Foliage dark respiration in Abies amabilis (Dougl.) Forbes: variation within the canopy

Tree Physiology 9,325-338 0 1991 Heron Publishing-Victoria, Canada

Foliage dark respiration in Abies amabilis (Dougl.) Forbes: variation within the canopy

J. RENEE BROOKS,’ THOMAS M. HINCKLEY,’ E. DAVID FORD2 and DOUGLAS G. SPRUGEL’ ’ College of Forest Resources, AR-IO, University of Washington, Seattle, WA 98195, USA 2 Centerfor Quantitative Sciences, HR-20, University @Washington, Seattle, WA 98195, USA

Received January 25, 1991

Summary

Dark respiration of foliage was measured in a 30-year-old stand of Abies amabilis in western Washington from June to November. Both laboratory and field measurements were used to study the effect of environmental and tree variables on respiration. Foliage respiration rates were most strongly influenced by needle temperature. After accounting for leaf temperature differences, foliage respiration decreased with depth in the canopy for all age classes of foliage. Respiration differences attributed to location within the canopy were greatest early in the growing season, but were still significant in November. Younger foliage respired more than older foliage in the upper canopy, but not in the lower canopy. Respiration differences due to foliage age were highly significant in the early growing season, but were not detectable by mid-October.

Introduction

Photosynthesis, its variation within the canopy of conifers, and the factors that affect it have been well described (e.g., Woodman 197 1, Schulze et al. 1977, Beadle et al. 1985, Ku11 and Koppel 1987). In contrast, except for a few studies (Linder 1981, Matyssek and Schulze 1988), foliar respiration in conifers, particularly over a wide range of foliage age classes and canopy positions, has been largely ignored even though respiration is a very important component in the carbon budget and growth of conifers. Whittaker (1975) estimated that 40 to 60 percent of the carbon initially fixed is lost through respiration in a temperate forest. How respiration varies temporally and spatially, and how this variation is related to environmental factors, has only been described in a few studies (Linder and Troeng 1980, Linder 1981). Differences in respiration among tissue types (roots, stems, cones, and leaves) and the factors controlling respiration of each tissue type have only begun to be investi- gated (e.g., Kuroiwa 1960, Linder and Troeng 1981, Linder 1981, Dick et al. 1990, Ryan 1990, Sprugel 1990, Mori and Hagihara 1991).

Abies amahilis (Dougl.) Forbes (Pacific silver fir) is a common species in the upper montane forests of the Pacific Northwest and grows naturally in a wide range of light conditions (Teskey et al. 1984, Tucker et al. 1987). Because morphological differences between sun and shade foliage are quite marked (Tucker et al. 1987), one might expect the foliage to exhibit significant environmentally controlled variation in photosynthesis and respiration. There might also be considerable age- and position-

326 BROOKS ET AL.

related variation in foliage respiration rates within a tree. Teskey et al. (1984) documented a wide variation of photosynthetic rates related to age in foliage from a single A. umahilis branch. Abies amahilis foliage is very long lived, and older foliage constitutes a large proportion of total foliage biomass. Needles live for 9-12 years in young trees and 18-23 years in mature trees (Grier et al. 198 1).

The objective of this study was to quantify temporal and spatial variations of foliage respiration within the crown of Abies umubilis. We used both field and laboratory investigations to characterize the effect of foliage age, position within the canopy, and temperature on rates of dark respiration.

Materials and methods

Overall study design

The study includes two components: one carried out under ambient conditions in the field and one carried out in controlled environments in the laboratory. The field study was designed to examine variation in respiration rates with foliage age and position within the canopy. Repeated measurements were made on the same foliage samples, but because all measurements were made at ambient temperatures, it was impractical to use these data to examine seasonal variation in respiration rates at any location. Only fully developed foliage was used in these studies because it was not possible to measure leaf area or biomass of growing foliage non-destructively at the time of each measurement. The controlled environment studies, in contrast, used different branches on each sampling date, and were designed to examine the influence of temperature on respiration of foliage of different ages, and to follow seasonal trends in respiration rates measured at the same temperature. Respiration of current foliage was included in the controlled-environment studies, with leaf area and mass measured immediately after respiration measurements.

Site

The research was conducted at a subalpine site (1140 m elevation) dominated by A. amubilis located in the Cedar River Watershed in the Cascade Mountains of western Washington (Grier et al. 1981). The stand was regenerated naturally following clearcutting in 1957, and is essentially even aged. Mean stand density in 1986 was 96,000 trees ha-’ (with about 30% of the trees < 1.3 m), but the stand was heterogeneous consisting of both open patches and dense clusters.

Two 9-m’ plots, which were similar in tree size and canopy structure, were selected for the study. Tree location, diameter, height, and height of the lowest living branch were recorded for all trees within the plots. Trees in the first plot ranged in height from 0.45 to 5.36 m with a mean of 3.45 m, and in diameter from 0.9 to 9.9 cm with a mean of 4.5 cm. Trees in the second plot ranged in height from 0.73 to 5.77 m (mean of 2.52 m), and in diameter from 1.1 to 10.9 cm (mean of 3.8 cm). Plot densities were 6.1 and 9.6 trees rne2, respectively (i.e., 61,000 and 96,000 trees ha-‘).

The first plot was used in the field study. During the growing season, respiration

FOLIAGE DARK RESPIRATION IN ABIES AMABZLZS 327

was measured repeatedly, under the prevailing field conditions, at permanent sampling locations within the canopy. The second plot was used as a source of sample branches for laboratory studies; one branch was harvested every other week and foliage respiration measured at different temperatures in a controlled environment chamber.

Techniques and measurements

Dark respiration was measured between 1000 and 1600 h on each sampling day using a portable IRGA (Analytical Development Company) and the Parkinson Conifer Chamber (chamber dimensions: 2.2 cm radius, 6.1 cm length). The IRGA and chamber were used in an open configuration. To measure dark respiration, the chamber was covered with a layer of black paper and then a layer of white paper to exclude light within the cuvette. A stabilized reading could be obtained between 1 and 5 min after the chamber had been sealed around a particular foliage sample and a measurement was recorded immediately after the reading stabilized. The CO2 differential between input and output air of the chamber typically ranged between 15 and 60 pl 1-l. To provide stable input concentrations of CO2 while making field measurements, air was drawn from a 2-liter bottle located on the forest floor several meters from the measurement site. Flow through the chamber caused the air in the bottle to be replaced approximately every 7 or 8 min. In the controlled environment study, compressed air from the laboratory was bubbled through water and pumped into the bottle. Source CO2 concentrations ranged from 340 to 380 ~11~’ under both field and laboratory conditions.

In both the field and laboratory studies, foliage temperature was measured immediately after each dark respiration measurement, using a cold junction compen- sated copper-constantan thermocouple made of thirty-gauge wire. Foliage temperatures remained at or near air temperature because all foliage samples were shaded before and during respiration measurements. Relative humidity, which was moni- tored using the sensor within the Parkinson chamber, remained relatively constant during measurement periods.

Projected foliage area was determined using a Li-Cor Model 3 100 leaf area meter. Needles were placed on clear sheets in a single non-overlapping row using double- sided tape, and measured in groups. Foliage samples were weighed after drying at 70 “C for 48 h.

Profiles of photosynthetic photon flux density (PPFD, 400-700 nm) were made in the first plot using the Li-Cor LI-1915B Line Quantum Sensor. For each profile, five light readings were recorded at 0.5-m intervals from ground level to 6.0 m. Four profiles were made on September 19 between 1000 and 1500 h. These profiles were averaged to describe the attenuation of light within the canopy.

Air temperature was measured periodically throughout the day while respiration was being measured. Air temperature was measured above the canopy using the shaded Parkinson chamber held open to permit ambient air to enter. Care was taken to ensure that shading did not interfere with air flow.

328 BROOKS ET AL.

Field study

Eight branches from five trees in the first plot were used to examine dark respiration under field conditions (Table 1). The trees ranged from 3.2 to 5.4 m in height and from dominant to moderately suppressed. Branches were selected from a range of canopy heights, and foliage samples on a branch were chosen to provide a range of foliage age classes (Table 1). Dark respiration was measured in situ every two weeks from June 20 to September 29, 1986. Samples were limited to mature tissue (1 year old and older), so leaf area of the samples remained constant over the measurement period. Each branch was covered for one hour before sampling to eliminate bursts in CO;! efflux after a light period (Azcon-Bieto and Osmond 1983), and the branch remained covered while respiration was being measured at the various locations on that branch. The order in which branches were measured during a sampling day was randomized to reduce diurnal biases. Each foliage sample was measured once on each sampling date. At the end of the season, September 29, all sample branches were harvested, and leaf area and weight of all the foliage samples were measured. Each sample contained between 10 and 40 cm* of foliage and between 0.1 and 5 cm* twig surface area.

Controlled environment studies

Variation in respiration with foliage age and response of respiration to temperature were measured under controlled conditions. Every other week from June 20 to November 17, a branch was selected from an upper crown position of a codominant tree in the second plot. Each branch was taken at the same distance from the ground and was, therefore, in approximately the same light environment (about 60% of the light at the top of the canopy). Branch ages ranged from 4 to 7 years with most branches being 5 years old. Five to nine foliage samples on each branch were selected to span a range of age classes. In these studies, the current expanding foliage was included, because it was possible to measure both leaf area and weight immediately after the respiration measurements had been completed.

Once a branch was selected, respiration of each foliage sample was measured in

Table 1. Locations of field study sample branches within the canopy, and the age classes sampled on that branch.

Foliage age (years)

Branch number (Height(m))

1 (4.7) 2 (4.7) 3 (4.0) 4 (3.5) 5 (3.1) 6 (2.6) 7 (2.4) 8 (1.9)

X X X X X X X X X X X X X X X X X X X

X X X X X

X

FOLIAGE DARK RESPIRATION IN ABIES AMABILIS 329

the field. After these measurements, the branch was removed from the tree, placed with the stem base in water, covered with plastic film and transported to the laboratory. In the laboratory, the branch was recut under water and allowed to hydrate overnight at 4 “C. The following day, respiration was measured at 5, 15, 25, and 35 “C in the dark in a Conviron growth chamber. The branch was allowed to equilibrate for 30 min at each temperature before respiration was measured. After the respiration measurements had been made, leaf area and weight were determined for the foliage samples.

Regression analysis

Regression residual analysis was used to determine a suitable statistical model to describe the effect of temperature on respiration over the range of temperatures used in the experiments (5-35 “C). Of possible models, linear and exponential equations were emphasized, and analysis of residuals from these indicated that a linear model was statistically more appropriate than an exponential model.

Once a linear model was selected to account for variation related to temperature, other variables were explored to help explain the remaining variation in respiration. To determine the importance of these variables in the model, regression analysis using dummy variables was used (Neter et al. 1985). For example, in the controlled environment study, three equations were developed and compared to determine the importance of age: one in which each foliage sample was kept separate, a second equation in which foliage samples in the same age class were combined, and a third in which all the samples were combined to give a simple linear equation between temperature and respiration. These equations were compared using a partial F test (Neter et al. 1985).

Results

Stand PPFD characteristics

Photosynthetic photon flux density decreased from a maximum of 1500 pmol mm2 S -’ at the top of the canopy (5.7 m) to 3 pmol m-2 s-’ at ground level. The greatest decrease in PPFD occurred in the top 3 m of the canopy, so that at 2.5 m above ground, PPFD was less than 10% of the above canopy value. At 4.5 and 3.5 m above ground, PPFD was 72 and 40% of the above canopy value, respectively. The light characteristics of the stand remained relatively constant throughout the season because of the the high density of the stand and the retention of 10 or more age classes of foliage. Seasonal needle gain and loss had little effect on light attenuation through the canopy other than shifting values slightly upward each year.

The sharp gradient in light resulted in changes in shoot and foliar morphology through the canopy. Silhouette area ratio, a measure of the degree of self shading on a shoot calculated by dividing the silhouette area by the total leaf area of a shoot (Tucker et al. 1987), ranged from 0.45 -t 0.02 for sun shoots at the top of the canopy to 0.84 f 0.06 for shade shoots at 2.5 m from the ground. Specific leaf area for

330 BROOKS ET AL.

l-year-old foliage was 3 1.3 cm* g-’ at the top of the canopy, 37.1 cm2 g-’ at 3 m from the ground, and 49.5 cm2 g-’ at 2.5 m from the ground. Other morphological properties of the foliage, including needle length, width and thickness, changed as irradiance decreased. Most of the change in silhouette area ratio and specific leaf area occurred below 3 m where light was less than 20% of that at the top of the canopy.

Field respiration study

Because the respiration chamber always contained a woody twig as well as needles, a preliminary investigation was conducted to determine if twigs contributed significantly to the measured rates of respiration. The needles were stripped from several twig segments and the respiration rates of these segments were measured on the same days as the regular field measurements of foliage + twig respiration. In general, respiration rates of the twigs alone were too low to measure accurately with the Parkinson system; typically, they were one tenth to one thirtieth those of foliage + twig. This is not surprising, because foliage area or mass was usually an order of magnitude greater than twig area or mass for any sample. Thus, although the results reported below are for foliage and twigs combined, twigs were a minor component, and the trends and patterns observed mainly reflect variation in foliage respiration. (For more information on woody-tissue respiration in A. amabilis see Sprugel 1990.)

Of the measured variables, temperature had the largest influence on respiration rates in the field (Figure l), with high rates measured on warm days and low rates measured on cool days. Mean air temperature during the sampling period for each measurement day varied from a low of 6 “C on July 14 to a high of 27 “C on August 20.

Jun JUI A’-‘g Sep Dates

Figure 1. Respiration under ambient conditions of I -year-old foliage at five different locations within the canopy and daily average air temperature (v) during the summer. The foliage samples were located at 2.4 m (W), 2.6 m (A), 3.1 m (V), 3.5 m (0) and 4.7 m (+) above the ground. The lines connecting consecutive measurements do not depict overall seasonal patterns because temperature and respiration were only measured once every two weeks, they are included to make the graph easier to read.

FOLIAGE DARK RESPIRATION IN ABIES AMABZLZS 331

In addition to the expected variation with temperature, respiration rates were influenced by location of the foliage within the canopy. The eight branches selected for respiration measurements spanned a range of light environments from less than 5 to 85% of the PPFD at the top of the canopy. For a given age class of foliage, respiration rates decreased from the highest to the lowest branch for any sampling date (Figure l), and the greatest differences were observed on warm days. When respiration rates of l-year-old foliage for branches from different heights were plotted against leaf temperature (Figure 2a), branches higher in the canopy had (1) higher rates of respiration for any given temperature, and (2) greater absolute changes in respiration with a change in temperature compared with lower canopy branches. Respiration of the lowest two sample branches, which did not produce any new foliage during the growing season, had respiration rates that were so low that we could not detect a response to temperature.

4 l-year-old

C l-year-old

B 4-year-old

D 4-year-old

0 5 10 15 20 25 30 0 5 10 15 20 25 30 35

Leaf Temperature (“C)

Figure 2. The relationship between leaf temperature and respiration under ambient conditions. The data for both graphs are pooled over the season.

(A and C) l-year-old foliage: the foliage samples were located at 2.4 m (m), 2.6 m (A), 3.1 m (V), 3.5 m (0) and 4.7 m (+) above the ground. The regression equations are as follows: for 4.7 m, R(la) = -0.42 + 0.152T and R(g) = -1.31 + 0.478T (2 = 0.970); for 3.5 m, R(la) = -0.34 + 0.106T and R(g) = -0.81 + 0.27OT (r2 = 0.978); for 3.1 m, R(la) = -0.33 + 0.077T and R(g) = -1.28 + 0.29OT (r2 = 0.929).

(B and D) 4-year-old foliage: the foliage samples were located at 2.4 m (m), 2.6 m (A), 3.5 m (0) and 4.0 m (e) above the ground. The regression equations are as follows: for 4.0 m, R(la) = -0.75 + 0.104T and R(g) = -2.5 + 0.34T (r’ = 0.820); for 3.5 m, R(la) = -0.26 + 0.049T and R(g) = -0.83 + 0.16T (2 = 0.950); for 2.6 m R(la) =-0.21 + 0.029T and R(g) = -0.79 + O.llT (r* = 0.710).

332 BROOKS ET AL.

Foliage age also affected rates of respiration at any given height in the canopy. The regressions of respiration rates on temperature had decreasing slopes for foliage of increasing age; for example, the relationship for l-year-old foliage (Figure 2a) had a significantly greater slope than that for 4-year-old foliage (Figure 2b) at the same canopy location. The pattern remained the same when the data were expressed on a leaf dry weight basis (Figures 2c and 2d). Thus, the changes in respiration within the canopy are not related to changes in specific leaf area.

To examine the interaction between position and foliage age, we calculated the rates of respiration in one- and four-year-old foliage at 20 “C based on the data presented in Figures 2a and 2b (Figure 3). Respiration rates decreased at lower positions within the canopy for both age classes of foliage, but the respiration rates of 1 -year-old foliage changed more through the canopy than those of the 4-year-old foliage. At 3.5 m above ground, the l-year-old foliage respired at twice the rate of the 4-year-old foliage (1.80 versus 0.90 ,umol m-* SK’), but at 2.5 m above ground there was no difference between the respiration rates of the two age classes of foliage (0.38 versus 0.37 urn01 mm2 s-l).

Controlled environment respiration study

The response of respiration to temperature for different age classes of foliage is shown for samples taken at three dates during the growing season (Figure 4). Respiration rates for all age classes changed during the season, but the changes in fully developed foliage were minor; only current-year foliage showed a dramatic change in respiration rates during the growing season. For the branch harvested on July 14, during active shoot elongation, rates of respiration in currently expanding foliage were very high, reaching a rate of 6.3 pmol m-* SK’ at 33 “C. Rates were lower

6 ,

I 0.0 0.5 1.0 1.5 2.0 2.5 3.0

-2 -1 Respiration (pmol-m ‘s )

Figure 3. A comparison of respiration rates at 20 “C of l-year-old and 4-year-old foliage. The values were calculated using the equations from Figures 2a and 2b.


A ‘; cn

7

6 A Jul. 14 l

5 --

4 --

3 .-

2 --

1 --

0 N‘ 'E 6 -- t3 Aug. 21

z 6-- C Oct. 15

5 --

4 --

3 --

2 --

1 --

0 I I 0 5 10 15 20 25 30 35


Figure 4. The relationship between leaf temperature and respiration under controlled conditions (closed symbols) for current-year (+,O), I-2-year-old (0,O) and 3-5-year-old (A, A) foliage. Open symbols are respiration rates measured in the field under ambient conditions. For graphs A, B and C, the sample branches were located at 3.1,3.1 and 3.0 m above the ground and were 6,4 and 5 years old, respectively.

for the older age classes of foliage, but there was a significant difference in temperature responses between the 1- and 2-year-old foliage group and the 3- and Syear-old foliage group. At 33 “C, 1-Zyear-old foliage respired at an average of 3.0 ymP2 s-l, whereas 3-Syear-old foliage respired at 2.0 pmol mm2 s-’ at 33 “C. Temperature alone explained only 59% of the variation in early season respiration, but by including an age class variable with temperature, 96% of the variation could be explained. The added age variable was highly significant in predicting respiration for the early season sample (P < 0.001). On August 21, after shoot elongation had ceased, respiration rates of newly expanded foliage had declined to 3.6 pmol mm2 s-’ at 33 “C, whereas fully developed foliage respired at 2.5 pmol mS2 s-’ at 33 “C. Differences between age classes were smaller than earlier in the season, but foliage age and temperature together still explained significantly more variation in respira-

334 BROOKS ET AL.

tion (91%) than temperature alone (84%; P < 0.005). In mid-October, two months after growth had ceased, respiration rates of different age classes were not significantly different (P > 0.2). The highest rate, 2.7 pmol m-* SK’ at 33 ‘C, was measured on 3-year-old foliage. Temperature alone explained 91% of the variation.

The finding that differences in rates of respiration with age disappeared by mid-October suggested that differences associated with canopy position might also have disappeared at the end of the growing season. To test this, another controlled environment experiment was conducted on November 17 with branches from 3.5 and 2.0 m in the canopy (Figure 5). No significant difference in respiration was found between age classes on a branch, but there was a difference between the branches (P < 0.001). The highest rate for the upper branch was 2.0 pmol m-* SK’ at 28.5 “C measured on 3-year-old foliage, whereas the maximum rate for the lower branch was 1.1 pmol m-* SK’ at 29.0 “C measured on 5-year-old foliage. Temperature alone explained 75% of the variation in respiration rates; however, by including a branch location variable, the percentage of variation explained was increased to 90%.

Discussion

Comparisons with other work

Foliage respiration rates measured in this study (less than 0.1 to 3.2 pmol m-* s-l at 20 “C) are comparable to those measured previously by Teskey et al. (1984), who found rates ranging from 1.5 to 4.0 pmol mm2 SK’ for l-year-old foliage of A. amahilis. Our rates are generally higher than rates reported by Larcher (1983) for

I 0 5 10 15 20 25 30 35


Figure 5. The relationship between leaf temperature and respiration under controlled conditions for an upper (3.5 m) and a lower canopy (2 m) branch on November 17. Branch ages were 5 and 10 years old, respectively. Foliage ages of the upper branch were current-year, l-year and 3-year, and for the lower branch they were 3-year and S-year.


evergreen conifers (between 0.13 and 0.63 pmol m-* s-i at 20 “C), but other authors have also measured respiration rates higher than those given by Larcher: rates of 2.3, 2.5, and 3.2 pmol m -2 s-l have been reported for Pinus sylvestris (Leverenz and Jarvis 1979), Pseudotsuga menziesii (Brix 1971), and Chamaecyparis obtusa (Hagihara and Hozumi 1977), respectively.

Factors affecting respiration

Both canopy position and foliage age had significant effects on foliage respiration rates. Position had the greater effect; the respiration of l-year-old foliage at 4.7 m was about six times that of foliage of the same age at 2.6 m (Figure 3). The greatest age-related differences in respiration were between current and older foliage in mid-July (Figure 4a). Very high respiration rates in developing foliage have been observed previously (Brix 1971, Ceulemans and Impens 1979, Dougherty et al. 1979, Gowin et al. 1980, Teskey et al. 1984), reflecting the metabolic activity related to the construction of new foliage. However, even in mature foliage, respiration rates were found to vary with foliage age, season, and location within the canopy.

The pattern of respiration within the A. amabilis crown was similar to canopy photosynthetic patterns in A. amabilis (Teskey et al. 1984) and other conifers (e.g., Woodman 1971, Watts et al. 1976, Troeng and Linder 1982, Beadle et al. 1985, Ku11 and Koppel 1987), i.e., respiration rates were highest in the upper, exposed parts of the canopy and in younger tissues, and decreased with increasing canopy depth and needle age. The simplest explanation for this pattern is that respiration rates are closely coupled with photosynthetic rates (Ludwig et al. 1975), and that photosynthetic rates are controlled by light availability (which decreases with depth in the canopy) and foliage age (e.g., Ceulemans and Impens 1979, Mooney et al. 1981, Horn and Oechel 1983, Teskey et al. 1984, Ticha et al. 1985, Nilsen et al. 1988).

The existence of a close relationship between photosynthesis and dark respiration is not surprising. According to Penning de Vries (1975), the major processes respon- sible for respiration in mature tissues are protein turnover and active transport to maintain ionic gradients. The rate of both processes will decrease with a decrease in photosynthetic activity. Over the longer term, decreased PPFD would lead to a decrease in the size of the photosynthetic enzyme pool (Gauhl 1976, Bjorkman 1981), which would decrease respiration even more.

Decreased respiration in older leaves is also not surprising. As foliage ages, it exists in an increasingly shady environment as new foliage grows above and around it. Further, leaf nitrogen decreases as leaves age (Kuroiwa 1960, Field 1983, Field and Mooney 1983, Meier et al. 1985) and leaves become further removed from the actively growing shoots (strong sinks). All of these changes will tend to decrease photosynthetic activity and, consequently, to decrease respiration (Ludwig et al. 1975, Hagihara and Hozumi 1977, Bassman and Dickmann 1982, Baysdorfer and Bassham 1985, Field and Mooney 1986).

The absence of respiration differences associated with age classes at the end of the season (Figure 4c) was somewhat surprising because Teskey et al. (1984) found age related variation in photosynthesis at the end of the season. However, the greatest

336 BROOKS ET AL.

seasonal change in respiration was noted in current tissue; respiration decreased sharply as tissue matured. Older age classes of foliage showed only small changes in respiration during the growing season. These changes in mature tissue may reflect a change in the overall metabolic activity of the tree. During the active growing season, when shoot growth was rapid, foliage-especially young foliage near the actively growing shoots-was probably functioning at high rates and respiration was high. Teskey et al. (1984) found that photosynthetic rates of l-year-old needles under optimal conditions were highest in July and were 36% lower in September. When aboveground growth ceased, all respiration rates were much lower, so differences in respiration rates among different age classes of foliage may have been too small to detect.

Implications

Descriptions of temporal and spatial variations of foliage respiration can be useful in understanding branch, canopy, and stand level processes, particularly those relating to carbon exchange and productivity. In a closed canopy, the PPFD a branch receives decreases each growing season. Initially, new foliage is added each year, but even- tually the production of new foliage decreases and finally stops and the branch dies (Forward and Nolan 1961, Hinckley et al. 1984). The present study indicates that the energy needs of foliage also decrease sharply as it is overtopped in the canopy. This reduction in carbohydrate demand may explain the persistence of A. amabilis branches in extremely low light environments. Some branches on trees in this study had produced no new shoots for at least eight years. A few of them had needles up to 15 years old. With rates of foliage respiration in the lower canopy approximately one sixth of that in the upper canopy, it is easier to understand how the lower branches survive.

Acknowledgments

We are grateful to L. Soden and S. Ohmann for their assistance in the field. J. Simpson provided statistical advice. Unpublished data from G.F. Tucker and K. Sorrenson are acknowledged. The City of Seattle (Cedar River Watershed) granted access to and use of the research site. This research was supported by National Science Foundation Grant BSR - 8415990 and USDA Competitive Grant 86.FSTY-9-0220.

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Documents

Foliage dark respiration in Abies amabilis (Dougl.) Forbes: variation within the canopy