A unifying conceptual model for the environmental responses of isoprene emissions from plants

Background and Aims

Isoprene is the most important volatile organic compound emitted by land plants in terms of abundance and environmental effects. Controls on isoprene emission rates include light, temperature, water supply and CO₂ concentration. A need to quantify these controls has long been recognized. There are already models that give realistic results, but they are complex, highly empirical and require separate responses to different drivers. This study sets out to find a simpler, unifying principle.

Methods

A simple model is presented based on the idea of balancing demands for reducing power (derived from photosynthetic electron transport) in primary metabolism versus the secondary pathway that leads to the synthesis of isoprene. This model''s ability to account for key features in a variety of experimental data sets is assessed.

Key results

The model simultaneously predicts the fundamental responses observed in short-term experiments, namely: (1) the decoupling between carbon assimilation and isoprene emission; (2) a continued increase in isoprene emission with photosynthetically active radiation (PAR) at high PAR, after carbon assimilation has saturated; (3) a maximum of isoprene emission at low internal CO₂ concentration (c_i) and an asymptotic decline thereafter with increasing c_i; (4) maintenance of high isoprene emissions when carbon assimilation is restricted by drought; and (5) a temperature optimum higher than that of photosynthesis, but lower than that of isoprene synthase activity.

Conclusions

A simple model was used to test the hypothesis that reducing power available to the synthesis pathway for isoprene varies according to the extent to which the needs of carbon assimilation are satisfied. Despite its simplicity the model explains much in terms of the observed response of isoprene to external drivers as well as the observed decoupling between carbon assimilation and isoprene emission. The concept has the potential to improve global-scale modelling of vegetation isoprene emission.     

Carbonyl sulfide (COS) as a tracer for canopy photosynthesis, transpiration and stomatal conductance: potential and limitations

The theoretical basis for the link between the leaf exchange of carbonyl sulfide (COS), carbon dioxide (CO(2)) and water vapour (H(2)O) and the assumptions that need to be made in order to use COS as a tracer for canopy net photosynthesis, transpiration and stomatal conductance, are reviewed. The ratios of COS to CO(2) and H(2)O deposition velocities used to this end are shown to vary with the ratio of the internal to ambient CO(2) and H(2)O mole fractions and the relative limitations by boundary layer, stomatal and internal conductance for COS. It is suggested that these deposition velocity ratios exhibit considerable variability, a finding that challenges current parameterizations, which treat these as vegetation-specific constants. COS is shown to represent a better tracer for CO(2) than H(2)O. Using COS as a tracer for stomatal conductance is hampered by our present poor understanding of the leaf internal conductance to COS. Estimating canopy level CO(2) and H(2)O fluxes requires disentangling leaf COS exchange from other ecosystem sources/sinks of COS. We conclude that future priorities for COS research should be to improve the quantitative understanding of the variability in the ratios of COS to CO(2) and H(2)O deposition velocities and the controlling factors, and to develop operational methods for disentangling ecosystem COS exchange into contributions by leaves and other sources/sinks. To this end, integrated studies, which concurrently quantify the ecosystem-scale CO(2), H(2)O and COS exchange and the corresponding component fluxes, are urgently needed.     

A dynamic leaf gas‐exchange strategy is conserved in woody plants under changing ambient CO2: evidence from carbon isotope discrimination in paleo and CO2 enrichment studies

Rising atmospheric [CO₂], c_a, is expected to affect stomatal regulation of leaf gas‐exchange of woody plants, thus influencing energy fluxes as well as carbon (C), water, and nutrient cycling of forests. Researchers have proposed various strategies for stomatal regulation of leaf gas‐exchange that include maintaining a constant leaf internal [CO₂], c_i, a constant drawdown in CO₂ (c_a ? c_i), and a constant c_i/c_a. These strategies can result in drastically different consequences for leaf gas‐exchange. The accuracy of Earth systems models depends in part on assumptions about generalizable patterns in leaf gas‐exchange responses to varying c_a. The concept of optimal stomatal behavior, exemplified by woody plants shifting along a continuum of these strategies, provides a unifying framework for understanding leaf gas‐exchange responses to c_a. To assess leaf gas‐exchange regulation strategies, we analyzed patterns in c_i inferred from studies reporting C stable isotope ratios (δ¹³C) or photosynthetic discrimination (?) in woody angiosperms and gymnosperms that grew across a range of c_a spanning at least 100 ppm. Our results suggest that much of the c_a‐induced changes in c_i/c_a occurred across c_a spanning 200 to 400 ppm. These patterns imply that c_a ? c_i will eventually approach a constant level at high c_a because assimilation rates will reach a maximum and stomatal conductance of each species should be constrained to some minimum level. These analyses are not consistent with canalization toward any single strategy, particularly maintaining a constant c_i. Rather, the results are consistent with the existence of a broadly conserved pattern of stomatal optimization in woody angiosperms and gymnosperms. This results in trees being profligate water users at low c_a, when additional water loss is small for each unit of C gain, and increasingly water‐conservative at high c_a, when photosystems are saturated and water loss is large for each unit C gain.     

Overcoming drought-induced decreases in soybean leaf photosynthesis by measuring with CO2-enriched air

Soybean [Glycine max (L.) Merr. cv. Williams 82 and A3127] plants were grown in the field under long-term soil moisture deficit and irrigation to determine the effects of severe drought stress on the photosynthetic capacity of soybean leaves. Afternoon leaf water potentials, stomatal conductances, intercellular CO₂ concentrations and CO₂-assimilation rates for the two soil moisture treatments were compared during the pod elongation and seed enlargement stages of crop development. Leaf CO₂-assimilation rates were measured with either ambient (340 l CO₂ l^–1) or CO₂-enriched (1800 l CO₂ l^–1) air. Although seed yield and leaf area per plant were decreased an average of 48 and 31%, respectively, as a result of drought stress, leaf water potentials were reduced only an average of 0.27 MPa during the sampling period. Afternoon leaf CO₂-assimilation rates measured with ambient air were decreased an average of 56 and 49% by soil moisture deficit for Williams 82 and A3127, respectively. The reductions in leaf photosynthesis of both cultivars were associated with similar decreases in leaf stomatal conductance and with small increases in leaf intercellular CO₂ concentration. When the CO₂-enriched air was used, similar afternoon leaf CO₂-assimilation rates were found between the soil moisture treatments at each stage of crop development. These results suggest that photosynthetic capacity of soybean leaves is not reduced by severe soil moisture deficit when a stress develops gradually under field conditions.Abbreviations C_i intercellular CO₂ concentrations - A_a rates of CO₂ assimilation measured with ambient air - A_e rates of CO₂ assimilation measured with CO₂-enriched air - g_s stomatal conductances - RuBPCase ribulose-1,5-bisphosphate carboxylase     

Effects of water vapour pressure deficit and stomatal conductance on photosynthesis,internal pressurization and convective flow in three emergent wetland plants

Internal pressurization and convective gas flow in emergent wetland plants is a function of the water vapour pressure deficit (WPD) and stomatal conductance (G _s) separating the external atmosphere from the internal aerenchyma. We have compared the effects of WPD and G _s under a range of light intensities on static pressures and convective flows in Phragmites australis, Typha orientalis and Baumea articulata. The capacity of the three species to generate flows per unit leaf area differed, being greatest in P. australisand lowest in B. articulata. In all three species, decreasing light intensity from full sunlight (2200 mol m^–2 s^–1 photosynthetically active photon flux density (PPFD)) to < 200 and < 10 mol m^–2 s^–1PPFD caused immediate decreases in photosynthetic assimilation, followed by more gradual decreases in transpiration and G _s. However, internal pressures and flows in the two low light intensities remained similar to values recorded in full sunlight. WPD was more significantly related to pressures and flows in P. australis and T. orientalis than G _s. In B. articulata, pressures increased at low G _s values but flow rates were unaffected, as predicted by earlier models describing pore size effects on pressures and flows. The data suggest that emergent macrophytes can maintain significant internal convection even at low light intensities, and this may be beneficial for nocturnal aeration, particularly in arid climates where the atmospheric humidity at night is low.     

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.     

Parameter estimation in surface exchange models using nonlinear inversion: how many parameters can we estimate and which measurements are most useful?

Models of mass and energy exchanges between the biosphere and the atmosphere generally contain a nonlinear dependence between fluxes and model parameters, and thus estimation of these parameters from measurements in a heterogeneous landscape depends on the scale of the observations. The scale‐dependence of a typical surface‐exchange model (the CSIRO Biospheric Model, CBM) is examined using the diurnal variation of hourly fluxes of CO₂, latent heat, sensible heat and soil heat. The fluxes were measured using micrometeorological techniques over six sites in a grazing/pasture system in SE Australia during a period of three weeks in 1995. Nonlinear parameter inversion was used to determine model parameters. Analysis of the covariance of the estimates of the parameters and the unexplained residuals of the model showed that a maximum of three or four parameters could be determined independently from the observations for all six sites. Estimates of a key model parameter, j_max, the mean of maximum potential electron transport rate of all leaves within the canopy, was best determined by the measurements of net CO₂ flux at all sites examined. Measurements of ground heat flux provide little information about any of the model parameters in CBM. Because of nonlinearities in the surface exchange model, calculated fluxes will be in error if parameters for the component vegetation types are simply averaged in proportion to their areal fraction. The magnitude of these errors was examined for CBM using a hypothetical land surface consisting of two surface types, each with different parameter values. Predictions of net CO₂, latent heat and ground heat fluxes using a linear combination of model parameters for the two surface types were quite similar with those found using optimal estimates of the parameters for the landscape, but were significantly poorer for sensible heat fluxes.     

Decreased hydraulic conductance in plants at elevated carbon dioxide

Previous work indicated that long-term exposure to elevated carbon dioxide levels can reduce hydraulic conductance in some species, but the basis of the response was not determined. In this study, hydraulic conductance was measured at concentrations of both 350 and 700 cm³ m^–3 carbon dioxide for plants grown at both concentrations, to determine the reversibility of the response. In Zea mays and Amaranthus hypochondriacus , exposure to the higher carbon dioxide concentration for several hours reduced whole-plant transpiration rate by 22–40%, without any consistent change in leaf water potential, indicating reversible reductions in hydraulic conductance at elevated carbon dioxide levels. Hydraulic conductance in these species grown at both carbon dioxide concentrations responded similarly to measurement concentration of carbon dioxide, indicating that the response was reversible. In Glycine max , which in earlier work had shown a long-term decrease in hydraulic conductance at elevated carbon dioxide levels, and in Abutilon theophrasti , no short-term changes in hydraulic conductance with measurement concentration of carbon dioxide were found, despite lower transpiration rates at elevated carbon dioxide. In G. max and Medicago sativa , growth at high dew-point temperature reduced transpiration rate and decreased hydraulic conductance. The results indicate that both reversible and irreversible decreases in hydraulic conductance can occur at elevated carbon dioxide concentrations, and that both could be responses to reduced transpiration rate, rather than to carbon dioxide concentration itself.     

城市植物源挥发性有机化合物排放特征及其大气环境效应研究进展

在外界环境的刺激下,植物会通过释放挥发性有机化合物来维护自身生长。城市是人类活动的主要集聚地,剧烈的人为干扰导致城市环境特征呈现出复杂的变化趋势,从而使城市植物排放挥发性有机化合物的过程与自然界出现较大差异。城市中的植物源挥发性有机化合物(Biogenic Volatile Organic Compounds, BVOCs)会直接与城市中的氧化物质接触,生成二次污染物,并在高温、强光照的条件下发生光化学反应,严重破坏城市大气环境,危害居民健康。总结了城市BVOCs的常见类型、作用机制及现有研究方法,分析了不同时间、空间和人类活动背景下的城市BVOCs排放特征,并进一步梳理了当前研究的不足,提出未来重点研究方向,旨在为大气环境治理、环境空间规划、居民健康保障等方面的城市管理工作提供指导。     

Measuring and modelling carbon dioxide and water vapour exchange over a temperate broad-leaved forest during the 1995 summer drought

Forests in the south-eastern United States experienced a prolonged dry spell and above-normal temperatures during the 1995 growing season. During this episode, nearly continuous, eddy covariance measurements of carbon dioxide and water vapour fluxes were acquired over a temperate, hardwood forest. These data are used to examine how environmental factors and accumulating soil moisture deficits affected the diurnal pattern and magnitude of canopy-scale carbon dioxide and water vapour fluxes. The field data are also used to test an integrative leaf-to-canopy scaling model (CANOAK), which uses micrometeorological and physiological theory, to calculate mass and energy fluxes. When soil moisture was ample in the spring, peak rates of net ecosystem CO₂ exchange (N_F) occurred around midday and exceeded 20 μmol m^?2 s^?1. Rates of N_K were near optimal when air temperature ranged between 22 and 25°C. The accumulation of soil moisture deficits and a co-occurrence of high temperatures caused peak rates of daytime carbon dioxide uptake to occur earlier in the morning. High air temperatures and soil moisture deficits were also correlated with a dramatic reduction in the magnitude of N_E. On average, the magnitude of N_E decreased from 20 to 7 μmol m^?2 s^?1 as air temperature increased from 24 to 30°C and the soil dried. The CANAOK model yielded accurate estimates of canopy-scale carbon dioxide and water vapour fluxes when the forest had an ample supply of soil moisture. During the drought and heat spell, a cumulative drought index was needed to adjust the proportionality constant of the stomatal conductance model to yield accurate estimates of canopy CO₂ exchange. The adoption of the drought index also enabled the CANOAK model to give improved estimates of evaporation until midday. On the other hand, the scheme failed to yield accurate estimates of evaporation during the afternoon.     

Photosynthesis of cotton plants exposed to elevated levels of carbon dioxide in the field

The cotton (Gossypium hirsutum L.) plant responds to a doubling of atmospheric CO₂ with almost doubled yield. Gas exchange of leaves was monitored to discover the photosynthetic basis of this large response. Plants were grown in the field in open-top chambers with ambient (nominally 350 l/l) or enriched (nominally either 500 or 650 l/l) concentrations of atmospheric CO₂. During most of the season, in fully-irrigated plants the relationship between assimilation (A) and intercellular CO₂ concentration (c_i) was almost linear over an extremely wide range of c_i. CO₂ enrichment did not alter this relationship or diminish photosynthetic capacity (despite accumulation of starch to very high levels) until very late in the season, when temperature was somewhat lower than at midseason. Stomatal conductance at midseason was very high and insensitive to CO₂, leading to estimates of c_i above 85% of atmospheric CO₂ concentration in both ambient and enriched chambers. Water stress caused A to show a saturation response with respect to c_i, and it increased stomatal closure in response to CO₂ enrichment. In fully-irrigated plants CO₂ enrichment to 650 l/l increased A more than 70%, but in water-stressed plants enrichment increased A only about 52%. The non-saturating response of A to c_i, the failure of CO₂ enrichment to decrease photosynthetic capacity for most of the season, and the ability of the leaves to maintain very high c_i, form in part the basis for the very large response to CO₂ enrichment.Abbreviations c_a- atmospheric CO₂ concentration - c_i- intercellular CO₂ concentration - A- rate of assimilation of CO₂ - g_s- stomatal conductance to water vapor - g_b- boundary layer conductance to water vapor - g_m- mesophyll conductance to CO₂ - VPD- vapor pressure deficit - _w leaf water potential - L- stomatal limitation to CO₂ uptake     

Photosynthetic carbon assimilation and associated metabolism in relation to water deficits in higher plants

Experimental studies on CO2 assimilation of mesophytic C3 plants in relation to relative water content (RWC) are discussed. Decreasing RWC slows the actual rate of photosynthetic CO2 assimilation (A) and decreases the potential rate (Apot). Generally, as RWC falls from c. 100 to c. 75%, the stomatal conductance (gs) decreases, and with it A. However, there are two general types of relation of Apot to RWC, which are called Type 1 and Type 2. Type 1 has two main phases. As RWC decreases from 100 to c. 75%, Apot is unaffected, but decreasing stomatal conductance (gs) results in smaller A, and lower CO2 concentration inside the leaf (Ci) and in the chloroplast (Cc), the latter falling possibly to the compensation point. Down-regulation of electron transport occurs by energy quenching mechanisms, and changes in carbohydrate and nitrogen metabolism are considered acclimatory, caused by low Ci and reversible by elevated CO2. Below 75% RWC, there is metabolic inhibition of Apot, inhibition of A then being partly (but progressively less) reversible by elevated CO2; gs regulates A progressively less, and Ci and CO2 compensation point, Gamma rise. It is suggested that this is the true stress phase, where the decrease in Apot is caused by decreased ATP synthesis and a consequent decreased synthesis of RuBP. In the Type 2 response, Apot decreases progressively at RWC 100 to 75%, with A being progressively less restored to the unstressed value by elevated CO2. Decreased gs leads to a lower Ci and Cc but they probably do not reach compensation point: gs becomes progressively less important and metabolic limitations more important as RWC falls. The primary effect of low RWC on Apot is most probably caused by limited RuBP synthesis, as a result of decreased ATP synthesis, either through inhibition of Coupling Factor activity or amount due to increased ion concentration. Carbohydrate synthesis and accumulation decrease. Type 2 response is considered equivalent to Type 1 at RWC below c. 75%, with Apot inhibited by limited ATP and RuBP synthesis, respiratory metabolism dominates and Ci and Gamma rise. The importance of inhibited ATP synthesis as a primary cause of decreasing Apot is discussed. Factors determining the Type 1 and Type 2 responses are unknown. Electron transport is maintained (but down-regulated) in Types 1 and 2 over a wide range of RWC, and a large reduced/oxidized adenylate ratio results. Metabolic imbalance results in amino acid accumulation and decreased and altered protein synthesis. These conditions profoundly affect cell functions and ultimately cause cell death. Type 1 and 2 responses may reflect differences in gs and in sensitivity of metabolism to decreasing RWC.     

Nonstructural carbohydrates of soybean plants grown in subambient and superambient levels of CO2

Photosynthesis Research - Elevated carbon dioxide (CO2) concentration increases plant photosynthesis, biomass and carbohydrate accumulation. Since plants have grown in low CO2 (200 to 300 µmol...     

植物源VOCs及其对陆地生态系统碳循环的贡献

综述了近20a来国内外关于植物源VOCs的研究进展。分析了植物源VOCs主要组成成分、生理-生态基础,以及影响植物VOCs释放速率的主要因素。重点探讨了植物源VOCs对陆地生态系统碳循环的潜在重要性,提出一些值得关注的问题。     

Sensitivity of infrared water vapor analyzers to oxygen concentration and errors in stomatal conductance

Use of infrared analyzers to measure water vapor concentrations in photosynthesis systems is becoming common. It is known that sensitivity of infrared carbon dioxide and water vapor analyzers is affected by the oxygen concentration in the background gas, particularly for absolute analyzers, but the potential for large errors in estimates of stomatal conductance due to effects of oxygen concentration on the sensitivity of infrared water vapor analyzers is not widely recognized. This work tested three types of infrared water vapor analyzers for changes in sensitivity of infrared water vapor analyzers depending on the oxygen content of the background gas. It was found that changing from either 0 or 2% to 21% oxygen in nitrogen decreased the sensitivity to water vapor for all three types of infrared water vapor analyzers by about 4%. The change in sensitivity was linear with oxygen mole fraction. The resulting error in calculated stomatal conductance would depend strongly on the leaf to air vapor pressure difference and leaf temperature, and also on whether leaf temperature was directly measured or calculated from energy balance. Examples of measurements of gas exchange on soybean leaves under glasshouse conditions indicated that changing from 21% to 2% oxygen produced an artifactual apparent increase in stomatal conductance which averaged about 30%. Similar errors occurred for `conductances' of wet filter paper. Such errors could affect inferences about the carbon dioxide dependence of the sensitivity of photosynthesis to oxygen. This revised version was published online in June 2006 with corrections to the Cover Date.     

Effect of elevated CO2 on the stomatal distribution and leaf physiology of Alnus glutinosa

Variation in stomatal development and physiology of mature leaves from Alnus glutinosa plants grown under reference (current ambient, 360 μmol mol⁻¹ CO₂) and double ambient (720 μmol mol⁻¹ CO₂) carbon dioxide (CO₂) mole fractions is assessed in terms of relative plant growth, stomatal characters (i.e. stomatal index and density) and leaf photosynthetic characters. This is the first study to consider the effects of elevated CO₂ concentration on the distribution of stomata and epidermal cells across the whole leaf and to try to ascertain the cause of intraleaf variation. In general, a doubling of the atmospheric CO₂ concentration enhanced plant growth and significantly increased stomatal index. However, there was no significant change in relative stomatal density. Under elevated CO₂ concentration there was a significant decrease in stomatal conductance and an increase in assimilation rate. However, no significant differences were found for the maximum rate of carboxylation ( V _cmax) and the light saturated rate of electron transport ( J _max) between the control and elevated CO₂ treatment.     

Variations in daytime net carbon and water exchange in a montane shrubland ecosystem in southeast Spain

Carbon and water fluxes in a semiarid shrubland ecosystem located in the southeast of Spain (province of Almería) were measured continuously over one year using the eddy covariance technique. We examined the influence of environmental variables on daytime (photosynthetically active photons, F _P >10 μmol m⁻² s⁻¹) ecosystem gas exchange and tested the ability of an empirical eco-physiological model based on F _P to estimate carbon fluxes over the whole year. The daytime ecosystem fluxes showed strong seasonality. During two solstitial periods, summer with warm temperatures (>15 °C) and sufficient soil moisture (>10 % vol.) and winter with mild temperatures (>5 °C) and high soil moisture contents (>15 % vol.), the photosynthetic rate was higher than the daytime respiration rate and mean daytime CO₂ fluxes were ca. −1.75 and −0.60 μmol m⁻² s⁻¹, respectively. Daytime evapotranspiration fluxes averaged ca. 2.20 and 0.24 mmol m⁻² s⁻¹, respectively. By contrast, in summer and early autumn with warm daytime temperatures (>10 °C) and dry soil (<10 % vol.), and also in mid-winter with near-freezing daytime temperatures the shrubland behaved as a net carbon source (mean daytime CO₂ release of ca. 0.60 and 0.20 μmol m⁻² s⁻¹, respectively). Furthermore, the comparison of water and carbon fluxes over a week in June 2004 and June 2005 suggests that the timing—rather than amount—of spring rainfall may be crucial in determining growing season water and carbon exchange. Due to strongly limiting environmental variables other than F _P, the model applied here failed to describe daytime carbon exchange only as a function of F _P and could not be used over most of the year to fill gaps in the data.     

Winter gas exchange between the atmosphere and snow-covered soils on Niwot Ridge,Colorado, USA

Background: There is a growing interest in understanding the gas exchange between the atmosphere and seasonally snow-covered regions, especially in light of projections that climate change will alter the timing and extent of seasonal snow cover. In snow-covered ecosystems, gas fluxes are due both to microbial activity in the snow-covered soils and to chemical and physical reactions with the various gases and/or dissolved constituents in the snowpack. Niwot Ridge, in the Colorado Rocky Mountains, has one of the most extensive sets of measurements of winter gas exchange globally.

Aims: Our goal was to examine the temporal patterns and environmental controls on Niwot Ridge of gas fluxes for gases with different sources and sinks.

Methods: Here, we review the concentrations and fluxes that have been measured for carbon dioxide, nitrous oxide, methane, nitrogen oxides, ozone, gaseous elemental mercury and volatile organic carbon compounds.

Results and Conclusions: We looked for similarities and differences among the gases, but in many cases, the origin, fate and controls of these fluxes still need to be determined. However, we believe that many of the biologically driven reactions are the result of exponential growth of a winter microbial community during the long period of stable environmental conditions under the seasonal snowpack.