Joan Llusià

Human-induced nitrogen–phosphorus imbalances alter natural and managed ecosystems across the globe

The availability of carbon from rising atmospheric carbon dioxide levels and of nitrogen from various human-induced inputs to ecosystems is continuously increasing; however, these increases are not paralleled by a similar increase in phosphorus inputs. The inexorable change in the stoichiometry of carbon and nitrogen relative to phosphorus has no equivalent in Earths history. Here we report the profound and yet uncertain consequences of the human imprint on the phosphorus cycle and nitrogen:phosphorus stoichiometry for the structure, functioning and diversity of terrestrial and aquatic organisms and ecosystems. A mass balance approach is used to show that limited phosphorus and nitrogen availability are likely to jointly reduce future carbon storage by natural ecosystems during this century. Further, if phosphorus fertilizers cannot be made increasingly accessible, the crop yields projections of the Millennium Ecosystem Assessment imply an increase of the nutrient deficit in developing regions.

Seasonal patterns of terpene content and emission from seven mediterranean woody species in field conditions.

The seasonal pattern of terpene content and emission by seven Mediterranean woody species was studied under field conditions. Emission rates were normalized at 30°C and 1000 μmol·m·s PFD (photosynthetic photon flux density). Bupleurum fruticosum, Pinus halepensis, and Cistus albidus stored large amounts of terpenes (0.01-1.77% [dry matter]) with maximum values in autumn and minimum values in spring. They emitted large amounts of terpenes (2-40 μg·g DM·h), but with no clear seasonal trend except for Cistus albidus, which had maximum values in spring and minimum values in autumn. The nonstoring species Arbutus unedo, Erica arborea, Quercus coccifera and Quercus ilex also emitted large amounts of terpenes (0-40 μg·g DM·h) and also tended to present maximum emission rates in spring, although this trend was significant only for A. unedo. At the seasonal scale, emission rates did not follow changes in photosynthetic rates; instead, they mostly followed changes in temperature. From autumn to spring, the least volatile monoterpenes such as limonene were emitted at highest rates, whereas the most volatile monoterpenes such as α-pinene and β-pinene were the most emitted in summer. The monoterpene emission rates represented a greater percentage of the photosynthetic carbon fixation in summer (from 0.51% in Arbutus unedo to 5.64% in Quercus coccifera) than in the rest of the seasons. All these seasonality trends must be considered when inventorying and modeling annual emission rates in Mediterranean ecosystems.

BVOCs: plant defense against climate warming?

Plants emit a substantial amount of biogenic volatile organic compounds (BVOCs) into the atmosphere. These BVOCs represent a large carbon loss and can be up to approximately 10% of that fixed by photosynthesis under stressful conditions and up to 100gCm(-2) per year in some tropical ecosystems. Among a variety of proven and unproven BVOC functions in plants and roles in atmospheric processes, recent data intriguingly link emission of these compounds to climate. Ongoing research demonstrates that BVOCs could protect plants against high temperatures. BVOC emissions are probably increasing with warming and with other factors associated to global change, including changes in land cover. These increases in BVOC emissions could contribute in a significant way (via negative and positive feedback) to the complex processes associated with global warming.

The complexity of factors driving volatile organic compound emissions by plants

The emissions of volatile organic compounds, VOC, from plants have strong relevance for plant physiology, plant ecology, and atmospheric chemistry. We report here on the current knowledge of the many internal (genetic and biochemical) and external (abiotic - temperature, light, water availability, wind, ozone, and biotic - animal, plant and microorganisms interactions) factors that control emission rates of different VOC by altering their synthesis, vapour pressure or diffusion to the atmosphere. The complex net of these factors, their interactions and the different responses of the different VOC produces the large qualitative and quantitative, spatial and temporal variability of emissions and the frequent deviations from current standard emission models. The need for a co-operative multidisciplinary multiscale research to disentangle this complex and important issue of plant VOC emissions is reminded.

The Capacity for Thermal Protection of Photosynthetic Electron Transport Varies for Different Monoterpenes in Quercus ilex

Heat stress resistance of foliar photosynthetic apparatus was investigated in the Mediterranean monoterpene-emitting evergreen sclerophyll species Quercus ilex. Leaf feeding with fosmidomycin, which is a specific inhibitor of the chloroplastic isoprenoid synthesis pathway, essentially stopped monoterpene emission and resulted in the decrease of the optimum temperature of photosynthetic electron transport from approximately 38°C to approximately 30°C. The heat stress resistance was partly restored by fumigation with 4 to 5 nmol mol−1 air concentrations of monoterpene α-pinene but not with fumigations with monoterpene alcohol α-terpineol. Analyses of monoterpene physicochemical characteristics demonstrated that α-pinene was primarily distributed to leaf gas and lipid phases, while α-terpineol was primarily distributed to leaf aqueous phase. Thus, for a common monoterpene uptake rate, α-terpineol is less efficient in stabilizing membrane liquid-crystalline structure and as an antioxidant in plant membranes. Furthermore, α-terpineol uptake rate (U) strongly decreased with increasing temperature, while the uptake rates of α-pinene increased with increasing temperature, providing a further explanation of the lower efficiency of thermal protection by α-terpineol. The temperature-dependent decrease of α-terpineol uptake was both due to decreases in stomatal conductance, gw, and increased volatility of α-terpineol at higher temperature that decreased the monoterpene diffusion gradient between the ambient air (FA) and leaf (FI; U = gw[FA − FI]). Model analyses suggested that α-pinene reacted within the leaf at higher temperatures, possibly within the lipid phase, thereby avoiding the decrease in diffusion gradient, FA − FI. Thus, these data contribute to the hypothesis of the antioxidative protection of leaf membranes during heat stress by monoterpenes. These data further suggest that fumigation with the relatively low atmospheric concentrations of monoterpenes that are occasionally observed during warm windless days in the Mediterranean canopies may significantly improve the heat tolerance of nonemitting vegetation that grows intermixed with emitting species.

Effects of Carbon Dioxide, Water Supply, and Seasonality on Terpene Content and Emission by Rosmarinus officinalis

Rosmarinus officinalis L. plants were grown under carbon dioxide concentrations of 350 and 700 μmol/mol (atmospheric CO2 and elevated CO2) and under two levels of irrigation (high water and low water) from October 1, 1994 to May 31, 1996. Elevated CO2 led to increasingly larger monthly growth rates than the atmospheric CO2 treatments. The increase was 9.5% in spring 1995, 23% in summer 1995, and 53% in spring 1996 in the high-water treatments, whereas in low-water treatments the growth response to elevated CO2 was constrained until the second year spring, when there was a 47% increase. The terpene concentration was slightly larger in the elevated CO2 treatments than in atmospheric CO2 treatments and reached a maximum 37% difference in spring 1996. There was no significant effect of water treatment, likely as a result of a mild low water treatment for a Mediterranean plant. Terpene concentration increased throughout the period of study, indicating possible age effects. The most abundant terpenes were α-pinene, cineole, camphor, borneol, and verbenone, which represented about 75% of the total. No significant differences were found in the terpene composition of the plants in the different treatments or seasons. The emission of volatile terpenes was much larger in spring (about 75 μg/dry wt/hr) than in autumn (about 10 μg/dry wt/hr), partly because of higher temperature and partly because of seasonal effect, but no significant difference was found because of CO2 or water treatment. The main terpene emitted was α-pinene, which represented about 50% of the total. There was no clear correlation between content and emission, either quantitatively or qualitatively. More volatile terpenes were proportionally more important in the total emission than in total content and in autumn than in spring.

Effect of arbuscular mycorrhizal (AM) colonization on terpene emission and content of Artemisia annua L.

Plant roots interact with a wide variety of rhizospheric microorganisms, including bacteria and the symbiontic arbuscular mycorrhizal (AM) fungi. The mycorrhizal symbiosis represents a series of complex feedbacks between plant and fungus regulated by their physiology and nutrition. Despite the widespread distribution and ecological significance of AM symbiosis, little is known about the potential of AM fungi to affect plant VOC metabolism. The purpose of this study was to investigate whether colonization of plant roots by AM fungi and associated soil microorganisms affects VOC emission and content of Artemisia annua L. plants (Asteraceae). Two inoculum types were evaluated: one consisted of only an arbuscular mycorrhizal (AM) fungus species (Glomus spp.), and the other was a mixture of different Glomus species and associated soil bacteria. Inoculated plants were compared with non-inoculated plants and with plants supplemented with extra phosphorus (P) to obtain plants of the same size as mycorrhizal plants, thus excluding potentially-confounding mycorrhizal effects on shoot growth. VOC emissions of Artemisia annua plants were analyzed by leaf cuvette sampling followed by off-line measurements with pre-concentration and gas chromatography mass spectrometry (GC-MS). Measurements of CO(2) and H(2)O exchanges were conducted simultaneously. Several volatile monoterpenes were identified and characterized from leaf emissions of Artemisia annua L. by GC-MS analysis. The main components identified belong to different monoterpene structures: alpha-pinene, beta-pinene, camphor, 1,8-cineole, limonene, and artemisia ketone. A good correlation between monoterpene leaf concentration and leaf emission was found. Leaf extracts included also several sesquiterpenes. Total terpene content and emission was not affected by AM inoculation with or without bacteria, while emission of limonene and artemisia ketone was stimulated by this treatment. No differences were found among treatments for single monoterpene content, while accumulation of specific sesquiterpenes in leaves was altered in mycorrhizal plants compared to control plants. Growth conditions seemed to have mainly contributed to the outcome of the symbiosis and influenced the magnitude of the plant response. These results highlight the importance of considering the below-ground interaction between plant and soil for estimating VOC emission rates and their ecological role at multitrophic levels.

Sensitivity of terpene emissions to drought and fertilization in terpene-storing Pinus halepensis and non-storing Quercus ilex

We studied the effects of water stress, fertilization and time course on foliar volatile terpene emission rates by Quercus ilex and Pinus halepensis in a garden experiment. The terpenes mostly emitted by both species were alpha-pinene, beta-pinene, beta-myrcene and Delta(3)-carene. P. halepensis emission rates (average 31.45 microg g(-1) DM h(-1)) were similar to those of Q. ilex (average 31.71 microg g(-1) DM h(-1)). The effects of drought (reduction to one-third of full watering) and fertilization (250 kg N ha(-1), 250 kg P ha(-1), or both) were different depending on the species: the drought treatment significantly increased the terpene emissions from Q. ilex by 33%, and the fertilization treatments reduced the terpene emissions from P. halepensis by 38%. Terpene emission rates increased with time course in parallel to raising summer temperatures in P. halepensis and Q. ilex, whose emission rates were temperature related (r = 0.42 and r = 0.68, respectively) and light related (r = 0.32 and r = 0.57, respectively). There was a positive relationship for P. halepensis, and a negative relationship for Q. ilex, between emission rates and relative water contents. No relationship was found between emission rates and N or P foliar concentrations. The results of this study show complex species-specific responses with stronger and faster short-term responses in terpene-non-storing than in storing species and indicate that terpene emissions may significantly change in the warmer, drier and more fertilized conditions predicted for the next decades in the Mediterranean region.

Effects of ozone concentrations on biogenic volatile organic compounds emission in the Mediterranean region

Abstract Measurements of air volatile organic compounds (VOCs) and ozone concentrations in different rural sites of Catalonia (NE Spain) were conducted during 1995 and 1996, and the effects of ozone concentrations on biogenic emissions of Mediterranean plants were studied in open top chambers. A significant positive relationship was found between tropospheric ozone and VOC concentrations, which followed seasonal (maximum in early summer and minimum in early winter) and geographical (slightly larger concentrations in interior than in coastal sites) patterns. Results in the open top chambers fumigation experiments showed species-specific responses. There was no significant effect of ozone on VOCs and terpene emission by Aleppo pines, Pinus halepensis L., but there was an order of magnitude increase in VOC emission with increasing tropospheric ozone concentrations (plus 40 nl L −1 ) in tomatoes, Solanum lycopersicum L. var. Tiny Tim. This response of tomato plants thus opens the possibility of a positive feedback for tropospheric ozone formation.

Short-term responses of terpene emission rates to experimental changes of PFD in Pinus halepensis and Quercus ilex in summer field conditions

Abstract The diurnal relationships of monoterpene emission with PFD and photosynthetic rates were studied in the Mediterranean trees Pinus halepensis , a terpene storing species, and Quercus ilex , a non-storing species, under summer field conditions. At morning, midday and evening, leaves were submitted to different irradiance levels by differentially shading them. Both species emitted large amounts of monoterpenes (about 20 μg g DM −1 h −1 ). The most emitted terpene by P. halepensis was Δ 3 -carene followed by β-myrcene, α-pinene and β-pinene. The most emitted terpene by Q. ilex was limonene followed by α-pinene and β-pinene. No clear correlation to temperature was found for Q. ilex emission within the diurnal range of 21–33°C, whereas P. halepensis emissions increased with the temperature. There was no consistent link between terpene emissions and PFD or photosynthetic rates for P. halepensis but there were significant relationships for Q. ilex . However, emissions by Q. ilex became inhibited at highest PFDs and during the course of the day when net photosynthesis decreased under summer drought. The study shows that the emission rates of both species are highly variable and that during a hot Mediterranean summer day (with limited water availability) the diurnal variation of emission is not only driven by the common light and temperature dependencies. Water stress, branch-to-branch variability and other influences must explain great part of the observed variability.