Partitioning of canopy and soil CO2 fluxes in a pine forest at the dry timberline across a 13-year observation period

Partitioning carbon fluxes is key to understanding the process underlying ecosystem response to change. This study used soil and canopy fluxes with stable isotopes (13C) and radiocarbon (14C) measurements in an 18 km2, 50year-old, dry (287 mm mean annual precipitation; nonirrigated) Pinus halepensis forest plantation in Israel to partition the net ecosystem’s CO2 flux into gross primary productivity (GPP) and ecosystem respiration (Re) and (with the aid of isotopic measurements) soil respiration flux (Rs) into autotrophic (Rsa), heterotrophic (Rh), and inorganic (Ri) components. On an annual scale, GPP and Re were 655 and 488 g C m−2, respectively, with a net primary productivity (NPP) of 282 g C m−2 and carbon-use efficiency (CUE=NPP /GPP) of 0.43. Rs made up 60 % of the Re and comprised 24± 4 %Rsa, 23± 4 %Rh, and 13± 1 %Ri. The contribution of root and microbial respiration toRe increased during high productivity periods, and inorganic sources were more significant components when the soil water content was low. Comparing the ratio of the respiration components to Re of our mean 2016 values to those of 2003 (mean for 2001– 2006) at the same site indicated a decrease in the autotrophic components (roots, foliage, and wood) by about −13 % and an increase in the heterotrophic component (Rh/Re) by about +18 %, with similar trends for soil respiration (Rsa/Rs decreasing by −19 % and Rh/Rs increasing by +8 %, respectively). The soil respiration sensitivity to temperature (Q10) decreased across the same observation period by 36 % and 9 % in the wet and dry periods, respectively. Low rates of soil carbon loss combined with relatively high belowground carbon allocation (i.e., 38 % of canopy CO2 uptake) and low sensitivity to temperature help explain the high soil organic carbon accumulation and the relatively high ecosystem CUE of the dry forest.


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The annual net storage of carbon in the land biosphere, known as net ecosystem production (NEP), is the 30 balance between carbon uptake during gross primary productivity (GPP) and carbon loss during growth, 31 maintenance respiration by plants (i.e., autotrophic respiration, Ra), and decomposition of litter and soil 32 organic matter (i.e., heterotrophic respiration, Rh; Bonan, 2008). The difference between GPP and Ra 33 expresses the net primary production (NPP) and is the net carbon uptake by plants that can be used for new 34 biomass production. Measurements from a range of ecosystems have shown that total plant respiration can 35 be as large as 50% of GPP (e.g., Etzold et al., 2011)

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Half-hour auxiliary measurements used in this study included photosynthetic activity radiation (PAR mol 144 m -2 s -1 ), vapor pressure deficit (VPD, kPa), wind speed (m s -1 ), and relative humidity (RH, %), with 145 additional measurements as described elsewhere (Tatarinov et al., 2016). Furthermore, the soil 146 microclimatology half-hour measurements were measured and calculated with soil chamber 147 measurements, using the LI-8150-203 (LI-COR, Lincoln, NE), as described below, namely air temperature 148 (Ta, °C) and relative humidity (RH, %) at 20 cm above the soil surface and soil temperature (Ts, °C) at a 149 5 cm soil depth using a soil temperature probe, as well as volumetric soil water content (SWC0-10, m 3 m -3 ) 150 in the upper 10 cm of the soil near the chambers, using the ThetaProbe model ML2x (Delta-T Devices   151 Ltd., Cambridge, UK), which was calibrated to the soil composition based on the manufacturer's equations.

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where dC/dt is the rate of change in the water-corrected CO2 mole fraction (μmol CO2 mol -1 air s -1 ), v is 167 the system volume (m 3 ), P is the chamber pressure (Pa), s is the soil surface area within the collar (m 2 ), Ta 168 is the chamber air temperature (K), and R is the gas constant (J mol -1 K -1  CO2-free air at room temperature close to field conditions. The CO2 was allowed to accumulate to at least 231 2,000 ppm (~2 h).

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The heterotrophic (δ 13 Ch) endmember was estimated as in Taylor

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On the diurnal timescale, CO2 fluxes showed typical daily cycles (Fig. 1). As expected, on average, all CO2 327 fluxes were higher during the wet period compared to the dry season by a factor of ~2. However, Rs and 328 Re peaked around midday in both the wet and dry seasons, while the more physiologically controlled NEE 329 and GPP showed a shift from midday (around 11:00-14:00) to early morning (08:00-11:00) in the dry 330 season, with a midday depression and a secondary afternoon peak (Fig. 1d).

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The temporal variations across the seasonal cycle are reported in Fig. 2, based on monthly mean values, 332 exhibiting sharp differences between the wet and dry seasons. As previously observed in this semi-arid 333 site, all CO2 fluxes peak in early spring between March and April. The corresponding high-resolution data 13 are reported in Fig. SI-6, which show also that the high winter (February) Rs rates were associated with 335 clear days when photosynthetic active radiation (PAR) increased with air temperature, Ta. These data also 336 show that, following rainy days, daily Rs values could reach 6.1 µmol m -2 s -1 , although the average was 337 1.1 ± 0.2 µmol m -2 s -1 during the wet period, which diminished by ~55% in the dry season to mean daily 338 values of 0.5 ± 0.1 µmol m -2 s -1 . In spring (April), all CO2 fluxes peaked during the crossover trends of 339 decreasing soil moisture content and increasing both temperature and PAR (Fig. SI-6).  (Table SI-2). These equations explained 43% and 70% of the variation in Rs in the dry and wet seasons, 353 respectively (Table SI- (Tables 3 and SI-1).   402 On average across the measurement period, Rs was the main CO2 flux to atmosphere, making up 60 ± 6% 403 of Re (295 ± 4 g C m -2 y -1 ; Tables 3 and SI-1), and Rf was another significant component accounting for 404 40 ± 6% of Re (Fig. 3b), which reflected the low density (300 trees ha -1 ) nature of the semi-arid forest. As 405 indicated above, Re partitioning showed a decrease in Rs/Re and an increase in Rf/Re from winter to 406 summer, which is clearly apparent in Fig. 3b. On an annual scale, during the study period, estimates of Rf, 407 Rsa, Rh, and Ri values were 194 ± 36, 119 ± 21, 115 ± 20, and 61 ± 6 g C m -2 y -1 , respectively. Despite 408 relatively high rates of respiration fluxes, the CUE of the ecosystem remained high at 0.43.

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Using the site records of nearly 20 years, long-term trends in GPP, NPP, Re, and NEP were obtained. Soil

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Carbon partitioning belowground (TBCA/GPP) was relatively high (~38%), with little change across the 437 long-term observation period. It is, however, within the range of mean value for forests in different biomes 438 (Litton et al., 2007). High belowground allocation helps explain the high rate of SOC accumulation 439 observed over the period since afforestation (Grünzweig et al., 2007;Qubaja et al., in press). Note that, 440 irrespective of the soil carbon accumulation, the abiotic component to the CO2 flux seems to be significant 441 in dry environments (Table 3)  The long-term perspective from the 13-year observation period indicates emerging trends that can be a 466 basis for assessing the effects of forest age and the marked increase in LAI (Table 3) Table 3). This shows a shifting trend from the autotrophic components to the heterotrophic, with 472 little change in the contribution of Rs to the overall efflux. The ratios of Rsa, Rl, and Rw to Re tended to 473 decrease by about 13%, while that of Rh increased by about 18%; similar trends were seen in soil 474 respiration, with Rsa/Rs decreasing by -19% and Rh/Rs increasing by +8% (Table 3) (Reichstein et al., 2003;Tang et al., 2005). This is also consistent with soil warming experiments by 0.76°C 484 in Mediterranean ecosystems, which decreased the Rs by 16%, and Q10 by 14% (Wang et al., 2014). Note 485 also that the low temperature sensitivity in the dry season is likely to be related to reduced microbial 486 activity, but may also involve downregulation of plant activity (Maseyk et al., 2008a) and drought-induced 487 dormancy of shallow roots (Schiller, 2000). Finally, we also note that the greater importance of moisture 488 availability in influencing respiration is clearly apparent from the observed relationships of Rs and Rh to