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Annals of Botany 90: 325-335, 2002
© 2002 Annals of Botany Company

Measuring and Simulating Crown Respiration of Scots Pine with Increased Temperature and Carbon Dioxide Enrichment

K.-Y. WANG*,1,2, TIANSHAN ZHA1 and S. KELLOMÄKI1

1 Faculty of Forestry, University of Joensuu, PO Box 111, FIN-80101 Joensuu, Finland 2 Chengdu Institute of Biology, Chinese Academy of Sciences, PO Box 416, 610041 Chengdu, P. R. China

* For correspondence. Chengdu Institute of Biology, Chinese Academy of Sciences, PO Box 416, 610041 Chengdu, P.R. China. Fax +86 28 85222 753, e-mail wangky{at}cib.ac.cn

Received: 14 March 2002; Returned for revision: 1 May 2002; Accepted: 22 May 2002


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 APPENDIX
 LITERATURE CITED
 

Acclimation to elevated atmospheric carbon dioxide concentration and temperature of respiration by the foliage in the crown of Scots pine (Pinus sylvestris) trees is measured and modelled. Starting in 1996, individual 20-year-old trees were enclosed in chambers and exposed to either normal ambient conditions (CON), elevated CO2 concentration (EC), elevated temperature (ET) or a combination of EC and ET (ECT). Respiration of individual leaves within the crown was measured in 2000. To extrapolate the response of respiration of individual leaves to the whole crown, a multi-layer model was developed and used to predict daily and annual crown respiration, in which the crown structure and corresponding microclimate data were used as input. Respiration measurements showed that EC led to higher Q10 values (4·6 %) relative to CON, but lower basal respiration rates at 20 °C [Rl.d(20)] (–7·1 %) during the main growth season (days 120–240), whereas ET and ECT both reduced Q10 (–12·0 and –9·8 %, respectively) throughout the year but increased Rl.d(20) (27·2 and 21·6 %, respectively) during the period of no-growth, and slightly reduced Rl.d(20) (–1·7 and –2·8 %, respectively) during the main growth season. Model computations showed that annual crown respiration increased: (1) by 16 % in EC, with 92 % of this increase attributable to the increase in foliage area; (2) by 35 % in ET, with 66 % related to the increase in foliage area and 17 % to the rise in ambient temperature; and (3) by 27 % in the case of ECT, with 43 % attributable to the increase in foliage area and 29 % to the rise in ambient temperature. Changed respiration parameters for individual leaves, induced by treatments, made only a small contribution to the annual crown respiration compared with the increased foliage area. The effects of changes in crown architecture and nitrogen distribution, caused by treatments, on the daily and annual course of crown respiration are discussed.

Key words: Environment-controlled chambers, CO2 and temperature elevation, crown respiration, simulation, Scots pine.


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 APPENDIX
 LITERATURE CITED
 
The importance of the response of plant respiration to changes in atmospheric CO2 and temperature is acknowledged not only because respiration supports growth and maintenance processes, but also because it is an important component of plant productivity and carbon balance (Penning de Vries, 1972; Amthor, 2000). Given the 30–60 % loss of assimilated carbon due to respiration (Ryan, 1991a), study of the variation in the rate of respiration is critical in determining the response of plants and vegetation on a wide scale to predicted global change.

Respiration of leaves is significantly affected by CO2 enrichment (reviewed by Amthor, 1991; Ryan, 1991a; Drake et al., 1999). Based on the literature, Amthor (1991) proposed two ways in which CO2 could influence respiration: directly through respiratory metabolism, or indirectly through acclimation of growth. These mechanisms have been examined to improve the understanding of respiratory responses of leaves to CO2 enrichment (Wullschleger et al., 1992; Drake et al., 1999; Gonzalez-Meler et al., 1999). Although responses of the canopy can, in part, reflect those of the leaf, canopy respiration could be greatly affected by canopy architecture (Wang, 1996; Gielen et al., 2002), microclimate (Bazzaz and Williams, 1991; Kellomäki and Wang, 2000) and variations in the properties of leaves in different positions within the canopy (Terashima and Hikosaka, 1995; Wang et al., 1998; Griffin et al., 2001).

Long-term experiments have shown that elevated CO2 and temperature can change canopy structure and the pattern of nitrogen distribution, as well as the physiological characteristics of foliage (Radoglou and Jarvis, 1990; EI Kohen and Mousseau, 1994; Kellomäki and Wang, 1997; Gielen et al., 2002). These changes may not only alter the respiratory surface area per unit ground area, but also affect the responses of individual leaves within the canopy to CO2 and temperature. This may increase the difficulty of scaling-up respiration from individual leaves to the canopy, and could be one of the reasons for the inconsistency in the response of respiration between individual leaves and the whole plant (Gonzalez-Meler and Siedow, 1999).

Respiration of a whole tree or whole ecosystem can be estimated by measuring gas exchange in an experimental chamber (Baker et al., 2000), but it is difficult to quantify the relative importance of direct vs. indirect effects in determining the respiratory response of a whole tree subjected to long-term CO2 enrichment or temperature change, or to assess the contributions of different components (soil, leaves or stems). Several models for scaling up respiration from leaves to canopy appear to have great potential for integrating information on leaf physiology to the canopy (Ryan, 1991b, 1995; Amthor, 1994; Reich et al., 1998), where respiration by leaves can be estimated as a function of temperature and tissue nitrogen concentration (Ryan, 1991b; Amthor, 1994). Annual canopy respiratory losses can be modelled from the relationship between respiration and nitrogen concentration, annual temperature data and estimates of total leaf biomass or surface area (Ryan, 1991b). However, little work has been done to characterize the spatial distribution of respiration within the tree crown, and to assess how it may vary with season and duration of exposure to elevated CO2 and temperature.

Starting in 1996, the growth responses of Scots pines (Pinus sylvestris L.) to long-term elevation in CO2 and temperature were studied under controlled conditions (Kellomäki et al., 2000). The aims of the present work were to: (1) measure acclimation of crown properties and respiration of individual leaves to elevated CO2 and temperature in the fourth year of exposure; (2) investigate the annual course of respiration of leaves; and (3) simulate the response of crown respiration to CO2 and temperature elevation by means of a simple respiration model, using leaf-respiration parameters, crown structure and the microclimatic records for each treatment throughout the year (2000) as input.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 CONCLUSIONS
 APPENDIX
 LITERATURE CITED
 
Chamber system and treatments
Experiments were performed in a naturally seeded and growing stand of Scots pine located near the Mekrijärvi Research Station (62°47'N, 30°58'E, 145 m a.s.l.), Univer sity of Joensuu, Finland. The soil is a sandy loam with a water-holding capacity of 40 mm at field capacity and 20 mm at the wilting point for the top 30 cm. Details of the site were provided by Kellomäki and Wang (1997).

In 1996, 16 trees were enclosed individually in closed-top chambers. The trees were approx. 20 years old and had a similar mean height (3·5 m) and crown size. The effects of four treatment combinations of CO2 and temperature were studied: (1) ambient temperature and CO2 concentration (CON); (2) elevated CO2 (EC); (3) elevated temperature (ET); and (4) elevated CO2 and temperature (ECT). Each treatment had four replicates.

The chambers were approximately cylindrical, with eight walls, an internal volume of approx. 26·5 m3 and a ground area of 5·9 m2. The four walls facing south and west were constructed of special heating glass with a thin resistance element converting electricity into heat (K-glass + AS Green; Eglas Oy, Imatra, Finland), and the four north- and east-facing walls of dual-layer acrylic sheets (Standard 16-mm BMMA-polymethyl-methacrylate). Unfiltered air was fed into the chamber by a fan blower through a duct approx. 3·5 m above the ground, and the air flow was determined periodically with a hot wire anemometer and adjusted with a butterfly valve. A computer-controlled heat exchanger linked to a refrigeration unit (CAJ-4511YHR; L’Unite-Hermetique, Barentin, France) was installed in the top of each chamber. The computer-controlled heating and cooling system, together with a set of magnetoelectric valves (controlling the pure CO2 supply), enabled temperature and CO2 concentration inside the chambers to be adjusted automatically to follow ambient conditions, or to achieve a specified enrichment in CO2 (+350 µmol mol–1) and/or rise in temperature [+2 °C during the ‘growing season’ (days 120–240) and +6 °C during the ‘off’ season]. The CO2 concentration was enriched all day throughout the year. Performance of the chamber system has been detailed previously (Kellomäki et al., 2000).

Respiration measurement
In this paper, foliage respiration is defined as the apparent respiration, which consists of light respiration in the light (Brooks and Farquhar, 1985) and dark respiration in the dark [eqn (A1) in Appendix]. Measurements of dark respiration were made with a portable gas analyser (LCA-4; Analytic Development Co. Ltd, Hoddesdon, Herts, UK), equipped with a temperature-controlled chamber. Two groups of measurements of needle respiration were performed on each experimental tree in 2000: (1) temperature respiration response curves were measured monthly for attached 1-year-old needles in the middle of the crown. The needles were dark-acclimated for at least 20 min, and thereafter acclimated to the target temperature for a further 30 min before the readings. All measurements were made at the growth CO2 concentration and at five air temperatures: 5, 15, 20, 25, and 30 °C (± 0·5°C). (2) The spatial distribution of needle respiration within the crown was measured on five sample shoots representing five crown layers and three age classes in August (cf. Zha et al., 2002). Measurements were made at 20 °C and the growth CO2 concentration. After the gas-exchange measurements, needle nitrogen concentrations were determined using the micro-Kjeldahl method. Nitrogen–respiration relationships were determined.

Foliage area and foliage nitrogen distribution in the crown
The distribution of foliage area in the four experimental trees in each treatment was assessed by three methods. First, the annual change in the area of current-year needles was calculated by multiplying the needle expansion rate by the number of needles in the current-year shoots, the former being measured on the sample shoot after bud burst (see Zha et al., 2001). Secondly, the annual change in crown foliage area was estimated from hemispherical photographs taken from the base of the crown (Hemi View v.2·1), assuming a half-ellipsoid crown when calculating the gap fractions (Campbell, 1986). And thirdly, in May and August, the sample-branch method (cf. Wang, 1996; Kellomäki and Wang, 1997) was used to determine the age classes as proportions of the total foliage area and their distribution within the crown, and to calibrate the estimate of foliage area obtained from the hemispherical photograph.

When measurements of foliage area were made, about 40 needle fascicles of each age class in each whorl branch were randomly taken for determination of the foliage nitrogen distribution within the crown (cf. Kellomäki and Wang, 1997). Additionally, a mixed sample of needles was collected each month throughout the year to estimate foliage nitrogen and its change during the year (Fig. 2G and H). Needle area was measured using a scanner with analysis software (WinFOLIATM, Regent Instruments Inc., Quebec, Canada), and nitrogen concentration was analysed by the modified micro-Kjeldahl method.



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  		Fig. 2. Annual variation of total projected foliage area (Lp; m2 per tree) for treatments CON and EC (A), and ET and ECT (B). Lp was estimated by means of hemispherical photographs taken from the base of the crown, combined with measurements performed on sample branches. Arrows indicate two independent measurements made separately in May and August of the same year using the sample branch method; fitted respiration parameters [eqn (A3)], Q10 (C and D) and Rl.d (20) (E and F) for 1-year-old needles in the middle of the pine crown; and foliage nitrogen content of 1-year-old needles in the middle of the crown (Nl; g N m–2) (G and H). Symbols are means (± s.e.) of measurements from four trees per treatment.

 
Calculating respiration of leaves within the crown
The crown was divided into five horizontal layers of equal depth, and the foliage in each layer into three age classes. The cumulative leaf area index [eqn (A7) in the Appendix] and mean foliage nitrogen content [eqn (A9)] were then calculated as functions of the layer and foliage age class. Finally, the instantaneous foliage respiration rates of each foliage class were calculated as a function of air temperature, nitrogen content, CO2 concentration and light intensity [eqns (A2)–(A11)], and crown respiration was calculated by including the contributions of three age classes of foliage in each of the five layers.

Several assumptions and simplifications apply to these computations. (1) Dark respiration was assumed to follow an exponential function of temperature [eqn (A3); see Amthor, 1994]. (2) Foliage respiration rate at the reference temperature Rl.d(20) was assumed to be a linear function of foliage nitrogen content [eqn (A5); see also Ryan, 1995; Reich et al., 1998], whereas Q10 does not change with foliage nitrogen content (Bolstad et al., 1999; Zha et al., 2002). (3) Differences in respiration between foliage age classes or crown positions are reflected in differences in foliage nitrogen content (Kellomäki and Wang, 1997; Zha et al., 2002). (4) Total foliage nitrogen content per tree varies with day of the year but not within a day. (5) The continuous daily change of crown parameters such as total foliage area, branch expansion and total nitrogen content, and respiration parameters such as Q10 and Rl.d(20) were obtained by linear interpolation from monthly measurements for each treatment, but the distribution pattern of foliage area and nitrogen concentration within the crown, obtained for a given treatment in August, was used to represent the whole year.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 CONCLUSIONS
 APPENDIX
 LITERATURE CITED
 
Crown profiles and respiration parameters
The total foliage area (Lp; Table 1), proportions of the different age classes in the total foliage area in each layer, and the relative height of the layer with the maximum foliage area were altered significantly by the treatments (Fig. 1). Maximum foliage area shifted towards the crown base in the case of EC, but towards the top when temperature increased. Based on the August measurements, the total foliage area per tree increased by 11 % for EC (P < 0·041), 20 % for ET (P < 0·038) and 14 % for ECT (P < 0·046) relative to CON (Table 1). Similarly, differences in total foliage area per tree between the treatments and CON depended greatly on the day of the year (Fig. 2A and B).


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  		Table 1 . Parameter values for the crown of Pinus sylvestris as a function of the treatments and needle age classes
 


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  		Fig. 1. Vertical distribution of foliage area (A) and foliage nitrogen (B) in current-year (1c), 1-year-old (2c) and older needles (3c) within the crowns of pine trees growing in four environment-controlled conditions: CON, ambient CO2 concentration and temperature; EC, elevated CO2 concentration; ET, elevated temperature; and ECT, elevated CO2 and temperature. The figures are means of measurements from four trees per treatment; numbers in parentheses are total needle area in m2 per tree (A) and mean nitrogen content in g N m–2 (B) for each age class.

 
Compared with CON, both EC and ECT decreased significantly the mean concentration of foliar nitrogen (Nl.m; Table 1), but increased the total nitrogen content per tree (Nt; Table 1), although the extent of the change was related to the foliage age class (Fig. 1E–H). By contrast, ET did not significantly alter Nl.m but increased Nt. The nitrogen allocation coefficient (kn; Table 1) ranged from 0·37 to 0·74 depending on the foliage age class and treatment, but in general it increased with needle age regardless of the treatment. In terms of the annual mean of the measurements (Fig. 2), Nl.m decreased by 16·3 % for EC (P = 0·003), 1·2 % for ET (P = 0·218) and 7·4 % for ECT (P = 0·085), but crown total nitrogen increased significantly, by 11 % for EC, 21 % for ET and 14 % for ECT due to the enhancement in the crown foliage area caused by the treatments. The changes in Q10 and Rl.d(20) caused by the treatments did not follow this pattern (Fig. 2C–F), the change in Q10 generally being less than that in Rl.d(20). Both ET and ECT increased Rl.d(20) in winter but slightly reduced it in the main growing season. Although there was a marked scattering of data for the relationship between Rl.d(20) and foliage nitrogen concentrations (Nl) (Fig. 3), the linear relationships between Rl.d(20) and Nl were significant at P < 0·05 for all treatments. The regressions had the greatest slope value for EC (P < 0·032), and the smallest for ET (P < 0·038) and ECT (P < 0·047) (Table 1).



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  		Fig. 3. Linear regression of dark respiration rate at the reference temperature of 20 °C [Rl.d(20)] on foliage nitrogen content (Nl) in the four treatments: CON, ambient CO2 concentration and temperature; EC, elevated CO2 concentration; ET, elevated temperature; and ECT, elevated CO2 and temperature. Parameter values are given in Table 1.

 
Daily crown respiration on a typical sunny day
Using profiles of foliage area and foliage nitrogen in August and half-hourly microclimate recordings in the chambers for the same treatments, respiration of leaves in the crown on a typical sunny day (26 Jul. 2000) was calculated to gain an understanding of the contribution of crown elements to total daily carbon loss (Fig. 4). Daily courses of crown foliage respiration were closely coupled with daily variations in air temperature, regardless of treatment. Calculated crown respiration rates around noon were about three times those at night. Total daily crown respiration reached 18·3, 23·7, 25·4 and 24·3 g C per tree d–1 in CON, EC, ET and ECT, respectively. It was also noticed that relative to CON, all treatments led to a reduction in respiration during the afternoon when air temperatures were around 30 °C, but an increase during the night. Of the different age classes, the current-year needles (1c in Fig. 4) made the biggest contribution to crown foliage respiration, between 48 and 62 % for the four treatments, while older needles (3c) accounted for only 9–16 % for the four treatments. Furthermore, the increased crown respiration caused by the treatments could be attributed to different age classes, resulting mainly from the current-year and 2-year-old foliage in the case of EC, for example, from the current-year and 1-year-old foliage in the case of ET, and from three age classes in ECT (Fig. 4A–D). In view of the contribution of the crown layers to crown respiration (Fig. 4E–H), the treatments altered the relative contributions of all the layers; for example, the layer with greatest contribution to crown foliage respiration was the second layer in the case of CON (35 %) and ET( 39 %), but the third layer in the case of EC (36 %) and ECT (38 %).



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  		Fig. 4. Daily course of crown respiration in control chambers (CON, A) and percentage differences in crown respiration between treatments and CON separately for three foliage age classes (B–D), and percentage contributions of layers in the crown (E–H) to daily total respiration per tree on a typical sunny day in the summer of 2000 (26 July). E–H, Numbers above bars give daily total respiration rates (g C per day) for the corresponding layer of the crown.

 
Calculated annual crown-foliage respiration
Using the annual courses of the crown parameters and half-hourly microclimate data as inputs to the model, the annual course of crown respiration was calculated and showed a clear seasonal dependence (Fig. 5). Daily total respiration was highest from mid-June to mid-August, accounting for over 40 % of annual total respiration in all four treatments. Compared with CON (1210 g C per tree in 2000), EC, ET and ECT increased the annual sum of crown respiration by 16, 35 and 27 %, respectively. These increases resulted mainly from foliage respiration during the growing season (days 120–240), which accounted for 73, 68, 65 % in EC, ET and ECT, respectively.



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  		Fig. 5. Calculated crown respiration for pine trees over the whole year (2000) as a function of foliage age classes (1c, 2c and 3c) for control treatment (CON, A), and differences in the crown respiration between treatments and CON (B–E). Calculations were based on crown parameters (Table 1; Figs 1 and 2) and half-hourly recordings of microclimate variables in the chambers for each treatment.

 
Independent of the treatment, 1-year-old foliage made the largest contribution of the three age classes to the annual total respiration per tree, accounting for 47 % in CON, 52 % in EC, 64 % in ET and 58 % in ECT, whereas current-year foliage made a substantial contribution only after mid-June. However, the percentage contributions of the age classes to the increases in annual total respiration in the three factor-enriched treatments were different, with the order being 1c > 3c > 2c in the case of EC, 2c > 1c > 3c in the case of ET and 1c > 2c >3c in the case of ECT.

Contributions of foliage area and temperature to crown respiration
Using the same foliage area as in the case of CON, together with the crown parameters and microclimate data for each treatment as inputs to the model, annual respiration rates were calculated to approximate the contribution of the change in foliage area caused by the growth conditions to respiration (Fig. 6B). EC substantially decreased respiration almost throughout the year, while ET and ECT dramatically increased respiration for most of the year. Hourly statistics indicated that EC decreased annual respiration by 12 % for 91 % of the year and increased it by only 1 % for the rest of the year, ET increased it by 15 % for 89 % of the year and reduced it by 3 % for the rest of the year, and ECT increased it by 10 % for 81 % of the year and reduced it by 4 % for the rest of the year.



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  		Fig. 6. Calculated crown respiration for pine trees over the whole year (2000) for control treatment (CON, A), and differences in the crown respiration between treatments and CON (B–D). Calculations were based on different inputs or assumptions: total foliage area in the three factor-enriched treatments (EC, ET and ECT) was assumed to be the same as in CON (B); air temperature was assumed to be the same as in CON (C); and total foliage area and air temperature were assumed to be the same as in CON (D).

 
To estimate the effect on respiration of the immediate air temperature rise in the experimental chambers, annual respiration courses for ET and ECT were calculated using the same temperature as the CON chambers (Fig. 6C). The increase in crown respiration induced by ET and ECT was similar in its seasonal pattern, i.e. there was a small, almost constant increase in respiration before mid-May, then a large decline around midsummer, followed by a substantial increase. Hourly statistics indicated that ET increased annual respiration by 28 % for 98 % of the year and reduced it by only 0·5 % for the rest of the time, and ECT increased it by 13 % for 88 % of the year and reduced it by 2 % for the rest of the time.

Finally, some interesting results were seen when the computation was based on the same foliage area and temperature data as under CON conditions (Fig. 6D). ET and ECT increased crown respiration by 7 and 10 %, respectively, in the period of no-growth but reduced it by 17 and 8 %, respectively, in the main growing season. Moreover, both ET and ECT led to a greater decline in crown respiration after mid-June than did EC, with ET > ECT > EC.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
CONCLUSIONS
 APPENDIX
 LITERATURE CITED
 
The effects of elevated CO2 concentration on trees depend greatly on the temperature during growth (Long and Drake, 1991; Wang et al., 1996), and forest ecosystems of the boreal zone will experience the greatest warming in the future (IPCC, 1996). Thus, the challenge faced when studying responses of boreal forest trees to climate change is how to assess the long-term interaction between elevated CO2 concentration and temperature, particularly for tree species with specific characteristics, such as great size, longevity, complexity and enormous adaptability and potential for acclimation. Few long-term field experiments that involve simultaneous manipulations of CO2 and temperature have been carried out on mature trees in the boreal zone until now, due, in part, to the problems associated with establishing control experimental conditions and the high running costs. Our closed chamber system provides a means of investigating the long-term responses of larger trees to elevated CO2 and temperature in a boreal forest. Over a 3-year period, the system maintained good control of environmental conditions (Kellomäki et al., 2000).

Elevated CO2 reduced the respiration rate of leaves at 20 °C [Rl.d(20)] in our experiment with Scots pine, consistent with reports for other tree species (Idso and Kimball, 1992; Ceulemans et al., 1999; Drake et al., 1999; Jach and Ceulemans, 2000), although there are contradictory results (Jarvis, 1998). There are two important features of our study. First, the reduction in Rl.d(20) increased with age and depth in the crown for the same needle age class, regardless of whether results were expressed on a dry mass or area basis. Secondly, trees growing in the elevated CO2 chambers had higher Q10 values in the growing season (Fig. 2C and D). The difference in response of respiration to elevated CO2 caused by ageing is partly related to exposure time, i.e. there is a progressive acclimation in respiration, or indirect effects associated with foliage growth and active sink functions (Sprugel et al., 1995; Jarvis, 1998; Kellomäki and Wang, 1998; Jach and Ceulemans, 2000). In our case, the large differences in leaf nitrogen concentration induced by elevated CO2, and the changes in leaf structure (K.-Y. Wang, unpubl. res.) with ageing may be the most direct explanations for the differences in respiration associated with leaf age and position in the crown. A higher Q10 under elevated CO2 conditions was observed in our earlier experiment (Kellomäki and Wang, 1998). Although there is no theoretical justification for the concept of Q10 (Johnson and Thornley, 1985), a CO2-induced modification in respiratory enzymes is possible (Gonzalez-Meler et al., 1999). Further work is necessary to clarify this.

Elevated temperature increased the size of individual leaves, but did not alter the leaf nitrogen concentration significantly (Fig. 2G and H), while Q10 and Rl.d(20) both decreased during the summer, reflecting a different response mechanism from that affected by CO2. Leaf respiration has been recognized as having a relatively large potential for acclimation to growth temperature, e.g. by phenotypic or genetic adjustment (Larcher, 1995; Amthor, 1999). However, a small, gradual elevation in temperature is often considered unnecessary to alter the rate of leaf respiration (Amthor, 1991). Thus, the observed reduction in respiratory parameters indicates that trees in the boreal zone will have more physiological adjustment to a given increase in growth temperature than those in other zones.

It is clear that crown-foliage respiration cannot be calculated simply from the rate of respiration of individual leaves, although the response of the crown can, in part, reflect that of the leaves. As showed in our measurements, changes in total leaf area caused by the treatments, the seasonal development of leaf area, the crown structure or the response of individual leaves to gradients within the crown will alter the relationship between the instantaneous respiration rates of individual leaves and daily total respiration of the whole crown. Our computations were, in general, based on Ryan’s respiration model (1991b), i.e. respiration was estimated as a function of temperature and tissue nitrogen concentration. Further details included in the present computations were that (1) values for all parameters in the model [eqns (A2)–(A11)] were dynamically coupled to the distribution of leaf area and nitrogen content in the crown, and (2) the seasonal dependence of several key parameters such as Q10, Rl.d(20), leaf area index and total nitrogen content of the tree were considered for each treatment. These allowed contributions of changes, induced by the treatments, in crown components to respiration of the whole tree to be estimated over time and space.

On a typical sunny day during the growth season, daily total crown respiration increased by 29·5 % in the case of EC, 38·8 % in ET and 32·7 % in ECT, relative to CON, apparently in conflict with the results for individual leaves [e.g. Rl.d(20) in Fig. 2]. This can be attributed to the large increases in crown foliage area and total nitrogen caused by the treatments (Table 1). Moreover, due to changes in crown structure (Fig. 1A–D), and the pattern of the response of respiration to temperature between foliage age classes caused by the treatments, the largest contribution to daily total respiration did not come from the same layer of the crown in all four treatments (Fig. 4), nor did the treatments change in the course of daily respiration in the same direction (increase or decrease) (Fig. 4).

No experimental measurements have previously been made over a whole year for trees grown at elevated CO2 and temperature. The model-based carbon budget analysis for young Betula pendula trees grown in CO2-enriched chambers for 3 years by Wang et al. (1998) indicated that the annual loss of carbon (g C per tree year–1) from leaves grown at elevated CO2 increased by 10 % relative to that in ambient conditions, although there was a 23 % reduction in leaf respiration in elevated CO2. The 16 % increase in the annual respiration rate of pine trees grown in elevated CO2 in our study is higher than that for birch. The difference is due to the larger size of the pine trees and is also partly associated with the large cumulation of needle area during the previous years caused by elevated CO2 because older needles on pine trees make a considerable contribution to the increase in annual crown respiration (Fig. 1A–D).

Under boreal conditions, low temperature is a key factor limiting tree growth and development for most of the year, thus the role of temperature in controlling respiration is not surprising. We have shown that the increase in temperature during growth increased the size of individual leaves (Kellomäki and Wang, 1998, 2001), advanced leaf development in the early spring, and led to the retention of a larger leaf area per tree late in the season. As a result, current-year foliage made the greatest contribution to the increment in respiration of the whole crown during the late summer and autumn (Fig. 5), whereas daily crown respiration rates in winter were three to four times higher than under control conditions, and annual total respiration consequently increased by 35 and 27 % in the case of elevated temperature and the combined treatment of CO2 and temperature, respectively.

In spite of modifications to respiration and the crown architecture caused by the treatments, the increase in total leaf area per tree and the consequent increase in total nitrogen made the greatest contributions to the annual increase in crown respiration regardless of the treatments, and accounted for 92 % of the increase in annual crown respiration in EC, 66 % in ET and 43 % in ECT (Fig. 6A), followed by growth temperature, which accounted for 17 % in ET and 29 % in ECT (Fig. 6B). Adjustment in respiration parameters caused by the treatments made the smallest contribution, suggesting that when modelling respiration of whole trees or of stands, priority should be given to the change in total leaf area or leaf area index caused by climate.


   CONCLUSIONS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
APPENDIX
 LITERATURE CITED
 
(1) After 4 years’ growth in elevated CO2 and temperature, Scots pine trees showed increased daily and annual crown respiration in the EC, ET and ECT treatments, although the respiration rates of individual leaves decreased in EC in all seasons, and in ET and ECT in the summer. (2) Under boreal conditions, a mean increase in ambient air temperature of 2 °C (in summer) and 6 °C (in winter) had a greater effect on leaf area and leaf respiration rate than a doubling of atmospheric CO2 concentration. (3) As a result, both crown architecture and daily or annual respiration patterns in the combined treatment of elevated CO2 and temperature were similar to those in the elevated temperature treatment alone. (4) Increases in total foliage area per tree and consequent total nitrogen content caused by the treatments contributed more to annual crown respiration than did adjustments in physiological parameters related to respiration processes.


   ACKNOWLEDGEMENTS
 
We thank Matti Lemettinen, Alpo Hassinen and Risto Ikonen for developing and maintaining the experimental infrastructure and Leena Kuusisto for nitrogen analysis. This work forms part of the Finnish Centre of Excellence Programme (Project no. 64308) funded by the Academy of Finland, the National Technology Agency (Tekes) and the University of Joensuu, the China–Finland cooperation project ‘Responses of the Ecosystem Processes of High-Frigid Coniferous Forest to Climate Change’ funded by the Academy of Finland and the NSFC, and the ‘Programme of 100 Distinguished Young Scientists’ funded by the Chinese Academy of Sciences.


   APPENDIX
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 APPENDIX
LITERATURE CITED
 
In this paper, foliage respiration is defined as the apparent respiration, which consists of light respiration in the light (Rl.l) (Brooks and Farquhar, 1985) and dark respiration in the dark (Rl.d). Daily leaf respiration Rl was calculated as the sum of Rl.d and Rl.l:


Rl.d in the ith layer of the crown was assumed to be a function of leaf nitrogen (Nl), air temperature (Ta), ambient CO2 concentration (Ca) and foliage area in the layer (La.i):


The short-term response of Rl.d to temperature was given by the exponential function (Landsberg, 1986; Amthor, 1992):


Where Rl.d(20) is the value of Rl.d at the reference temperature of 20 °C, and Q10 the relative change in respiration for a 10 °C change in temperature.

An inverse relationship between Rl.d and short-term changes in Ca in the dark has been observed on many occasions (Amthor, 1992), although the underlying mechanism is unknown. The function, f(Ca), is given by an approximation (Amthor, 1992):


Several measurements have shown that the dependence of Rl.d on Nl is mainly related to the impact of Nl on the basal respiration rate, Rl.d(20), and less on Q10 (Bolstad et al., 1999; Griffin et al., 2001; Zha et al., 2002). Therefore, a linear relation between Rl.d(20) and Nl was adopted (Kellomäki and Wang, 1997):


where cnx are fitting parameters.

Nl in the crown can be approximated by:


where Nl.o is foliage nitrogen per unit of projected foliage area in the uppermost whorl of the crown (g N m–2 foliage), Lc (m2 m–2 ground) and Lt (m2 m–2 ground) are the cumulative foliage area index for the top of the crown and the total foliage area index, respectively, and kn is the coefficient of foliage nitrogen allocation (Kellomäki and Wang, 1987).

Lc is calculated here as:


where Hr is the relative height from the bottom of the crown, Bmax is the mean branch length of the whorl with maximum total branch length in each tree, Ts is the mean angle with respect to the main stem of the branches of the whorl, and Lp the needle projected area (m2 per tree) at any height within the crown, expressed by a beta function,


where a is the needle age class and cHx.a are fitting parameters.

Integration of eqn (A6) with respect to Lc gives the total leaf nitrogen per unit ground area in the crown (Nt; g N m–2 ground):


Thus, when kn, Nt and Lc/Lt are given, the distribution of Nl within the crown can be calculated by:


Respiration under light conditions is poorly understood, but Rl.l is assumed to be linearly related to Rl.d (Wang, 1996):


where 0·69 is the ratio of Rl.l to Rl.d for needles of Scots pine under full light conditions (Wang, 1996), Qi is the mean light flux incident on the ith layer of the crown, as calculated using eqns (A17)–(A20) of Kellomäki and Wang (1997b), and max[x, y] means the maximum of either x or y. Here, y depicts a linear decline in Rl.l as Qi increases from 0 to 10 µmol m–2 s–1, at which Rl.d is depressed by 31 %, but with no effect of any further increase in Qi on Rl.d (Amthor, 1994).


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 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 APPENDIX
 LITERATURE CITED
 

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K.-Y. WANG, S. KELLOMAKI, C. LI, and T. ZHA
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