Soil moisture supply and atmospheric demand for water independently limit-and profoundly a ect-vegetation productivity and water use during periods of hydrologic stress [1][2][3][4] . Disentangling the impact of these two drivers on ecosystem carbon and water cycling is di cult because they are often correlated, and experimental tools for manipulating atmospheric demand in the field are lacking. Consequently, the role of atmospheric demand is often not adequately factored into experiments or represented in models 5-7 . Here we show that atmospheric demand limits surface conductance and evapotranspiration to a greater extent than soil moisture in many biomes, including mesic forests that are of particular importance to the terrestrial carbon sink 8,9 . Further, using projections from ten general circulation models, we show that climate change will increase the importance of atmospheric constraints to carbon and water fluxes in all ecosystems. Consequently, atmospheric demand will become increasingly important for vegetation function, accounting for >70% of growing season limitation to surface conductance in mesic temperate forests. Our results suggest that failure to consider the limiting role of atmospheric demand in experimental designs, simulation models and land management strategies will lead to incorrect projections of ecosystem responses to future climate conditions. Ecosystem moisture stress is often characterized by changes in soil water availability 10,11 . Declining soil moisture impedes the movement of water to evaporating sites at the soil or leaf surface 12 , reducing the surface conductance to water vapour (G S )-a key determinant of carbon and water cycling-and thereby evapotranspiration (ET). However, atmospheric demand for water, which is directly related to the atmospheric vapour pressure deficit (VPD), also affects G S and ET. Plants close their stomata to prevent excessive water loss when VPD is high [13][14][15][16] and thus, increases in VPD during periods of hydrologic stress represent an independent constraint on plant carbon uptake and water use in ecosystems.While the plant physiological community has long recognized the critical role of VPD in determining plant functioning, VPD is often overlooked in many fields of hydrologic and climate science. For example, precipitation manipulation experiments are frequently used to draw conclusions about ecosystem response to drought stress, even though VPD is unaffected by precipitation manipulation 10 . Some terrestrial ecosystem and ecohydrological models do not permit stomatal conductance to vary with atmospheric demand 5,11 . Many models designed to capture these impacts rely on empirical parameterizations for soil moisture and VPD stress that promote compensating effects and model equifinality 5 , and/or use relative humidity instead of VPD as the primary driver, with significant consequences for projections of
6 ). The SOC model was fully integrated into a global terrestrial carbon cycle model to run global simulations of elevated CO 2 e ects. Although protected carbon provides an important constraint on priming e ects, priming nonetheless reduced SOC storage in the majority of terrestrial areas, partially counterbalancing SOC gains from enhanced ecosystem productivity.Soils contain more carbon (C) than plant biomass and the atmosphere combined 7 . Although a large body of literature has explored the effects of elevated CO 2 on plant growth 8 , there is considerable uncertainty as to how such changes will affect SOC stocks 5,9 . A large fraction of this uncertainty is due to the complexity of soil processes and structure: an enormous variety of chemical compounds and a diverse community of bacteria and fungi in the soil respond in complex ways to changes in temperature, moisture and inputs of fresh plant C (refs 2,10). Furthermore, recent advances in isotopic, genomic and spectroscopic tools have revealed that a suite of physical, chemical and biological factors control not only SOC decomposition, but also SOC formation and stabilization 4,11 . Current global-scale land surface models represent SOC decay as a first-order process that depends only on abiotic factors such as temperature and moisture 1 , with limited representations of root and microbial influences on SOC. Whereas microbial models have been applied at global scales 12 , rhizosphere processes and microbial influences on SOC stabilization and mineralization have not previously been integrated into global land surface models. Hence, the development of global-scale SOC models that represent essential processes and interactions while remaining tractable for parameterization in Earth system models (ESMs) remains a major challenge.There is now substantial evidence from both empirical and modelling studies that inputs of simple, readily assimilated C compounds such as glucose and amino acids (hereafter referred to as 'simple C') can accelerate the decomposition of complex organic compounds 2 . Such 'priming effects' are likely to have important consequences for global SOC stocks. Rising atmospheric CO 2 concentrations generally increase the inputs of simple C to soils through greater leaf and root production 13 and enhanced root exudation 14 . Such increases have been identified as responsible for accelerated losses of SOC in multiple CO 2 -enrichment experiments 6,9,15,16 , as well as in a broad synthesis of ecosystem responses to elevated CO 2 (ref. 17). The importance of priming is further supported by modelling efforts, as ecosystem models based on first-order decomposition have been unable to explain observed changes in C and N cycling under elevated CO 2 (refs 18,19), and land surface models that include coarse representations of priming have produced more accurate maps of global SOC stocks 20 .Although priming effects are critically important and globally significant, an important constraint on their impact is that plantderived inputs can also lead to the ...
We combined Eddy-covariance measurements with a linear perturbation analysis to isolate the relative contribution of physical and biological drivers on evapotranspiration (ET) in three ecosystems representing two end-members and an intermediate stage of a successional gradient in the southeastern US (SE). The study ecosystems, an abandoned agricultural field [old field (OF)], an early successional planted pine forest (PP), and a late-successional hardwood forest (HW), exhibited differential sensitivity to the wide range of climatic and hydrologic conditions encountered over the 4-year measurement period, which included mild and severe droughts and an ice storm. ET and modeled transpiration differed by as much as 190 and 270 mm yr À1 , respectively, between years for a given ecosystem. Soil water supply, rather than atmospheric demand, was the principal external driver of interannual ET differences. ET at OF was sensitive to climatic variability, and results showed that decreased leaf area index (L) under mild and severe drought conditions reduced growing season (GS) ET (ET GS ) by ca. 80 mm compared with a year with normal precipitation. Under wet conditions, higher intrinsic stomatal conductance (g s ) increased ET GS by 50 mm. ET at PP was generally larger than the other ecosystems and was highly sensitive to climate; a 50 mm decrease in ET GS due to the loss of L from an ice storm equaled the increase in ET from high precipitation during a wet year. In contrast, ET at HW was relatively insensitive to climatic variability. Results suggest that recent management trends toward increasing the land-cover area of PP-type ecosystems in the SE may increase the sensitivity of ET to climatic variability.
The influence of rainstorm on soil respiration of a mixed forest in southern New England, USA was investigated with eddy covariance, rain simulation and laboratory incubation. Soil respiration is shown to respond rapidly and instantaneously to the onset of rain and return to the prerain rate shortly after the rain stops. The pulse-like flux, most likely caused by the decomposition of active carbon compounds in the litter layer, can amount to a loss of 0.18 t C ha À1 to the atmosphere in a single intensive storm, or 5-10% of the annual net ecosystem production of midlatitude forests. If precipitation becomes more variable in a future warmer world, the rain pulse should play an important part in the transient response of the ecosystem carbon balance to climate, particularly for ecosystems on ridge-tops with rapid water drainage.
Orthonormal wavelet transformation (OWT) is a computationally efficient technique for quantifying underlying frequencies in nonstationary and gap-infested time series, such as eddy-covariance-measured net ecosystem exchange of CO2 (NEE). We employed OWT to analyze the frequency characteristics of synchronously measured and modeled NEE at adjacent pine (PP) and hardwood (HW) ecosystems. Wavelet cospectral analysis showed that NEE at PP was more correlated to light and vapor pressure deficit at the daily time scale, and NEE at HW was more correlated to leaf area index (LAI) and temperature, especially soil temperature, at seasonal time scales. Models were required to disentangle the impacts of environmental drivers on the components of NEE, ecosystem carbon assimilation (Ac) and ecosystem respiration (RE). Sensitivity analyses revealed that using air temperature rather than soil temperature in RE models improved the modeled wavelet spectral frequency response on time scales longer than 1 day at both ecosystems. Including LAI improved RE model fit on seasonal time scales at HW, and incorporating parameter variability improved the RE model response at annual time scales at both ecosystems. Resolving variability in canopy conductance, rather than leaf-internal CO2, was more important for modeling Ac at both ecosystems. The PP ecosystem was more sensitive to hydrologic variables that regulate canopy conductance: vapor pressure deficit on weekly time scales and soil moisture on seasonal to interannual time scales. The HW ecosystem was sensitive to water limitation on weekly time scales. A combination of intrinsic drought sensitivity and non-conservative water use at PP was the basis for this response. At both ecosystems, incorporating variability in LAI was required for an accurate spectral representation of modeled NEE. However, nonlinearities imposed by canopy light attenuation were of little importance to spectral fit. The OWT revealed similarities and differences in the scale-wise control of NEE by vegetation with implications for model simplification and improvement.
Forest floor CO 2 efflux (F ff ) depends on vegetation type, climate, and soil physical properties. We assessed the effects of biological factors on F ff by comparing a maturing pine plantation (PP) and a nearby mature Oak-Hickory-type hardwood forest (HW). F ff was measured continuously with soil chambers connected to an IRGA during 2001-2002. At both sites, F ff depended on soil temperature at 5 cm (T 5 ) when soil was moist (soil moisture, h40.20 m 3 m À3 ), and on both T 5 and h when soil was drier. A model (F ff (T 5 , h)) explained X92% of the variation in the daily mean F ff at both sites. Higher radiation reaching the ground during the leafless period, and a thinner litter layer because of faster decomposition, probably caused higher soil temperature at HW compared with PP. The annual F ff was estimated at 1330 and 1464 g C m À2 yr À1 for a year with mild drought (2001) at PP and HW, respectively, and 1231 and 1557 g C m À2 yr À1 for a year with severe drought (2002). In the wetter year, higher soil temperature and moisture at HW compared with PP compensated for the negative effect on F ff of the response to these variables resulting in similar annual F ff at both stands. In the drier year, however, the response to soil temperature and moisture was more similar at the two stands causing the difference in the state variables to impel a higher F ff at HW. A simple mass balance indicated that in the wetter year, C in the litter-soil system was at steady state at HW, and was accruing at PP. However, HW was probably losing C from the mineral soil during the severe drought year of 2002, while PP was accumulating C at a lower rate because of a loss of C from the litter layer. Such contrasting behavior of two forest types in close proximity might frustrate attempts to estimate regional carbon (C) fluxes and net C exchange.
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