JXB Advance Access originally published online on May 8, 2007
Journal of Experimental Botany 2007 58(8):2159-2168; doi:10.1093/jxb/erm069
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RESEARCH PAPER |
CO2 fluxes and respiration of branch segments of sycamore (Platanus occidentalis L.) examined at different sap velocities, branch diameters, and temperatures
1Warnell School of Forestry and Natural Resources, University of Georgia, Athens, Georgia 30602, USA
2Instituto Superior de Agronomia, Universidade Tecnica de Lisboa, Tapada da Ajuda, 1349-017 Lisboa, Portugal
* To whom correspondence should be addressed. E-mail: mmcguire{at}uga.edu
Received 19 December 2006; Accepted 2 March 2007
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Abstract |
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Respiration of stems and branches of trees (RS) has typically been estimated by measuring radial CO2 efflux from woody tissue (EA) and rates of efflux are often scaled temporally using a temperature relationship (Q10). High concentrations of CO2 in xylem sap ([
]) have been shown to affect EA, and the transport of CO2 in the xylem stream has been suggested as a mechanism to explain field observations of temperature-independent fluctuations in EA. Sap velocity and temperature were manipulated in detached branch segments of sycamore (Platanus occidentalis L.) under controlled conditions to quantify these effects. Within individual branches of similar size, EA and [] were greater at low sap velocity, while the amount of respired CO2 transported in sap (transport flux, FT) was greater at high sap velocity. EA was linearly correlated with []. In branches of three diameter classes (1, 2, and 3 cm), volume-based EA, FT, and RS did not differ, but surface-area based CO2 fluxes increased with diameter class. Regardless of diameter, EA accounted for only 30% of respired CO2 at high sap velocity, while at low sap velocity, EA accounted for 71% of respired CO2. EA, FT, and RS measured at 5, 20, and 35 °C at the same sap velocity showed a typical exponential response to temperature. However, at the lowest temperature, EA accounted for only 18% of the CO2 released from respiring cells compared with 44% at the highest temperature, perhaps due to the effect of temperature on the solubility of CO2 in water. These results directly demonstrate the transport of respired CO2 in the xylem stream and may help to explain inconsistencies in stem and branch respiration measurements made in situ. Key words: Branch respiration, Henry's law, Q10, stem respiration, xylem CO2 concentration
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Introduction |
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Internal CO2 concentrations of stems and branches can be an order of magnitude greater than the atmospheric CO2 concentration ([CO2]) (Bushong, 1907; MacDougal and Working, 1933; Chase, 1934; Jensen, 1967; Eklund, 1990, 1993; Hari et al., 1991; Levy et al., 1999). It has been suggested that CO2 transported in xylem sap may affect measurements of woody tissue respiration (Ryan, 1990; Sprugel, 1990) and that respiration measurements based on gas exchange have been misinterpreted because xylem-transported CO2 was not considered (Carrodus and Triffett, 1975; Hari et al., 1991; Stringer and Kimmerer, 1993; Levy et al., 1999). Previously, in field experiments, a direct relationship was observed between radial CO2 efflux from woody tissues of trees and the internal [CO2] in the xylem (Teskey and McGuire, 2002; McGuire and Teskey, 2004). By artificially manipulating internal xylem [CO2] it was found that CO2 in xylem sap had large effects on CO2 efflux from detached branch segments, severed shoots, and intact stems in the field (Teskey and McGuire, 2002, 2005). It was also observed that [CO2] increased with height in intact stems (McGuire and Teskey, 2004), indicating that CO2 was added to sap as it flowed through woody tissue. The flow of sap appeared to remove CO2 from the site of production and transport it upward, reducing radial CO2 efflux as suggested by Negisi (1979) and Martin et al. (1994). These studies indicated that the transport of CO2 in xylem sap modifies CO2 efflux to the atmosphere and apparent rates of respiration, but they did not experimentally isolate the respiring tissue from the influence of xylem-transported CO2. In this study, a new measurement approach was developed that enabled previously-transported CO2 to be removed from branch segments, and allowed direct measurement of the quantity of respiratory CO2 that subsequently dissolved in the xylem sap. Simultaneously, both CO2 efflux and internal transport of respiratory CO2 in detached branch segments of sycamore (Platanus occidentalis L.) trees were quantified without the confounding effect of imported CO2. The study's objectives were to determine, under controlled conditions, (i) the rate of respiration of woody branch tissue; (ii) the maximum capacity for respired CO2 to dissolve in xylem sap; (iii) the effect of sap velocity on the relative quantity of CO2 transported in the xylem (FT) or released to the atmosphere (EA); (iv) the effect of branch diameter on these relationships; and (v) the effect of temperature on the total amount of CO2 produced by woody tissue respiration and on the relative proportions of EA and FT.
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Materials and methods |
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Three experiments were performed on excised branch segments in an environmental chamber (GC36, Environmental Growth Chambers, Chagrin Falls, OH, USA) at the School of Forestry and Natural Resources of the University of Georgia in Athens, Georgia, USA. The experimental approach allowed both internal and external fluxes of respired CO2 from the branch segments to be measured under controlled sap flow and temperature conditions. Experiments were conducted during September, October, and November of 2005. Branch segments were cut in the morning from coppiced sycamore trees growing in Whitehall Forest, an experimental unit of the University of Georgia located
10 km from campus. The lower cut ends of the branch segments were immediately placed in water and transported to the environmental chamber. Experiments were started within 1 h of collecting the branch segments. A 40 cm length of soft tubing (Tygon, Saint-Gobain Ceramics & Plastics, Northboro, MA, USA) was used to connect the upstream (lower) end of each branch segment to a sealed 10.0 l reservoir filled with water in equilibrium with ambient atmospheric [CO2]. To control the flow rate of water moving through the xylem, a regulator and compressed air cylinder were used to vary positive pressure in the reservoir. The downstream end of each branch segment was enclosed in soft tubing fitted with a reducing elbow and smaller diameter tubing to facilitate collection of sap samples and measurement of flow rate. Three branch segments were measured per experimental run and each segment was attached to a separate reservoir, regulator, and compressed air cylinder. To help maintain a consistent flow rate through the branches, the water was amended with KCl to make a 40 mM solution (Zwieniecki et al., 2001). The reservoirs were located inside the environmental chamber and were equilibrated with the chamber temperature prior to initiation of the experiment.
Before measuring internal and external respiratory fluxes, an attempt was made to remove pre-existing CO2 from the xylem by perfusing at least 500 ml of water through the stem segment at a high flow rate. This initial flushing period (1 h) removed residual CO2 stored in the branches that could confound subsequent flux measurements. It was assumed that 500 ml of water perfused at a high flow rate would be sufficient to remove all of the pre-existing CO2 since the volume of even the largest branches was less than 80 cm3, of which 50% was assumed to be wood.
To determine the internal flux of respiratory CO2, the rate of flow through each branch was first measured with a graduated cylinder and stopwatch at the downstream end of the segment. Then, sap was collected (6 ml) from the downstream end of the branch segments in glass tubes for [CO2] measurements. Sample tubes were sealed with closed cell foam stoppers and allowed to equilibrate to room temperature. A CO2 microelectrode (MI-720, Microelectrodes Inc., Bedford, NH, USA) was submerged in the water in the sample tube and allowed to equilibrate (30 min). Henry's solubility constant for CO2 and dissociation constants for HCO3 and CO3 were used to convert measured [CO2] to the concentration of all dissolved products of CO2 in the water ([], µmol CO2 l–1 water) (Butler, 1991; Stumm and Morgan, 1996; Levy et al., 1999; McGuire and Teskey, 2002). The dissolution of CO2 into bicarbonate and carbonate ions increases with increasing pH; therefore to calculate [], pH must be known. The pH of the water was measured with a solid state microsensor and meter (Red-Line Standard sensor, Argus meter, Sentron Europe, Roden, NL). The transport of respiratory CO2 in the xylem stream (transport flux, FT, µmol m–3 s–1) was calculated as
 | (1) |
= the change in [] of water entering and leaving the branch segment (µmol l–1), fW=water flux (l s–1), and v=volume of woody tissue (m3).
Simultaneously, the external flux of CO2 was measured by enclosing each branch segment in a fan-stirred cylindrical PVC cuvette (diameter=6 cm, length=13.5 cm). The cuvette was sealed to the segment at each end with 2 cm thick closed cell foam gaskets. Compressed air from a cylinder with 360 µmol mol–1 CO2 was supplied to each cuvette with a mass flow controller (FMA 5514, Omega Engineering, Stamford, CT, USA) at 500 ml min–1. A long length of tubing between the compressed air cylinder and mass flow controller was coiled inside the environmental chamber to allow the air supply to equilibrate to the chamber temperature. The [CO2] of the air exiting the cuvettes was measured with an infrared gas analyser (IRGA) (LI-7000, Li-Cor, Lincoln, NE, USA) and the rate of efflux (EA, µmol CO2 m–3 woody tissue s–1) was determined using standard calculations (Long and Hallgren, 1985) as
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[CO2]=the difference in [CO2] of air entering and exiting the cuvette (µmol mol–1), fA=flow rate of air through the cuvette (mol s–1), and v=volume of woody tissue (m3). Respiration (RS) was calculated as
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Sap velocity (cm min–1) was calculated by dividing water flux (cm3 min–1) by the cross-sectional area of the branch segment (cm2).
Experiment 1: effects of sap velocity
CO2 flux measurements were made on 15 branch segments (five experimental runs) using a range of high and low sap velocities. Segment diameters ranged from 1.39–1.71 cm with mean of 1.50 cm. Measurements were made at 30 °C to promote a high rate of respiration. EA and FT at high sap velocity were measured at the end of the initial flushing period. Water flow was then reduced and the measurements were repeated on the same branches at low sap velocity after equilibration for 1.5 h. Differences in fluxes and [] between high and low sap velocity were determined with paired t tests. Relationships among variables were determined by linear and non-linear regression (SigmaPlot 9.01, SigmaStat 3.11, Systat Software Inc., Richmond, CA, USA).
Experiment 2: effects of branch segment diameter
Measurements were made at high and low sap velocities as in the first experiment on five segments of each diameter class (small, 1 cm; medium, 2 cm; large, 3 cm). Small diameter branch segments ranged from 0.94–1.10 cm with mean of 1.06 cm, medium diameter ranged from 1.86–2.25 cm with mean of 2.02 cm, and large diameter ranged from 2.78–3.04 cm with mean of 2.88 cm. One segment of each diameter class was measured in each of five experimental runs. To facilitate the size comparison, water flow was manipulated to achieve similar high and low velocities among the different size branches. In this experiment, in addition to flux calculations based on branch volume, CO2 fluxes were determined on a branch surface area basis by substituting surface area for volume as the size term in equations 1 and 2. Differences in fluxes and [] between high and low sap velocities were determined with paired t tests. Differences in fluxes among diameter classes were determined by one-way ANOVA. Relationships among variables were determined by linear and non-linear regression (SigmaPlot 9.01, SigmaStat 3.11, Systat Software Inc., Richmond, CA, USA).
Experiment 3: effects of temperature
Measurements were made on 18 branch segments, six at each temperature (low, 5 °C; medium, 20 °C; high, 35 °C; two experimental runs at each temperature). Segment diameters ranged from 1.65–1.90 cm with mean of 1.81 cm. As in the first two experiments, water was first forced through the segments at a high rate until 500 ml had passed through each segment to flush existing CO2 out of the xylem, but in this experiment no measurements were made at the end of the high flow period. Water flow was reduced to a lower rate and the segments were allowed to equilibrate for 1.5 h, after which sampling was done as in the two earlier experiments. Relationships among variables were determined by linear and non-linear regression (SigmaPlot 9.01, SigmaStat 3.11, Systat Software Inc., Richmond, CA USA).
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Results |
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Experiment 1: effects of sap velocity
Fluxes were measured in each branch segment at both a high and a low sap velocity. High velocity ranged from 2.2–11.2 cm min–1 with mean of 5.3 cm min–1 and low velocity ranged from 0.1–2.6 cm min–1 with mean of 0.6 cm min–1. Respiration (RS) was significantly less at high sap velocity (533 µmol m–3 s–1) compared with low sap velocity (668 µmol m–3 s–1, t= –2.478, P=0.027) (Fig. 1). At high sap velocity, the transport of CO2 in xylem sap (FT) was significantly greater (375 µmol m–3 s–1) than at low sap velocity (197 µmol m–3 s–1, t=4.003, P=0.001; Fig. 1). The opposite response to sap velocity occurred in CO2 efflux to the atmosphere (EA). At high sap velocity, EA was significantly less (158 µmol m–3 s–1) than at low sap velocity (471 µmol m–3 s–1, t= –5.662, P= <0.001; Fig. 1). In other words, at high sap velocity, mean FT was 1.9 times greater than mean EA, but at low sap velocity the relative magnitude of the two fluxes reversed and EA was 3.0 times greater than FT. At high sap velocity EA accounted for only 30% of the CO2 released from respiring cells, but at low sap velocity EA accounted for 71% of RS.
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Mean [
] of xylem sap exiting the branches was significantly greater at low velocity (0.7 mmol l–1) compared with high velocity (0.1 mmol l–1, t= –5.636, P= <0.001). When data from individual branches at high and low sap velocities were combined, both [] and EA exhibited a similar negative correlation with velocity (Fig. 2; Table 1). The relationship between xylem sap [] and sap velocity indicates that [] was progressively diluted as sap velocity increased. In addition to the almost identical inverse relationship between EA and sap velocity, the linear correlation of EA with [] (Fig. 3) suggests that the concentration of CO2 in the xylem affected EA. As sap velocity decreased, [] increased, and more CO2 fluxed to the atmosphere (EA), suggesting that the relationship between EA and sap velocity is driven by variation in the dilution of [] caused by sap movement in the xylem. FT and RS were also correlated with sap velocity (Table 1), but the relationships were weaker.
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Experiment 2: effects of branch segment diameter
The relationships between branch size and CO2 fluxes were similar at high and low sap velocity, but are shown here only at low velocity. When calculated on the basis of branch volume, EA, FT, and RS did not differ significantly among branch diameter classes and were not correlated with diameter (Fig. 4A; Table 1). Respiration rates were similar to those in the first experiment and the dominant flux was FT. However, when calculated on a branch surface area basis, EA, FT, and RS increased significantly with diameter class and were directly correlated with diameter (Fig. 4B; Table 1). The rate of respiration on a surface area basis was almost three times greater in the 3 cm diameter branches than in the 1 cm diameter branches. Branch diameter had no effect on the relative contributions of EA and FT to RS.
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Regardless of branch diameter, or whether fluxes were calculated on the basis of branch volume or surface area, the effect of sap velocity on FT and EA was similar to Experiment 1 (Table 1). As in Experiment 1, EA and FT were opposite in their response to sap velocity. On a volume basis, EA was significantly less at high velocity (159 µmol m–3 s–1) compared with low velocity (216 µmol m–3 s–1, t= –7.597, P= < 0.001) and FT tended to be greater at high velocity (561 µmol m–3 s–1) compared with low velocity (464 µmol m–3 s–1, t=2.071, P=0.057), but the difference was not significant. The variation in CO2 flux rates was smaller than in Experiment 1 because in Experiment 2, the differences between, and ranges within, high and low sap velocities were smaller than in Experiment 1. In Experiment 2, mean high sap velocity was 2.7 cm min–1 (range 2.0–3.6 cm min–1) and mean low velocity was 1.3 cm min–1 (range 0.5–1.9 cm min–1). A ‘low’ sap velocity was selected in Experiment 2 that was twice that of Experiment 1 (1.3 versus 0.6 cm min–1). Therefore, in Experiment 2, FT was the dominant flux at low velocity (Fig. 4A) as well as at high velocity, whereas EA was the dominant flux at low velocity in Experiment 1. In Experiment 2, the ‘low’ velocity was not low enough to cause EA to become the dominant flux.
Experiments 1 and 2: combined data
The significant relationship between sap velocity and the proportion of RS attributed to EA or FT was consistent between Experiments 1 and 2 (Fig. 5; Table 1). Only at very low sap velocities (below 0.7 cm min–1) was EA the dominant flux (Fig. 5). As sap velocity increased, the CO2 concentration in the xylem was diluted and the amount of CO2 that was transported in xylem sap (FT) simultaneously increased. This movement of CO2 away from the site of respiration resulted in a proportional decrease in EA. Thus, the strong negative relationship between EA and sap velocity (Table 1) appears to result from increased diffusion of CO2 associated with increased sap [] at low velocities. Additional evidence for this effect is shown by the linear relationships of EA to [] demonstrated in Experiment 1 (Fig. 3) and in the combined data set (Table 1).
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Experiment 3: effects of temperature
As expected, temperature had an exponential effect on EA, FT, and RS as well as xylem sap [
] (Fig. 6; Table 1). At all temperatures, at the measurement sap velocity (mean 1.0 cm min–1, range 0.7–1.3), FT was the dominant flux, consistent with Experiments 1 and 2. At 5 °C, EA was less than 20% of RS, while at 20 °C and 35 °C it increased to over 30% of RS (Fig. 7). Average Q10 of RS was 1.95 from 5–20 °C and 3.19 from 20–35 °C. The overall Q10 of RS from 5–35 °C was 2.49.
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Effects of sap velocity
This study was designed, in part, to test the concepts that respired CO2 dissolves in xylem sap and is transported away from the site of respiration, and that the rate of transport is affected by sap velocity. In the three experiments, the increase in xylem [
] was solely the result of recent branch respiration, since water entering the branch segments was at atmospheric CO2 concentration and no other source of CO2 was present. We directly demonstrated for the first time that respired CO2 was transported away from the site of respiration in xylem sap. Lower sap [] at high sap velocity versus low velocity appeared to be caused by a dilution effect. However, although sap [] decreased with increasing sap velocity, the amount of CO2 transported in sap was greater at high velocity than low velocity.
Sap velocity also affected the rate of CO2 efflux to the atmosphere. When velocity was reduced, CO2 efflux to the atmosphere increased. Negisi (1979) obtained similar results in a study where the sap flow rate through detached branches of Pinus densiflora trees was artificially manipulated, but because xylem [] was not measured, no direct conclusions could be made about the mechanism that caused the changes in CO2 efflux that were related to changes in sap velocity. Negisi speculated that the reduction in CO2 efflux with increasing sap velocity was caused by the transport of respired CO2 in the xylem stream. Previous manipulative experiments showed that artificially increasing or decreasing the CO2 concentration of water flowing through detached branches without changing the flow rate caused a proportional change in CO2 efflux (Teskey and McGuire, 2002, 2005), and similarly, in the current experiments, EA was correlated with xylem []. Together, these results suggest that radial CO2 efflux from stems and branches is partially a function of xylem sap [] and sap velocity.
We did not expect to see any effect of sap velocity on respiration, but in the first experiment the results showed that respiration was greater at low sap velocity. The cause for this response is unknown. It is possible that respiration increased over time, independent of sap velocity, perhaps due to wound respiration at the cut ends of the branches. Alternatively, the observed response may have been an artefact of the measurement techniques. Respiration was calculated as the sum of internal and external fluxes of CO2, which are determined by measuring many variables: temperature, pH, aqueous [CO2], sap flow rate, gaseous [CO2], and air flow rate. Errors associated with these measurements may have affected calculations of respiration or its components (McGuire and Teskey, 2002, 2004), but the magnitude of these errors is unknown.
Results of these experiments showed unequivocally that only a portion of respired CO2 fluxed to the atmosphere. The EA fraction of RS was correlated with the rate of sap velocity. Respiration was the active process that produced the CO2, while EA and FT were passive processes affected by physical factors: concentration gradients, barriers to diffusion, and mass flow. As CO2 was produced by respiring cells, it diffused in two directions: toward the atmosphere and into xylem sap. Although the diffusion coefficient for CO2 is four orders of magnitude greater in air than in water, barriers created by cambium and bark tissue maintained high concentration gradients between the xylem and the atmosphere and allowed CO2 to dissolve in xylem sap.
The purpose of these experiments was to determine the respiration rate of woody branch tissue and the capacity of xylem sap to absorb CO2 released by respiring cells. The use of water in equilibrium with ambient [CO2] to perfuse the stems allowed these determinations to be made without the effect of imported CO2 that has confounded all previous measurements. Imported CO2 affects measurements of CO2 efflux by constantly diffusing radially as it moves through the xylem in flowing sap. Within the xylem, imported CO2 mingles with CO2 that is released by local respiring cells, impeding accurate estimates of internal CO2 flux. By eliminating imported CO2, the rate of respiration was measured directly from the production of CO2. However, the use of water at near-zero [] to perfuse the xylem and, in some instances, very high sap velocities, increased the potential for diffusion of CO2 into the xylem sap above that which would normally occur in nature, so the estimates of FT and the relative proportion of FT in comparison with EA should be considered theoretical maxima.
Increased sap velocity reduces xylem [] by diluting the concentration of CO2 in the stem. Although the [] of the water used to perfuse the stems in these experiments was lower than reports of [] of xylem sap measured in the field (McGuire and Teskey, 2004), the dilution effect of flowing sap on xylem [] in the field should be similar to what was observed in these experiments, although its magnitude could be reduced. The dilution effect occurs in situ because [] of water entering the roots (Hamada and Tanaka, 2001) is substantially lower than [] of xylem sap. As flow rate increases, sap [] becomes progressively more diluted. The amount of respiratory CO2 that flowing sap can entrain and transport is dependent on factors that can vary substantially in the field: the initial [] of water entering the roots, the rate of root and stem respiration, temperature, sap pH, and sap flow rate.
Theoretically, if sap is not flowing and the rate of respiration is constant, CO2 will build up in the xylem to an equilibrium [] where the diffusion gradient from cell to xylem sap is equal to the barrier-attenuated diffusion gradient from xylem to atmosphere; after this equilibrium is achieved, all additional respiratory CO2 will flux to the atmosphere. When sap is flowing, this equilibrium will be affected in two ways. First, cells producing CO2 are bathed in sap, so the rate of sap flow will affect the rate at which respired CO2 is transported by mass flow away from the site of respiration. Second, water entering the stems or branches at lower [] will dilute the CO2 concentration of xylem sap and reduce the CO2 diffusion gradient from xylem to atmosphere, thereby slowing the rate of efflux and allowing more CO2 to dissolve in the sap. When sap flow slows or stops at night, the [] in the xylem will increase towards the equilibrium concentration. At the same time, CO2 efflux to the atmosphere will increase as the concentration gradient from stem to atmosphere increases.
However, in the field there are many factors that can influence the fate of dissolved CO2. First, if CO2 is transported in flowing sap from a large stem into a small branch, efflux from the branch might increase because the ratio of surface area to volume increases and barriers to diffusion to the atmosphere may be lower in the branch than in the stem (Sprugel, 1990; Cavaleri et al., 2006). Second, seasonal changes in xylem [] have been observed. In winter, xylem [] can decrease to near-atmospheric (MacDougal and Working, 1933; Eklund, 1990, 1993), probably due to negligible rates of respiration and sap flow. In this case, EA is likely to be a good estimator of woody tissue respiration. Third, the amount and fate of CO2 stored in heartwood of large stems is unknown. This CO2 might diffuse radially or axially at different rates due to differences in the air and water content of heartwood versus sapwood. If a large amount of CO2 is stored in heartwood it might buffer the effects of sap velocity on efflux.
The effect of sap flow on CO2 efflux has been demonstrated in situ. Gansert and Burgdorf (2005) showed a strong positive correlation in Betula pendula stems between the rate of sap flow and the reduction of daytime CO2 efflux. Bowman et al. (2005) found a positive relationship between sap flux density and the difference between respiration predicted by temperature and measured CO2 efflux in Dacrydium cupressinum stems. These results suggest that transport of CO2 was responsible for the negative correlations between sap flow rate and CO2 efflux. Despite the limitations imposed by the use of unrealistic sap velocities and [] in the current experiments, the processes elucidated here can explain observations of mid-day depression of CO2 efflux from tree stems in the field (Edwards and McLaughlin, 1978; Negisi, 1979; Hari et al., 1991; Martin et al., 1994; Levy et al., 1999; Bowman et al., 2005; Gansert and Burgdorf, 2005).
Results of these experiments demonstrated the theoretical maximum effect of sap velocity on efflux in small sycamore branches. At the highest velocity, the EA proportion of RS was reduced in some cases to less than 10%. Maximum sap velocity of sycamore branches measured with thermal dissipation sensors in the field in August 2006 was 0.53 cm min–1 (RO Teskey and MA McGuire, unpublished data). At that velocity, EA would account for 55% of respired CO2 based on the relationship between sap velocity and EA shown here. Substantially higher sap velocities have been reported in diffuse porous species (e.g. 4.6 cm min–1 in Liriodendron tulipifera, Huber and Schmidt, 1937, as reported in Kramer and Boyer, 1995), suggesting that greater reductions in EA are possible. In a previous field experiment on mature intact stems it was found that the EA proportion of respired CO2 during the diurnal period of highest transpiration (12. 00 h to 18.00 h) averaged 51% in a beech tree (Fagus grandifolia Ehrh.), 23% in a sycamore, and 72% in a sweetgum (Liquidambar styraciflua L.) (McGuire and Teskey, 2004). During the period of lowest transpiration (00.00 h to 06.00 h) all three species had EA proportions over 90%. While EA may be an inadequate measure of respiration in the field, it is possible use a mass balance approach (McGuire and Teskey, 2004) to estimate stand or ecosystem respiration, as long as differences among and within species and trees in tissue size, age, and growth rate are accounted for.
Effects of branch diameter
It is hypothesized that branch diameter would not have any effect on rates of CO2 fluxes if sap velocity remained constant among branches. This hypothesis should be true if the rate of cellular respiration, the distribution of living cells, and the pathway for CO2 diffusion to the atmosphere are similar in stems or branches of similar age, morphology and species. The hypothesis was supported when RS was calculated on a volume basis, but not on a surface area basis. There are many conflicting reports of relationships between CO2 efflux rates and diameter. In contrast to this study's results, negative relationships between volume-based efflux and diameter have been reported in the desert shrub Combretum micranthum (Levy and Jarvis, 1998), Pinus ponderosa trees growing in montane and desert environments (Carey et al., 1997), and a Pinus cembra tree growing at the alpine treeline (Wieser and Bahn, 2004). Meir and Grace (2002) found relationships between stem diameter and both surface area-based and volume-based efflux in 38 tropical rainforest tree species in Brazil and Cameroon. The lack of consistency among these studies, while puzzling, may indicate differences in the proportion of living cells in the xylem and cambium (Levy and Jarvis, 1998), differences in their respiratory potential (Pruyn et al., 2002a) or aeration, or variation in sap velocity, CO2 permeability of the periderm (Cernusak and Marshall, 2000), or the amount of CO2 transported in the xylem sap. In the current experiment, the difference in branch diameter classes was small (from 1 to 3 cm), yet there was a strong relationship between diameter and area-based fluxes (EA, FT, RS), but no relationship between diameter and volume-based fluxes. It is unlikely that the rate of cellular respiration could have been three times greater in a 3 cm diameter branch compared with a 1 cm branch under controlled temperature and sap velocity conditions, suggesting that volume was preferable over surface area for calculating CO2 fluxes.
However, CO2 flux rates are likely to vary among woody tissues of different sizes and growth rates (i.e. stems versus branches) at different times of year (Sprugel, 1990). For example, Stockfors and Linder (1998) found that living cells in the phloem of Picea abies trees dominated tissue efflux in April, June, and September, but not in July. The proportion of live cells in woody tissue also changes with age and position. Negisi (1974) measured CO2 efflux from detached parts of Pinus densiflora trees and found that efflux rates of younger trees were higher than older trees when comparing between stem or branch sections of similar diameter. Pruyn et al. (2002a) found a gradient of respiratory potential from inner bark >outer sapwood >inner sapwood of increment cores of Pseudotsuga menziesii trees and respiratory potential differed with vertical position of sampling. In a similar study, Pruyn et al. (2002b) also found variation in respiratory potential with age, i.e. sapwood of younger trees had a higher respiratory potential than that of older trees. In a study of CO2 efflux from woody parts of a Pinus pinaster tree, Bosc et al. (2003) found that phloem tissue contributed a decreasing proportion of the total mass of stems and branches with increasing age, and this change was reflected in measurements of efflux that varied with age, regardless of the diameter. Thus, even within a single tree, flux/volume and flux/area relationships can differ.
Effects of temperature
Temperature had a typical exponential effect on CO2 fluxes and respiration. The Q10 of RS was within the range of values reported in other studies of woody tissue respiration (1.0–3.2) as reviewed by Damesin et al. (2002). However, these studies reported efflux measurements as representing respiration without accounting for CO2 transported in xylem sap. In the current study, at the low temperature (5 °C), efflux accounted for only 18% of total respiration, on average, compared with 44% at the high temperature (35 °C). Therefore, using the Q10 of efflux to estimate respiration will cause a greater underestimation at low temperatures than at higher temperatures. A possible explanation for variation in the proportion of EA with temperature is the effect of temperature on the solubility of CO2 in water. At higher temperatures, CO2 is less soluble in water, so a smaller percentage of CO2 will dissolve in xylem sap, resulting in proportionally greater efflux to the atmosphere. Thus an increase in temperature will have a 3-fold effect: along with an increase in the rate of cellular respiration, the rate of CO2 diffusion to the atmosphere will increase (Fick's law), and the solubility of CO2 in sap will decrease (Henry's law). Although at higher temperatures a greater proportion of respired CO2 fluxed to the atmosphere, xylem [] also increased with temperature, indicating that barriers to diffusion prevent the immediate escape of respired CO2 and that the rate of respiration affects the amount of CO2 that can be temporarily stored in stems and branches. When sap is flowing, some of the stored CO2 will also be transported away from the site of respiration and sap velocity will control the rate of CO2 transport. This interaction of the effects of temperature and sap velocity on the proportion of CO2 that fluxes to the atmosphere confounds attempts to estimate respiration by measuring EA.
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Conclusions |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionConclusionsReferences |
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These experiments provided direct evidence that in woody branches a substantial amount of CO2 released from respiring cells can dissolve in xylem sap and be transported away from the site of respiration. The EA proportion of respired CO2 was negatively correlated with sap velocity and positively correlated with temperature. Diameter had no effect on EA, FT, or RS expressed on a volume basis, but it had a significant positive effect when fluxes were expressed on a surface area basis. It is concluded that sap velocity, which typically varies substantially throughout the day, is an important factor controlling the proportion of respired CO2 that diffuses from woody tissues into the atmosphere.
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This research was supported by USDA Cooperative State Research, Education, and Extension Service NRI Grant 2003-35100-13783 and National Science Foundation Grant IOB 0445495. Sofia Cerasoli was funded by the Government of Portugal through FCT Grant SFRH/BPD/14603/2003. We appreciate the insightful comments and suggestions of the anonymous reviewers and the subject editor.
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