter (p \ 0.05; Fig. 7d).

Experiment 3: Leaf-Level Responses Within Native


Summer net assimilation and WUE in poplars was higher

in the plantations than in the natural stand (p \ 0.001;

Table 2 Mean diameter at breast height (1.3 m, dbh, cm ± standard

deviation) and mean tree height (m, ± standard deviation) of white

poplar (Populus alba), ash (Fraxinus angustifolia), and hawthorn

(Crataegus monogyna) in the natural stand (zone A), the 1994 plan-

tation (zone B), and the 1999 plantation (zone C) for the restoration of

the Henares floodplain

Zone Species Dbh (cm) Height (m)

A Mature Populus alba 35.8 ± 7.47 23.73 ± 4.29

A Juvenile Populus alba 6.05 ± 2.14 6.11 ± 1.90

B Populus alba 16.5 ± 5.21 a 9.17 ± 1.52 a

B Fraxinus angustifolia 7.9 ± 2.66 b 5.21 ± 0.77 b

B Crataegus monogyna 2.92 ± 0.74 c

C Populus alba 7.25 ± 1.44 b 4.91 ± 0.69 b

C Fraxinus angustifolia 3.20 ± 1.18 c 3.36 ± 0.75 c

C Crataegus monogyna 2.09 ± 0.59 d

Values of the same column with the same letter are not significantly

different at the 0.05 level (LSD test)

Fig. 4 (a) Net assimilation rate (A, lmol CO2 m–2 s–1), (b)

transpiration rate (E, mmol m–2 s–1), and (c) conductance to water

vapor (gs, mmol m–2 s–1) in 9-year-old (zone B) and 4-year-old (zone

C), Crataegus monogyna (Cm), Fraxinus angustifolia (Fa), and

Populus alba (Pa) plantations, during the summer period (June, July,

and August). (d) Net assimilation rate (A, lmol CO2 m–2 s–1) in the

interaction species-plantation zone. Vertical bars denote 95% least





123

Fig. 8a,b). The trees in the natural stand also received

lower PPFD (Fig. 8c) and had higher VPG (p \ 0.001;

Fig. 8d) than the plantations. As expected, in all cases,

sunlit leaves had higher assimilation rates than shaded

leaves (p \ 0.001; Fig. 8a). As seen from the gas exchange

measurements taken in the natural stand (experiment 1),

net assimilation of sunlit leaves reached its highest value in

the morning and diminished during the day (Fig. 9a). In

contrast to the net assimilation pattern, transpiration rate

was highest at midday and the conductance to water vapor

progressively diminished from the maximum at 8 to 10 h

(data not shown). Water-use efficiency diminished during

the day, in parallel with net assimilation (Fig. 9b). How-

ever, IWUE increased during the afternoon for shaded

leaves, and decreased slightly for sunlit leaves (Fig. 9c).

Discussion




Our results support the hypothesis that gas exchange

parameters at the leaf level can be used as indicators of the

acclimation capacity of plantations with woody species for

the restoration of riparian areas. White poplars from both

natural and plantation stands showed the highest rates of

net assimilation, transpiration, and WUE at the beginning

of the day and decreased rates later in the day, in parallel

with stomatal conductance (experiment 1a). This midday

depression has been described in Eastern cottonwood (P.

deltoides), in which a high vapor pressure deficit made a

more significant contribution than a high PPFD to the A

and gs reduction (Pathre and others 1998). A midday

depression of photosynthesis has also been observed in

white poplar leaves as a consequence of stomatal closure

(Barta and Loreto 2006). Mature trees in the natural stand

had greater conductance to water vapor than juvenile

plants, implying that IWUE was lower in mature than in

young trees in June, July, and August. In all cases, sunlit

leaves showed higher A and gs rates than shaded leaves

(experiment 1b). These relationships are consistent with

objective 1.


Ash, and Hawthorn

The net assimilation and transpiration rates of planted

white poplar were superior to those of ash and hawthorn in

June and July in association with greater conductance rates,

whereas in August, gs of white poplar decreased, which

was probably the limiting cause of both A and E. These

results support objective 2 (experiment 2a). Populus shows

higher levels of stomatal conductance than other tree

genera with the same PPFD and vapor pressure deficit

conditions (Will and Teskey 1997). A tight stomatal reg-

ulation of transpiration and a narrow cavitation safety

margin has been observed in other Populus species (Sparks

and Black 1999). This more active gas exchange rate in

poplar implies that this species behaves as a water-con-

sumer, maximizing carbon assimilation and growth

(Hetherington and Woodward 2003), but with lower WUE

than ash. This is in agreement with the boundary-line

analysis of the gs–VPG curves (Fig. 5b), which shows that

white poplar has a higher gs than ash and hawthorn at low

VPG, but the steeper slope at high VPG indicates more

sensitivity to this parameter, supporting objective 2

(experiment 2a).

Table 3 Quantum efficiency of CO2 assimilation (Uc, parameter

estimate ± asymptotic standard error), light-saturated assimilation

(Amax, lmol m–2 s–1, parameter estimate ± asymptotic standard error),

and adjusted r2 statistic (%) of the regression model of the fitted Aversus PPFD curves for the species used in the restoration of the

Henares floodplain

Species Uc Amax Adj. r2

Populus alba 0.109 ± 0.035 26.92 ± 2.61 89.23

Fraxinus angustifolia 0.149 ± 0.043 32.54 ± 2.50 89.41

Crataegus monogyna 0.088 ± 0.030 24.62 ± 2.33 83.08

Fig. 5 (a) Net assimilation rate (A, lmol CO2 m–2 s–1) versus

photosynthetic photon flux density (PPFD, lmol m–2 s–1) and (b)

conductance to water vapor (gs, mmol m–2 s–1) versus vapor pressure

gradient (VPG, kPa) curves of Populus alba (thin solid line, ),

Fraxinus angustifolia (dotted line, - - -), and Crataegus monogyna(thick solid line, ) plantations (June and July 2003)


123

Disalvo and Hart (2002) observed that the relative basal

area increment of P. trichocarpa was negatively correlated

with vapor pressure deficit. Horton and others (2001a,b)

also reported that the vapor pressure deficit limited both net

carbon assimilation and gs in P. fremontii, which is adapted

to warm and dry climates, with thresholds of between 1.6

and 1.2 kPa, respectively, well below those recorded in our

study (Fig. 5b). In box elder, a negative association was

also found between A and gs and vapor pressure deficit

(Kolb and others 1997). These results are in agreement

with those obtained from our gs-VPG boundary-line anal-

ysis in white poplar.

Ash expanded leaves later than the other species, and

foliar activity was delayed in June, but it had a greater

WUE than poplar. The photosynthetic capacity of ash was

also assessed in Central Europe (Kazda and others 2000),

where lower estimated Amax values were found (16.67

versus 32.54 lmol m–2 s–1 in this study); our higher value

was probably due to the greater availability of light.

Hawthorn had a lower assimilation rate than the tree

species studied. These differences in water use efficiency

and carbon uptake among species can influence ecosystem

processes such as decomposition and nutrient cycling (Fi-

scher and others 2004).

Net assimilation of all three species was similar in

August 2002 and in August 2003, whereas E was signifi-

cantly greater in August 2003 than in August 2002 (Fig. 6).

This variation in gas exchange behavior at the leaf-level

may be due to meteorological differences between both

years. The average temperature in August 2002 (22.7� C)

was 2.9� C lower than in August 2003 (25.6� C; Fig. 1),

and average relative humidity in August 2002 (42%) was

11.8 % higher than in August 2003 (30.2%) as a conse-

quence of precipitation differences (1163 mm in 2002

versus 440 mm in 2003); these annual differences could

have influenced E significantly but not A (experiment 2b).

Experiment 3: Leaf Level Responses Within Native


The comparison of leaf level responses within native riparian

plots to adjacent restoration plots, as indicators of the eco-

physiological competence of woody species to restore the

natural vegetation of riparian forests under a Mediterranean

climate (objective 3), demonstrated that planted poplars had a

higher A than mature poplars from the natural stand. This

result may be attributed to a higher light availability in the

restoration zones or to lower VPG (Fig. 8), which was

probably due to the lower stand density of the planted white

poplars. Wittig and others (2005) found in white poplar and

other Populus species that canopy closure caused the decline

of light availability and the subsequent reduction in the car-

bon assimilation rate and gross primary production. Positive

relationships between conductance and photosynthetic rates

have long been recognized (Kozlowski and Pallardy 1997,

Wang and others 2000, Pena-Rojas and others 2004). Similar

results have also been observed in P. fremontii (Horton and

others 2001c), in P. tremuloides (Noormets and others 2001),

and in the floodplain tree, Acer negundo (Foster 1992), in

which PPFD was the primary factor influencing net carbon

assimilation. Leaf level gas exchange was also limited by

VPG in P. fremontii (Horton and others 2001a). As with

young native poplars, planted poplars also had higher rates of

Table 4 Polynomial regression models fitted between water vapor conductance (gs, mmol m–2 s–1) and water vapor pressure gradient (VPG,

kPa), p-value of the model analysis of variance, and adjusted r2 statistic (%) of white poplar (Populus alba), ash (Fraxinus angustifolia), and

hawthorn (Crataegus monogyna) used for the restoration of the Henares floodplain

Species Model p Adj. r2 (%)

Populus alba gs = 332.57 + 195.15VPG – 28.67VPG2 0.0071 87.38

Fraxinus angustifolia gs = 32.28 + 204.53VPG – 21.72VPG2 0.0279 94.41

Crataegus monogyna gs = 15.79 + 122.55VPG – 12.29VPG2 0.0013 94.55

Fig. 6 Annual variation in (a) net assimilation rate (A, lmol CO2 m–2

s–1) and (b) transpiration (E, mmol m–2 s–1), of Crataegus monogyna(Cm), Fraxinus angustifolia (Fa), and Populus alba (Pa) plantations

during the annual period from August 2002 to August 2003. Vertical

bars denote 95% least significant difference (LSD) intervals. Means

of one treatment not overlapped by the vertical bars of other

treatments are statistically different at the 0.05 level


123

WUE than the mature trees in the natural stand (Fig. 8b), and

showed a good growth in both restoration zones (Table 2).

These similarities in leaf level responses between planted and

young native poplars support objective 3.

Conclusions and Management Implications

We conclude that gas exchange parameters at the leaf level

have been used successfully as indicators of the capacity of

acclimation of plantations with woody species for the

restoration of riparian areas, supporting our hypothesis. We

also conclude that there are significant differences in

physiological performance between mature and young

white poplars in the natural stand, consistent with objective

1, and among planted species, supporting objective 2.

White poplar behaved as a fast-growing, water-consuming

species with a more sensitive gas exchange dynamic than

the other species used for restoration purposes. The eco-

physiological competence and tolerance of the young

regenerating poplars is probably due to the establishment

of a deep root system and to the ability to tap soil water

reserves, according to the model of drought-avoiding,

water-spending plants, and to their maintaining photosyn-

thetically active leaves during longer periods than the

species with a greater WUE. Ash had a lower growth in

diameter and height than white poplar in spite of having

higher Amax, probably because of its shorter leaf duration

and other limiting factors of A.

We propose the use of white poplar for the rapid res-

toration of riparian vegetation in semi-arid Mediterranean

environments, consistent with objective 3. Ash and haw-

thorn can also play a role as accompanying species for the

purposes of biodiversity. These findings should be taken

into consideration by environmental managers for the

establishment of specific goals, including the conservation

of all the important native species present in Mediterranean

riparian ecosystems.

Acknowledgments We thank the Spanish Ministry of Education

and Science for funding the research project, RTA01-009. Maria F.

Martınez-Chacon was recipient of a scholarship from the Madrid

Institute of Agricultural Research (IMIDRA). We also thank Pru

Brooke-Turner for the linguistic revision of the manuscript.

Fig. 7 Species-zone

interactions in (a) net

assimilation rate (A, lmol CO2

m–2 s–1), (b) transpiration (E,

mmol m–2 s–1), (c) conductance

to water vapor (gs, mmol m–2 s–

1), and (d) intrinsic water use

efficiency (IWUE) of 9-year-old

(zone B) and 4-year-old (zone

C) Crataegus monogyna (Cm),

Fraxinus angustifolia (Fa), and

Populus alba (Pa) plantations,

during the annual period from

August 2002 to August 2003.

Vertical bars denote 95% least

significant difference (LSD)

intervals. Means of one

treatment not overlapped by the

vertical bars of other treatments

are statistically different at the

0.05 level


123

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Documents

Ecophysiological Competence of Populus alba L., Fraxinus angustifolia Vahl., and Crataegus monogyna Jacq. Used in Plantations for the Recovery of Riparian Vegetation