David R. Bowling

The application and interpretation of Keeling plots in terrestrial carbon cycle research

[1] Photosynthesis and respiration impart distinct isotopic signatures to the atmosphere that are used to constrain global carbon source/sink estimates and partition ecosystem fluxes. Increasingly, the ‘‘Keeling plot’’ method is being used to determine the carbon isotope composition of ecosystem respiration (d 13 CR) in order to better understand the processes controlling ecosystem isotope discrimination. In this paper we synthesize emergent patterns in d 13 CR by analyzing 146 Keeling plots constructed at 33 sites across North and South America. In order to interpret results from disparate studies, we discuss the assumptions underlying the Keeling plot method and recommend standardized methods for determining d 13 CR. These include the use of regression calculations that account for error in the x variable, and constraining estimates of d 13 CR to nighttime periods. We then recalculate d 13 CR uniformly for all sites. We found a high degree of temporal and spatial variability in C3 ecosystems, with individual observations ranging from � 19.0 to � 32.6%. Mean C3 ecosystem discrimination was 18.3%. Precipitation was a major driver of both temporal and spatial variability of d 13 CR, suggesting (1) a large influence of recently fixed carbon on ecosystem respiration and (2) a significant effect of previous climatic effects on d 13 CR. These results illustrate the importance of water availability as a key control on atmospheric 13 CO2 and highlight the potential of d 13 CR as a useful tool for integrating environmental effects on dynamic canopy and ecosystem processes. INDEX TERMS: 0315 Atmospheric Composition and Structure: Biosphere/atmosphere interactions; 0322 Atmospheric Composition and Structure: Constituent sources and sinks; 1615 Global Change: Biogeochemical processes (4805); 1694 Global Change: Instruments and techniques; 3322 Meteorology and Atmospheric Dynamics: Land/atmosphere interactions; KEYWORDS: carbon cycle, carbon isotopes, ecosystem respiration, carbon dioxide, terrestrial ecosystems

Carbon isotopes in terrestrial ecosystem pools and CO2 fluxes

Stable carbon isotopes are used extensively to examine physiological, ecological, and biogeochemical processes related to ecosystem, regional, and global carbon cycles and provide information at a variety of temporal and spatial scales. Much is known about the processes that regulate the carbon isotopic composition (delta(13)C) of leaf, plant, and ecosystem carbon pools and of photosynthetic and respiratory carbon dioxide (CO(2)) fluxes. In this review, systematic patterns and mechanisms underlying variation in delta(13)C of plant and ecosystem carbon pools and fluxes are described. We examine the hypothesis that the delta(13)C of leaf biomass can be used as a reference point for other carbon pools and fluxes, which differ from the leaf in delta(13)C in a systematic fashion. Plant organs are typically enriched in (13)C relative to leaves, and most ecosystem pools and respiratory fluxes are enriched relative to sun leaves of dominant plants, with the notable exception of root respiration. Analysis of the chemical and isotopic composition of leaves and leaf respiration suggests that growth respiration has the potential to contribute substantially to the observed offset between the delta(13)C values of ecosystem respiration and the bulk leaf. We discuss the implications of systematic variations in delta(13)C of ecosystem pools and CO(2) fluxes for studies of carbon cycling within ecosystems, as well as for studies that use the delta(13)C of atmospheric CO(2) to diagnose changes in the terrestrial biosphere over annual to millennial time scales.

Tunable diode laser absorption spectroscopy for stable isotope studies of ecosystem–atmosphere CO2 exchange

The stable isotope content of atmospheric CO2 provides information about ecosystem carbon–water relations and biosphere– atmosphere carbon exchange. Virtually every isotope study within these fields has required air sample collection at remote locations followed by isotope analysis at a laboratory. This requirement severely limits sampling frequency and experiment duration. In this paper, we evaluate a tunable diode laser absorption spectrometer (TDL) for measuring the carbon isotope content of CO2 at atmospheric mole fractions (350–700mol mol −1 ) and isotopic abundance (δ 13 Co f− 6t o−16‰). Using infrared absorption, the TDL system determines the mole fractions of 12 CO2 and 13 CO2 independently, rather than their ratio as in mass spectrometry (MS). The ability of the instrument to measure isotope ratios (δ 13 C) was tested outdoors in a grassland and compared to standard laboratory-based MS measurements made on field-collected flask samples. The TDL was operated at a sampling flow rate of 230 ml min −1 and a sampling interval of 2 min for two intake heights. There was a consistent offset for δ 13 C of 1.77‰ between the TDL and MS measurements, and the standard deviation of the error (MS− TDL) was 0.35‰ (n = 82). Removal of two outliers improved this standard deviation to 0.25‰ (n = 80). After removing the offset, 62 out of 82 samples had absolute differences less than 0.3‰. Subsequent laboratory experiments indicated that the TDL/MS offset was caused by pressure broadening, and can be avoided in the future by calibrating the TDL with CO2 mixed with air rather than nitrogen. Based on these results we estimate the precision for δ 13 C to be 0.25‰ for our sampling scheme. A similar comparison with flask-based measurements of CO 2 mole fraction ( 12 CO2 + 13 CO2) made with a calibrated infrared gas analyzer indicated a TDL precision of 0.4% (1.6mol mol −1 at 400mol mol −1 ). The TDL was used to investigate the vertical and temporal variation in the carbon isotope content of respired CO2 (δ 13 CR) from the grassland. Measurements of δ 13 Co f CO 2 in air were made during four separate nights at 1 and 60 cm height above ground. δ 13 CR did not vary with height, but it did vary from one night to the next. Hourly measurements of δ 13 CR showed it changed as much as 6.4‰ (−29.1 ± 0. 4t o−22.7 ± 0.8‰) in a single night. Temporal changes in δ 13 CR during the night have not been reported in prior studies. Such observations could provide a new way to investigate temporal dynamics of the carbon substrates utilized for ecosystem respiration.

Seasonal cycle of carbon dioxide and its isotopic composition in an urban atmosphere: Anthropogenic and biogenic effects

ratios of source CO2 showed a seasonal pattern with isotopically depleted values in the wintertime and isotopically enriched values in the spring and summer. The effects of gasoline combustion, natural gas combustion, and biogenic respiration of plants and soils on CO2 mixing ratio were quantified with a mass balance calculation using dual carbon and oxygen isotopic tracers. The calculations showed large contributions of natural gas combustion in the winter and significant nighttime biogenic respiration in the spring and late summer/early fall. The isotope-tracer technique used shows promise for quantifying the impacts of urban processes on the isotopic composition of the atmosphere and partitioning urban CO2 sources into their component parts. INDEX TERMS: 0315 Atmospheric Composition and Structure: Biosphere/atmosphere interactions; 0345 Atmospheric Composition and Structure: Pollution—urban and regional (0305); 1040 Geochemistry: Isotopic composition/chemistry; 1610 Global Change: Atmosphere (0315, 0325); KEYWORDS: CO2 mixing ratio, carbon isotopes, oxygen isotopes, urban pollution, biosphere-atmosphere interactions, Keeling plots

SPATIAL VARIABILITY OF TURBULENT FLUXES IN THE ROUGHNESS SUBLAYER OF AN EVEN-AGED PINE FOREST

The spatial variability of turbulent flow statistics in the roughness sublayer (RSL) of a uniform even-aged 14 m (= h) tall loblolly pine forest was investigated experimentally. Using seven existing walkup towers at this stand, high frequency velocity, temperature, water vapour and carbon dioxide concentrations were measured at 15.5 m above the ground surface from October 6 to 10 in 1997. These seven towers were separated by at least 100m from each other. The objective of this study was to examine whether single tower turbulence statistics measurements represent the flow properties of RSL turbulence above a uniform even-aged managed loblolly pine forest as a best-case scenario for natural forested ecosystems. From the intensive space-time series measurements, it was demonstrated that standard deviations of longitudinal and vertical velocities (σu, σw) and temperature (σT) are more planar homogeneous than their vertical flux of momentum (u*2) and sensible heat (H) counterparts. Also, the measured H is more horizontally homogeneous when compared to fluxes of other scalar entities such as CO2 and water vapour. While the spatial variability in fluxes was significant (>15 %), this unique data set confirmed that single tower measurements represent the ‘canonical’ structure of single-point RSL turbulence statistics, especially flux-variance relationships. Implications to extending the ‘moving-equilibrium’ hypothesis for RSL flows are discussed. The spatial variability in all RSL flow variables was not constant in time and varied strongly with spatially averaged friction velocity u*, especially when u* was small. It is shown that flow properties derived from two-point temporal statistics such as correlation functions are more sensitive to local variability in leaf area density when compared to single point flow statistics. Specifically, that the local relationship between the reciprocal of the vertical velocity integral time scale (Iw) and the arrival frequency of organized structures (ū/h) predicted from a mixing-layer theory exhibited dependence on the local leaf area index. The broader implications of these findings to the measurement and modelling of RSL flows are also discussed.

Dynamics of isotopic exchange of carbon dioxide in a Tennessee deciduous forest

The combination of isotopic measurements and micrometeorological flux measurements is a powerful new approach that will likely lead to new insight into the dynamics of CO 2 exchange between terrestrial ecosystems and the atmosphere. Since the biological processes of photosynthesis and respiration modify the stable isotopic signature of atmospheric CO 2 in different ways, measurements of the net fluxes of CO 2 , 13 CO 2 , and C 18 OO can be used to investigate the relative contribution of each process to net ecosystem CO 2 exchange. We used two independent approaches to measure isotopic fluxes of CO 2 over a Tennessee oak-maple-hickory forest in summer 1998. These approaches involved (1) a combination of standard eddy covariance with intensive flask sampling, and (2) a modification to the relaxed eddy accumulation technique. Strong isotopic signals associated with photosynthesis and respiration were observed and persisted in forest air despite the potential for mixing due to atmospheric turbulence. Calm nights allowed a buildup of respiratory CO 2 below the canopy and were associated with isotopically depleted forest air in the morning. Windy nights were followed by a relatively more enriched early-morning isotopic signal. Entrainment of air from above the decaying nocturnal boundary layer during daytime mixed layer growth exerted strong control on isotopic composition of forest air, resulting in similar isotope ratios in the late afternoon despite different isotopic starting points following calm or windy nights. The influences of the convective boundary layer and turbulent mixing within the forest cannot be ignored when using isotopes of CO 2 to investigate biological processes.

Response of the carbon isotopic content of ecosystem, leaf, and soil respiration to meteorological and physiological driving factors in a Pinus ponderosa ecosystem

applications of isotope-based models of the global carbon budget as well as for understanding ecosystem-level variation in isotopic discrimination (D). Discrimination may be strongly dependent on synoptic-scale variation in environmental drivers that control canopy-scale stomatal conductance (Gc) and photosynthesis, such as atmospheric vapor pressure deficit (vpd) photosynthetically active radiation (PAR) and air temperature (Tair). These potential relationships are complicated, however, due to time lags between the period of carbon assimilation and ecosystem respiration, which may extend up to several days, and may vary with tissue (i.e., leaves versus belowground tissues). Our objective was to determine if relationships exist over a short-term period (2 weeks) between meteorological and physiological driving factors and d 13 CR and its components, soil-respired d 13 C( d 13 CR-soil) and foliage-respired d 13 C( d 13 CR-foliage). We tested for these hypothesized relationships in a 250-year-old ponderosa pine forest in central Oregon, United States. A cold front passed through the region 3 days prior to our first sample night, resulting in precipitation (total rainfall 14.6 mm), low vpd (minimum daylight average of 0.36 kPa) and near-freeze temperature (minimum air temperature of 0.18� C± 0.3� C), followed by a warming trend with relatively high vpd (maximum daylight average of 3.19 kPa). Over this 2-week period Gc was negatively correlated with vpd (P < 0.01) while net ecosystem CO2 exchange (NEE) was positively correlated with vpd (P < 0.01), consistent with a vpd limitation to conductance and net CO2 uptake. Consistent with a stomatal influence over D, a negative correlation was observed between d 13 CR and Gc measured 2 days prior (i.e., a 2-day time lag, P = 0.04); however, d 13 CR was not correlated with other measured variables. Also consistent with a stomatal influence over discrimination, d 13 CR-soil was negatively correlated with Gc (P < 0.01) and positively correlated with vpd and PAR measured one to 3 days prior (P = 0.01 and 0.04, respectively). In contrast, d 13 CR-foliage was not correlated with vpd or Gc, but was negatively correlated with minimum air temperature measured 5 days previously (P < 0.01) supporting the idea that cold air temperatures cause isotopic enrichment of respired CO2. The significant driving parameters differed for d 13 CR-foliage and d 13 CR-soil potentially due to different controls over the isotopic content of tissue-specific respiratory fluxes, such as differing carbon transport times from the site of assimilation to the respiring tissue or different reliance on recent versus old photosynthate. Consistent with Gc control over photosynthesis and D, both d 13 CR-soil and d 13 CR-foliage became enriched as net CO2 uptake decreased (more positive NEE, P < 0.01 for both). The d 13 C value of Pinus ponderosa foliage (� 27.1%, whole-tissue) was 0.5 to 3.0% more negative than any observed respiratory signature, supporting the contention that foliage d 13 C can be a poor proxy for the isotopic content of respiratory fluxes. The strong meteorological controls

The use of relaxed eddy accumulation to measure biosphere-atmosphere exchange of isoprene and other biological trace gases

Abstract The micrometeorological flux measurement technique known as relaxed eddy accumulation (REA) holds promise as a powerful new tool for ecologists. The more popular eddy covariance (eddy correlation) technique requires the use of sensors that can respond at fast rates (10 Hz), and these are unavailable for many ecologically relevant compounds. In contrast, the use of REA allows flux measurement with sensors that have much slower response time, such as gas chromatography and mass spectrometry. In this review, relevant micrometeorological details underlying REA are presented, and critical analytical and system design details are discussed, with the goal of introducing the technique and its potential applications to ecologists. The validity of REA for measuring fluxes of isoprene, a photochemically reactive hydrocarbon emitted by several plant species, was tested with measurements over an oak-hickory forest in the Walker Branch Watershed in eastern Tennessee. Concurrent eddy covariance measurements of isoprene flux were made using a newly available chemiluminesence instrument. Excellent agreement was obtained between the two techniques (r2 = 0.974, n = 62), providing the first direct comparison between REA and eddy covariance for measuring the flux rate of a reactive compound. The influence of a bias in vertical wind velocity on the accuracy of REA was examined. This bias has been thought to be a source of significant error in the past. Measurements of normalized bias () alone would lead us to think that a large potential error exists at this site. However, with our isoprene data and through simulations of REA with fast-response H2O and CO2 data, we conclude that accurate REA flux measurements can be made even in the presence of a bias in w.

Persistent wind-induced enhancement of diffusive CO2 transport in a mountain forest snowpack

mountain forest seasonal snowpack. Observations of 12 CO2 and 13 CO2 within the snowpack, soil, and air of a subalpine forest were made over three winters in the Rocky Mountains, USA. These molecules differ in their rates of diffusion, providing a means to quantify the relative importance of diffusion and advection. An empirical model was developed to describe the transport of these gases through the snowpack, assuming that isotopic variability was caused solely by wind. We found that advection was a persistent phenomenon within the snowpack. Under calm conditions, isotopic patterns followed those associated with diffusion. In the presence of wind, the 4.4‰ isotopic effect of diffusion was diminished, and transport was enhanced beyond the diffusive rate for a given mole fraction gradient. Pressure pumping in our forest snowpack enhanced transport of CO2 beyond molecular diffusion by up to 40% in the short term (hours) but by at most 8%–11% when integrated over a winter. These results should be applicable to trace gas transport in a variety of biogeochemical applications.

Critical evaluation of micrometeorological methods for measuring ecosystem-atmosphere isotopic exchange of CO2

Isotopic net ecosystem exchange (isofluxes, or flux densities of 13 CO2) can be combined with standard eddy covariance methods to partition net ecosystem exchange of carbon dioxide (F) into its component one-way fluxes, photosynthesis and respiration. At present, the approaches used to estimate isotopic fluxes are labor-intensive and dependent on several assumptions. To assess the relative utility of the available methods, we studied an ecosystem associated with large CO 2 fluxes and maximal isotopic exchange. Three independent techniques were used to measure isotopic flux densities over an irrigated alfalfa field: (1) a combination of standard eddy covariance and flask sampling; (2) the flux-gradient method; and (3) hyperbolic relaxed eddy accumulation (HREA). Consistent isotopic flux results were obtained via the three methods, with similar diurnal patterns and peak midday isotopic flux densities of 600–700 mol m −2 s −1 ‰. Air samples were collected over a wide range of CO2 mole fractions (325.3–597.5mol mol −1 ) and isotopic composition (−5.9 to −15.4‰). The relationship between isotopic composition (δ 13 C) and CO2 mole fraction was consistent among types of samples, except for HREA samples during the morning boundary layer transition. Total ecosystem respiration was estimated based on a regression against soil temperature, and the flux and isotopic flux measurements were used to examine whole-canopy photosynthetic discrimination (∆canopy) and the isotopic composition of the photosynthetic flux. ∆canopy weighted by net ecosystem exchange was 17.9‰. The isotopic content of total ecosystem respiration, soil respiration, and foliar respiration, and δ 13 C of various organic components (leaves, roots, soil organic matter) were examined and evaluated relative to ∆canopy. The δ 13 C of organic components does not appear to be a good predictor of δ 13 C of ecosystem CO2 fluxes.