Agricultural and Forest Meteorology 217 (2016) 101–107
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Agricultural and Forest Meteorology
j our na l ho me page: www.elsev ier .com/ locate /agr formet
new canopy photosynthesis and transpiration measurement systemCAPTS) for canopy gas exchange research
ingfeng Songa,b,c, Han Xiaob,d, Xianglin Xiaod, Xin-Guang Zhua,b,c,∗
CAS Key Laboratory of Computational Biology, Chinese Academy of Sciences, Shanghai 200031, ChinaCAS-MPG (Chinese Academy of Sciences-German Max Planck Society) Partner Institute for Computational Biology, Shanghai Institutes for Biologicalciences, Chinese Academy of Sciences, Shanghai 200031, ChinaState Key Laboratory of Hybrid Rice, CAS-MPG Partner Institute for Computational Biology, Shanghai Institutes for Biological Sciences, Chinese Academy ofciences, Yueyang Road 320, Shanghai 200031, ChinaSchool of Biomedical Engineering, Shanghai Jiao Tong University, Dongchuan Road 800, Shanghai, China
r t i c l e i n f o
rticle history:eceived 11 May 2015eceived in revised form2 September 2015ccepted 26 November 2015
a b s t r a c t
Accurate measurement of canopy gas exchange rates is crucial for studying canopy photosyntheticresource use efficiencies. We designed, created, and evaluated a new canopy photosynthesis and tran-spiration measurement system (CAPTS). The CAPTS included: (1) modular chamber sides, (2) sensors fortemperature, 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 uptakerate, which was demonstrated with both rice and tobacco. The CAPTS provides a basic ability to measurerates of photosynthesis, respiration, and transpiration of plot-size canopies and other components ofagro-ecosystems.
Canopy photosynthetic CO2 uptake rates, i.e., the integratedhotosynthetic rates of all leaves inside of a canopy, are positivelyorrelated to crop yields (Wells et al., 1982; Zelitch, 1982). There-ore, identifying methods to improve canopy photosynthetic CO2ptake rate is important for breeding high-yielding crops. How-ver, to date there is no easy-to-use effective and quick tool forcreening and measuring canopy photosynthesis, particularly inlot-size canopies. Historically, canopy photosynthetic CO2 uptakeate (Ac) was measured by micrometeorological approaches, suchs the Bowen ratio/energy balance method (Held et al., 1990),he eddy correlation method (McMillen, 1988), and canopy cham-er approaches (Bugbee, 1992). The canopy chamber approach
ncludes both open chamber systems (Long et al., 1996; Dragonit al., 2005; Graydon et al., 2006; Burkart et al., 2007; Muller et al.,
∗ Corresponding author at: Partner Institute for Computational Biology, Chinesecademy of Sciences, CAS-MPG Partner Institute of Computational Biology, Shanghai
nstitute of Biological Sciences, Chinese Academy of Sciences, Shanghai 200031,hina. Tel.: +86 21 54920486; fax: +86 21 54920451.
2009) and closed chamber systems (Reicosky, 1990; Wagner andReicosky, 1992; Steduto et al., 2002; Pérez-Priego et al., 2010).
The Bowen ratio/energy balance (BREB) method measures thegradient of humidity and temperature for use in calculating theBowen ratio, which is the ratio of light energy dissipated as sen-sible heat to the light energy dissipated as latent heat. The Bowenratio is then used to calculate the flux of sensible and latent heatfrom a canopy with an energy balance equation (Cellier and Olioso,1993). The BREB method is usually used to measure water vaporflux, but it can also be used to measure CO2 fluxes assuming thatthe eddy transfer coefficients for sensible heat, water vapor andCO2 are equal (Held et al., 1990; Johnson et al., 2003). The eddycorrelation method measures the vertical wind velocity and CO2or H2O concentration simultaneously, which are used to estimatethe vertical fluxes of CO2 or H2O (McMillen, 1988). The advantage ofthese two micrometeorological methods is that they do not disturbplant canopy structure and canopy microclimate; however, thesemethods cannot be used for plot-size canopies.
For a plot-size measurement, canopy chambers are a suitableoption (Dugas et al., 1991, 1997; Dugas, 1993; Angell et al., 2001;
Johnson et al., 2003). Canopy chambers have been used for study-ing the influence of plant age on photosynthesis (Peng and Krieg,1991), for tracing 13C in soil respiration (Barthel et al., 2010), andfor studying the effects of elevated CO2 concentration on plant
102 Q. Song et al. / Agricultural and Forest Meteorology 217 (2016) 101–107
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 differentp le logim
pcGmb(socsiTcew
tpaiesfto
ositions inside the CAPTS, one top cover that integrated sensors, a programmabonitor. (B) The sensors mounted on the top cover of the CAPTS.
hotosynthesis and transpiration (Hileman et al., 1994). The openanopy chamber system (Long et al., 1996; Dragoni et al., 2005;raydon et al., 2006; Burkart et al., 2007; Muller et al., 2009)easures gas concentrations at a gas inlet and outlet of a cham-
er as well as the gas flux rate through a canopy chamberLong et al., 1996). A canopy chamber can continuously mea-ure gas exchange rates inside a chamber with precise controlf environmental parameters (Muller et al., 2009). The closedanopy chamber system measures gas exchange rate by mea-uring the changes in concentrations of CO2 and water vapornside the chamber (Reicosky, 1990; Wagner and Reicosky, 1992).o continuously measure canopy photosynthesis, an automatedlosed-system canopy chamber has also been developed (Stedutot al., 2002) and been used for studies of small canopies, such aseeds.
With recent emerging interest in improving canopy photosyn-hesis for improved crop yields, the development of new canopyhotosynthesis and transpiration measurement systems that canccurately measure canopy gas exchange in a plot-size canopys needed. This report describes the design, implementation, andvaluation of a new canopy photosynthesis and transpiration mea-
urement system (CAPTS). This CAPTS had a number of noveleatures which enables it to be used as a basic tool to study pho-osynthesis, respiration, and transpiration of plot-size canopies orther components of agro-ecosystems.
c controller that can collect and analyze signals from sensors, and a touchscreen
2. CAPTS design
2.1. Components of the CAPTS
The canopy photosynthesis and transpiration measurement sys-tem (CAPTS) consisted of a number of parts that can be easilydissembled and re-assembled using custom-designed connectionunits (Fig. 1). The CAPTS was one meter long, one meter wide, and1 to 1.5 m high. Rubber material was used between the chambercover and chamber sides to prevent gas leakage. A polycarbonateplate, which has a light transmittance of ∼0.9, was used to build thechamber sides and the chamber cover. The frame of the CAPTS wasmade of aluminum (Fig. 1B). All controllers and sensors (discussedin detail below) were fixed on the cover of the CAPTS. Air at fourpositions inside the CAPTS was sampled, pooled, and analyzed byan infrared CO2 gas analyzer. Four fans were installed inside theCAPTS to ensure sufficient gas mixing. The power of the fans wereselected to ensure sufficient air mixing.
2.2. Sensors
Two photosynthetic active radiation (PAR) sensors (LI-190 andLI-191, Licor, USA) were fixed on the cover, with one (LI-190) fixedon the top side of the cover to measure total incident PAR and theother (LI-191) fixed below the cover to measure PAR transmitted
Q. Song et al. / Agricultural and Forest Meteorology 217 (2016) 101–107 103
Table 1Sensors used by the CAPTS.
Parameters Sensors Input (DC) Output (mA, V) Measuring range
CO2 LI-840A 24VDC 0–5 V 300–500 ppm (adjustable)H2O LI-840A 24VDC 0–5 V 10–60 ppt (adjustable)Temperature PT100 N/A
◦
Pressure GT000 24VDC
PAR LI-190/191 N/A
Fig. 2. CO2 concentration and H2O partial pressure inside the CAPTS measured at 1 sintervals for a tobacco canopy in a growth room. The black arrows show when thecps
tGtsat(
2
PaPorpsi
3t
t2
E
A
over was closed and the red arrows show when the cover was opened. The canopyhotosynthetic CO2 uptake rate and transpiration rate were calculated based on thelopes of CO2 and H2O concentration changes over time after the cover was closed.
hrough the cover. The pressure sensor used by the CAPTS was aT000 (Beijing, China), which was installed on the cover inside of
he CAPTS. CO2 and H2O concentrations inside the CAPTS were mea-ured with an infrared gas analyzer (LI-840A, Licor, USA) linked to
pump that sampled gas from the CAPTS. Outputs provided byhese sensors were analog signals, i.e. voltage (U) or resistance (R)Table 1).
.3. Signal collection
The analog signals provided by the sensors were collected by aLC (programmable logic controller) based system, which included
main module, a PT100 module and two extension modules. TheLC system converted a voltage signal ranging between 0 and 10 Vr a current signal ranging between 0 and 20 mA to a number in theange between 0 and 2000. A linear relationship between the out-ut and the voltage or current was used during the conversion. Fig. 2hows the dynamic changes in the CO2 and H2O concentrationsnside the CAPTS when the CAPTS was opened or closed.
. Signal processing to obtain canopy photosynthesis andranspiration rates
The canopy photosynthetic CO2 uptake rate (Ac) and transpira-ion rate (Ec) were calculated as in a previous study (Steduto et al.,002) (Eqs. (1) and (2)).
dw V × Pa
c =
dt×
S × R × T(1)
c = dc
dt× V × Pa
S × R × T(2)
0–100 C0–10 V Normal air pressure0–15 mV 0–3000 �mol m−2 s−1
Quadratic regression of water vapor and CO2 concentrations totime were applied and
(dw/dt
)and
(dc/dt
)were the first deriva-
tives at the time of canopy closure. V was the gas volume in theCAPTS which was equal to the volume of the CAPTS minus the vol-ume of the plant leaves inside of the CAPTS. Considering that thevolume of a canopy is usually less than 0.005 m3, which was muchless than the volume of the CAPTS (1–1.5 m3), V was approximatedas the volume of the CAPTS. In Eqs. (1) and (2), S was the groundarea covered by the canopy (m2) inside the CAPTS, Pa was air pres-sure (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
To evaluate the accuracy of the CAPTS in measuring canopy CO2exchange rate, we compared measured Ac and calculated Ac for arice canopy and a tobacco canopy. Rice was planted in a paddy fieldin the Songjiang experimental station of the Shanghai Institute forPlant Physiology and Ecology (121E, 31N). Both the row and col-umn spacing of rice plantings were 20 cm. Tobacco was plantedin 12-L pots filled with Pindstrup substrate (Pindstrup, Denmark).The pots were watered every 2 days. For the rice canopy, measure-ments 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 aninterval 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 mea-suring Ac, canopy photosynthetic CO2 uptake rates of both rice andtobacco canopies were also estimated with a canopy photosynthe-sis model (Song et al., 2013). To do this, we measured the canopyarchitectural parameters (Song et al., 2013) manually and also mea-sured leaf photosynthetic parameters with a portable gas exchangesystem (LI-6400XT; LI-COR, Lincoln, Neb.). For rice, measurementswere conducted using rice in the same plot as those for canopyphotosynthesis measurements. For tobacco, we measured leaf pho-tosynthetic properties using the same plants which were used forthe canopy photosynthesis measurements. Leaf temperatures weremaintained at 25 ◦C during all measurements and incident PPFDabove the canopy was maintained at 1500 �mol m−2 s−1 using red-blue LEDs with 10% blue light.
A photosynthetic CO2 uptake rate versus intercellular CO2 con-centration curve (ACi curve) was first created. CO2 concentrationwas initially set at 400 �mol mol−1 and then it was decreased in astepwise manner to 50 �mol mol−1. Next, CO2 concentration wasset to 425 �mol mol−1 and then increased in a stepwise mannerto 1800 �mol mol−1. The RuBP- and CO2-saturated rate of RuBPcarboxylation (Vcmax) and light saturated rate of electron transfer(Jmax) were estimated by fitting the measured ACi curves using asteady state biochemical model of photosynthesis (Farquhar et al.,1980). The data points below the transition point between Rubisco-and RuBP regeneration-limited photosynthesis were used to fit Rdand Vcmax, while the data points above the transition point were
used to fit Jmax (Farquhar et al., 1980). The transition point betweenRubisco-limited photosynthesis and RuBP-limited photosynthesiswas determined based on equations from Farquhar et al. (1980). Weestimated Vcmax and Jmax for 5 different layers of leaves for both
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he rice and tobacco canopies. With the measured canopy archi-ectural parameters and leaf photosynthetic parameters, canopyhotosynthesis rate was calculated with a canopy photosynthesisodel (Song et al., 2013).To test the leakage of the CAPTS, we injected CO2 with a con-
entration of 1100 �mol mol−1 into the CAPTS chamber with theop cover closed. CO2 concentration changes were recorded everywo seconds after closing the cover. The leakage of a chamber wasalculated as:
L = L × �c (3)
here rL (ppm s−1) was the leakage rate, �c (ppm) was the CO2oncentration difference between the inside and outside of theAPTS, and L was the leakage coefficient. The recorded linear rela-ionship between the leakage and �c (Fig. 3) was used to estimate
using Eq. (3). This led to an estimate of L being 2.3 × 10−4 s−1.hen the CAPTS chamber was used in the field, the maximal �cas ∼30 �mol mol-1, which can in theory result in a leakage rate
f about 0.007 �mol mol−1 s−1 with an L of 2.3 × 10−4 s−1, whichntroduces an error of about 0.28 �mol m−2 s−1 based on Eq. (2).or a mature rice canopy under high light Ac is usually higher than0 �mol m−2 s−1, and thus the relative error cause by this leakage
s less than 1%. In addition to leakage, the potential fluctuations inas pressure and temperature inside the CAPTS chamber were alsoested. The air pressure inside the CAPTS remained stable after thehamber cover was closed (Fig. 3) due to the slow flow rate of gasetween the CAPTS chamber and the IRGA, which was ∼1 L/min.he air temperature inside the CAPTS was nearly constant (Fig. 3)uring the first 35 s after the cover was closed.
The CAPTS was used to measure diurnal changes in Ac, Ec andnvironmental parameters for both a rice canopy and a tobaccoanopy. Fig. 4 shows diurnal changes in Ac for a rice canopy. Theighest PAR was recorded at 10:00 (Fig. 4) because it was sunny inhe morning but cloudy in the afternoon on the day of the exper-ment. CO2 concentrations in the rice canopy fluctuated diurnallyrom 380 �mol mol−1 in the early morning to 340 �mol mol−1 at
idday, increasing back to 380 �mol mol−1 in the late afternoonFig. 4). Air temperature varied from 20 ◦C to 27 ◦C (Fig. 4). A pos-tive Ac was estimated when PAR was high and a negative Ac wasstimated when PAR was lower than ∼130 �mol m−2 s−1 in the latefternoon (Fig. 4).
Using a four-plant tobacco canopy, we also measured Ec (Fig. 5A),C (Fig. 5B), PAR (Fig. 5C), air temperature (Fig. 5D), water vaporoncentration (Fig. 5E) and CO2 concentration (Fig. 5F). The mea-ured Ac and Ec were higher around noon and lower in the earlyorning and late afternoon (Fig. 5B), as a result of the diurnal
ariation in environmental parameters, in particular PAR and tem-erature (Fig. 5C–F).
We estimated Ac using a canopy photosynthesis model (Songt al., 2013) and compared it to the CAPTS-measured Ac. In bothice and tobacco canopies, measured and calculated Ac had a highevel of correlation, with R2 higher than 0.9 (Fig. 6), suggesting thathe CAPTS can accurately measure canopy CO2 uptake rates.
. Discussion
This report describes the design, implementation and evalua-ion of a canopy photosynthesis and transpiration measurementystem (CAPTS). The CAPTS had a number of new features, such asull integration of sensors on a removable cover, capability of diur-al measurements due to fully automated control of cover opening
nd closing, a user-friendly console for data acquisition and anal-sis, and modular chamber sides that can be easily assembled toase field transportation. These features enable the CAPTS to besed as an effective tool for measuring canopy photosynthesis,
eteorology 217 (2016) 101–107
respiration, and transpiration. In this paper, we first describe thesenew features of the CAPTS and the evaluation of its accuracy andthen 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 canopyphotosynthesis and transpiration measurements. It is worth men-tioning that the CAPTS used a closed-chamber design, which issimilar to some earlier efforts in developing canopy photosynthe-sis chambers (Reicosky, 1990; Pickering et al., 1993; Muller et al.,2009). The CAPTS used a top cover which integrated different sen-sors. The cover can be easily removed and resembled onto differentchambers. The integration of sensors on a removable top covermake it possible to use one set of sensors on different chambers.For instance, we can measure ten canopies with intervals of 5 minby moving the top cover with its integrated sensors sequentiallyonto 10 different chambers. Users can operate the CAPTS througha user-friendly console, which controls the opening and closingof the cover, data storage, display, and analysis. All data collectedfrom the CAPTS can be directly downloaded into an external com-puter for further detailed analysis and illustration. The ability of theCAPTS to automatically open and close the cover for data collectionand to automatically store collected data enables it to be used fordiurnal measurements of photosynthesis and transpiration. Fur-thermore, 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 riceand tobacco canopies (Figs. 4 and 5). The canopy photosyntheticrates reached up to 40 �mol m−2 s−1 for the rice canopy shown inFig. 4. Many factors influence canopy photosynthesis, including leafphotosynthetic properties, leaf area index, and ambient light, tem-perature, humidity etc. For any particular combinations of thesedifferent parameters, different canopy photosynthetic rates can berealized. Following the changes in photosynthetic photon flux den-sities, the measured Ac showed a gradual increase in the morning,reached its maximum around noon and then gradually declined inthe afternoon (Figs. 4 and 5). For canopies used in this study, weestimated values of Ac to be ∼20–40 �mol m−2 s−1, which is withinthe range of earlier reported values of Ac (Held et al., 1990; Stedutoet al., 2002). The reported values of canopy photosynthetic CO2uptake rates in Figs. 4 and 5 included plant photosynthesis, plantrespiration, and also soil respiration. Technically, soil respirationcan be measured independently using the chamber on bare soilwithout plants. Fig S1 shows an independent measurement of soilrespiration in paddy soil. The measured soil respiration in paddysoil is around −1.8 �mol m−2 s−1, which was about 5% of the maxi-mal total canopy photosynthetic CO2 uptake rates (Fig. 4). Similarly,root respiration can be obtained as the difference between mea-sured respiratory rate for soil only and rate for soil-root systemtogether.
We further validated the accuracy of the CAPTS by comparingthe measured Ac to the Ac calculated using a canopy photosynthe-sis model (Song et al., 2013). High correlation coefficients betweenmeasured Ac and calculated Ac were obtained with slopes of 0.937and 0.822 for tobacco and rice canopy, respectively. The large scat-tering in the measured Ac was due to the dynamic changes oflight levels during the day. Though high R2 values were obtainedbetween the measured canopy photosynthesis and calculatedcanopy photosynthesis for both rice and tobacco, however, thereis a deviation of the slopes of the derived linear regression equa-tion from the 1:1 line. This deviation can potentially be related todynamic 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 CAPTScan measure an Ac within 2 min. In contrast, if an Ac is calculatedwith a canopy photosynthesis model using the manually measuredparameters, it will take at least half of a day for an experienced
Q. Song et al. / Agricultural and Forest Meteorology 217 (2016) 101–107 105
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 concentrationwas 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 unitof 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 theCAPTS.
F concer ultiva
rm
i
ig. 4. Diurnal canopy photosynthetic CO2 uptake rate (Ac), temperature (T), CO2
adiation (PAR) measured using the canopy chamber from 8:00 to 18:00 in a rice (c
esearcher. The CAPTS therefore provides an approach to rapidlyeasure the rate of canopy CO2 uptake rates.The CAPTS has a wide range of potential applications. First,
t can be used to measure Ac as demonstrated in this study.
ntration (CO2), and photosynthetic photon flux density of photosynthesis activer IR64) canopy.
Furthermore, by providing different measurement protocols, theCAPTS can measure other CO2 and water exchange fluxes importantin agro-ecosystems. For example, if incident light can be blocked,net CO2 released from a canopy together with the soil and root
106 Q. Song et al. / Agricultural and Forest Meteorology 217 (2016) 101–107
Fig. 5. Diurnal variation of canopy transpiration rate (A), photosynthetic CO2 uptake rate (B), photosynthesis active radiation (C), temperature (D), water vapor concentrationin 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.
F ake raT e regr
swtc
ig. 6. Relationship between the CAPTS-measured canopy photosynthetic CO2 upthe black line represents the line with a slope of 1; while the red line represents theader is referred to the web version of this article.)
ystem can be measured. If the CAPTS is used to cover only soilithout any plants or roots, it can be used to measure soil respira-
ion. Similarly, spike photosynthesis in cereal crops such as wheatan be estimated as the difference in CO2 uptake rates for a canopy
tes (Ac) and Ac calculated with a canopy photosynthesis model (Song et al., 2013).ression line. (For interpretation of the references to color in this figure legend, the
with spikes with or without illumination. In this study, we did notuse a model to estimate the Ec. However, considering that H2O andCO2 diffuse through stomata following similar physical laws, theCAPTS should also provide an accurate estimate of Ec.
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The principle of the closed system is to use the changes of CO2nd water vapor concentration with time to estimate the canopyhotosynthetic and transpiration rates. One potential problem inhis method is that the internal microclimates in the chamber cane altered during the measurements. This is clearly indicated inig. 2, where the water vapor concentration and temperature grad-ally increased while the CO2 concentration gradually decreasedpon the closure of the chamber cover. To minimize the potential
mpacts of this modified microclimates on the leaf physiology, weave minimized the duration of the chamber closure to be 35 s.urthermore, we only used the derivative at the time of the closureo estimate the transpiration and photosynthesis rate to minimizehe impacts of these altered microclimates on the measurements.urthermore, we have used fans to ensure sufficient air mixing tonsure similar air and temperature at the time of the cover closureFig. 1A).
In summary, here we report the design, implementation, andvaluation of a canopy photosynthesis and transpiration measure-ent system. We demonstrated that it can accurately measure
anopy photosynthetic CO2 uptake rates. Under defined measure-ent protocols, it can also be used to measure respiration of
ifferent components of agro-ecosystems as well. This system cane widely used in studying CO2 and water exchange of canopies orgro-ecosystems, which is of particular importance to improvingesource, especially light, use efficiencies for crop breeding.
cknowledgements
The authors thank anonymous reviewers for constructiveomments. The authors acknowledge funding from National Nat-ral Science Foundation of China young scientist grant (grant #1501240) to QS and Shanghai Institutes for Biological Sciencesoung scientist frontier grant (grant # 2014KIP213) to QS, CAStrategic pilot project “Designer Breeding by Molecular Modules”grant # XDA08020301) to XGZ, and the CAS-CSIRO Cooperativeesearch Program GJHZ1501 to XGZ.
ppendix A. Supplementary data
Supplementary data associated with this article can be found, inhe online version, at http://dx.doi.org/10.1016/j.agrformet.2015.1.020.
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