Annals of Botany 77: 623-628, 1996
Respiratory Behaviour of Young Hinoki Cypress {Chamaecyparis obtusa) Trees
under Field Conditions
STEPHEN ADU-BREDU, TAKETO YOKOTA* and AKIO HAGIHARA
Forest Ecophysiology Laboratory, Forest Sciences Division, School of Agricultural Sciences,
Nagoya University, Nagoya 464-01, Japan
Received: 28 July 1995 Accepted: 4 December 1995
Night-time respiration rates of aerial parts of six sample trees in a 9-year-old hinoki cypress [Chamaecyparis obtusa
(Sieb. et Zucc.) Endl.] stand were measured at monthly intervals over a 1-year period, by an enclosed whole-tree
method. When the relationships between annual respiration rate and mean phytomass, and between annual
respiration rate and annual phytomass increment were examined, one sample tree, which was under stress, did not
follow the trend of the rest, indicating that its lower respiration rate did not correspond to its size because of its
negligible phytomass increment. Respiration was partitioned into maintenance and growth respiration to explain this
phenomenon. The maintenance coefficients were 0-0345,0-0373, 00352,0-0211, 0-0316 and 00200 g CO 2 g"1 month" 1 ,
in decreasing order of tree size. The maintenance coefficients of the stressed (i.e. 00211 g CO 2 g"1 month" 1 ) and
suppressed (i.e. 0-0200 g CO 2 g"1 month" 1 ) trees were similar and smaller than those of the rest which were larger and
alike, indicating that stress and suppression reduced the coefficient. The growth coefficients were 1-45, 1-51, 1-28, 1-80,
1-45 and 1-64 g CO 2 g"1, in decreasing order of tree size. The growth coefficient of the stressed tree (i.e. 1-80 g CO 2 g"1)
was the largest followed by that of the smallest and suppressed tree (i.e. 1-64 g CO 2 g"1), suggesting that stress and
suppression reduced the efficiency of conversion of substrate into new structural phytomass. The stressed tree respired
mainly to maintain itself. The respiratory behaviour of the sample trees, including the stressed tree, was compatible
with the concept of growth and maintenance respiration.
© 1996 Annals of Botany Company
Key words: Chamaecyparis obtusa, growth respiration, hinoki cypress, maintenance respiration, phytomass,
phytomass increment, size dependence, stressed tree, suppressed tree.
Hagihara and Hozumi, 1991, 1992; Yokota, Ogawa and
Hagihara, 1994; Yokota and Hagihara, 1995), has rarely
The two-component functional model considers respiration received much attention because of the inherent large
in broad terms as being composed of growth and main- phytomass of trees (e.g. Jarvis and Leverenz, 1983; Hagihara
tenance components (e.g. Hesketh, Baker and Duncan, and Hozumi, 1991; Sprugel and Benecke, 1991).
1971). According to the model, growth respiration is coupled
In the present study, night-time respiration rate of the
to growth rate, that is, an increase in growth rate is aerial parts of six sample trees was measured nonassociated with an increase in growth respiration and vice destructively at monthly intervals by an enclosed whole-tree
versa, whereas maintenance respiration is coupled to plant method (Ninomiya and Hozumi, 1981, 1983; Yokota et al.,
size, such that an increase in phytomass is associated with 1994). Estimated annual respiration rate of the sample trees
an increase in maintenance respiration. A major effect of was related to the annual mean aerial phytomass and
stress is the promotion of senescence, accompanied by low phytomass increment, and partitioned into growth and
rates of growth (Waisel, 1991), which in turn result in a maintenance respiration to clarify the respiratory behaviour
decrease in growth respiration. When growth is arrested, of the trees.
respiration will be dominated by metabolism associated
with survival (Amthor, 1989).
Respiration of trees under stress has received little
M A T E R I A L S AND M E T H O D S
attention compared with that of crop plants (Amthor,
Plant materials
1989). Although there have been studies of the respiration
of excised or small parts of trees over short periods, The study was carried out in a 9-year-old (as of 1992) stand
respiration at the whole-tree scale, particularly under field of hinoki cypress [Chamaecyparis obtusa (Sieb. et Zucc.)
conditions (with a few exceptions, e.g. Butler and Landsberg, Endl.] in an experimental field of the School of Agricultural
1981; Ninomiya and Hozumi, 1981, 1983; Paembonan, Sciences, Nagoya University, Japan, from Jul. 1992 to Jun.
1993. Tree population density, mean tree height, mean stem
volume
and mean stem cross-sectional area at the crown
* Present address: Global Environment Research Division,
base of all trees in the stand in Jun. 1992 were 10148 trees
National Institute for Environmental Studies, Onogawa 16-2,
ha"1, 3-59 m, 4-16 dm3 and 20-4 cm2, respectively. General
Tsukuba, Ibaraki 305, Japan.
INTRODUCTION
0305-7364/96/060623 + 06 $18.00/0
1996 Annals of Botany Company
624
Adu-Bredu et al.—Respiratory Behaviour of Hinoki Cypress Trees
features of the sample trees, which were chosen to reflect the
size class distribution of individual trees in the stand, are
given in Table 1.
Monthly measurements were made of tree height, stem
girth at the crown base and stem girth at 50-cm intervals of
all trees in the stand. From the measurements, stem volume
was calculated by Smalian's formula (e.g. Avery and
Burkhart, 1994). Aerial phytomass, uT (kg per tree), was
estimated from stem volume, vs (dm3 per tree), by the
formula of Hagihara, Yokota and Ogawa (1993) as
H> = 0-626 y.0954.
Night-time respiration measurement
An enclosed whole-tree method (Ninomiya and Hozumi,
1981, 1983; Yokota et al., 1994) was used for the respiration
measurements. The aerial parts of each sample tree were
enclosed in a transparent cylindrical assimilation chamber
made of 0-2 mm thick polyvinyl chloride film (Takafuji
Chem. & Syn. Co., Ltd., Japan). In order to avoid air
leakage, potter's clay was applied to the base of the stem
before tying the skirt of the chamber firmly to the stem base.
A fan was installed to stir the air inside the chamber to
maintain uniform CO2 concentration. A temperature sensor
installed at 1-0 m above the ground monitored air temperature inside the chamber. For gas sampling, a pump
circulated the air through vinyl pipes inserted into the
chamber through three different intakes (top, middle and
bottom of the chamber) and a gas sampling nozzle outside
the chamber at a rate of 8 dm3 min"1.
Microsyringes of volume 20 cm3 were used to collect five
gas samples at a time from each sample tree chamber at
2-h intervals. The gas samples were analysed immediately
using an infrared gas analyser (URA-2S Shimadzu
Seisakusho Ltd., Japan). The measurements were made
from dusk to dawn.
respiration rate of white clover in the dark during the day
time responded to air temperature in the same manner as
the rate during the night time. The respiration rate, r,
observed at a particular air temperature, 6, can be used to
estimate monthly mean respiration rate, rmo (mg CO2 per
tree lr 1 ), which corresponds to a monthly mean air
temperature, 6m (°C), as (Yokota et al., 1994)
o
=
r-exp[k(6m-0)],
(2)
where coefficient k is the reaction rate for respiration.
Paembonan et al. (1991) found that the reaction rate for
night-time respiration of the aerial parts of a 12-year-old
hinoki cypress tree was inversely related to air temperature,
and that the value was not affected by tree size. The
coefficient k was calculated from
= 0-130-0-00311
(3)
The estimated monthly mean value of k was inserted into
eqn (2) to give the corresponding monthly respiration rate.
Annual respiration rate was calculated by summing the
monthly respiration rates.
Relative growth rate, RGR, was calculated by the formula
RGR =
AwT
(4)
where Awr is the phytomass increment between the
beginning and end of the sampling period and vvT is the
mean phytomass during the period.
A two-component model developed by Hesketh et al.
(1971) was used to partition respiration into growth and
maintenance respiration. This model was expressed by the
relationship
= g- AwT/wT
(5)
where rmo/wT is specific respiration rate (g CO2 g 1 month J),
AwT/wT is relative growth rate (g g^month"1), g is growth
coefficient and m is maintenance coefficient.
Data analysis
From the volume of the assimilation chamber, V (m3),
RESULTS
mean air temperature, 6 (°C), and mean rate of CO2
increment, dC/dt (/tmol mol * per tree h"1), in the chamber Tree growth
during the experimental period, night-time respiration rate, Tree height and stem volume increments, and relative
r (mg CO2 per tree lr 1 ), was calculated as
growth rate of the sample trees are given in Table 1. The
height increment of tree 4 was only 0-020 m year"1, whereas
273-2 44-0 dC
that of the remaining trees ranged between 0-38 and 0-60 m
r= V(1) year \ This indicates that the apical meristem of tree 4 had
273-2 + 0 224 ~d7'
virtually ceased functioning. Similarly, the stem volume
It was assumed that the night-time respiration was measured increment of tree 4 was only 0-037 dm3 year"1 compared
under standard barometric pressure and the volume of the with the range 0-20-2-6 dm3 year"1. As a result, the relative
trees was negligible compared to the volume of the chambers. growth rate of tree 4 showed a low value of 0-012 kg kg"1
Air temperature recorded at 3-min intervals in the year x compared with values of between 0-18 and
neighbourhood of the stand was used in the calculation of 0-30 kg kg"1 year"1.
monthly mean air temperature. The night-time respiration
The cause of stress was not investigated directly but tree
rate observed at a particular air temperature was used to 4 was close to five other trees which had died recently. On
estimate monthly mean respiration rate from monthly mean uprooting one of these trees soon after death, it was
air temperature. This extrapolation is supported by the observed that fine roots were absent, possibly caused by
work of McCree and Amthor (1982) who found that the flooding stress during the rainy season when water accumu-
Adu-Bredu et al.—Respiratory Behaviour of Hinoki Cypress Trees
TABLE
625
1. General features of the sample trees in June 1992
Tree number
1
Features
Tree height (m)
Stem cross-sectional area at the
crown base (cm2)
Stem volume (dm3)
Tree height increment* (m year"1)
Stem volume increment* (dm3 year"1)
Relative growth rate* (kg kg" 1 year"1)
4-2
44
2
3
3-8
20
3-3
12
7-8
0-57
2-6
0-27
5-1
0-60
1-2
0-22
2-9
0-59
1-1
0-30
4
5
6
31
8-8
2-9
8-0
2-6
6-9
30
0-02
0-037
0-012
1-6
0-17
0-39
0-21
0-94
0-38
0-20
018
* From Jun. 1992 to Jun. 1993.
Mar.
May
Month
FIG. 1. Seasonal variations in monthly mean temperature (A) and monthly respiration rate (B). O, Tree I: • . tree 2; • , tree 3; A, tree 4;
• , tree 5; A, tree 6.
lates in these shallow soils. Since hinoki cypress trees are
known to be flood-intolerant, it is likely that root damage
was responsible for the stress experienced by tree 4.
Seasonal variations in temperature and respiration
Seasonal variations in the respiration rate of the sample
trees, and monthly mean air temperature, are shown in Fig.
1. The seasonal trend in respiration largely followed that of
air temperature except in August, when the atmosphere was
warm and dry. In general, the respiration rate decreased
from July (mid-summer) reaching a minimum value in
January (mid-winter), and then increased towards summer.
The seasonal trend was evident in all the sample trees, with
the exception of tree 4, and there was a distinct tree size
dependence in the respiratory consumption every month.
The respiration rate of tree 4 was intermediate between
those of trees 5 and 6 in Jul. 1992, and it dropped to below
that of tree 6 in Jun. 1993.
Phytomass (kg per tree)
FIG. 2. Relationship between annual respiration rate and mean
phytomass. # , Tree 4.
Relationships between annual respiration rate and
phytomass, and phytomass increment
Figure 2 shows the relationship between annual respiration rate of the individual sample trees and their
corresponding phytomass plotted on logarithmic coor-
dinates, which shows that tree 4 (the tree under stress) is out
of trend with the rest, indicating that its respiratory
consumption does not correspond to its size. The annual
respiration rate of each tree was also plotted against its
Adu-Bredu et al.—Respiratory Behaviour of Hinoki Cypress Trees
626
annual phytomass increment as shown in Fig. 3. Again, tree
4 was out of trend with the rest, suggesting that its lower
respiratory consumption could be attributed to its negligible
phytomass increment.
Regression of specific respiration rate on relative growth
rate
0.01
0.1
Phytomass increment (kg per tree year"1)
FIG. 3. Relationship between annual respiration rate and phytomass
increment. The legend as in Fig. 2.
o
V
0.15
A
0.10 —
0.05
0.00
-0.01
0.15 B
0.10 —
_
0.05
0.00
-0.01
0.15 -C
0.10 _
0.05
1
0.00
-0.01
0.10 - D
u
o
o
o
_—•—--"•""
1
1
0
1
1
1
1
1
Y#° i
1
1
I
—
_
—
•
—
0
0.00
-0.001 0
-
-
—
-
•
1
1
,
0.04
1
I
0.05
1
I
1
0.06
o
o
___——-o—
o
o
1
~~&o
1 ° 1 I
I
0.03
o
°o
o
o
0.01 0.02
0
______-T)
_—-—"
—-—
-0.001
1
0.01 0.02 0.03 0.04 0.05 0.06 0.07
o
-0.05
o
° o
o
0.05 0.00 -
-0.01
0 _______—
1 1
1
1 1
0.01 0.02 0.03 0.04 0.05 0.06 0.07
O
o
yi
0
u
1
DISCUSSION
Ninomiya and Hozumi (1981) found, in a young Pinus
densi-thunbergii stand, that the annual respiration rate was
almost proportional to aerial phytomass, and Yokota et al.
(1994) also found in a young hinoki cypress stand that the
annual respiration rate increased with both increasing aerial
phytomass and phytomass increment. Ogawa, Hagihara
and Hozumi (1985) also demonstrated, in a seedling
population of hinoki cypress, that the respiration rate was
approximately proportional to the phytomass. On the basis
of these findings (Ninomiya and Hozumi, 1981; Ogawa et
al, 1985), Hagihara and Hozumi (1991) concluded that
respiration rate of individual trees in younger stands may be
directly proportional to their phytomass. However, from
this study, it can be said that these findings can hold only
when all the trees are under similar physiological • and
environmental conditions.
o
b o
1
0.001 0.002
1
0.003 0.005
,
1
0.005
0.01 0.02 0.03 0.04 0.05 0.06 0.07
0.01
A plot of specific respiration rate as a function of relative
growth rate for the sample trees presented in Fig. 4 shows a
close correlation between the two variables. The regression
was based on eqn (5). The maintenance coefficients, m, for
trees 1, 2, 3, 4, 5 and 6 were 0-0345, 0-0373, 0-0352, 0-0211,
0-0316 and 0-0200 g CO2 g 1 month 1 , respectively. The
growth coefficients, g, for trees 1, 2, 3, 4, 5 and 6 were 1-45,
1-51, 1-28, 1-80, 1-45 and 1-64 g CO2 g \ respectively.
0.02
0.03
0.04
0.05
' ( g g 1 month *)
FIG. 4. Plot of specific respiration rate, rm0/wT, as a function of relative
growth rate, AwT/wT. The regression lines are based on eqn (5):
A, Tree 1, rmo/wT = 1 -45 AwT/wT + 0-0345;
B, Tree 2, rmo/wT = 1-51 AwT/wT + 0-0373;
C, Tree 3, rmo/wT = l-28zlvvT/irT + 0-0352;
D, Tree 4, rmo/vvT = 1 -80 AwT/wT + 0-0211;
E, Tree 5, r mo /w T = 1-45 AwT/wT + 0-0316;
F, Tree 6, r mo /u' T = 1 -64AwT/\vT + 0-0200.
Maintenance and growth respiration
The maintenance coefficient values, m, for trees 1,2, 3 and
5 were similar and larger than those for trees 4 and 6 which
were also similar (Fig. 4). McCree (1986) and Amthor and
McCree (1990) pointed out that stress which results
primarily in a decrease in carbon gain and utilization will
cause a reduction in the general level of metabolism, and, in
turn, a decrease in the value of m. Wilson, van Bavel and
McCree (1980) found that the value of m for whole plants
decreased under increasing levels of water stress when the
stress developed slowly, as is the case in the field. It can,
therefore be concluded that it was the stress and suppression
which reduced the value of m in the present study. The m
values given are low compared with values given by Ledig,
Drew and Clark (1976), Wullschleger and Norby (1992) and
Wullschleger, Norby and Gunderson (1992) for the leaves
and shoots of seedlings which range between 1-11 and 411 g
CO2 g"1 month"1, but Hole and Barnes (1980) pointed out
that in bulky tissues m decreases with increasing size. Such
a decline in m may result from a progressive increase in the
Adu-Bredu et al.—Respiratory Behaviour of Hinoki Cypress Trees
TABLE 2. Comparison between annual growth respiration rg,
10 c
and maintenance respiration, rm
r
Tree
1 1 tt
number
1
2
3
4
5
6
g
rm
g '
627
; r m = 0.295 wT
1243
m
1
(kg CO 2 per tree year" )
2-03
(49-5 %)
1-12
(43-5 %)
0-781
(48-2%)
0-0551
(10-9%)
0-331
(45-0%)
0196
(56-2%)
2-07
(50-5 %)
1-45
(56-5 %)
0-838
(51-8%)
0-450
(89-1%)
0-404
(55-0%)
0-153
(43-8 %)
410
(100%)
2-57
(100%)
1-62
(100%)
0-505
(100%)
0-735
(100%)
0-349
(100%)
O
O
bp O . l h
0.01
proportion of woody tissues with very low maintenance
costs, which is a characteristic of woody plants.
The growth coefficient value, g, for tree 4 (i.e. 180 g
CO 2 g" 1 ), the tree under stress, was the largest followed by
tree 6 (i.e. 1-64 g CO 2 g" 1 ), the smallest and suppressed tree,
suggesting that stress and suppression reduced the efficiency
of conversion of substrate into new structural phytomass.
Shone and Gale (1983) reported increases in the value of g
owing to salinity. According to Amthor and McCree (1990),
the value of g can be changed by stress if the composition of
the substrate used in growth, or the composition of the
products of growth are changed. The g values given are
large compared with values given for leaves and shoots of
seedling by Ledig et al. (1976), Wullschleger and Norby
(1992) and Wullschleger et al. (1992), which vary between
0-470 and 0-964 g CO 2 g"1. However, Havranek (1985)
calculated g to be 1-60 g CO 2 g x for the direct cost of wood
production by Larix decidua, a value which is similar to
those in this study. Jarvis and Leverenz (1983) pointed out
that, in view of the substantial amounts of wood produced
in trees, the g value is likely to be high.
Equation (5) can be rewritten as
rmo =
(6)
where the first term on the right-hand side (g • AwT) represents
monthly growth respiration rate and the second term
(m • n'T) denotes monthly maintenance respiration rate. Since
the coefficients g and m of the individual sample trees were
constant over the year (Fig. 4), growth respiration predominated over maintenance respiration in the months with
a great deal of growth (from Apr. to Aug.), whereas
maintenance respiration predominated in the months with
little or no growth. However, with tree 4, maintenance
respiration predominated throughout the season.
Annual maintenance and growth respiration rates were
calculated by the summation of the respective monthly
rates. Contributions of the annual maintenance and growth
respiration towards total respiration are given in Table 2.
The proportion of annual maintenance respiration for trees
1, 2, 3, 4, 5 and 6 was respectively 50-5, 56-5, 51-8, 89-1, 55-0
0.1
1
wT (kg per tree)
10
FIG. 5. Dependence of maintenance respiration, rm on mean phytomass,
wT. # . Tree 4.
and 43-8 %, whereas that for annual growth respiration was
49-5, 43-5, 48-2, 10-9, 450 and 56-2 %, respectively. Only tree
6 had a higher growth respiration than maintenance
respiration, whereas for the other trees the proportion of the
maintenance respiration was slightly greater than that of
growth respiration. However, with tree 4, the tree under
stress, pattern of the contribution was different. The
contribution from maintenance respiration was very high
(891%) compared with growth respiration (10-9%).
Wanner and Tinnin (1986) found that dark respiration rates
of twigs with mistletoe were significantly lower than
uninfected twigs. In that case the respiration rate was
presumably mostly maintenance. Ryan (1990) also found
that lodgepole pine trees infected with mistletoe had very
low respiration rates. It can therefore be concluded that
trees under stress respire largely to maintain the existing
phytomass.
Dependence of maintenance and growth respiration on
phytomass and phytomass increment
The relationships between maintenance respiration and
mean phytomass, and between growth respiration and
phytomass increment were examined on logarithmic coordinates as shown in Figs 5 and 6, respectively (Adu-Bredu,
Yokota and Hagihara, 1996). Unlike Figs 2 and 3, the
relationships could be described by the power function. In
Fig. 5, tree 4 fell between trees 3 and 5, its expected position,
whereas in Fig. 6 it was behind tree 6.
In conclusion, it can be said that stress and suppression
are associated with decreases and increases in the maintenance and growth coefficients, respectively, and under
field conditions, variability among trees may be high as a
result of variation of environmental and physiological
factors. It can be concluded that under such conditions the
respiratory behaviour of trees is compatible with the concept
of maintenance and growth respiration.
Adu-Bredu et al.—Respiratory Behaviour of Hinoki Cypress Trees
628
0.01
AwT (kg per tree year ~1)
FIG. 6. Dependence of growth respiration, r , on aerial phytomass
increment, u T . # , Tree 4.
ACKNOWLEDGEMENTS
We thank our colleagues for their valuable assistance during
the field work. This study was supported in part by a Grantin-Aid for Scientific Research (Nos. 05556023, 07456071)
from the Ministry of Education, Science and Culture,
Japan.
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