Tree Physiology 18, 155--166
© 1998 Heron Publishing----Victoria, Canada
Effect of nitrogen on the seasonal course of growth and maintenance
respiration in stems of Norway spruce trees
JAN STOCKFORS and SUNE LINDER
Swedish University of Agricultural Sciences, Department for Production Ecology, P.O. Box 7042, SE-750 07 Uppsala, Sweden
Received January 10, 1997
Summary To determine effects of stem nitrogen concentration ([N]) on the seasonal course of respiration, rates of stem
respiration of ten control and ten irrigated--fertilized (IL),
30-year-old Norway spruce trees (Picea abies (L.) Karst.),
growing in northern Sweden, were measured on seven occasions from June 1993 to April 1994. To explore sources of
seasonal variation and mechanisms of fertilization effects on
respiration, we separated total respiration into growth and
maintenance respiration for both xylem and phloem bark.
Stem respiration increased in response to the IL treatment
and was positively correlated with growth rate, volume of
living cells and stem nitrogen content. However, no significant
effect of IL treatment or [N] in the living cells was found for
respiration per unit volume of live cells. Total stem respiration
during the growing season (June to September) was estimated
to be 16.7 and 29.7 mol CO2 m −2 for control and IL-treated
trees, respectively. Respiration during the growing season accounted for approximately 64% of total annual respiration.
Depending on the method, estimated growth respiration varied
between 40 and 60% of total respiration during the growing
season. Between 75 and 80% of the live cell volume in the
stems was in the phloem, and phloem maintenance accounted
for about 70% of maintenance respiration. Because most of the
living cells were found in the phloem, and the living xylem
cells were concentrated in the outer growth rings, we concluded that the best base for expressing rates of stem growth
and maintenance respiration in young Norway spruce trees is
stem surface area.
Keywords: annual respiration, fertilization, phloem, Picea
abies, Q10, xylem.
Introduction
Considering that plant respiration is estimated to consume up
to 60% of gross carbon assimilation in a forest ecosystem (cf.
Whittaker 1970, Ryan 1991a), it is surprising that there are so
few respiration studies of forest trees and ecosystems. Although woody tissue respiration in trees had been studied since
the beginning of the century (see Johansson 1933), it was not
until the 1960s and 1970s that the importance of woody tissue
respiration was recognized (cf. Linder 1979, 1981).
In recent decades, studies have widened the perspective
from relating CO2 efflux to growth and temperature only, to
more detailed studies of anatomical and physiological factors
that may affect rates of stem and branch CO2 evolution (e.g.,
Little 1975, Havranek 1981, Larcher and Bauer 1981, AzcónBieto et al. 1983, Lambers 1985, Ryan 1990). During the
1980s the functional model of respiration (McCree 1970,
Thornley 1970), which separates respiration needed to maintain life processes of living cells (maintenance respiration) and
respiration costs related to building new biomass (growth
respiration), became generally accepted. The separation of
respiration into growth and maintenance fractions is difficult
because the two sources of respiratory CO2 are not biochemically distinct (Amthor 1984). Thus, we have to rely on rough
indirect methods to separate the two components. Already in
1933 Johansson separated what he called rest-respiration from
production-respiration by referring to a temperature-dependent component and a temperature-independent respiration
component. Since then, many methods have been developed to
separate the components of respiration (cf. Amthor 1984, Lambers 1985), but only a few are applicable in field studies of
large trees. A common approach, for trees, is to let dormant
season respiration rates represent maintenance respiration
throughout the season, and let any respiration exceeding this
maintenance rate represent growth respiration (e.g., Ryan
1990, Sprugel 1990, Sprugel and Benecke 1991, Lavigne
1996). Another way to separate the two main fractions of
respiration is to use various regression techniques, mainly
multiple linear regressions (Ryan 1990, Sprugel 1990). Penning de Vries (1972, 1974) developed a theoretical method to
estimate the energetic costs of building new plant material that
was based on the chemical composition of the plant tissue and
the production cost for each component.
Because maintenance respiration in living cells is closely
related to rate of protein turnover (Penning de Vries 1975),
nutrient status, especially nitrogen concentration ([N]), is
likely to have an effect on respiration rates. Strong linear
relationships between [N] and respiration in various species
and organs have been reported (e.g., Kuroiwa 1960, Keller
1971, Kawahara et al. 1976, Ryan 1991a, 1995); however,
most of these studies were done on seedlings or leaves. Apart
from studies by Kawahara et al. (1976) and Ryan et al. (1996),
reports on the relationship between woody tissue respiration
156
STOCKFORS AND LINDER
and nutrient status in trees are scarce (cf. Linder and Rook
1984, Sprugel et al. 1995).
When stem respiration measurements are made on trees of
varying size, nutrient status, or age, interpretation of the results
may be affected by the base chosen to express the results, i.e.,
surface area, volume or dry mass (cf. Sprugel et al. 1995). The
most appropriate base for maintenance respiration should be
determined from the distribution of respiring cells in the stems,
and for growth respiration from the distribution of active cambium. Since Johansson addressed these problems in 1933, the
most common base for respiration measurements has been
stem (branch) surface area (von Geurten 1950, Negisi 1972,
1975, Kinerson 1975, Linder and Troeng 1980, 1981, Lavigne
1988), or wood mass (Yoda et al. 1965, Kira 1968, Hagihara
and Hozumi 1981). Reasons for choosing surface area as the
base are that respiration may be assumed to take place mainly
in the cambial region and it is the most convenient base to
measure in the field. After the acceptance of the ‘functional
model,’ studies showed live cell volume and sapwood volume
to be better estimators of maintenance respiration than surface
area (cf. Ryan 1990, Sprugel et al. 1995). Ryan (1990) found
that, for lodgepole pine (Pinus contorta Dougl.), live cell
volume or sapwood volume were the best estimators of maintenance respiration, but that these relationships were weaker
for Engelmann spruce (Picea engelmannii (Parry) Engelm.).
Sprugel (1990) reported that sapwood volume was a better
estimator of maintenance respiration than surface area for
Pacific silver fir (Abies amabilis (Dougl.) Forbes).
Objectives of the present study were: (i) to determine the
effect of fertilization on stem respiration in young Norway
spruce trees, (ii) to estimate the contribution of growth, phloem
maintenance and xylem maintenance to total respiration, (iii)
to compare different methods for separating the sources of
respiration, and (iv) to examine seasonal variation in stem
respiration and variation in contribution of different fractions
to total respiration.
Materials and methods
Site
The study was performed in a nutrient optimization experiment at Flakaliden (64°07′ N; 19°27′ E; alt. 310 m a.s.l.) in
northern Sweden (cf. Linder and Flower-Ellis 1992, Linder
1995). The experiment was laid out in a young Norway spruce
(Picea abies (L.) Karst.) stand that had been planted in 1963
after clearfelling. Two nutrient optimization treatments began
in 1987. The first treatment was a complete nutrient solution
(IL) that was injected into the irrigation water and supplied
every day during the growing season (June to August). The
second treatment was a solid fertilizer mix (F) that was applied
in early June of each year. Controls (C) and plots with irrigation (I) were also included. The treatments were replicated four
times. Further details about the nutrient optimization experiment are provided by Linder (1995).
Monthly mean air temperature at the site varies from --8.7 °C
in February to 14.4 °C in July and snow usually covers the
ground from mid-October to mid-May. Mean annual precipitation is approximately 580 mm.
The respiration study was performed from June 1993 to
April 1994 using trees growing on control plots (C) or plots
receiving irrigation and fertilization (IL). Out of 20 randomly
selected trees per treatment, 10 trees per treatment (C and IL)
were chosen for the study. In spring
_ 1993, diameters of the
selected trees were,_ 6.8--10.2 cm ( x = 8.6 cm) for control trees,
and 6.5--10.2 cm ( x = 9.5 cm) for IL trees.
Diameter increment of each tree was monitored throughout
the season with dendrometer bands placed at breast height
(1.3 m). The dendrometers were measured three to six times a
week with a calliper (± 10 µm). Rate of stem growth in terms
of mass increment was considered as rate of diameter increase
with a time lag of between 1 and 25 days. The introduction of
a time lag between diameter increase and growth respiration
was needed because there is a lag between diameter growth
and increase in dry matter in terms of secondary and tertiary
wall thickening and lignification. For Norway spruce, it has
been reported that this time lag could vary between 1 and 25
days (Zumer 1969). Therefore, the growth variable used in the
regression models (Table 2) is stem expansion rate with the
time lag giving the best fit between stem expansion rate and
respiration at a standard temperature of 10 °C.
Stem respiration
Gas exchange of stems was measured on six occasions during
the growing season 1993 (June to September) and once in April
1994. Measurements were made on the north-facing side of the
stem, at a height of 1.0 to 1.5 m, with a Plexiglas® half-cylinder
chamber that covered 40 cm2 of the stem surface. Before the
chamber was attached, the stem surface was brushed to remove
loose bark, lichens and algae. The chamber, which was attached to the stem during measurements only, was sealed with
foam plastic and Vaseline, and tightened to the stem with
straps. To exclude light and minimize heating, the chamber
was covered with aluminum foil during measurements.
Stem temperatures were measured with copper-constantan
thermocouples inserted directly below the measurement area
5 mm from the stem surface. Throughout the season, with a
few exceptions, temperatures were recorded every minute with
a data logger (CR 10, Campbell Scientific, Logan, UT), and
each hour maximum, minimum, and mean temperatures were
calculated and stored. During periods when respiration was
measured, 10-min mean values were also stored.
Rates of CO2 evolution were measured for all stems during
the same day with a portable infrared CO2 analyzer and photosynthesis system, LI-6200 (Li-Cor, Inc., Lincoln, NE). Before
measurements began, ambient air was flushed through the
chamber and porometer. After closing the supply of ambient
air, the system was allowed to stabilize for 30 to 60 s before
measurements started. The increase in CO2 concentration was
measured every second for one minute and the mean rate of
CO2 increase calculated. The measurement was repeated three
times for each tree with an interval of 3 min between measurements. On each occasion, all trees were measured once in the
morning and once in the afternoon. Rates of respiration are
TREE PHYSIOLOGY VOLUME 18, 1998
STEM RESPIRATION IN NORWAY SPRUCE
expressed per unit of stem surface area, and CO2 efflux is
assumed to originate from the enclosed stem section only (cf.
Sprugel et al. 1995).
To determine the temperature dependence and time lag of
stem CO2 evolution to changes in temperature, continuous
measurements of stem respiration were made on each occasion, on two trees per treatment during a period of 24 to 48 h.
Measurements were made with an open gas exchange system
with an IRGA (ADC Mark 3, Analytical Development Co.,
Hoddesdon, U.K.) and flow control by means of thermal mass
flow meters (HI-TEL, The Hague, The Netherlands).
Stem characteristics
To determine internal structure and stem [N], trees were harvested at the end of the 1994 growing season and three discs
were taken from the stem, directly above and below as well as
in the middle of the area where respiration measurements had
been made. The discs were stored at --20 °C until further
processing. For determination of [N], sections of the discs
were separated into xylem and phloem and dried in a ventilated
oven (85 °C, 48 h). Total nitrogen was determined with an
elemental combustion analyzer (Carlo Erba, NA 1500, Carlo
Erba Strumentatzione, Milan, Italy) by a modified version of
the method described by Kirsten and Hesselius (1983).
The amounts of heartwood and sapwood were determined
from discs taken from the middle of the measurement areas.
When discs were thawed but not dried, heartwood and sapwood could be clearly identified and their respective diameters
were measured in four directions with a caliper, accurate to
0.01 mm.
For determination of live cell volumes, three increment
cores were taken from within the measurement area of each
tree and stored in a 1:1 (v/v) mix of formaldehyde and acetic
acid. The increment cores were sectioned at four depths, approximately 1--2, 8, 15, and 25 mm inside the cambium with a
cryostat microtome. For stems with a large sapwood depth, the
last section was taken at a depth of 35 mm instead of 25 mm.
To ensure that at least one, and preferably two, cell layers were
intact, sections were cut to a thickness of 40 µm.
Sections were stained for 20 min in petri dishes containing
Coomassie Blue solution (0.5 g Coomassie Blue R250 stain
dissolved in 500 ml of methanol, 400 ml of water and 100 ml
acetic acid). Sections were then de-stained for another 20 min
in an identical solution, but without the stain, rinsed in water
and mounted on glass in a solution of equal parts of water and
glycerol (cf. Andrews 1981, Gahan 1984).
The volume of live phloem cells was determined from two
cores per tree. Because the major live cell fraction was found
in the phloem parenchyma rather than in the rays, phloem was
sectioned transversally. Samples were stained for 25 min and
then de-stained for 15 min.
The percentage live cell area of each section was determined
with a computer image analysis system (AnalySIS, SIS Software, Inc., Münster, Germany). Only the stained, protein-containing parts of the living cells were included in the
measurements, i.e., cell walls were excluded. The total volume
of living cells in the xylem was estimated as the live cell area
157
fraction, integrated over the wood volume (cylinder section)
enclosed by the chamber. To estimate the volume of live
phloem cells, the average fraction of living cells from the two
cores was multiplied by the total phloem volume in the area
that had been enclosed by the chamber.
Calculations
For each measurement occasion, the time lag of respiration to
a change in stem temperature was determined as the time lag
giving the best fit between data and an exponential equation.
The time lag was tested in steps of 10 min.
Estimates of total daily respiration were made using a model
developed by Ågren and Axelsson (1980), where temperature
was assumed to vary sinusoidally around daily mean temperature (Tm) giving:
T(t) = Tm + TaSin(2πt/u),
(1)
where T(t) is the temperature at time t, Ta the temperature
amplitude, and u the time step (one day). The temperature
dependence of respiration was assumed to follow an exponential equation:
R = R0ek(T),
(2)
where R = respiration, R0 = respiration at 0 °C, k = (lnQ10)/10,
and T = actual temperature in °C. An integration over one day
then gives:
u
R = ∫ R0ek(Tm + TaSin (2
t/u))
dt = u(R0ekTm I0(kTa)),
(3)
0
where I0(kTa) is a modified Bessel function of zero order that
can be approximated to:
I0(kTa) = 1 + 0.25 (kTa)2 + 0.016(kTa)4 + 0.0004 (kTa)6, (4)
This approximation gives less than 1% error if (kTa) ≤ 2 (Ågren
and Axelsson 1980). Total seasonal and annual respiration per
unit surface area were obtained by using the measured stem
temperatures and summed daily respiration.
Separating components of respiration
Three methods were used to estimate the contributions of
growth and maintenance respiration of xylem and phloem to
total respiration. All trees were included in the analyses, therefore, the results represent an average across tree sizes and
treatments.
Method 1 was based on linear regressions, where each
measurement occasion during the season was analyzed separately. To minimize errors caused by between-tree variation in
stem temperatures, all measurements were normalized to a
temperature close to the mean temperature of the actual day by
using a Q10 derived from the diurnal measurements. In a first
run, respiration at the fixed temperature was tested against
several variables (xylem and phloem nitrogen content, volume
of living xylem and phloem cells, and stem growth rate), using
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158
STOCKFORS AND LINDER
Type III multiple regressions where nonsignificant variables
were eliminated from the model. In a second run, variables
with the best correlation to respiration throughout the season
(live cell volumes) were chosen as predictors for xylem and
phloem respiration. Total respiration at each measurement
occasion was tested separately, in a multiple regression,
against the three variables, xylem and phloem live cell volumes and growth rate (time-lagged stem expansion rate), representing xylem and phloem maintenance respiration and
growth respiration, respectively. We used new standardized
regression coefficients (Bring 1994) as indices for the contribution of selected fractions to total respiration. New standardized regression coefficients, according to Bring (1994), are
similar to the usual standardized regression coefficients, but
use partial standard deviation (s∗i ) instead of standard deviation
for normalization:
s∗i =
si 


√
VIF 
=
_
xi − xi
s∗xi
Stem structure
Fertilizer, applied in the irrigation water, had pronounced effects on several measured stem properties (Table 1), causing
highly significant (P < 0.0001) increases in ring width, xylem
and phloem [N], and live cell volumes. The IL treatment
increased live cell fractions of both phloem and xylem (Table 1), but the increase in xylem live cell volume was most
pronounced in the inner rings (Figure 1).
Table 1. Effects of fertilization on stem properties in 30-year-old
Norway spruce trees. Numbers shown are mean values for 10 trees
from both the control (C) and irrigated--fertilized (IL) treatment.
Volume of living xylem and phloem cells is given as the percentage
protein-containing tissue in relation to the total volume of sapwood
and phloem, respectively.
n−1 
√

,
n−k 
Control
where si is standard deviation, VIF is the variance inflation
factor and k is the number of independent variables in the
regression analysis.
All variables are standardized according to:
x∗i
Results
,
and regression coefficients of the standardized variables are
the new standardized regression coefficients.
Method 2 was similar to the first method, but used the total
seasonal (June to September) respiration, estimated as the sum
of daily respiration rates with the model of Ågren and Axelsson
(1980). On a seasonal basis, linear regressions were used to
separate accumulated respiration into its components. Seasonal growth was represented by the volume increment in 1993
of the stem section enclosed by the chamber.
Method 3 was based on the assumptions that respiration
during the dormant period represented maintenance respiration and that maintenance respiration at constant temperature
was constant over the season. In the present study, only the
measurement made in April 1994 can be assumed to lack a
growth component. For each tree, maintenance respiration
rate, based on measurements in April, was subtracted from the
respiration rate on each measurement occasion. Residuals
were assumed to represent growth respiration, which was estimated for each date. The maintenance components were separated by linear regressions derived from the spring
measurements.
Statistical analyses were conducted by the general linear
models GLM procedure of the SYSTAT statistical package
(1992; SYSTAT Inc., Evanston, IL).
Ring width 1993 (mm)
Xylem N (mg g −1)
Phloem N (mg g −1)
Xylem live cell vol. (%)
Phloem live cell vol. (%)
Phloem-bark depth
Sapwood depth (mm)
Heartwood diam. (mm)
Wood density (g cm −3)
IL-Treatment t-test
Mean
SD
Mean
SD
P-value
1.4
0.69
3.75
0.89
20.9
3.34
27.7
8.7
0.49
0.53
0.07
0.34
0.95
3.2
0.26
6.1
3.3
0.11
3.6
0.79
5.53
1.93
30.4
2.86
37.2
4.7
0.37
0.75
0.06
0.30
1.39
3.3
0.44
5.12
1.3
0.04
< 0.0001
0.0001
< 0.0001
0.07
< 0.0001
0.009
0.001
0.004
0.009
Figure 1. Distribution of volume of living cells in the xylem of Norway
spruce trees growing in control (C) and irrigated-fertilized stands (IL).
Results are expressed in % of xylem volume at a certain depth from
the cambium. Lines represent means of individual power regressions
for ten C (dashed line) and ten IL-treated (solid line) trees. Symbols j
and s are means at approximate section depths for C and IL-treated
trees, respectively. Error bars indicates standard error of the mean.
TREE PHYSIOLOGY VOLUME 18, 1998
STEM RESPIRATION IN NORWAY SPRUCE
159
The volume of living phloem cells was correlated to phloem
[N], (r 2 = 0.49, P = 0.0006), but there was no significant
correlation between xylem live cell volume and xylem [N], (r 2
= 0.096, P = 0.15). For both control and irrigated--fertilized
treatments, the major fraction of living cells was found in the
phloem. In the IL treatment, the fraction of living cells in the
xylem increased from 20 to 32% of the total, but the change
was not significant (P = 0.17). Annual volume growth was
correlated to both xylem and phloem [N], but the strongest
correlation was to phloem [N], (r 2 = 0.67, P < 0.0001).
Respiration
The temperature dependence of stem respiration (Q10) varied
over the season (Figure 2), but on each occasion it was consistent with an exponential increase with increasing temperature
(r 2 > 0.99) (Figure 3). The highest and lowest values of Q10
were in June (2.55) and August (1.92), respectively. There was
also a pronounced seasonal variation in the time lag between
changes in temperature and changes in CO2 evolution (Figure 4). The time lag was shortest in June and reached a maximum in September.
When respiration rates were normalized to a standard temperature (10 °C) with the Q10 values (Figure 2) derived from
the diurnal measurements, there was a large seasonal variation
within and between treatments (Figure 5). The highest respiration rates were always found in IL-treated trees, but respiration
rates in all trees peaked in early July and were lowest in
September. The peak in respiration rate (Figure 5B) occurred
10 to 20 days after the peak in stem expansion rate (Figure 5A).
Note that the respiration rate in control trees at 10 °C was
higher in April than in September.
When Method 1 was used to separate different components
of respiration, three variables showed a significant contribution to total respiration on one or more of the sampling occasions (Table 2). Growth rate was the most important variable
on all occasions during the growing season. Living cells in the
phloem showed a significant contribution to respiration in
April, June, and September, but not in July. The volume of
living xylem cells showed a significant, but weak (r 2 = 0.15,
P = 0.026) influence in September only. Nitrogen concentration per unit live cell volume did not show a significant contribution at any time during the year.
New standardized regression coefficients of growth rate and
volume of living phloem and xylem cells were used as indices
to estimate the relative contribution of each component to total
respiration during the season (Table 3). The contribution of
each fraction to total respiration was interpolated between the
measurement occasions and applied to the calculated daily
Figure 2. Seasonal variation in the relationship between stem
respiration and temperature (Q10) in Norway spruce trees. Values
were derived from measurements made on four trees on each
occasion.
Figure 4. Time lag between stem CO2 evolution and changes in stem
temperature in Norway spruce trees. Temperature was measured 1-2 mm below the cambium. Error bars show standard error of the mean
(n = 4).
Figure 3. Relationship between temperature and stem respiration
(µmol m −2 s −1) in stems of Norway spruce trees growing in control
(filled symbols) and irrigated--fertilized (open symbols) treatments.
Measurements were made in mid-July on two trees per treatment; Q10
= 2.03, SE = 0.015.
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160
STOCKFORS AND LINDER
Figure 5. Seasonal
variations in rate of
diameter growth
(A) and respiration
(B) at 10 °C in
stems of Norway
spruce trees. Results are based on in
situ measurements
of 10 trees per treatment; control (j)
and irrigated-fertilized (s).
Table 2. Regression analysis of growth respiration (G) and maintenance respiration of xylem (X) and phloem (P) in Norway spruce trees. The
model equation included all variables that gave a significant (P < 0.05) contribution to total respiration using Type III sums of squares. In the model,
growth was the time-lagged stem expansion rate (cf. Figure 5) except for the whole-season estimate (June to September), where growth was total
seasonal increase in volume of measured stem section. Regressions were based on all 20 trees (C and IL). Abbreviations: ns = nonsignificant at
5% significance level; na = not applicable. Units for growth are mm day --1 and mm year --1 for single date and June--September equations,
respectively. Phloem and xylem are both expressed as cm3 of live cells in the cuvette.
Date
Component
P-value
r2
Model equation
r2
June 5, 1993
Growth (G)
Phloem (P)
Xylem (X)
0.0001
0.0193
ns
0.612
0.046
ns
19.2G + 0.194P + 0.249
0.891
June 19, 1993
Growth
Phloem
Xylem
0.0001
0.0023
ns
0.399
0.148
ns
22.9G + 0.490P -- 0.260
0.818
July 10, 1993
Growth
Phloem
Xylem
0.0001
ns
ns
0.669
ns
ns
30.5G + 1.795
0.669
July 28, 1993
Growth
Phloem
Xylem
0.0001
ns
ns
0.694
ns
ns
34.6G + 1.173
0.694
August 19, 1993
Growth
Phloem
Xylem
0.0001
ns
ns
0.749
ns
ns
44.4G + 0.499
0.749
September 15, 1993
Growth
Phloem
Xylem
0.0062
0.0253
0.0255
0.259
0.145
0.145
50.8G + 0.2993P + 0.120X -- 0.219
0.646
April 24, 1994
Growth
Phloem
Xylem
na
0.0019
ns
na
0.423
ns
0.405P -- 0.082
0.423
June to September 1993
Growth
Phloem
Xylem
0.0001
ns
ns
0.794
ns
ns
4.14G + 10.2
0.794
respiration rates (Figure 6). This simulation indicated that from
mid-June to mid-September growth respiration was the main
source of respiratory CO2. The main part of maintenance
respiration was related to the phloem (Table 3). Maintenance
respiration reached its highest values in mid-May, whereas the
growth respiration fraction peaked during July (Figure 6). The
high maintenance respiration in May was the result of exceptionally warm weather, with a mean temperature of 8.6 °C and
TREE PHYSIOLOGY VOLUME 18, 1998
STEM RESPIRATION IN NORWAY SPRUCE
161
Table 3. Estimated contributions of different components to total
respiration in stems of Norway spruce trees, using new standardized
regression coefficients (Bring 1994). In the regressions, growth was
the time-lagged stem expansion rate (cf. Figure 5), except for the
whole-season estimate (June to September), where growth was the
total seasonal increase in volume of the measured stem section. Regressions were based on all 20 trees (C and IL).
Date
Component
New standardized coefficient
June 5
1993
Growth
Phloem
Xylem
1.674
0.561
0.225
June 19
1993
Growth
Phloem
Xylem
1.887
1.376
0.201
July 10
1993
Growth
Phloem
Xylem
1.818
1.439
0.476
July 28
1993
Growth
Phloem
Xylem
2.077
0.600
0.234
August 19
1993
Growth
Phloem
Xylem
2.735
1.061
0.538
September 15
1993
Growth
Phloem
Xylem
1.426
0.537
0.415
April 24
1994
Growth
Phloem
Xylem
0
1.182
0.602
June to September
1993
Growth
Phloem
Xylem
3.778
2.631
1.308
daily means up to 19 °C. Integration of each fraction over the
growing season showed that growth respiration was the largest
respiratory cost (59%, 13.7 mol m −2), followed by phloem
maintenance (30%, 7.0 mol m −2) and xylem maintenance
(11%, 2.5 mol m −2). On an annual basis, growth respiration
was approximately 40% of total respiration (Table 4) and
maintenance respiration of the phloem was of similar magnitude.
The partitioning of different sources of respiration was
slightly different when regressions were estimated from total
seasonal respiration of each tree (Method 2). When the growing season respiration was regressed against annual growth and
phloem and xylem live cell volumes, the new standardized
regression coefficients were 3.78, 2.63 and 1.31, respectively.
Method 2 thus implied that growth was the source of 51% of
evolved CO2 (11.8 mol m −2), which was close to the estimate
obtained by Method 1 (59%, 13.7 mol m −2).
The results obtained when assuming that maintenance respiration, measured at 10 °C in April, would be constant
throughout the year (Method 3) differed from the other meth-
Figure 6. Annual variations in daily mean stem temperatures (A)
measured 1--2 mm inside the cambium, and estimated daily stem
respiration rates (B) separated into growth respiration and maintenance respiration of xylem and phloem, respectively (Method 1). For
further explanations, see text.
ods used. The main difference was the proportion between
growth and maintenance respiration (Table 4).
Growth respiration was estimated as the residual after subtracting total respiration measured in April from total respiration measured on each occasion (Figure 7). The residuals were
Table 4. Estimated absolute and relative contributions of different
components to seasonal and annual stem respiration in Norway spruce
trees. Values were estimated for an average tree and expressed in
mol m −2 (stem surface) or as a percentage (%) of the total. Three
methods were used for the estimations. For further explanations, see
text.
Method
Component
June to September January to December
mol m −2 (%)
mol m −2 (%)
1
1
1
Growth
Phloem
Xylem
13.7 (59)
7.0 (30)
2.5 (11)
14.4 (40)
15.9 (44)
6.1 (16)
2
2
2
Growth
Phloem
Xylem
11.8 (51)
7.7 (33)
3.7 (16)
17.8 (49)
12.4 (34)
6.2 (17)
3
3
3
Growth
Phloem
Xylem
8.7 (38)
11.5 (49)
3.0 (13)
9.0 (26)
18.1 (59)
9.3 (15)
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162
STOCKFORS AND LINDER
Figure 7. Rate of stem growth in
relation to estimated growth respiration rates at 10 °C for different
sampling occasions during the
growing season. Growth respiration was estimated as the residual
after subtracting respiration (maintenance) rates (at 10 °C) in April.
Sampling dates were June 5 (A),
June 19 (B), July 10 (C), July 28
(D), August 19 (E), and September 15 (F). Solid lines represent regressions where the intercept was
set to zero, and broken lines indicate regressions where the intercepts were significantly different
from zero. Symbols (s) and (j)
are irrigated--fertilized and control
trees, respectively. When the intercept was set to zero, the r 2-values
(squared correlation coefficients)
of regressions were 0.65 (June 5),
0.86 (June 19), 0.67 (July 10),
0.93 (July 28), 0.84 (August 19),
and 0.21 (September 15), respectively. The intercepts on July 10
(0.65) and September 15 (--0.21)
were significantly different from
zero (P = 0.0003 and 0.041, respectively). For further explanations, see text.
significantly affected by growth (time-lagged stem expansion
rates) at all times, but the correlation was weak in September
(r 2 = 0.21, P = 0.046), when the growth of most trees had
ceased (Figure 7F). Rates of respiration were lower in September than in April, except for some of the fastest growing trees.
With the intercept set to zero, r 2-values, calculated as the
squared correlation coefficient between the regressand and the
regressor, varied between 0.65 and 0.93. The intercept was
significantly different from zero on July 10 and September 15.
When Method 3 was used to estimate the contribution of
growth respiration to total respiration during the growing season, the lowest proportion was in June (23%) and the highest
in July (51%). In September, growth respiration was zero or
became negative (Figure 7F). Interpolation of the estimated
growth respiration for the growing season showed that the
sources of total seasonal respiration were growth (38%, 8.7
mol m −2), phloem maintenance (49%, 11.5 mol m −2), and
xylem maintenance (13%, 3.0 mol m −2). On an annual basis,
this method indicated that growth respiration was less than a
third of the annual respiration cost, which was dominated by
the cost of phloem maintenance (Table 4).
The IL treatment affected both growth and respiration (Figure 5). Growth rates (stem expansion rates) were higher for
fertilized trees throughout the season (Figure 5A), and stem
growth ceased later for fertilized trees than for control trees.
This result was supported by the finding that partitioning
between growth and maintenance respiration, according to the
methods used here, was similar for the two treatments from
April to July (t-test, P > 0.25). In August and September,
however, the fraction of respiratory CO2 related to growth was
almost twice as high for fertilized trees as for control trees
(August, P = 0.004; September, P = 0.002). The IL treatment
also increased maintenance respiration by increasing [N] and
live cell volumes in both phloem and xylem tissues (Table 1);
however, it did not change the amount of nitrogen per unit of
live cell volume, which was 85.8 (C) and 84.5 (IL) mg cm −3,
respectively.
TREE PHYSIOLOGY VOLUME 18, 1998
STEM RESPIRATION IN NORWAY SPRUCE
Discussion
Tissue [N] and maintenance respiration are strongly correlated
in crop legumes (Irving and Silsbury 1987), but data showing
such a relationship for woody tissue in conifers is lacking (see
review by Sprugel et al. 1995). It has, however, been suggested
that tissue nitrogen concentration may be used to predict maintenance respiration for all tissues (Ryan 1991a, 1991b). Increased stem respiration in response to fertilization has been
reported by Brix (1971) and Ryan et al. (1996). Nitrogen
fertilization may affect stem respiration (i) by increasing
growth rates, (ii) by increasing live cell volumes, i.e., size or
number of living cells, and (iii) by increasing the protein
concentration of the cells ([N]) and thereby protein turnover.
Fertilization of young Norway spruce stands resulted in
increased stem growth, as well as increased [N] in xylem and
phloem (Table 1). There was an effect on the distribution of
living cells in the xylem and phloem (Figure 1) and a significant increase in their relative volume (Table 1). Most live cells
were found in the phloem, 80% in control trees and 68% in
IL-treated trees, which contrasts with data obtained for Pinus
contorta and Picea engelmannii, where the xylem contained
most of the living cells (Ryan 1990). Nitrogen was, however,
more evenly distributed between the two fractions, with
phloem containing 46% and 41% of nitrogen in control and
fertilized trees, respectively. The skewed distribution of living
cells and, to a lesser extent, nitrogen, toward the stem surface
indicated that, for these young Norway spruce trees, surface
area should be a better base than sapwood volume for expressing rates of respiration. In practice, however, there was no
major difference between use of surface area (r 2 = 0.79) and
sapwood volume (r 2 = 0.70) when estimating seasonal respiration.
On each measurement occasion, the relationship between
temperature and rate of respiration had a good fit to an exponential equation (Figure 3), but the Q10-values had a pronounced seasonal variation (Figure 2), although this variation
(1.92--2.55) was within the normal range reported for conifer
respiration (cf. Ryan et al. 1994, Sprugel et al. 1995). This
seasonal variation in Q10 contrasts with data obtained for Pinus
sylvestris L., where Q10 was close to 2.0 throughout the year,
but base respiration at constant temperature exhibited a large
variation during the year (Linder and Troeng 1980, 1981).
Seasonal variation similar to that found in the present study
was reported by Paembonan et al. (1991), when they monitored CO2 efflux from a Chamaecyparis obtusa (Siebold &
Zucc.) Endl. tree over 3 years.
The pronounced seasonal effect on the time lag between a
change in stem temperature and CO2 efflux (Figure 4) indicates a problem when scaling seasonal respiration based on
short time measurements. Respiration measurements should
preferably extend over at least 24 h. Variation in tissue temperature within and between trees is also a problem when small
sample measurements are scaled to whole trees (cf. Darby and
Gates 1966). In the present study, all measurements were
performed at the same height and direction on all trees; however, Sprugel (1990) reported a 10- to 40-fold difference in
rates of respiration, expressed per unit of stem area, both
163
within and between young trees of Abies amabilis Dougl. Ex
J. Forbes. By contrast, Ryan et al. (1996) did not find such
variation when measuring stem respiration in tall trees of Pinus
radiata D. Don, indicating a species-specific variation.
Reasons for a time lag between changes in stem temperature
and efflux of CO2 are not clear, but low permeability of gases
through cambium and bark would result in such a response
pattern. Another suggestion is that there is a significant upward
transport of CO2 in the transpiration stream and that CO2
released at a certain level of the stem, or from the needles,
partly originates from lower parts of the stem or the roots (e.g.,
Negisi 1979, Hari et al. 1991, Martin et al. 1994). This assumption is based on the coincidence of observed midday depressions in stem respiration rates with increased transpiration
rates (Negisi 1972, 1975, Martin et al. 1994). Such midday
depressions were not observed at any time during our measurements, and xylem transport cannot explain the observed lag
between temperature changes and CO2 efflux (Figure 4).
The seasonal pattern of time lag between respired CO2 and
temperature is similar to the seasonal pattern in sapwood CO2
concentration found in Norway spruce by Eklund (1990). He
reported that sapwood CO2 concentration in stems increased
through June and July, then decreased again until the end of
August reaching a new peak in late September. These fluctuations could be explained by changing rates of respiration
(Figure 5B) in combination with a seasonal variation in permeability of the cambial region. Increase in sapwood CO2 concentration found by Eklund (1990) in autumn may be the effect of
decreased permeability caused by winter-hardening processes,
which involve changes in protoplasmic viscosity, cell sizes and
concentration of cell constituents (cf. Larcher et al. 1973).
The IL treatment had a pronounced effect on the absolute
amount of total respiration, but no major effect on the seasonal
course when compared at a constant temperature (Figure 5B).
The increase in maintenance respiration was mainly the effect
of increased live cell volumes, but no fertilization (or nitrogen)
effect could be seen on respiration per unit of live cells (P =
0.57). The other major contributor to the increase in total
respiration was growth respiration.
Nitrogen content and live cell volume were equally strong
predictors of total respiration during the growth period. In
April, however, when no growth respiration occurred, respiration was more closely correlated with live cell volume (P =
0.0017, r 2 = 0.53) than with nitrogen content (P = 0.020, r 2 =
0.35). This difference in the usefulness of nitrogen content as
a predictor of respiration may be caused by the strong relationship between nitrogen content, especially xylem nitrogen content, and growth (P < 0.0001, r 2 = 0.69). Nitrogen content is
therefore a more useful predictor of growth and growth respiration than of maintenance respiration. A limitation to the
derived relationships, however, is that all structural components were determined at the end of the growing season and
cannot be assumed to have been the same throughout the
period of study.
The different methods used to separate growth and maintenance respiration gave somewhat different results (Tables 3
and 4). Methods based on linear regressions (Methods 1 and 2)
estimated that growth was the source of 51 to 59% of total
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164
STOCKFORS AND LINDER
respiration on a seasonal (June to September) basis, and 40 to
49% on a whole-year basis. The third method, which was
based on the assumption that maintenance respiration, at constant temperature, is constant throughout the year, gave a much
lower estimate of growth respiration; only 38% of the respiration from June to September, and 26% of annual respiration,
was related to growth (Table 4). It should be noted that the
absolute and relative proportions between different components of respiration will be affected by species, by length of
growing season, by site fertility and by climate, and should
therefore not be used as constants when modeling respiration
of trees and stands. In the present study, for instance, maintenance respiration was probably higher than normal as a result
of an unusually warm May (Figure 6).
The assumption that base respiration is constant throughout
the season can be questioned. Respiration has been shown to
acclimate to changes in temperature, both in seedlings grown
under controlled conditions (e.g., Rook 1969, Strain et al.
1976) and trees grown under natural conditions in the field
(Larcher 1961, Linder and Troeng 1980, 1981, Paembonan
et al. 1991). Respiration rates of control trees were lower in
September than in April (dormant season). In IL-treated trees,
where four trees were still growing in September, the rates in
September were similar to those in April (Figure 4). According
to Method 3, many trees had negative values for growth respiration in August and September (Figure 7). Similar results
were obtained by Sprugel (1990) who used mid-September
measurements to represent dormant season (maintenance) respiration rates. In Sprugel’s study, some trees even showed
negative growth respiration in the middle of the growing season.
Because plants acclimated to higher temperatures have
lower respiration rates than plants acclimated to low temperatures, when measured at the same temperature, the use of
dormant-season rates to represent seasonal base respiration is
likely to overestimate maintenance respiration during the
warmer period. Therefore, despite inherent uncertainties, estimates based on regression techniques of the contribution of the
various sources of respiration should be regarded as more
reliable than estimates based on the assumption of a constant
basal rate of maintenance respiration.
A common approach to estimation of growth respiration is
to use a theoretically derived ratio between the amount of
carbon respired and the amount of biomass produced (Penning
de Vries 1972, Chung and Barnes 1977, Ryan et al. 1996).
When calculating this ratio, based on the different estimates of
growth respiration for our trees, there was considerable variation, depending on the method used. Estimates based on
Methods 1 and 2 gave similar results, 0.16 and 0.20 g carbon
(C) respired per g C incorporated into biomass, respectively.
When we tested the method of Vertregt and Penning de Vries
(1987), using carbon and ash content of the stem discs taken
after the growing season 1994, we obtained a similar result
(0.20 g C respired per g C incorporated into biomass). These
values are higher than those reported by Chung and Barnes
(1977) for Pinus Elliottii Engelm. stems (0.123--0.149), but
lower than those estimated by Ryan et al. (1996) for stems of
Pinus radiata (0.25), and by Penning de Vries (1972) for maize
(0.27). The use of Method 3 resulted in a construction constant
of 0.11, which is lower than any value reported in the literature.
Conclusions
The IL treatment affected stem respiration by increasing both
growth and live cell volumes of the stems. Fertilized trees had
higher respiration rates throughout the season, but there was no
fertilization or nitrogen effect on maintenance respiration per
unit of living cells.
The major source of total stem respiration was growth and
phloem maintenance. None of the methods used to separate the
sources of respiration ascribed more than 16% of evolved CO2
during the growing season (June to September) to xylem maintenance. The two regression methods gave similar partitioning
between growth and maintenance respiration, 51 and 59% to
growth respiration, respectively. Annually, growth respiration
accounted for 40 to 50% of total respiration. When using
dormant-season respiration to represent base maintenance respiration for the whole year, it is likely that growth respiration
is underestimated and maintenance respiration is overestimated.
Stem surface area was a better (not significantly) estimator
of respiration than sapwood volume, but the best estimator of
maintenance respiration was stem live cell volume. Stem [N]
was better correlated to stem growth than to maintenance
respiration, but these relationships should be used with caution, because the destructive sampling took place after the
growing season.
Acknowledgments
This study was made possible by financial support from The Swedish
Council of Forestry and Agricultural Research, and Swedish Environmental Protection Agency. We are grateful to G.I. Ågren and
T. Ericsson for constructive criticism during the preparation of the
manuscript, and to M.G. Ryan and D.G. Sprugel for valuable comments on the manuscript. Many thanks are due also to B.-O. Wigren
and U. Nylander for their skillful help in the field. This work contributes to the Global Change and Terrestrial Ecosystems (GCTE) Core
Project of the International Geosphere--Biosphere Programme
(IGBP).
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