沙漠研究 23-4, 161 -165 (2014 )－APCSEET2013 Refereed Papers－

Journal of Arid Land Studies

Growth and Physiological Characteristics of Seedlings, Coppices,and Intact Adults of Eucalyptus camaldulensis under Saline Conditionsin Western Australia
Shin-ichi AIKAWA*1) 2), Hideki SUGANUMA3), Akira UEMUMA4) and Hajime UTSUGI4)
Abstract: In Australia, a rise in the water table usually causes soil salinization, for which afforestation has been encouraged to
manage the groundwater level. In this study, the growth and physiological characteristics of afforested trees of Eucalyptus
camaldulensis were measured to evaluate the ability of this species to grow and regenerate under saline conditions. The
photosynthetic capacity of seedlings at predawn in winter was higher than those of coppices and intact adults. However, themaximum rate of photosynthesis in winter did not differed among them, and in summer, the lowest values were observed in seedlings.
The lowest stomatal conductance and the highest ratio of carbon stable isotopes were also observed in seedlings, thus indicating thatthe seedlings were exposed to severe water stress in summer. The water stress affected the growth and survival of each seedling.
The biomass growth of coppices and intact adults were significantly larger than that of seedlings, and the survival rates of coppices andintact adults were higher than that of seedlings. The survival rate of seedlings was only 33%, as the severe water stress in summer
would cause high seedling mortality. When comparing the growth forms of coppices, seedlings, and adults, only seedlings havesmall root systems. A well-developed root system contributes to a larger water supply and more successful growth in semiarid saline
areas. Our results suggest the importance of taking countermeasures to avoid summer water stress for successful regeneration byplanting seedlings.
Key Words: Afforestation, Dry land, Eucalyptus camaldulensis, Regeneration, Salinity.

1. Introduction
Soil salinization had been reported in many regions of theworld (Rengasamy, 2006). Soil salinity reduces the area
available for agriculture and the productivity of affectedfarmland. This problem is quite severe in Australia, where
dryland salinity affects more than 2.5 million ha, and with thearea affected expanding at an annual rate of about 3 to 5%(Marcar and Crawford, 2004). Moreover, the National Landand Water Resources Audit (NLWRA) predicted that areas
with a high potential to develop dryland salinity will cover 17
million ha by 2050 (NLWRA, 2001a). As a result, thedevelopment of countermeasures against salinity is now
considered an urgent need.
In many cases, salinization results from a rise in the watertable (Barrett-Lennard et al., 2003). A rising water tablemobilizes the salts stored in unsaturated soil horizons, andtransports the salts to the ground surface (Bell, 1999). Achange from forest vegetation to farmland can disturb acatchment's water balance. Therefore, in the wheat belt ofWestern Australia, afforestation is being encouraged to
improve the water balance by increasing the amount of water
extracted from the soil by plants. Previous research has
shown that one potential approach to the treatment of
secondary salinization is through the management of water use
by vegetation (Greenwood and Beresford, 1979). In Australia,
many researchers have studied tree-water relations (e.g.
Boomsma and Hunter, 1990; Whitehead and Beadle, 2004).
Some studies focused on the amount of water used byafforested stands, and assessed the ability of afforestation to
manage shallow water tables that can lead to salinization(Cramer et al., 1999; White et al., 2002; Aikawa et al., 2009).
The management of planted trees would be also important
for the long-term management of shallow water tables.
Several approaches have been taken in southwestern Australia
to integrate environmental restoration and the use of carbon
stored on such plantations (Harper et al., 2011). After the useof forest carbon, the felled trees should be regenerated bycoppicing or planting new seedlings. Therefore, the growthand physiological characteristics of coppices, seedlings, andadult trees were measured to reveal their growth and any（Received, August 21st, 2013; Accepted, January 17th, 2014）* Corresponding Author: aikawas@jafta.or.jp
7 Rokubancho, Chiyoda, Tokyo 102-0085, Japan
1) Japan Forest Technology Association

3) Seikei University

2) Tokyo Metropolitan University

4) Forestry and Forest Products Research Institutefactors that may limit that growth.

Table 1. Allometric equations developed from felled trees.
organ(unit)

2. Materials and Methods
Adults2.1. Study site and species
The study was conducted at an afforestation site nearCalingiri, Western Australia (31°12’S, 116°28’E). The
average annual rainfall between 2000 and 2010 was 315.7 mm,
and most of the rainfall had observed in winter. The standwas afforested in 2001 by planting Eucalyptus camaldulensis
in a flat marginal area of abandoned saline farmland. The
trees were spaced 2.0 m apart within the rows and 3.0 m
between the rows, and the resulting stand density was 1667
trees ha-1. Calingiri was considered to be at moderate risk ofsalinization in 2000, but is now considered to be at high risk
after 2020 (Short and McConnell, 2000). The dominant soil
type in this area was a Sodosol (NLWRA, 2001b). This is a
specific kind of sodic soil with a clear or abrupt textural
horizon that is not strongly acidic in its sandy or loamy surface
soil. The subsoil is usually clayey, with restricted hydraulicconductivity essentially caused by the dispersive nature of
sodic clay. The depth to the water table was less than 2.0 m,
and the electrical conductivity of the groundwater ranged from25 to 50 dS m-1 around the site (Short and McConnell, 2000).
The electrical conductivity of the surface soil was less than 0.5
dS m-1 at our study site (Aikawa et al., 2009). As is often thecase in lands at risk of salinization, waterlogging destroyed thevegetation in low-lying areas of the catchment.
Eucalyptus camaldulensis is one of the most widelydistributed Eucalyptus species in Australia (Boland et al.,2006). The species is called "River red gum" due to its
abundance near rivers, and shows both a high tolerance forwaterlogging and a fast growth rate. These traits make E.
camaldulensis a promising species for afforestation andenvironmental restoration.
2.2. Measurements
In August 2009, a 96 × 15 m plot was established in theafforestation stand. Four 12 × 15 m sub-plots were alsoestablished in the plot, and in the two of the sub-plots allplanted trees were cleared to measure coppice regeneration.
At the same time, 158 seedlings were planted beside the plot.
The heights (H) and diameters at 0.3 m above the ground (D0.3)
were then measured in all stems of 60 intact adults, 60
coppices, and 158 seedlings twice a year. We calculated theaboveground biomass (dry weight) of the trees by using
allometric equations obtained from the felled trees (Table 1).
The photosynthetic capacity of the adults, coppices, andseedlings were measured by using a portable photosynthesis
system (Li-6400, LI-COR Inc., USA). In September 2010

Coppices

Seedlings

Coefficient
a

R

b

2

P

stem (kg)107.760

0.963

0.907

<0.05

branch (kg)48.943

1.096

0.980

<0.01

leaf (kg)

8.697

0.643

0.830

<0.05

stem (g)

0.570

0.808

0.933

<0.01

branch (g)

0.127

0.951

0.755

<0.05

leaf (g)

1.493

0.648

0.915

<0.01

stem (g)8.0×10

-6

3.014

0.964

<0.01

branch (g)2.0×10leaf (g)

-6

3.166

0.760

<0.05

-4

2.276

0.836

<0.01

4.0×10The dry weight in each organ was estimated by the power function (Drywight = a xb ). The independent variable (x) was D0.32H (cm3 ) in adults andcoppices, and was H (cm) in seedlings.

(winter) and in January 2011 (summer), the maximum rate of
Rubisco carboxylase activity (Vcmax) and the maximum rate ofphotosynthetic electron transport (Jmax) were measured tocompare the photosynthetic capacity among adults, coppices,and seedlings. Vcmax and Jmax are key parameters used todescribe photosynthetic capacity (Farquhar et al., 1980; Fan etal., 2011). These parameters measured in winter and summer
were converted to normalized values at 25°C by using amethod described by Kosugi et al. (2003). The normalized
Vcmax and Jmax are represented as Vcmax25 and Jmax25,
respectively. The maximum rate of photosynthesis (Amax) andstomatal conductance (gs) were also measured in winter and insummer.
The stable carbon isotope composition of leaves wasmeasured by using a system that combined an elemental
analyzer (Flash 2000, Thermo Fisher Scientific Inc., USA) anda mass spectrometer (DELTA V, Thermo Fisher Scientific Inc.,
USA). The 13C/12C isotope ratios (δ13C) were calculated
relative to the Pee Dee Belemnite international standard.

3. Results and Discussion
3.1. Physiological characteristics
In winter, the mean (± standard error) values of Vcmax25 forthe leaves of coppices, seedlings, and adults were 86.0 ± 4.7μmol m-2 s-1, 91.4 ± 5.7 μmol m-2 s-1, and 70.5 ± 6.2 μmol m-2
s-1, respectively (Fig. 1). The Vcmax25 values in seedlings
were significantly higher than those of adults in winter (Tukey
test, P <0.05). In summer, the Vcmax25 values of coppices andadults were 58.9 ± 1.2 μmol m-2 s-1, and 64.0 ± 7.7 μmol m-2 s-1,
respectively. The summer Vcmax25 values in coppices weresignificantly lower than those of winter values (ANOVA, P<0.001), however, the winter Vcmax25 values were notsignificantly differed between coppices and adults (ANOVA, P>0.05). In winter, the Jmax25 values for the leaves of coppices,
seedlings, and adults were 160.9 ± 7.6 mol m-2 s-1, 196.5 ± 10.1

ab***

a
b

80

20

a

a

60
40
20
0
coppiceseedling

adult

coppice

winter

Jmax25 (mol m-2 s-1)

240
200

a

seedling

Amax (μmol m-2 s-1)

100

a***

ab
b

5

0

ab***

0.8

coppice

a

a

80
40
0
coppiceseedling
winteradult

coppiceseedling

0.6

seedling

adult

coppice

winter

b***

120

a

a

10

summer

160

a***

15

adult

gs (mol m-2 s-1)

Vcmax25 (μmol m-2 s-1)

120

Fig. 1. Maximum rate of Rubisco carboxylase activity (Vcmax) andmaximum rate of photosynthetic electron transport (Jmax) ofseedlings, coppices, and adults. The summer values inseedlings could not be measured due to the severe water stressthroughout the day. Different alphabets indicate significant
difference between the values in each season (Tukey test, P<0.05). Asterisks indicate significant difference between winterand summer (* P <0.05, ** P <0.01, *** P <0.001).

adultsummer

a***

a***

a**

0.4

a

0.2

a

b

adult

summerseedling

0.0
coppiceseedling

adult

coppice

winterseedling

adultsummerFig. 2. Maximum rate of photosynthesis (Amax) and stomatal
conductivity (gs) of seedlings, coppices, and adults. Different
alphabets indicate significant difference between the values ineach season (Tukey test, P <0.05). Asterisks indicate significant
difference between winter and summer (*P <0.05, ** P <0.01,*** P <0.001).

mol m-2 s-1, and 188.2 ± 10.1 mol m-2 s-1, respectively. The
Jmax25 values in seedlings were significantly higher than thoseof coppices in winter (Tukey test, P <0.05). In summer, theJmax25 values of coppices and adults were 105.0 ± 5.3 mol m-2
s-1 and 110.1 ± 3.9 mol m-2 s-1, respectively. There was no
significant difference in the summer Jmax25 values of coppices
and adults (ANOVA, P >0.05), although the summer values
were significantly lower (ANOVA, P <0.001). The summer
values of Vcmax and Jmax in seedlings could not be measured
due to severe water stress throughout the day.
The maximum rates of photosynthesis (Amax) and stomatal
conductance (gs) were also measured in winter and summer(Fig. 2). The Amax values of coppices, seedlings, and adults inwinter were 17.9 ± 0.6 μmol m-2 s-1, 16.3 ± 1.5 μmol m-2 s-1,
and 14.9 ± 1.1 μmol m-2 s-1, respectively, with no significant
difference being observed (Tukey test, P >0.05). The Amax
values of coppices, seedlings, and adults in summer were 10.8
± 0.4 μmol m-2 s-1, 7.6 ± 1.5 μmol m-2 s-1, and 14.7 ± 2.3 μmol
m-2 s-1, respectively, with a significant difference between the
Amax values of seedlings and adults (Tukey test, P <0.05).
The winter values were significantly higher in coppices andseedlings (ANOVA, P <0.001). The gs values of coppices,
seedlings, and adults in winter were 0.47 ± 0.05 mol m-2 s-1,
0.49 ± 0.07 mol m-2 s-1, and 0.34 ± 0.06 mol m-2 s-1,
respectively, with no significant difference being observed

Table 2. Rate of carbon stable isotope in summer leaves.
organ

Mean

SE

Adults

leaf

-27.5

±

0.29

a

Coppices

leaf

-27.2

±

0.27

a

Seedlings

leaf

-25.4

±

0.57

b

Different alphabets indicate significant difference between the values(Tukey test, P <0.05).

(Tukey test, P >0.05). In contrast, the gs values in summer
were 0.13 ± 0.01 mol m-2 s-1, 0.05 ± 0.01 mol m-2 s-1, and 0.10
± 0.02 mol m-2 s-1, respectively, with seedlings showing asignificantly lower value relative to the coppices and adults(Tukey test, P <0.05).
The ratio of stable carbon isotopes represented as (δ13C)
indicated the intensity of a plant’s water stress, because theδ13C value is related to the long-term stomatal conductance ofleaves. The δ13C values of coppices, seedlings, and adults insummer were -27.2 ± 0.3‰, -27.5 ± 0.3‰, and -25.4 ± 0.6‰,
respectively (Table 2). The δ13C value in seedlings was
significantly higher than the δ13C values in coppices and adults(Tukey test, P <0.05).
The results of δ13C and stomatal conductance results
indicated severe water stress in summer, especially in seedlings.
The decline in stomatal conductance in seedlings had also beenAboveground mass (kg / tree)

50
40
30
20
10

coppiceseedling
adult0Fig. 3. Growth in aboveground biomass of seedlings, coppices, andadults.

Leaf mass (kg / tree)

4
3
2
1
0

Fig. 4. Growth in leaf mass of seedlings, coppices, and adults.

Survival rate (%)

100
80
60
40
20

coppiceseedling
adult0Fig. 5. Survival rate of seedlings, coppices, and adults.

reported by a previous study (Blake, 1980). When comparing
the growth forms of coppices, seedlings, and adults, only
seedlings have small root systems. A well-developed rootsystem in adults and coppices would contribute to a larger
water supply and higher photosynthetic rate in summer.
3.2. Growth and survival rates
At the end of our study period (i.e., 27 months after fellingand planting), the aboveground biomass of coppices, seedlings,
and adults derived from the equations (Table 1) became 5.1 ±0.4 kg tree-1, 0.026 ± 0.009 kg tree-1, and 41.5 ± 5.6 kg tree-1,
respectively (Fig. 3). The increases in the abovegroundbiomass of coppices, seedlings, and adults were 2.3 ± 0.2 kg

tree-1 y-1, 0.011 ± 0.004 kg tree-1 y-1, and 4.3 ± 0.6 kg tree-1 y-1,
respectively. The aboveground biomass and growth rate werethus significantly different among coppices, seedlings, andadults (Tukey test, P <0.05). The leaf mass of coppices,
seedlings, and adults at the end of our study period were 1.7 ±0.1 kg tree-1, 0.014 ± 0.004 kg tree-1, and 3.4 ± 0.3 kg tree-1,
respectively (Fig. 4), thus showing significant differences inleaf mass (Tukey test, P <0.05).
The survival rates of coppices and adults during the study
period were 100%, but only 32.9% for seedlings (Fig. 5).
Most seedlings died after the first summer.
The growth rate of seedlings was less than one-hundredthof that for coppices and adults. Despite the small amount ofleaves in seedlings, the leaves of seedlings were exposed tosevere water stress. This indicated that the seedlings had poor
water absorption ability. The poor water supply in seedlings
raised water stress - the cause of high mortality. It had beenreported that the development of the root system plays animportant role in the growth of coppices in the arid region ofWestern Australia (Aikawa et al., 2013). Our results
indicated that a well-developed root system was also importantin semiarid saline areas.

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