A new canopy photosynthesis and transpiration measurement system (CAPTS) for canopy gas exchange research

Agricultural and Forest Meteorology 217 (2016) 101–107

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A new canopy photosynthesis and transpiration measurement system (CAPTS) for canopy gas exchange research Qingfeng Song a,b,c , Han Xiao b,d , Xianglin Xiao d , Xin-Guang Zhu a,b,c,∗ a

CAS Key Laboratory of Computational Biology, Chinese Academy of Sciences, Shanghai 200031, China CAS-MPG (Chinese Academy of Sciences-German Max Planck Society) Partner Institute for Computational Biology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200031, China c State Key Laboratory of Hybrid Rice, CAS-MPG Partner Institute for Computational Biology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Yueyang Road 320, Shanghai 200031, China d School of Biomedical Engineering, Shanghai Jiao Tong University, Dongchuan Road 800, Shanghai, China b

a r t i c l e

i n f o

Article history: Received 11 May 2015 Received in revised form 22 September 2015 Accepted 26 November 2015 Available online 8 December 2015 Keywords: Canopy photosynthesis Crop yield Field measurements Rice

a b s t r a c t Accurate measurement of canopy gas exchange rates is crucial for studying canopy photosynthetic resource use efficiencies. We designed, created, and evaluated a new canopy photosynthesis and transpiration measurement system (CAPTS). The CAPTS included: (1) modular chamber sides, (2) sensors for temperature, CO2 , air pressure and humidity that were integrated on a removable chamber cover, and (3) a user-friendly console for control of automatic opening and closing of the chamber cover for data recording, storage and analysis. The CAPTS can accurately measure canopy photosynthetic CO2 uptake rate, which was demonstrated with both rice and tobacco. The CAPTS provides a basic ability to measure rates of photosynthesis, respiration, and transpiration of plot-size canopies and other components of agro-ecosystems. © 2015 Published by Elsevier B.V.

1. Introduction Canopy photosynthetic CO2 uptake rates, i.e., the integrated photosynthetic rates of all leaves inside of a canopy, are positively correlated to crop yields (Wells et al., 1982; Zelitch, 1982). Therefore, identifying methods to improve canopy photosynthetic CO2 uptake rate is important for breeding high-yielding crops. However, to date there is no easy-to-use effective and quick tool for screening and measuring canopy photosynthesis, particularly in plot-size canopies. Historically, canopy photosynthetic CO2 uptake rate (Ac ) was measured by micrometeorological approaches, such as the Bowen ratio/energy balance method (Held et al., 1990), the eddy correlation method (McMillen, 1988), and canopy chamber approaches (Bugbee, 1992). The canopy chamber approach includes both open chamber systems (Long et al., 1996; Dragoni et al., 2005; Graydon et al., 2006; Burkart et al., 2007; Muller et al.,

∗ Corresponding author at: Partner Institute for Computational Biology, Chinese Academy of Sciences, CAS-MPG Partner Institute of Computational Biology, Shanghai Institute of Biological Sciences, Chinese Academy of Sciences, Shanghai 200031, China. Tel.: +86 21 54920486; fax: +86 21 54920451. E-mail address: [email protected] (X.-G. Zhu). http://dx.doi.org/10.1016/j.agrformet.2015.11.020 0168-1923/© 2015 Published by Elsevier B.V.

2009) and closed chamber systems (Reicosky, 1990; Wagner and Reicosky, 1992; Steduto et al., 2002; Pérez-Priego et al., 2010). The Bowen ratio/energy balance (BREB) method measures the gradient of humidity and temperature for use in calculating the Bowen ratio, which is the ratio of light energy dissipated as sensible heat to the light energy dissipated as latent heat. The Bowen ratio is then used to calculate the flux of sensible and latent heat from a canopy with an energy balance equation (Cellier and Olioso, 1993). The BREB method is usually used to measure water vapor flux, but it can also be used to measure CO2 fluxes assuming that the eddy transfer coefficients for sensible heat, water vapor and CO2 are equal (Held et al., 1990; Johnson et al., 2003). The eddy correlation method measures the vertical wind velocity and CO2 or H2 O concentration simultaneously, which are used to estimate the vertical fluxes of CO2 or H2 O (McMillen, 1988). The advantage of these two micrometeorological methods is that they do not disturb plant canopy structure and canopy microclimate; however, these methods cannot be used for plot-size canopies. For a plot-size measurement, canopy chambers are a suitable option (Dugas et al., 1991, 1997; Dugas, 1993; Angell et al., 2001; Johnson et al., 2003). Canopy chambers have been used for studying the influence of plant age on photosynthesis (Peng and Krieg, 1991), for tracing 13 C in soil respiration (Barthel et al., 2010), and for studying the effects of elevated CO2 concentration on plant

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Fig. 1. Design of the CAPTS. (A) The CAPTS included the following components: four sides that can be assembled to form a chamber, four fans that were fixed at different positions inside the CAPTS, one top cover that integrated sensors, a programmable logic controller that can collect and analyze signals from sensors, and a touchscreen monitor. (B) The sensors mounted on the top cover of the CAPTS.

photosynthesis and transpiration (Hileman et al., 1994). The open canopy chamber system (Long et al., 1996; Dragoni et al., 2005; Graydon et al., 2006; Burkart et al., 2007; Muller et al., 2009) measures gas concentrations at a gas inlet and outlet of a chamber as well as the gas flux rate through a canopy chamber (Long et al., 1996). A canopy chamber can continuously measure gas exchange rates inside a chamber with precise control of environmental parameters (Muller et al., 2009). The closed canopy chamber system measures gas exchange rate by measuring the changes in concentrations of CO2 and water vapor inside the chamber (Reicosky, 1990; Wagner and Reicosky, 1992). To continuously measure canopy photosynthesis, an automated closed-system canopy chamber has also been developed (Steduto et al., 2002) and been used for studies of small canopies, such as weeds. With recent emerging interest in improving canopy photosynthesis for improved crop yields, the development of new canopy photosynthesis and transpiration measurement systems that can accurately measure canopy gas exchange in a plot-size canopy is needed. This report describes the design, implementation, and evaluation of a new canopy photosynthesis and transpiration measurement system (CAPTS). This CAPTS had a number of novel features which enables it to be used as a basic tool to study photosynthesis, respiration, and transpiration of plot-size canopies or other components of agro-ecosystems.

2. CAPTS design 2.1. Components of the CAPTS The canopy photosynthesis and transpiration measurement system (CAPTS) consisted of a number of parts that can be easily dissembled and re-assembled using custom-designed connection units (Fig. 1). The CAPTS was one meter long, one meter wide, and 1 to 1.5 m high. Rubber material was used between the chamber cover and chamber sides to prevent gas leakage. A polycarbonate plate, which has a light transmittance of ∼0.9, was used to build the chamber sides and the chamber cover. The frame of the CAPTS was made of aluminum (Fig. 1B). All controllers and sensors (discussed in detail below) were fixed on the cover of the CAPTS. Air at four positions inside the CAPTS was sampled, pooled, and analyzed by an infrared CO2 gas analyzer. Four fans were installed inside the CAPTS to ensure sufficient gas mixing. The power of the fans were selected to ensure sufficient air mixing. 2.2. Sensors Two photosynthetic active radiation (PAR) sensors (LI-190 and LI-191, Licor, USA) were fixed on the cover, with one (LI-190) fixed on the top side of the cover to measure total incident PAR and the other (LI-191) fixed below the cover to measure PAR transmitted

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Table 1 Sensors used by the CAPTS. Parameters

Sensors

Input (DC)

Output (mA, V)

Measuring range

CO2 H2 O Temperature Pressure PAR

LI-840A LI-840A PT100 GT000 LI-190/191

24VDC 24VDC N/A 24VDC N/A

0–5 V 0–5 V ˝ 0–10 V 0–15 mV

300–500 ppm (adjustable) 10–60 ppt (adjustable) 0–100 ◦ C Normal air pressure 0–3000 ␮mol m−2 s−1

Quadratic regression of water  vapor  andCO2 concentrations to time were applied and dw/dt and dc/dt were the first derivatives at the time of canopy closure. V was the gas volume in the CAPTS which was equal to the volume of the CAPTS minus the volume of the plant leaves inside of the CAPTS. Considering that the volume of a canopy is usually less than 0.005 m3 , which was much less than the volume of the CAPTS (1–1.5 m3 ), V was approximated as the volume of the CAPTS. In Eqs. (1) and (2), S was the ground area covered by the canopy (m2 ) inside the CAPTS, Pa was air pressure (kPa), R was the gas constant (8.314 × 10−3 m3 kPa mol−2 K−1 ) and T was air temperature (K).

4. Experiments for evaluating the accuracy of the CAPTS

Fig. 2. CO2 concentration and H2 O partial pressure inside the CAPTS measured at 1 s intervals for a tobacco canopy in a growth room. The black arrows show when the cover was closed and the red arrows show when the cover was opened. The canopy photosynthetic CO2 uptake rate and transpiration rate were calculated based on the slopes of CO2 and H2 O concentration changes over time after the cover was closed.

through the cover. The pressure sensor used by the CAPTS was a GT000 (Beijing, China), which was installed on the cover inside of the CAPTS. CO2 and H2 O concentrations inside the CAPTS were measured with an infrared gas analyzer (LI-840A, Licor, USA) linked to a pump that sampled gas from the CAPTS. Outputs provided by these sensors were analog signals, i.e. voltage (U) or resistance (R) (Table 1). 2.3. Signal collection The analog signals provided by the sensors were collected by a PLC (programmable logic controller) based system, which included a main module, a PT100 module and two extension modules. The PLC system converted a voltage signal ranging between 0 and 10 V or a current signal ranging between 0 and 20 mA to a number in the range between 0 and 2000. A linear relationship between the output and the voltage or current was used during the conversion. Fig. 2 shows the dynamic changes in the CO2 and H2 O concentrations inside the CAPTS when the CAPTS was opened or closed. 3. Signal processing to obtain canopy photosynthesis and transpiration rates The canopy photosynthetic CO2 uptake rate (Ac ) and transpiration rate (Ec ) were calculated as in a previous study (Steduto et al., 2002) (Eqs. (1) and (2)). Ec =

dw V × Pa × S×R×T dt

(1)

Ac =

dc V × Pa × S×R×T dt

(2)

To evaluate the accuracy of the CAPTS in measuring canopy CO2 exchange rate, we compared measured Ac and calculated Ac for a rice canopy and a tobacco canopy. Rice was planted in a paddy field in the Songjiang experimental station of the Shanghai Institute for Plant Physiology and Ecology (121E, 31N). Both the row and column spacing of rice plantings were 20 cm. Tobacco was planted in 12-L pots filled with Pindstrup substrate (Pindstrup, Denmark). The pots were watered every 2 days. For the rice canopy, measurements were conducted at the booting stage. For the tobacco canopy, measurements were conducted on the 50th day after emergence. The Ac was measured with the CAPTS from 8:00 to 18:00 with an interval of ∼10 min for rice and from 6:30 to 18:00 with interval of ∼5 min for tobacco. To evaluate the accuracy of the CAPTS in measuring Ac , canopy photosynthetic CO2 uptake rates of both rice and tobacco canopies were also estimated with a canopy photosynthesis model (Song et al., 2013). To do this, we measured the canopy architectural parameters (Song et al., 2013) manually and also measured leaf photosynthetic parameters with a portable gas exchange system (LI-6400XT; LI-COR, Lincoln, Neb.). For rice, measurements were conducted using rice in the same plot as those for canopy photosynthesis measurements. For tobacco, we measured leaf photosynthetic properties using the same plants which were used for the canopy photosynthesis measurements. Leaf temperatures were maintained at 25 ◦ C during all measurements and incident PPFD above the canopy was maintained at 1500 ␮mol m−2 s−1 using redblue LEDs with 10% blue light. A photosynthetic CO2 uptake rate versus intercellular CO2 concentration curve (ACi curve) was first created. CO2 concentration was initially set at 400 ␮mol mol−1 and then it was decreased in a stepwise manner to 50 ␮mol mol−1 . Next, CO2 concentration was set to 425 ␮mol mol−1 and then increased in a stepwise manner to 1800 ␮mol mol−1 . The RuBP- and CO2 -saturated rate of RuBP carboxylation (Vcmax ) and light saturated rate of electron transfer (Jmax ) were estimated by fitting the measured ACi curves using a steady state biochemical model of photosynthesis (Farquhar et al., 1980). The data points below the transition point between Rubiscoand RuBP regeneration-limited photosynthesis were used to fit Rd and Vcmax , while the data points above the transition point were used to fit Jmax (Farquhar et al., 1980). The transition point between Rubisco-limited photosynthesis and RuBP-limited photosynthesis was determined based on equations from Farquhar et al. (1980). We estimated Vcmax and Jmax for 5 different layers of leaves for both

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the rice and tobacco canopies. With the measured canopy architectural parameters and leaf photosynthetic parameters, canopy photosynthesis rate was calculated with a canopy photosynthesis model (Song et al., 2013). To test the leakage of the CAPTS, we injected CO2 with a concentration of 1100 ␮mol mol−1 into the CAPTS chamber with the top cover closed. CO2 concentration changes were recorded every two seconds after closing the cover. The leakage of a chamber was calculated as: rL = L × c

(3)

where rL (ppm s−1 ) was the leakage rate, c (ppm) was the CO2 concentration difference between the inside and outside of the CAPTS, and L was the leakage coefficient. The recorded linear relationship between the leakage and c (Fig. 3) was used to estimate L using Eq. (3). This led to an estimate of L being 2.3 × 10−4 s−1 . When the CAPTS chamber was used in the field, the maximal c was ∼30 ␮mol mol-1 , which can in theory result in a leakage rate of about 0.007 ␮mol mol−1 s−1 with an L of 2.3 × 10−4 s−1 , which introduces an error of about 0.28 ␮mol m−2 s−1 based on Eq. (2). For a mature rice canopy under high light Ac is usually higher than 30 ␮mol m−2 s−1 , and thus the relative error cause by this leakage is less than 1%. In addition to leakage, the potential fluctuations in gas pressure and temperature inside the CAPTS chamber were also tested. The air pressure inside the CAPTS remained stable after the chamber cover was closed (Fig. 3) due to the slow flow rate of gas between the CAPTS chamber and the IRGA, which was ∼1 L/min. The air temperature inside the CAPTS was nearly constant (Fig. 3) during the first 35 s after the cover was closed. The CAPTS was used to measure diurnal changes in Ac , Ec and environmental parameters for both a rice canopy and a tobacco canopy. Fig. 4 shows diurnal changes in Ac for a rice canopy. The highest PAR was recorded at 10:00 (Fig. 4) because it was sunny in the morning but cloudy in the afternoon on the day of the experiment. CO2 concentrations in the rice canopy fluctuated diurnally from 380 ␮mol mol−1 in the early morning to 340 ␮mol mol−1 at midday, increasing back to 380 ␮mol mol−1 in the late afternoon (Fig. 4). Air temperature varied from 20 ◦ C to 27 ◦ C (Fig. 4). A positive Ac was estimated when PAR was high and a negative Ac was estimated when PAR was lower than ∼130 ␮mol m−2 s−1 in the late afternoon (Fig. 4). Using a four-plant tobacco canopy, we also measured Ec (Fig. 5A), AC (Fig. 5B), PAR (Fig. 5C), air temperature (Fig. 5D), water vapor concentration (Fig. 5E) and CO2 concentration (Fig. 5F). The measured Ac and Ec were higher around noon and lower in the early morning and late afternoon (Fig. 5B), as a result of the diurnal variation in environmental parameters, in particular PAR and temperature (Fig. 5C–F). We estimated Ac using a canopy photosynthesis model (Song et al., 2013) and compared it to the CAPTS-measured Ac . In both rice and tobacco canopies, measured and calculated Ac had a high level of correlation, with R2 higher than 0.9 (Fig. 6), suggesting that the CAPTS can accurately measure canopy CO2 uptake rates. 5. Discussion This report describes the design, implementation and evaluation of a canopy photosynthesis and transpiration measurement system (CAPTS). The CAPTS had a number of new features, such as full integration of sensors on a removable cover, capability of diurnal measurements due to fully automated control of cover opening and closing, a user-friendly console for data acquisition and analysis, and modular chamber sides that can be easily assembled to ease field transportation. These features enable the CAPTS to be used as an effective tool for measuring canopy photosynthesis,

respiration, and transpiration. In this paper, we first describe these new features of the CAPTS and the evaluation of its accuracy and then discuss potential applications of the CAPTS. The CAPTS can cover an area of ∼1 m2 and a height of up to 1.5 m, which makes the CAPTS appropriate for most plot-size canopy photosynthesis and transpiration measurements. It is worth mentioning that the CAPTS used a closed-chamber design, which is similar to some earlier efforts in developing canopy photosynthesis chambers (Reicosky, 1990; Pickering et al., 1993; Muller et al., 2009). The CAPTS used a top cover which integrated different sensors. The cover can be easily removed and resembled onto different chambers. The integration of sensors on a removable top cover make it possible to use one set of sensors on different chambers. For instance, we can measure ten canopies with intervals of 5 min by moving the top cover with its integrated sensors sequentially onto 10 different chambers. Users can operate the CAPTS through a user-friendly console, which controls the opening and closing of the cover, data storage, display, and analysis. All data collected from the CAPTS can be directly downloaded into an external computer for further detailed analysis and illustration. The ability of the CAPTS to automatically open and close the cover for data collection and to automatically store collected data enables it to be used for diurnal measurements of photosynthesis and transpiration. Furthermore, the CAPTS can be easily disassembled and re-assembled, which facilitates the transportation of the CAPTS in the field. The performance of the CAPTS was evaluated for both rice and tobacco canopies (Figs. 4 and 5). The canopy photosynthetic rates reached up to 40 ␮mol m−2 s−1 for the rice canopy shown in Fig. 4. Many factors influence canopy photosynthesis, including leaf photosynthetic properties, leaf area index, and ambient light, temperature, humidity etc. For any particular combinations of these different parameters, different canopy photosynthetic rates can be realized. Following the changes in photosynthetic photon flux densities, the measured Ac showed a gradual increase in the morning, reached its maximum around noon and then gradually declined in the afternoon (Figs. 4 and 5). For canopies used in this study, we estimated values of Ac to be ∼20–40 ␮mol m−2 s−1 , which is within the range of earlier reported values of Ac (Held et al., 1990; Steduto et al., 2002). The reported values of canopy photosynthetic CO2 uptake rates in Figs. 4 and 5 included plant photosynthesis, plant respiration, and also soil respiration. Technically, soil respiration can be measured independently using the chamber on bare soil without plants. Fig S1 shows an independent measurement of soil respiration in paddy soil. The measured soil respiration in paddy soil is around −1.8 ␮mol m−2 s−1 , which was about 5% of the maximal total canopy photosynthetic CO2 uptake rates (Fig. 4). Similarly, root respiration can be obtained as the difference between measured respiratory rate for soil only and rate for soil-root system together. We further validated the accuracy of the CAPTS by comparing the measured Ac to the Ac calculated using a canopy photosynthesis model (Song et al., 2013). High correlation coefficients between measured Ac and calculated Ac were obtained with slopes of 0.937 and 0.822 for tobacco and rice canopy, respectively. The large scattering in the measured Ac was due to the dynamic changes of light levels during the day. Though high R2 values were obtained between the measured canopy photosynthesis and calculated canopy photosynthesis for both rice and tobacco, however, there is a deviation of the slopes of the derived linear regression equation from the 1:1 line. This deviation can potentially be related to dynamic changes of photosynthetic activation status during the day (Pearcy, 1990), as contrast to the steady state assumption used in the calculation of the Ac . It is worth pointing out that the CAPTS can measure an Ac within 2 min. In contrast, if an Ac is calculated with a canopy photosynthesis model using the manually measured parameters, it will take at least half of a day for an experienced

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Fig. 3. Changes in environmental parameters when the CAPTS was closed. The initial CO2 concentration in the chamber was 1100 ␮mol mol−1 and ambient CO2 concentration was 400 ␮mol mol−1 . Gradual changes in CO2 concentration inside of the CAPTS are shown in (A). (B) shows the relationship between changes in CO2 concentration per unit of time and CO2 concentration difference between inside and outside of the chamber. (C) and (D) show gradual changes in air temperature and air pressure inside of the CAPTS.

Fig. 4. Diurnal canopy photosynthetic CO2 uptake rate (Ac ), temperature (T), CO2 concentration (CO2 ), and photosynthetic photon flux density of photosynthesis active radiation (PAR) measured using the canopy chamber from 8:00 to 18:00 in a rice (cultivar IR64) canopy.

researcher. The CAPTS therefore provides an approach to rapidly measure the rate of canopy CO2 uptake rates. The CAPTS has a wide range of potential applications. First, it can be used to measure Ac as demonstrated in this study.

Furthermore, by providing different measurement protocols, the CAPTS can measure other CO2 and water exchange fluxes important in agro-ecosystems. For example, if incident light can be blocked, net CO2 released from a canopy together with the soil and root

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Fig. 5. Diurnal variation of canopy transpiration rate (A), photosynthetic CO2 uptake rate (B), photosynthesis active radiation (C), temperature (D), water vapor concentration in canopy chamber (E) and CO2 concentration (F) in the CAPTS from 8:00 to 18:00. The measurement was conducted with a tobacco canopy of four tobacco plants.

Fig. 6. Relationship between the CAPTS-measured canopy photosynthetic CO2 uptake rates (Ac ) and Ac calculated with a canopy photosynthesis model (Song et al., 2013). The black line represents the line with a slope of 1; while the red line represents the regression line. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

system can be measured. If the CAPTS is used to cover only soil without any plants or roots, it can be used to measure soil respiration. Similarly, spike photosynthesis in cereal crops such as wheat can be estimated as the difference in CO2 uptake rates for a canopy

with spikes with or without illumination. In this study, we did not use a model to estimate the Ec . However, considering that H2 O and CO2 diffuse through stomata following similar physical laws, the CAPTS should also provide an accurate estimate of Ec .

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The principle of the closed system is to use the changes of CO2 and water vapor concentration with time to estimate the canopy photosynthetic and transpiration rates. One potential problem in this method is that the internal microclimates in the chamber can be altered during the measurements. This is clearly indicated in Fig. 2, where the water vapor concentration and temperature gradually increased while the CO2 concentration gradually decreased upon the closure of the chamber cover. To minimize the potential impacts of this modified microclimates on the leaf physiology, we have minimized the duration of the chamber closure to be 35 s. Furthermore, we only used the derivative at the time of the closure to estimate the transpiration and photosynthesis rate to minimize the impacts of these altered microclimates on the measurements. Furthermore, we have used fans to ensure sufficient air mixing to ensure similar air and temperature at the time of the cover closure (Fig. 1A). In summary, here we report the design, implementation, and evaluation of a canopy photosynthesis and transpiration measurement system. We demonstrated that it can accurately measure canopy photosynthetic CO2 uptake rates. Under defined measurement protocols, it can also be used to measure respiration of different components of agro-ecosystems as well. This system can be widely used in studying CO2 and water exchange of canopies or agro-ecosystems, which is of particular importance to improving resource, especially light, use efficiencies for crop breeding. Acknowledgements The authors thank anonymous reviewers for constructive comments. The authors acknowledge funding from National Natural Science Foundation of China young scientist grant (grant # 31501240) to QS and Shanghai Institutes for Biological Sciences young scientist frontier grant (grant # 2014KIP213) to QS, CAS strategic pilot project “Designer Breeding by Molecular Modules” (grant # XDA08020301) to XGZ, and the CAS-CSIRO Cooperative Research Program GJHZ1501 to XGZ. Appendix A. Supplementary data Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j.agrformet.2015. 11.020. References Angell, R.F., Svejcar, T., Bates, J., Saliendra, N.Z., Johnson, Da., 2001. Bowen ratio and closed chamber carbon dioxide flux measurements over sagebrush steppe vegetation. Agric. For. Meteorol. 108, 153–161. Barthel, M., Sturm, P., Gentsch, L., Knohl, A., 2010. Technical note: a combined soil/canopy chamber system for tracing ␦ 13 C in soil respiration after a 13 CO2 canopy pulse labelling. Biogeosci. Discuss 7, 1603–1631. Bugbee, B., 1992. Steady-state canopy gas exchange: system design and operation. HortScience 27, 770–776.

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