Marcy E. Litvak

Environmental and developmental controls over the seasonal pattern of isoprene emission from aspen leaves

Isoprene emission from plants represents one of the principal biospheric controls over the oxidative capacity of the continental troposphere. In the study reported here, the seasonal pattern of isoprene emission, and its underlying determinants, were studied for aspen trees growing in the Rocky Mountains of Colorado. The springtime onset of isoprene emission was delayed for up to 4 weeks following leaf emergence, despite the presence of positive net photosynthesis rates. Maximum isoprene emission rates were reached approximately 6 weeks following leaf emergence. During this initial developmental phase, isoprene emission rates were negatively correlated with leaf nitrogen concentrations. During the autumnal decline in isoprene emission, rates were positively correlated with leaf nitrogen concentration. Given past studies that demonstrate a correlation between leaf nitrogen concentration and isoprene emission rate, we conclude that factors other than the amount of leaf nitrogen determine the early-season initiation of isoprene emission. The late-season decline in isoprene emission rate is interpreted as due to the autumnal breakdown of metabolic machinery and loss of leaf nitrogen. In potted aspen trees, leaves that emerged in February and developed under cool, springtime temperatures did not emit isoprene until 23 days after leaf emergence. Leaves that emrged in July and developed in hot, midsummer temperatures emitted isoprene within 6 days. Leaves that had emerged during the cool spring, and had grown for several weeks without emitting isoprene, could be induced to emit isoprene within 2 h of exposure to 32°C. Continued exposure to warm temperatures resulted in a progressive increase in the isoprene emission rate. Thus, temperature appears to be an important determinant of the early season induction of isoprene emission. The seasonal pattern of isoprene emission was examined in trees growing along an elevational gradient in the Colorado Front Range (1829–2896 m). Trees at different elevations exhibited staggered patterns of bud-break and initiation of photosynthesis and isoprene emission in concert with the staggered onset of warm, springtime temperatures. The springtime induction of isoprene emission could be predicted at each of the three sites as the time after bud break required for cumulative temperatures above 0°C to reach approximately 400 degree days. Seasonal temperature acclimation of isoprene emission rate and photosynthesis rate was not observed. The temperature dependence of isoprene emission rate between 20 and 35°C could be accurately predicted during spring and summer using a single algorithm that describes the Arrhenius relationship of enzyme activity. From these results, it is concluded that the early season pattern of isoprene emission is controlled by prevailing temperature and its interaction with developmental processes. The late-season pattern is determined by controls over leaf nitrogen concentration, especially the depletion of leaf nitrogen during senescence. Following early-season induction, isoprene emission rates correlate with photosynthesis rates. During the season there is little acclimation to temperature, so that seasonal modeling simplifies to a single temperature-response algorithm.

Patterns of induced and constitutive monoterpene production in conifer needles in relation to insect herbivory

Abstract Studies were conducted to determine whether herbivore-induced synthesis of monoterpenes occurs in the needles of ponderosa pine (Pinus ponderosa Lawson), lodgepole pine (P. contorta Douglas var. latifolia Engelmann), white fir (Abies concolor Lindl. and Gordon) and Engelmann spruce [Picea engelmanii (Parry) Engelm.]. In the needles of all species except Engelmann spruce, simulated herbivory significantly induced the activity of monoterpene cyclases 4–8 days after wounding. In ponderosa pine, real herbivory by last-instar tiger moth larvae (Halisdota ingens Hy. Edwards: Lepidoptera) induced a significantly larger response (4.5-fold increase in monoterpene cyclase activity) than did simulated herbivory (2.5-fold increase). To our knowledge, this is the first report of herbivore-induced increases in monoterpene synthesis in needle tissue. Despite this increase in monoterpene synthesis, we observed no significant increase in total monoterpene pool size in wounded needles compared to controls. Large increases in the rate of monoterpene volatilization were observed in response to wounding. We conclude that the volatile losses caused by tissue damage compensate for herbivore-induced monoterpene synthesis, resulting in no change in pool size. Tiger moth larvae consume ponderosa pine needles in a pattern that begins at the tip and proceeds downward to midway along the needle, at which point they move to an undamaged needle. Constitutive monoterpene concentrations and monoterpene cyclase activities were highest in the lower half of ponderosa pine needles. The monoterpene profile also differed between the upper and lower needle halves, the lower half possessing an additional one to four monoterpene forms. We propose that the increasing gradient in monoterpene concentrations and number of monoterpenes along the needle from tip to base deters feeding beyond the midway point and provides time for the induction of increased cyclase activity and production of new monoterpenes. The induction of new monoterpene synthesis may have a role in replacing monoterpenes lost through damage-induced volatilization and preventing extreme compromise of the constitutive defense system.

Isoprene Emission from Velvet Bean Leaves (Interactions among Nitrogen Availability, Growth Photon Flux Density, and Leaf Development)

Although isoprene synthesis is closely coupled to photosynthesis, both via ATP requirements and carbon substrate availability, control of isoprene emission is not always closely linked to photosynthetic processes. In this study we grew velvet bean (Mucuna sp.) under different levels of photon flux density (PFD) and nitrogen availability in an effort to understand better the degree to which these two processes are linked. As has been observed in past studies, we found that during early leaf ontogeny the onset of positive rates of net photosynthesis precedes that of isoprene emission by 3 to 4 d. Other studies have shown that this lag is correlated with the induction of isoprene synthase activity, indicating that overall control of the process is under control of that enzyme. During leaf senescence, photosynthesis rate and isoprene emission rate declined in parallel, suggesting similar controls over the two processes. This coordinated decline was accelerated when plants were grown with high PFD and high nitrogen availability. The latter effect included declines in the photon yield of photosynthesis, suggesting that an unexplained stress arose during growth under these conditions, triggering a premature decline in photosynthesis and isoprene emission rate. In mature leaves, growth PFD and nitrogen nutrition affected photosynthesis and isoprene emission in qualitatively similar, but quantitatively different, ways. This resulted in a significant shift in the percentage of fixed carbon that was re-emitted as isoprene. In the case of increasing growth PFD, isoprene emission rate was more strongly affected than photosynthesis rate, and more carbon was lost as isoprene. In the case of increasing nitrogen, photosynthesis rate increased more than isoprene emission rate, and leaves containing high amounts of nitrogen lost a lower percentage of their assimilated carbon as isoprene. Taken together, our results demonstrate that, although the general correlation between isoprene emission rate and photosynthesis rate is consistently expressed, there is evidence that both processes are capable of independent responses to plant growth environment.

Plant chemical defense: monoterpenes and the growth-differentiation balance hypothesis

Recent studies of allocation to defensive chemicals in plants have provided insights into the ecological controls over plant defensive chemicals. Both developmental and ecological studies now suggest that we can understand the factors influencing allocation to defense by examining the relative availability of resources, external needs for chemical defense, and the internal demands for growth that plants face. These studies have also shed light on one of the more popular theories in plant evolutionary ecology, the growth-differentiation balance hypothesis of plant resource allocation.

Warm spring reduced carbon cycle impact of the 2012 US summer drought

Significance Carbon uptake by terrestrial ecosystems mitigates the impact of anthropogenic fossil fuel emissions on atmospheric CO2 concentrations, but the strength of this carbon sink is highly sensitive to large-scale extreme climate events. In 2012, the United States experienced the most severe drought since the Dust Bowl period, along with the warmest spring on record. Here, we quantify the impact of this climate anomaly on the carbon cycle. Our results show that warming-induced earlier vegetation activity increased spring carbon uptake, and thus compensated for reduced carbon uptake during the summer drought in 2012. This compensation, however, came at the cost of soil moisture depletion from increased spring evapotranspiration that likely enhanced summer heating through land-atmosphere coupling. The global terrestrial carbon sink offsets one-third of the world’s fossil fuel emissions, but the strength of this sink is highly sensitive to large-scale extreme events. In 2012, the contiguous United States experienced exceptionally warm temperatures and the most severe drought since the Dust Bowl era of the 1930s, resulting in substantial economic damage. It is crucial to understand the dynamics of such events because warmer temperatures and a higher prevalence of drought are projected in a changing climate. Here, we combine an extensive network of direct ecosystem flux measurements with satellite remote sensing and atmospheric inverse modeling to quantify the impact of the warmer spring and summer drought on biosphere-atmosphere carbon and water exchange in 2012. We consistently find that earlier vegetation activity increased spring carbon uptake and compensated for the reduced uptake during the summer drought, which mitigated the impact on net annual carbon uptake. The early phenological development in the Eastern Temperate Forests played a major role for the continental-scale carbon balance in 2012. The warm spring also depleted soil water resources earlier, and thus exacerbated water limitations during summer. Our results show that the detrimental effects of severe summer drought on ecosystem carbon storage can be mitigated by warming-induced increases in spring carbon uptake. However, the results also suggest that the positive carbon cycle effect of warm spring enhances water limitations and can increase summer heating through biosphere–atmosphere feedbacks.

Global satellite monitoring of climate-induced vegetation disturbances

Terrestrial disturbances are accelerating globally, but their full impact is not quantified because we lack an adequate monitoring system. Remote sensing offers a means to quantify the frequency and extent of disturbances globally. Here, we review the current application of remote sensing to this problem and offer a framework for more systematic analysis in the future. We recommend that any proposed monitoring system should not only detect disturbances, but also be able to: identify the proximate cause(s); integrate a range of spatial scales; and, ideally, incorporate process models to explain the observed patterns and predicted trends in the future. Significant remaining challenges are tied to the ecology of disturbances. To meet these challenges, more effort is required to incorporate ecological principles and understanding into the assessments of disturbance worldwide.

Positive feedback between microclimate and shrub encroachment in the northern Chihuahuan desert

Woody plant encroachment is affecting vegetation composition in arid grasslands worldwide and has been associated with a number of environmental drivers and feedbacks. It has been argued that the relatively abrupt character (both in space and in time) of grassland-to-shrubland transitions observed in many drylands around the world might result from positive feedbacks in the underlying ecosystem dynamics. In the case of the Chihuahuan Desert, we show that one such feedback could emerge from interactions between vegetation and microclimate conditions. Shrub establishment modifies surface energy fluxes, causing an increase in nighttime air temperature, particularly during wintertime. The resulting change in winter air temperature regime is important because the northern limit of the dominant shrub in the northern Chihuahuan Desert, Larrea tridentata, presently occurs where minimum temperatures are sufficiently low to be a potential source of mortality. Using freezing responses from published studies in combination with observed temperature records, we predict that a small warming can yield meaningful changes in plant function and survival. Moreover, we also suggest that the effect of the change in air temperature on vegetation depends on whether plants experience drought during winter. Thus, in the Chihuahuan region a positive feedback exists between shrub encroachment and changes in microclimate conditions, with implications for the response of this ecosystem to regional changes in temperature and precipitation.

Thermal optimality of net ecosystem exchange of carbon dioxide and underlying mechanisms.

• It is well established that individual organisms can acclimate and adapt to temperature to optimize their functioning. However, thermal optimization of ecosystems, as an assemblage of organisms, has not been examined at broad spatial and temporal scales. • Here, we compiled data from 169 globally distributed sites of eddy covariance and quantified the temperature response functions of net ecosystem exchange (NEE), an ecosystem-level property, to determine whether NEE shows thermal optimality and to explore the underlying mechanisms. • We found that the temperature response of NEE followed a peak curve, with the optimum temperature (corresponding to the maximum magnitude of NEE) being positively correlated with annual mean temperature over years and across sites. Shifts of the optimum temperature of NEE were mostly a result of temperature acclimation of gross primary productivity (upward shift of optimum temperature) rather than changes in the temperature sensitivity of ecosystem respiration. • Ecosystem-level thermal optimality is a newly revealed ecosystem property, presumably reflecting associated evolutionary adaptation of organisms within ecosystems, and has the potential to significantly regulate ecosystem-climate change feedbacks. The thermal optimality of NEE has implications for understanding fundamental properties of ecosystems in changing environments and benchmarking global models.

Differential effects of extreme drought on production and respiration: synthesis and modeling analysis

Extremes in climate may severely impact ecosys- tem structure and function, with both the magnitude and rate of response differing among ecosystem types and processes. We conducted a modeling analysis of the effects of extreme drought on two key ecosystem processes, production and res- piration, and, to provide a broader context, we complemented this with a synthesis of published results that cover a wide variety of ecosystems. The synthesis indicated that across a broad range of biomes, gross primary production (GPP) was generally more sensitive to extreme drought (defined as pro- portional reduction relative to average rainfall periods) than was ecosystem respiration (ER). Furthermore, this differen- tial sensitivity between production and respiration increased as drought severity increased; it occurred only in grassland ecosystems, and not in evergreen needle-leaf and broad-leaf forests or woody savannahs. The modeling analysis was de- signed to enable a better understanding of the mechanisms underlying this pattern, and focused on four grassland sites arrayed across the Great Plains, USA. Model results consis- tently showed that net primary productivity (NPP) was re- duced more than heterotrophic respiration (Rh) by extreme drought (i.e., 67 % reduction in annual ambient rainfall) at all four study sites. The sensitivity of NPP to drought was di- rectly attributable to rainfall amount, whereas the sensitivity of Rh to drought was driven by soil drying, reduced carbon (C) input and a drought-induced reduction in soil C content - a much slower process. However, differences in reductions in NPP and Rh diminished as extreme drought continued, due to a gradual decline in the soil C pool leading to further re- ductions in Rh. We also varied the way in which drought was imposed in the modeling analysis; it was either imposed by simulating reductions in rainfall event size (ESR) or by re- ducing rainfall event number (REN). Modeled NPP and Rh decreased more by ESR than REN at the two relatively mesic sites but less so at the two xeric sites. Our findings suggest that responses of production and respiration differ in magni- tude, occur on different timescales, and are affected by dif- ferent mechanisms under extreme, prolonged drought.

Terrestrial carbon balance in a drier world: the effects of water availability in southwestern North America

Global modeling efforts indicate semiarid regions dominate the increasing trend and interannual variation of net CO2 exchange with the atmosphere, mainly driven by water availability. Many semiarid regions are expected to undergo climatic drying, but the impacts on net CO2 exchange are poorly understood due to limited semiarid flux observations. Here we evaluated 121 site-years of annual eddy covariance measurements of net and gross CO2 exchange (photosynthesis and respiration), precipitation, and evapotranspiration (ET) in 21 semiarid North American ecosystems with an observed range of 100 - 1000 mm in annual precipitation and records of 4-9 years each. In addition to evaluating spatial relationships among CO2 and water fluxes across sites, we separately quantified site-level temporal relationships, representing sensitivity to interannual variation. Across the climatic and ecological gradient, photosynthesis showed a saturating spatial relationship to precipitation, whereas the photosynthesis-ET relationship was linear, suggesting ET was a better proxy for water available to drive CO2 exchanges after hydrologic losses. Both photosynthesis and respiration showed similar site-level sensitivity to interannual changes in ET among the 21 ecosystems. Furthermore, these temporal relationships were not different from the spatial relationships of long-term mean CO2 exchanges with climatic ET. Consequently, a hypothetical 100-mm change in ET, whether short term or long term, was predicted to alter net ecosystem production (NEP) by 64 gCm(-2) yr(-1). Most of the unexplained NEP variability was related to persistent, site-specific function, suggesting prioritization of research on slow-changing controls. Common temporal and spatial sensitivity to water availability increases our confidence that site-level responses to interannual weather can be extrapolated for prediction of CO2 exchanges over decadal and longer timescales relevant to societal response to climate change.