EcoCELL Research Publications

Verburg, P.S.J., D.W. Johnson, D.E. Schorran, L.L. Wallace, Y. Luo, J.A. Arnone III. In press. Impacts of an anomalously warm year on nutrient availability in experimentally manipulated tallgrass prairie ecosystems. Global Change Biology.

Arnone III, J.A., P.S.J. Verburg, D.W. Johnson, J.D. Larsen, R.L. Jasoni, A.J. Farnady, C.M. Batts, C. von Nagy, W.G. Coulombe, D.E. Schorran, P.E. Buck, B.H. Braswell, J.S. Coleman, R.A. Sherry, L.L. Wallace, Y. Luo, D.S. Schimel. 2008. Prolonged suppression of ecosystem carbon dioxide uptake after an anomalously warm year. Nature. 455:383-386.

Abstract: Terrestrial ecosystems control carbon dioxide fluxes to and from the atmosphere through photosynthesis and respiration, a balance between net primary productivity and heterotrophic respiration, that determines whether an ecosystem is sequestering carbon or releasing it to the atmosphere. Global and site-specific data sets have demonstrated that climate and climate variability influence biogeochemical processes that determine net ecosystem carbon dioxide exchange (NEE) at multiple timescales. Experimental data necessary to quantify impacts of a single climate variable, such as temperature anomalies, on NEE and carbon sequestration of ecosystems at interannual timescales have been lacking. This derives from an inability of field studies to avoid the confounding effects of natural intra-annual and interannual variability in temperature and precipitation. Here we present results from a four-year study using replicate 12,000-kg intact tallgrass prairie monoliths located in four 184-m3 enclosed lysimeters. We exposed 6 of 12 monoliths to an anomalously warm year in the second year of the study and continuously quantified rates of ecosystem processes, including NEE. We find that warming decreases NEE in both the extreme year and the following year by inducing drought that suppresses net primary productivity in the extreme year and by stimulating heterotrophic respiration of soil biota in the subsequent year. Our data indicate that two years are required for NEE in the previously warmed experimental ecosystems to recover to levels measured in the control ecosystems. This time lag caused net ecosystem carbon sequestration in previously warmed ecosystems to be decreased threefold over the study period, compared with control ecosystems. Our findings suggest that more frequent anomalously warm years, a possible consequence of increasing anthropogenic carbon dioxide levels, may lead to a sustained decrease in carbon dioxide uptake by terrestrial ecosystems.

Stamenkovic, J., M.S. Gustin, J.A. Arnone, D.W. Johnson, J.D. Larsen, P.S.J. Verburg. 2008. Atmospheric mercury exchange with tallgrass prairie ecosystem housed in mesocosms. Science of the Total Environment. 406:227-238.

Abstract: This study focused on characterizing air–surface mercury Hg exchange for individual surfaces (soil, litter-covered soil and plant shoots) and ecosystem-level flux associated with tallgrass prairie ecosystems housed inside large mesocosms over three years. The major objectives of this project were to determine if individual surface fluxes could be combined to predict ecosystem-level exchange and if this low-Hg containing ecosystem was a net source or sink for atmospheric Hg. Data collected in the field were used to validate fluxes obtained in the mesocosm setting. Because of the controlled experimental design and ease of access to the mesocosms, data collected allowed for assessment of factors controlling flux and comparison of models developed for soil Hg flux versus environmental conditions at different temporal resolution (hourly, daily and monthly). Evaluation of hourly data showed that relationships between soil Hg flux and environmental conditions changed over time, and that there were interactions between parameters controlling exchange. Data analyses demonstrated that to estimate soil flux over broad temporal scales (e.g. annual flux) coarse-resolution data (monthly averages) are needed. Plant foliage was a sink for atmospheric Hg with uptake influenced by plant functional type and age. Individual system component fluxes (bare soil and plant) could not be directly combined to predict the measured whole system flux (soil, litter and plant). Emissions of Hg from vegetated and litter-covered soil were lower than fluxes from adjacent bare soil and the difference between the two was seasonally dependent and greatest when canopy coverage was greatest. Thus, an index of plant canopy development (canopy greenness) was used to model Hg flux from vegetated soil. Accounting for ecosystem Hg inputs (precipitation, direct plant uptake of atmospheric Hg) and modeled net exchange between litter-and-plant covered soils, the tallgrass prairie was found to be a net annual sink of atmospheric Hg.

Obrist, D., M.S. Gustin, J.A. Arnone III, D.W. Johnson, D.E. Schorran, P.S.J. Verburg. 2005. Measurements of gaseous elemental mercury fluxes over intact tallgrass prairie monoliths during one full year. Atmospheric Environment. 39:957-965.

Abstract: The atmosphere is an important pathway by which mercury is transported and distributed to pristine ecosystems. The significance of anthropogenic versus natural mercury contributions to the atmosphere is controversial, and the importance of re-emission of deposited mercury from ecosystems is not known. Here we present a continuous year-long data set of gaseous elemental mercury exchange between intact soil–plant monoliths of tallgrass prairie and the atmosphere. Mercury fluxes were measured using large open-flow gas exchange chambers (7.3×5.5×4.5 m3, L×W×D). Approximately 60 μg m-2 of elemental gaseous mercury was lost from four replicate grassland ecosystems (9 m2 surface area each) to the atmosphere over the course of 1 yr. Deposition was an important flux in the winter and emissions were dominant in spring, summer, and fall. Solar radiation and air temperature were most strongly correlated with mercury emissions. Gaseous elemental mercury losses to the atmosphere exceeded other measured fluxes of mercury in and out of the grassland ecosystems. These results indicate that mercury emissions from uncontaminated terrestrial ecosystems to the atmosphere may be a significant source of atmospheric mercury. We hypothesize that most of the mercury being emitted is previously deposited mercury and that re-emissions of mercury from terrestrial ecosystems is an important process whereby mercury is continually cycled between the air and terrestrial ecosystems.

Verburg, P.S.J., J. Larsen, D.W. Johnson, D.E. Schorran, J.A. Arnone III. 2005. Impacts of an anomalously warm year on soil CO2 fluxes in experimentally manipulated tallgrass prairie ecosystems. Global Change Biology. 11:1720-1732.

Abstract: Modeling analyses suggest that an increase in growth rate of atmospheric CO2 concentrations during an anomalously warm year may be caused by a decrease in net ecosystem production (NEP) in response to increased heterotrophic respiration (Rh). To test this hypothesis, 12 intact soil monoliths were excavated from a tallgrass prairie site near Purcell, Oklahoma, USA and divided among four large dynamic flux chambers (Ecologically Controlled Enclosed Lysimeter Laboratories (EcoCELLs)). During the first year, all four EcoCELLs were subjected to Oklahoma air temperatures. During the second year, air temperature in two EcoCELLs was increased by 4°C throughout the year to simulate anomalously warm conditions. This paper reports on the effect of warming on soil CO2 efflux, representing the sum of autotrophic respiration (Ra) and Rh.

During the pretreatment year, weekly average soil CO2 efflux was similar in all EcoCELLs. During the late spring, summer and early fall of the treatment year, however, soil CO2 efflux was significantly lower in the warmed EcoCELLs. In general, soil CO2 efflux was correlated with soil temperature and to a lesser extent with moisture. A combined temperature and moisture regression explained 64% of the observed variation in soil CO2 efflux. Soil CO2 efflux correlated well with a net primary production (NPP) weighted greenness index derived from digital photographs. Although separate relationships for control and warmed EcoCELLs showed better correlations, one single relationship explained close to 70% of the variation in soil CO2 efflux across treatments and years. A strong correlation between soil CO2 efflux and canopy development and the lack of initial response to warming indicate that soil CO2 efflux is dominated by Ra. This study showed that a decrease in soil CO2 efflux in response to a warm year was most likely dominated by a decrease in Ra instead of an increase in Rh.

Obrist, D., M.S. Gustin, J.A. Arnone III, D.E. Schorran, P.S.J. Verburg, D.W. Johnson. 2004. Large annual Hg emissions over tallgrass prairie grasslands indicate vegetated terrestrial ecosystems to be sources of Hg to the atmosphere. RMZ- Materials and Geoenvironment. 51.3:1688-1690.

Verburg, P.S.J., J.A Arnone III, D. Obrist, R.D. Evans, D. LeRoux-Swarthout, D.W. Johnson, D.E. Schorran,Y. Luo, J.S. Coleman. 2004. Net ecosystem C exchange in two experimental grassland ecosystems. Global Change Biology. 10:498-508.

Abstract: Increases in net primary production (NPP) may not necessarily result in increased C sequestration since an increase in uptake can be negated by concurrent increases in ecosystem C losses via respiratory processes. Continuous measurements of net ecosystem C exchange between the atmosphere and two experimental cheatgrass (Bromus tectorum L.) ecosystems in large dynamic flux chambers (EcoCELLs) showed net ecosystem C losses to the atmosphere in excess of 300 g C m-2 over two growing cycles. Even a doubling of net ecosystem production (NEP) after N fertilization in the second growing season did not compensate for soil C losses incurred during the fallow period. Fertilization not only increased C uptake in biomass but also enhanced C losses through soil respiration from 287 to 469 g C m-2 , mainly through an increase in rhizosphere respiration. Fertilization decreased dissolved inorganic C losses through leaching of from 45 to 10 g C m-2 .

Unfertilized cheatgrass added 215 g C m-2 as root-derived organic matter but the contribution of these inputs to long-term C sequestration was limited as these deposits rapidly decomposed. Fertilization increased NEP but did not increase belowground C inputs most likely due to a concurrent increase in the production and decomposition of rhizodeposits. Decomposition of soil organic matter (SOM) was reduced by fertilizer additions. The results from our study show that, although annual grassland ecosystems can add considerable amounts of C to soils during the growing season, it is unlikely that they sequester large amounts of C because of high respiratory losses during dormancy periods. Although fertilization could increase NEP, fertilization might reduce soil C inputs as heterotrophic organisms favor root-derived organic matter over native SOM.

Large annual Hg emissions over tallgrass prairie grasslands indicate vegetated terrestrial ecosystems to be sources of Hg to the atmosphere. RMZ- Materials and Geoenvironment. Large annual Hg emissions over tallgrass prairie grasslands indicate vegetated terrestrial ecosystems to be sources of Hg to the atmosphere. RMZ- Materials and Geoenvironment.

Obrist, D., P.S.J. Verburg, M.H. Young, J.S. Coleman, D.E. Schorran, J.A. Arnone III. 2003. Quantifying effects of phenology on ecosystem evapotranspiration in planted grassland mesocosms using EcoCELL technology. Agricultural and Forest Meteorology. 118:173-183.

Abstract: Use of plant phenological variables in models predicting evapotranspiration (ET) has largely relied on relatively simple (e.g., linear) relationships which may not be sufficiently accurate to predict small—yet ecologically significant—changes in plant phenology that are expected to occur in response to global climate change. A dearth of experimental data reflects the difficulties in quantifying these relationships against the background of large environmental variability that occurs in the field. Our main objective was to quantify how plant phenology (leaf area index [LAI] and root length density [RLD]) affect ET and its components during an entire vegetation cycle in large-scale model grassland (Bromus tectorum) ecosystems using the Ecologically Controlled Enclosed Lysimeter Laboratory (EcoCELL)—a unique open flow and mass balance laboratory. We also aimed to compare the three methods employed by the EcoCELL laboratory to measure ecosystem ET (whole-ecosystem gas exchange, weighing lysimetry, and weighing lysimetry combined with time domain reflectometry [TDR]) in order to independently confirm the performance of the unique gas exchange technology. Cumulative ET during the 190 days of the experiment measured with the three different methods compared very well with each other (mean errors <1%). We found that ET reached maximum levels at relatively low LAI (2–3), but as LAI increased beyond this value, small increase in transpiration were more than offset by decreases in soil evaporation, thereby causing declines in ET. A combined rectangular hyperbola (effects on transpiration) and linear (effects on soil evaporation) function between LAI and ET accounted for almost 90% of all variability in measured daily ET. RLD showed relationships to ET similar to those observed for LAI due to high covariance between RLD and LAI, but root length densities did not explain any additional variability in daily ET beyond that explained by LAI under the well-watered conditions of the experiment. Taken together, our results show that: (i) the EcoCELL mesocosm laboratory can precisely and accurately quantify hydrologic processes of large soil–plant monoliths under controlled environmental conditions; (ii) plant canopy phenological changes affect ecosystem ET, and the contribution of transpiration, in non-linear ways; (iii) these non-linear responses must be accounted for when assessing the consequences of changes in plant phenology—e.g., due to global environmental change—on ecosystem hydrology.

Hui D., Luo Y., Cheng W., Coleman J.S., Johnson D.W., and Sims D.A.. (2001). Canopy radiation- and water-use efficiencies as effected by elevated [CO2]. Global Change Biology 7(1): 75-92.

Abstract: This study used an environmentally controlled plant growth facility EcoCELLs to directly measure canopy gas exchanges and to examine the effects of elevated [CO2] on canopy radiation and water use efficiencies. Sunflowers (Helianthus annuus var. Mammoth) were grown at ambient (399 µmol mol-1) and elevated [CO2] (746 µmol mol-1) for 53 days in EcoCELLs. Whole canopy carbon and water fluxes were continuously measured during the period of the experiment. The results indicated that elevated [CO2] enhanced daily total canopy carbon and water fluxes by 53% and 11%, respectively, on the ground area basis, resulting in a 54% increase in radiation use efficiency (RUE) based on intercepted photosynthetic active radiation and a 26% increase in water use efficiency (WUE) by the end of the experiment. Canopy carbon and water fluxes at both CO2 treatments varied with canopy development. They were small at 22 days after planting (DAP) and gradually increased to the maxima at 46 DAP. When canopy carbon and water fluxes were expressed on the leaf area basis, no effect of CO2 was found for canopy water flux while elevated [CO2] still enhanced canopy carbon flux by 29%, on average. Nighttime canopy carbon flux was 32% higher at elevated than at ambient [CO2]. In addition, RUE and WUE displayed strong diurnal variations, high at noon and low in the morning or afternoon for WUE but opposite for RUE. This study provided direct evidence that plant canopy may consume more, instead of less, water but utilize water and radiation more efficiently at elevated than at ambient [CO2], at least during the exponential growth period as illustrated in this experiment.

Cheng W., Sims D.A., Luo Y., Coleman J.S., and Johnson D.W. (2000). Photosynthesis, respiration, and net primary production of sunflower stands in ambient and elevated atmospheric CO2 concentrations: An invariant NPP:GPP ratio? Global Change Biology 6(8): 931-941.

Abstract: The effect of elevated CO2 on photosynthesis, respiration, and growth efficiency of sunflower plants at the whole-stand level was investigated using a whole-system gas exchange facility (the EcoCELLs at the Desert Research Institute) and a 13C natural tracer method. Total daily photosynthesis (GPP), net primary production (NPP), and respiration under the elevated CO2 treatment were consistently higher than under the ambient CO2 treatment. The overall level of enhancement due to elevated CO2 was consistent with published results for a typical C3 plant species. The patterns of daily GPP and NPP through time approximated logistic curves under both CO2 treatments. Regression analysis indicated that both the rate of increase (the parameter "r") and the maximum value (the parameter "k") of daily GPP and NPP under the elevated CO2 treatment were significantly higher than under the ambient CO2 treatment. Percent increase in daily GPP due to elevated CO2 varied systematically through time according to logistic equations of the two treatments. The GPP increase due to elevated CO2 ranged from approximately 10% initially to 73% at the peak while declining to about 33%, as predicted by the ratio of the two maximum values. Different values of percent increase in GPP and NPP were obtained at different sampling times. This result demonstrated that one-time measurements of percent increases due to elevated CO2 could be misleading, thereby making interpretation difficult. Although rhizosphere respiration was substantially enhanced by elevated CO2, no effect of elevated CO2 on R:P (respiration:photosynthesis) was found, suggesting an invariant NPP:GPP ratio during the entire experiment. Further validation of the notion of an invariant NPP:GPP ratio may significantly simplify the process of quantifying terrestrial carbon sequestration by directly relating total photosynthesis to net primary production.

Cheng W., Sims D.A., Luo Y., Johnson D.W., Ball J.T., and Coleman J.S. (2000). Carbon budgeting in plant-soil mesocosms under elevated CO2: locally missing carbon? Global Change Biology 6: 99-109.

Abstract: Studies have suggested that more carbon is fixed due to a large increase in photosynthesis in plant-soil systems exposed to elevated CO2 than could subsequently be found in plant biomass and soils -- the locally missing carbon phenomenon. To further understand this phenomenon, an experiment was carried out using EcoCELLs which are open-flow, mass-balance systems at the mesocosm scale. Naturally occurring 13C tracers were also used to separately measure plant-derived carbon and soil-derived carbon. The experiment included two EcoCELLs, one under ambient atmospheric CO2 and the other under elevated CO2 (ambient plus 350 µL L-1). By matching carbon fluxes with carbon pools, the issue of locally missing carbon was investigated. Flux-based net primary production (NPPf) was similar to pool-based primary production (NPPp) under ambient CO2, and the discrepancy between the two carbon budgets (12gC m-2, or 4% of NPPf) was less than measurement errors. Therefore, virtually all carbon entering the system under ambient CO2 was accounted for at the end of the experiment. Under elevated CO2, however, the amount of NPPf was much higher than NPPp, resulting in missing carbon of approximately 80g C m-2, or 19% of NPPf which was much higher than measurement errors. This was additional to the 96% increase in rhizosphere respiration and the 50% increase in root growth, two important components of locally missing carbon. The mystery of locally missing carbon under elevated CO2 remains to be further investigated. Volatile organic carbon, carbon loss due to root washing, and measurement errors are discussed as some of the potential contributing factors.

Sims D.A., Cheng W., Luo Y., and Seemann J.R. (2000). Photosynthetic acclimation to elevated CO2 in a sunflower canopy. Journal of Experimental Botany 50: 645-653.Photosynthetic acclimation to elevated CO2 in a sunflower canopy

Abstract: Sunflower canopies were grown in mesocosom gas exchange chambers at ambient and elevated CO2 concentrations (360 and 700 ppm) and leaf photosynthetic capacities measured at several depths within each canopy. Elevated [CO2] had little effect on whole-canopy photosynthetic capacity and total leaf area, but had marked effects on the distribution of photosynthetic capacity and leaf area within the canopy. Elevated [CO2] did not significantly reduce the photosynthetic capacities per unit leaf area of young leaves at the top of the canopy, but it did reduce the photosynthetic capacities of older leaves by as much as 40%. This effect was not dependent on the canopy light environment since elevated [CO2] also reduced the photosynthetic capacities of older leaves exposed to full sun on the south edge of the canopy. In addition to the effects on leaf photosynthetic capacity, elevated [CO2] shifted the distribution of leaf area within the canopy so that more leaf area was concentrated near the top of the canopy. This change resulted in as much as a 50% reduction in photon flux density in the upper portions of the elevated [CO2] canopy relative to the ambient [CO2] canopy, even though there was no significant difference in the total canopy leaf area. This reduction in PFD appeared to account for leaf carbohydrate contents that were actually lower for many of the shaded leaves in the elevated as opposed to the ambient [CO2] canopy. Photosynthetic capacities were not significantly correlated with any of the individual leaf carbohydrate contents. However, there was a strong negative correlation between photosynthetic capacity and the ratio of hexose sugars to sucrose, consistent with the hypothesis that sucrose cycling is a component of the biochemical signalling pathway controlling photosynthetic acclimation to elevated [CO2

].

Luo Y., Hui D., Cheng W., Coleman J.S., Johnson D.W., and Sims D.A. (1999). Canopy quantum yield in a mesocosm study. Agricultural and Forest Meteorology 100: 35-48.Canopy quantum yield in a mesocosm study.

Abstract: Due to past limitations in experimental technology, canopy function has generally been inferred from leaf properties through scaling and/or indirect measurements. The development of a facility (EcoCELLs) at the Desert Research Institute has now made it possible to directly measure canopy gas exchange. In this experiment, sunflowers (Helianthus annuus) were planted in the EcoCELLs and grown under ambient (399 µmol mol -1 ) and elevated (746 µmol mol -1 ) CO2 concentrations. We continuously measured carbon flux during canopy development from which canopy quantum yield (øC) was estimated. The results indicated that the total daily carbon flux was similar between elevated and ambient C2 treatments in the early stage of canopy development. After the canopy closed, carbon flux under elevated CO2 averaged 53% higher than that under ambient CO2 . Assimilation/incident irradiance (A/I) curves of leaves at different canopy positions were used to estimate leaf quantum yields (øC), and A/I curves of canopies at late development stages were used to estimate øC. Elevated CO2 enhanced øC by 24%. There was little difference in øC at different canopy positions, averaging 0.0542 at ambient CO2 and 0.0671 at elevated CO2 . Canopy quantum yield (øC) was higher by 32% at elevated than ambient CO2. It increased with canopy development and was strongly correlated with leaf area index (LAI) by øC = 0.0094 LAI/(0.0829 + 0.1137 LAI) at ambient CO2 and øC = 0.01382 LAI/(0.1129 + 0.1224 LAI) at elevated CO2 . In addition, the curvilinear relationship between radiation and canopy carbon fluxes suggests that canopy radiation use efficiency (CRUE) varied with radiation availability. The variability inøC and CRUE with canopy development and light levels warrants further research on the notion drawn from earlier work that CRUE in non-stressed conditions is relatively constant.

Griffin K.L., Ross P.D., Sims D.A., Luo Y., Seemann J.R., Fox C.A., and Ball J.T. (1996). EcoCELLs: tools for mesocosm scale measurements of gas exchange. Plant, Cell and Environment 19: 1210-1221. EcoCELLs: tools for mesocosm scale measurements of gas exchange

Abstract: We describe the use of a unique plant growth facility, which has as its centerpiece four "EcoCELLs", or 5x7 m mesocosms designed as open-flow, mass-balance systems for the measurement of carbon, water and trace gas fluxes. This system is unique in that it was conceived specifically to bridge the gap between measurement scales during long-term experiments examining the function and development of model ecosystems. There are several advantages to using EcoCELLs, including (i) the same theory of operation as leaf level gas exchange systems, but with continuous operation at a much larger scale; (ii) the ability to independently evaluate canopy-level and ecosystem models; (iii) simultaneous manipulation of environmental factors and measurement of system-level responses; and (iv) maximum access to, and manipulation of, a large rooting volume.

In addition to discussing the theory, construction and relative merits of EcoCELLs, we describe the calibration and use of the EcoCELLs during a "proof of concept" experiment. This experiment involved growing soybeans under two ambient CO2 concentrations (~360 and 710 µmol mol-1). During this experiment, we asked "How accurate is the simplest model that can be used to scale from leaf-level to canopy-level responses?" in order to illustrate the utility of the EcoCELLs in validating canopy-scale models.

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