The fate of carbon in a mature forest under carbon dioxide enrichment.

Atmospheric carbon dioxide enrichment (eCO2) can enhance plant carbon uptake and growth1-5, thereby providing an important negative feedback to climate change by slowing the rate of increase of the atmospheric CO2 concentration6. Although evidence gathered from young aggrading forests has generally indicated a strong CO2 fertilization effect on biomass growth3-5, it is unclear whether mature forests respond to eCO2 in a similar way. In mature trees and forest stands7-10, photosynthetic uptake has been found to increase under eCO2 without any apparent accompanying growth response, leaving the fate of additional carbon fixed under eCO2 unclear4,5,7-11. Here using data from the first ecosystem-scale Free-Air CO2 Enrichment (FACE) experiment in a mature forest, we constructed a comprehensive ecosystem carbon budget to track the fate of carbon as the forest responded to four years of eCO2 exposure. We show that, although the eCO2 treatment of +150 parts per million (+38 per cent) above ambient levels induced a 12 per cent (+247 grams of carbon per square metre per year) increase in carbon uptake through gross primary production, this additional carbon uptake did not lead to increased carbon sequestration at the ecosystem level. Instead, the majority of the extra carbon was emitted back into the atmosphere via several respiratory fluxes, with increased soil respiration alone accounting for half of the total uptake surplus. Our results call into question the predominant thinking that the capacity of forests to act as carbon sinks will be generally enhanced under eCO2, and challenge the efficacy of climate mitigation strategies that rely on ubiquitous CO2 fertilization as a driver of increased carbon sinks in global forests.

Strong isoprene emission response to temperature in tundra vegetation.

Emissions of biogenic volatile organic compounds (BVOCs) are a crucial component of biosphere-atmosphere interactions. In northern latitudes, climate change is amplified by feedback processes in which BVOCs have a recognized, yet poorly quantified role, mainly due to a lack of measurements and concomitant modeling gaps. Hence, current Earth system models mostly rely on temperature responses measured on vegetation from lower latitudes, rendering their predictions highly uncertain. Here, we show how tundra isoprene emissions respond vigorously to temperature increases, compared to model results. Our unique dataset of direct eddy covariance ecosystem-level isoprene measurements in two contrasting ecosystems exhibited Q10 (the factor by which the emission rate increases with a 10 °C rise in temperature) temperature coefficients of up to 20.8, that is, 3.5 times the Q10 of 5.9 derived from the equivalent model calculations. Crude estimates using the observed temperature responses indicate that tundra vegetation could enhance their isoprene emissions by up to 41% (87%)-that is, 46% (55%) more than estimated by models-with a 2 °C (4 °C) warming. Our results demonstrate that tundra vegetation possesses the potential to substantially boost its isoprene emissions in response to future rising temperatures, at rates that exceed the current Earth system model predictions.

Impact of three decades of warming, increased nutrient availability, and increased cloudiness on the fluxes of greenhouse gases and biogenic volatile organic compounds in a subarctic tundra heath.

Climate change is exposing subarctic ecosystems to higher temperatures, increased nutrient availability, and increasing cloud cover. In this study, we assessed how these factors affect the fluxes of greenhouse gases (GHGs) (i.e., methane (CH4), nitrous oxide (N2O), and carbon dioxide (CO2)), and biogenic volatile organic compounds (BVOCs) in a subarctic mesic heath subjected to 34 years of climate change related manipulations of temperature, nutrient availability, and light. GHGs were sampled from static chambers and gases analyzed with gas chromatograph. BVOCs were measured using the push-pull method and gases analyzed with chromatography-mass spectrometry. The soil temperature and moisture content in the warmed and shaded plots did not differ significantly from that in the controls during GHG and BVOC measurements. Also, the enclosure temperatures during BVOC measurements in the warmed and shaded plots did not differ significantly from temperatures in the controls. Hence, this allowed for assessment of long-term effects of the climate treatment manipulations without interference of temperature and moisture differences at the time of measurements. Warming enhanced CH4 uptake and the emissions of CO2, N2O, and isoprene. Increased nutrient availability increased the emissions of CO2 and N2O but caused no significant changes in the fluxes of CH4 and BVOCs. Shading (simulating increased cloudiness) enhanced CH4 uptake but caused no significant changes in the fluxes of other gases compared to the controls. The results show that climate warming and increased cloudiness will enhance CH4 sink strength of subarctic mesic heath ecosystems, providing negative climate feedback, while climate warming and enhanced nutrient availability will provide positive climate feedback through increased emissions of CO2 and N2O. Climate warming will also indirectly, through vegetation changes, increase the amount of carbon lost as isoprene from subarctic ecosystems.

Separating direct and indirect effects of rising temperatures on biogenic volatile emissions in the Arctic.

Volatile organic compounds (VOCs) are released from biogenic sources in a temperature-dependent manner. Consequently, Arctic ecosystems are expected to greatly increase their VOC emissions with ongoing climate warming, which is proceeding at twice the rate of global temperature rise. Here, we show that ongoing warming has strong, increasing effects on Arctic VOC emissions. Using a combination of statistical modeling on data from several warming experiments in the Arctic tundra and dynamic ecosystem modeling, we separate the impacts of temperature and soil moisture into direct effects and indirect effects through vegetation composition and biomass alterations. The indirect effects of warming on VOC emissions were significant but smaller than the direct effects, during the 14-y model simulation period. Furthermore, vegetation changes also cause shifts in the chemical speciation of emissions. Both direct and indirect effects result in large geographic differences in VOC emission responses in the warming Arctic, depending on the local vegetation cover and the climate dynamics. Our results outline complex links between local climate, vegetation, and ecosystem-atmosphere interactions, with likely local-to-regional impacts on the atmospheric composition.

Influence of increased nutrient availability on biogenic volatile organic compound (BVOC) emissions and leaf anatomy of subarctic dwarf shrubs under climate warming and increased cloudiness.

BACKGROUND AND AIMS: Climate change is subjecting subarctic ecosystems to elevated temperature, increased nutrient availability and reduced light availability (due to increasing cloud cover). This may affect subarctic vegetation by altering the emissions of biogenic volatile organic compounds (BVOCs) and leaf anatomy. We investigated the effects of increased nutrient availability on BVOC emissions and leaf anatomy of three subarctic dwarf shrub species, Empetrum hermaphroditum, Cassiope tetragona and Betula nana, and if increased nutrient availability modifies the responses to warming and shading. METHODS: Measurements of BVOCs were performed in situ in long-term field experiments in the Subarctic using a dynamic enclosure system and collection of BVOCs into adsorbent cartridges analysed by gas chromatography-mass spectrometry. Leaf anatomy was studied using light microscopy and scanning electron microscopy. KEY RESULTS: Increased nutrient availability increased monoterpene emission rates and altered the emission profile of B. nana, and increased sesquiterpene and oxygenated monoterpene emissions of C. tetragona. Increased nutrient availability increased leaf tissue thicknesses of B. nana and C. tetragona, while it caused thinner epidermis and the highest fraction of functional (intact) glandular trichomes for E. hermaphroditum. Increased nutrient availability and warming synergistically increased mesophyll intercellular space of B. nana and glandular trichome density of C. tetragona, while treatments combining increased nutrient availability and shading had an opposite effect in C. tetragona. CONCLUSIONS: Increased nutrient availability may enhance the protection capacity against biotic and abiotic stresses (especially heat and drought) in subarctic shrubs under future warming conditions as opposed to increased cloudiness, which could lead to decreased resistance. The study emphasizes the importance of changes in nutrient availability in the Subarctic, which can interact with climate warming and increased cloudiness effects.

The multidimensional nutritional niche of fungus-cultivar provisioning in free-ranging colonies of a neotropical leafcutter ant.

Foraging trails of leafcutter colonies are iconic scenes in the Neotropics, with ants collecting freshly cut plant fragments to provision a fungal food crop. We hypothesised that the fungus-cultivar's requirements for macronutrients and minerals govern the foraging niche breadth of Atta colombica leafcutter ants. Analyses of plant fragments carried by foragers showed how nutrients from fruits, flowers and leaves combine to maximise cultivar performance. While the most commonly foraged leaves delivered excess protein relative to the cultivar's needs, in vitro experiments showed that the minerals P, Al and Fe may expand the leafcutter foraging niche by enhancing the cultivar's tolerance to protein-biased substrates. A suite of other minerals reduces cultivar performance in ways that may render plant fragments with optimal macronutrient blends unsuitable for provisioning. Our approach highlights how the nutritional challenges of provisioning a mutualist can govern the multidimensional realised niche available to a generalist insect herbivore.

Synergistic effects of insect herbivory and changing climate on plant volatile emissions in the subarctic tundra.

Climate change increases the insect abundance, especially in Arctic ecosystems. Insect herbivory also significantly increases plant emissions of volatile organic compounds (VOCs), which are highly reactive in the atmosphere and play a crucial role in atmospheric chemistry and physics. However, it is unclear how the effects of insect herbivory on VOC emissions interact with climatic changes, such as warming and increased cloudiness. We assessed how experimental manipulations of temperature and light availability in subarctic tundra, that had been maintained for 30 years at the time of the measurements, affect the VOC emissions from a widespread dwarf birch (Betula nana) when subjected to herbivory by local geometrid moth larvae, the autumnal moth (Epirrita autumnata) and the winter moth (Operophtera brumata). Warming and insect herbivory on B. nana stimulated VOC emission rates and altered the VOC blend. The herbivory-induced increase in sesquiterpene and homoterpene emissions were climate-treatment-dependent. Many herbivory-associated VOCs were more strongly induced in the shading treatment than in other treatments. We showed generally enhanced tundra VOC emissions upon insect herbivory and synergistic effects on the emissions of some VOC groups in a changing climate, which can have positive feedbacks on cloud formation. Furthermore, the acclimation of plants to long-term climate treatments affects VOC emissions and strongly interacts with plant responses to herbivory. Such acclimation complicates predictions of how climate change, together with interacting biotic stresses, affects VOC emissions in the high latitudes.

Phenological stage of tundra vegetation controls bidirectional exchange of BVOCs in a climate change experiment on a subarctic heath.

Traditionally, biogenic volatile organic compound (BVOC) emissions are often considered a unidirectional flux, from the ecosystem to the atmosphere, but recent studies clearly show the potential for bidirectional exchange. Here we aimed to investigate how warming and leaf litter addition affect the bidirectional exchange (flux) of BVOCs in a long-term field experiment in the Subarctic. We also assessed changes in net BVOC fluxes in relation to the time of day and the influence of different plant phenological stages. The study was conducted in a full factorial experiment with open top chamber warming and annual litter addition treatments in a tundra heath in Abisko, Northern Sweden. After 18 years of treatments, ecosystem-level net BVOC fluxes were measured in the experimental plots using proton-transfer-reaction time-of-flight mass spectrometry (PTR-ToF-MS). The warming treatment increased monoterpene and isoprene emissions by ≈50%. Increasing temperature, due to diurnal variations, can both increase BVOC emission and simultaneously, increase ecosystem uptake. For any given treatment, monoterpene, isoprene, and acetone emissions also increased with increasing ambient air temperatures caused by diurnal variability. Acetaldehyde, methanol, and sesquiterpenes decreased likely due to a deposition flux. For litter addition, only a significant indirect effect on isoprene and monoterpene fluxes (decrease by ~50%-75%) was observed. Litter addition may change soil moisture conditions, leading to changes in plant species composition and biomass, which could subsequently result in changes to BVOC emission compositions. Phenological stages significantly affected fluxes of methanol, isoprene and monoterpenes. We suggest that plant phenological stages differ in impacts on BVOC net emissions, but ambient air temperature and photosynthetically active radiation (PAR) also interact and influence BVOC net emissions differently. Our results may also suggest that BVOC fluxes are not only a response to changes in temperature and light intensity, as the circadian clock also affects emission rates.

Volatile organic compound emission in tundra shrubs - Dependence on species characteristics and the near-surface environment.

Temperature is one of the key abiotic factors during the life of plants, especially in the Arctic region which is currently experiencing rapid climate change. We evaluated plant traits and environmental variables determining leaf temperature in tundra shrubs and volatile organic compound (VOC) emissions with field measurements on deciduous tundra shrubs, Salix myrsinites and Betula nana, and evergreen Cassiope tetragona and Rhododendron lapponicum. Higher leaf-to-air temperature difference was observed in evergreen, compared to deciduous shrubs. Evergreen shrubs also showed continuously increasing photosynthesis with increasing temperature, suggesting high thermal tolerance. For the deciduous species, the optimum temperature for net photosynthesis was between our measurement temperatures of 24 °C and 38 °C. Air temperature and vapor pressure deficit were the most important variables influencing leaf temperature and VOC emissions in all the studied plants, along with stomatal density and specific leaf area in the deciduous shrubs. Using climate data and emission factors from our measurements, we modelled total seasonal tundra shrub VOC emissions of 0.3-2.3 g m-2 over the main growing season. Our results showed higher-than-expected temperature optima for photosynthesis and VOC emission and demonstrated the relative importance of plant traits and local environments in determining leaf temperature and VOC emissions in a subarctic tundra.

Origin of volatile organic compound emissions from subarctic tundra under global warming.

Warming occurs in the Arctic twice as fast as the global average, which in turn leads to a large enhancement in terpenoid emissions from vegetation. Volatile terpenoids are the main class of biogenic volatile organic compounds (VOCs) that play crucial roles in atmospheric chemistry and climate. However, the biochemical mechanisms behind the temperature-dependent increase in VOC emissions from subarctic ecosystems are largely unexplored. Using 13 CO2 -labeling, we studied the origin of VOCs and the carbon (C) allocation under global warming in the soil-plant-atmosphere system of contrasting subarctic heath tundra vegetation communities characterized by dwarf shrubs of the genera Salix or Betula. The projected temperature rise of the subarctic summer by 5°C was realistically simulated in sophisticated climate chambers. VOC emissions strongly depended on the plant species composition of the heath tundra. Warming caused increased VOC emissions and significant changes in the pattern of volatiles toward more reactive hydrocarbons. The 13 C was incorporated to varying degrees in different monoterpene and sesquiterpene isomers. We found that de novo monoterpene biosynthesis contributed to 40%-44% (Salix) and 60%-68% (Betula) of total monoterpene emissions under the current climate, and that warming increased the contribution to 50%-58% (Salix) and 87%-95% (Betula). Analyses of above- and belowground 12/13 C showed shifts of C allocation in the plant-soil systems and negative effects of warming on C sequestration by lowering net ecosystem exchange of CO2 and increasing C loss as VOCs. This comprehensive analysis provides the scientific basis for mechanistically understanding the processes controlling terpenoid emissions, required for modeling VOC emissions from terrestrial ecosystems and predicting the future chemistry of the arctic atmosphere. By changing the chemical composition and loads of VOCs into the atmosphere, the current data indicate that global warming in the Arctic may have implications for regional and global climate and for the delicate tundra ecosystems.