Monoterpene emission responses to elevated CO<sub>2</sub> in a Mediterranean‐type ecosystem (2003)

Anthropogenic emissions have caused a 30% increase in atmospheric CO2 concentrations since the beginning of the industrial revolution. It is becoming clear that the terrestrial biosphere plays an important role in regulating atmospheric CO2 concentration (Woodward, 2002), and that the continued increases in atmospheric CO2 concentrations may directly affect growth, transpiration and the production of secondary metabolites of terrestrial ecosystems. Mediterranean-type ecosystems are predicted to be especially sensitive to increasing CO2 and global climate change (Strain & Bazzaz, 1983; Oechel et al., 1995) but their response remains largely unexplored. In particular, the role of rising CO2 in the emission of biogenic volatile organic compounds (BVOC), such as isoprene and monoterpenes, is a subject of active debate since the production of these trace gases by the vegetation is of importance for local and regional tropospheric ozone pollution, and yields relatively nonvolatile secondary oxidant products that form aerosols (Griffin et al., 1999; Pio et al., 2001). Here we evaluate, in situ, the CO2 response of a regenerating chaparral ecosystem exposed to CO2 concentrations ranging from preindustrial to 750 mol mol−1 for an extended period of time. This ecosystem is dominated by the resprouting shrub species Adenostoma fasciculatum, the most common species of the southern California chaparral, and the obligate seeder, Ceanothus greggii, a nitrogen fixer. The approach used in these experiments provided an efficient system to assess the effects of rising atmospheric CO2 on natural Mediterranean ecosystems both in terms of carbon uptake and the emission of volatile organic compounds. Biogenic emissions are of particular relevance in an environment characterized by high temperature and high radiation, typical of regions with Mediterranean-type climates (Fehsenfeld et al., 1992; Oechel et al., 1992; Winer et al., 1992; Guenther et al., 1995; Seufert et al., 1995; Poisson et al., 2000; Thunis & Cuvelier, 2000). These areas are often highly populated because of the favorable climatic conditions and, accordingly, are already known to be major source of anthropogenic pollutants capable of promoting the chemical transformation of BVOCs, leading to photochemical pollution. It is therefore important to better estimate the BVOC emissions in a future CO2 enriched world because an increase in hydrocarbon emission could have serious consequences leading to enhanced tropospheric ozone formation. The effect of higher than ambient CO2 concentrations on BVOC emission is still unclear. Short-term exposure to elevated CO2 has been shown to reduce (Monson & Fall, 1989; Loreto & Sharkey, 1990) or not affect the emission of isoprenoids in laboratory studies (Loreto et al., 1996) whereas long-term exposure to elevated CO2 reduced isoprene emissions in aspen but enhanced emissions from oaks (Sharkey et al., 1991; Staudt et al., 2001). Loreto et al. (2001) reported that the overall emission of monoterpenes from holm oak grown in the field in open-top chambers was inhibited, at the leaf level, while monoterpene emission exhibited no response to elevated CO2 in coniferous trees grown under similar conditions (Constable et al., 1999a). Similarly, long-term exposure to high atmospheric concentration of CO2 did not significantly affect the actual isoprenoid emission from Quercus spp. grown in springs with a naturally high CO2 environment (Rapparini et al., 2003). The study site took place at the Sky Oaks Biological Field Station (33°23′ N, 116°37′ W), located in Southern California, USA, at about 1420 m elevation and 75 km from the coast. Major shrubs present include Adenostoma fasciculatum and Ceanothus greggii. A. fasciculatum is the dominant species (70%) in California chaparral. This natural plant community was exposed for 4 consecutive yr to CO2 concentrations from preindustrial (250 mol mol−1) to double ambient (750 mol mol−1) in 100 mol mol−1 increments (n = 2) in naturally lit null-balance chambers (Tissue & Oechel, 1987; Grulke et al., 1990; Oechel et al., 1992). The computer-controlled glasshouse system consisting of 12 closed chambers was configured to track average ambient conditions, except for the variable of study (CO2). The size of each chamber (2 × 2 × 2-m) was adequate to enclose a representative sample of vegetation for gas exchange and other ecosystem processes. The CO2 treatment started in December 1995. Both diurnal and seasonal patterns of Net Ecosystem Exchange CO2 (NEE; carbon sequestration or loss) were accurately tracked with this system. Measurements of the volatile organic compounds were made by collecting 2–3 l of the air surrounding the vegetation grown inside the chambers at a flow rate of 100 ml−1 min−1 into two-stage glass traps consisting of glass tubes filled with Carbograph 1 and Carbograph 2 particles (LARA, Rome, Italy). Samplings were carried out in the morning, at midday and in the afternoon to follow the diurnal course of the emissions and repeated for three days in June and December. The trapped compounds were then analyzed by thermal desorption gas chromatography mass spectrometry. A detailed description is given in Baraldi et al. (1999) and Rapparini et al. (2001). The BVOC emission rates were expressed per unit ground area. To detect the influence of CO2 concentration on BVOC emission and NEE, the regression analysis was performed with SAS (SAS System 8.1, SAS Institute Inc., Cary, NC, USA). During the measurement periods, NEE responded to increasing CO2 concentrations (Fig. 1) with a positive linear response (r2 = 0.81 and r2 = 0.85 P < 0.0001 in December and June, respectively). The ecosystem was a sink for carbon at the highest CO2 concentration in both winter and summer but when exposed to subambient and ambient CO2 concentration, it was a small sink in June and a source in December. NEE strongly declined toward the end of the growing season as also observed in other ecosystems (Hättenschwiler & Körner, 1996; Maurer et al., 1999). NEE of the chaparral during the summer was almost doubled when the atmospheric CO2 concentrations were raised from preindustrial to current ambient levels. Ecosystem CO2 uptake was further enhanced in response to an increase of atmospheric CO2, from current levels (350 mol mol−1) to 750 mol mol−1. These results are consistent with previous observations made in tropical species where the net ecosystem carbon-exchange rates were almost doubled under elevated CO2 (Körner & Arnone, 1992). They contrast with those reported for a tussock tundra and alpine grassland, where complete downward adjustment of NEE developed after 3 or 4 years of exposure to elevated CO2 (Oechel et al., 1994; Körner et al., 1997). The effect of CO2 concentrations on NEE (circles) and overall monoterpene emissions (triangles) measured at different hours of the day in December 1999 and June 2000. As expected, monoterpenes were the main biogenic hydrocarbons emitted by the plants with only traces of isoprene (Winer et al., 1992). Eighteen different compounds were identified with α-pinene, camphene, β-myrcene, ρ-cymene and limonene, accounting for more than 70% of the total emission independently of the season (Table 1). The differences in relative contribution of each compound were not statistically significant with respect to CO2 concentration (data not shown). Compositional changes, mainly attributed to interactions among environmental variables and plant phenological processes, were observed essentially for β-myrcene and ρ-cymene, which enriched the emission profile in June while limonene proportion in the chaparral emission significantly decreased. However, the changes in overall type of emission profile were small compared to temporal variation in emission rates. In winter, with maximum photosynthetically active radiation (PAR) of 1200 mol m−2 s−1 and temperatures ranging from 0 to 14°C, total trace gas emissions expressed on a ground area basis were low (mean = 1.04 × 10−2 mg C m−2 h−1) and did not respond to increasing CO2 concentrations (Fig. 1). In June, with higher light levels (PAR maximum of 2000 mol m−2 s−1) and warmer temperatures (ranging from 15 to 30°C), BVOC emissions were of an order of magnitude greater than during winter (mean = 0.21 mg C m−2 h−1), but still the different levels of CO2 did not affect the emission rates. Temperature and light intensity strongly contributed to the observed seasonal fluctuations of BVOC, as well as the physiological activity and development of the plants. The enhancement of emission in summer and the inhibition in winter may be correlated with the activity of monoterpene synthases in the leaf (Fischbach et al., 2002) as well as with leaf development since emission capacity tends to decrease with increasing leaf age (Staudt et al., 2003). According to simulation studies on Mediterranean emitting species lacking specialized terpene-storage compartments, the nonspecific-storage effects and the physico-chemical characteristics of volatile monoterpenes significantly alter the long-term emission dynamics at both leaf and canopy scale in different environmental conditions (Niinemets & Reichstein, 2002). The overall carbon loss caused by monoterpene emission was negligible, ranging from 0.002 to 0.3% of the net carbon gain at the ecosystem level in winter and summer, respectively. The detected C-uptake enhancement under elevated CO2 did not translate into a significant change of BVOC emission. On the other hand, simulations with a physiological algorithm, coupling leaf photosynthetic characteristics to monoterpene emission (Niinemets et al., 2002), and laboratory experiments (Loreto et al., 1996) indicated that the monoterpene emission rates respond less to changes in ambient CO2 than the net assimilation rates. Previous works made at leaf (Sharkey et al., 1991; Loreto et al., 2001) and whole-ecosystem level (Rosenstiel et al., 2003) showed that BVOC emission may be reduced under elevated CO2 in response to an enzymatic and biochemical down-regulation. This is only apparently in contrast with our findings as in our case both the direct CO2 effects on BVOC emission at the leaf level and the indirect effects on leaf area and total plant biomass were considered. It is possible that under increasing CO2 concentration, in spite of pronounced daily and seasonal variations of monoterpene emission, BVOC emission can remain nearly constant as rising CO2 reduces emission per unit leaf area while stimulating biomass growth and leaf area per unit ground area. This would suggest the occurrence of a homeostatic adjustment of BVOC emission in Mediterranean-type vegetation in response to rising CO2 concentrations, even if such a hypothesis does not consider that this vegetation type often experiences multiple stresses such as high temperature/light and water shortage, which may counteract the inhibitory leaf level effect of elevated CO2 on BVOC emission (Loreto et al., 2001; Rapparini et al., 2003). Increases in temperature (Loreto et al., 1996; Constable et al., 1999a; Peñuelas & Luisià, 2001) and changes in plant species composition of Mediterranean-type ecosystems with climate change, which could alter the composition of BVOC emitting species to relatively nonemitting species, might also have effects on chaparral BVOC emissions under future conditions (Constable et al., 1999b). This research was supported by the US Department of Energy's Office of Science through its Program for Ecosystem Research and through the Western Regional Center of its National Institute for Global Environmental Change, by Southern California Edison, Electric Power Research Institute (EPRI), San Diego State University, and by the San Diego State University Foundation. Sampling and analysis of BVOC emissions were supported by the National Research Council (CNR) of Italy and by the EC-Environment project EVK2-CT-1999–00042 (Future-VOC). This support is gratefully acknowledged. We also thank Baosheng Liang for assisting with BVOC analyses.