Ecological controls over monoterpene emissions from Douglas-fir – Pseudotsuga menziesii
Monoterpene emission by plants is one of the principal factors regulating the oxidative capacity of the atmosphere (Seiler and Conrad 1987, Singh and Zimmerman 1992). The annual rate of monoterpene emission from vegetation is estimated at 120-150 Tg/yr of carbon, representing [approximately]0.1-0.3% of global net primary productivity, and approximately one-half the sum of anthropogenic plus biogenic methane emissions. Unlike methane, however, monoterpenes are extremely reactive in the troposphere and so exist at very low atmospheric concentrations (Muller 1992). This high reactivity (primarily with hydroxyl radical and ozone in sunlight, and nitrate radical at night) gives monoterpenes a critical role in determining concentrations of tropospheric ozone and carbon monoxide (both important pollutants and greenhouse gases), in producing organic nitrates and weak organic acids, and in controlling the atmospheric lifetime of methane, another greenhouse gas (Jacob and Wofsy 1988). Despite the importance of this biogenic emission in atmospheric chemistry, relatively little is known of the biological controls over monoterpene emissions.
Monoterpenes are 10-carbon hydrocarbons produced by a variety of flowering plants (most commonly in the Myrtaceae, Asteraceae, and Lamiaceae) and nearly all conifers (Banthorpe and Charlwood 1982). They are synthesized through the mevalonic acid pathway and are stored internally, either in specialized ducts or canals, or externally in glandular hairs (Croteau 1987). Within plants, monoterpenes are part of the chemical defense system, functioning as feeding deterrents to many mammals and generalist insects (but see Raffa 1991 for a discussion of adaptations by specialized insects), and as solvents for higher molecular weight hydrocarbons and organic acids (Hanover 1966, Berryman 1972, Loomis and Croteau 1973, Lorio 1986, Lewinsohn et al. 1993).
Previous studies of monoterpene emissions have concentrated on the effects of leaf temperature upon emissions over the time scale of minutes to days (Tyson et al. 1974, Dement et al. 1975, Zimmerman 1979, Tingey et al. 1980, 1991, Lamb et al. 1985, Guenther et al. 1991, 1993, Janson 1993). These studies have shown that temperature effects are sufficient to explain short-term variations in monoterpene emissions from any individual plant; they have not, however, addressed questions of why different plants, even of the same species, often have different emission rates at the same temperatures, or why emissions vary seasonally (Flyckt 1979, Yokouchi and Ambe 1984).
One factor that could cause between-plant variation in monoterpene emission rate is the difference in concentration within plant tissues (Lerdau 1991, Tingey et al. 1991). Concentration could affect emissions both by directly affecting partial pressure in the vapor phase according to Henry’s Law, and by affecting diffusion as the monoterpenes move from the resin canals to intercellular air spaces; concentration is linearly related to diffusion rate across a surface. An increase in diffusion rate from the resin canal to the interior of the leaf would lead to an increase in the vapor pressure gradient from leaf to atmosphere.
A number of factors can control chemical concentrations in plant tissues, including production and turnover rates. Because monoterpenes are defensive compounds, controls over their production can be evaluated in terms of resource allocation theory. This body of theory deals with the controls of plant allocation of resources to different types of compounds, e.g., resource gathering (photosynthetic tissues) and resource protecting (defensive compounds). The carbon/nutrient balance hypothesis (C.N.B.H.) (Bryant et al. 1983) and the growth differentiation balance hypothesis (G.D.B.H.) (Loomis 1932, as cited in Lorio 1986) both address how the relative availabilities of resources affect their allocation to the production of new tissue and to the defense of existing tissues. The C.N.B.H. predicts that when a resource, such as nitrogen, is scarce, a plant will allocate proportionately more of an abundant resource, such as carbon, to the acquisition of the scarce resource, and also will use the abundant resource in the construction of defense. When nitrogen is abundant, a plant will allocate less carbon toward defense and more toward growth. The G.D.B.H., in contrast, uses two physiological assumptions: (1) that whenever all necessary resources for growth are available, growth processes will be favored over defensive compound production, and (2) that growth is more sensitive to the availability of belowground resources than is assimilation of new carbon. From these assumptions comes the prediction that when nitrogen is moderately scarce, growth will be more constrained than carbon fixation, leading to a surplus of carbon and, thus, an increase in the allocation of carbon to defense.
These theories suggest that differences in the relative availability of carbon, water, or nitrogen should cause differences in allocation to growth (cell division and enlargement) and defense. As such, they provide a framework for evaluating the factors controlling variability in plant monoterpene pools and emission rates. To date, however, the studies that have used defense theories to examine the relationship between monoterpene concentrations and variations in light, nutrient, or carbon dioxide availabilities have found conflicting results. Some found the predicted negative relationship between resources and monoterpene concentrations (Clark and Menary 1980, Mihaliak and Lincoln 1985, 1989, Mihaliak et al. 1987). Others showed no relationship between nitrogen availability and monoterpene concentrations (Muzika et al. 1989, Johnson and Lincoln 1990, Reichardt et al. 1991) Two studies have shown a positive relationship between nitrogen and monoterpene concentrations (Bjorkman et al. 1991, McCullough and Kulmon 1991). Each of these studies examined monoterpene concentrations at one point in time; none, however, examined the relationship in the context of plant phenology or seasonality.
Seasonal variations in allocation to monoterpenes might be expected because a plant’s capacity for growth changes seasonally. In fact, seasonal variations in monoterpene emissions have been found previously in conifers, but the mechanisms underlying these changes were not explored (Flyckt 1979, Yokouchi and Ambe 1984). While some plants, i.e., annuals, grow for most of their lifetime, many plants have only a brief period of leaf expansion each year. During leaf expansion, there is a trade-off between allocation to growth and to defense. However, during the rest of the year, when growth is constrained because of factors other than resource availability, allocation to a mobile defense such as monoterpenes does not represent a cost in terms of foregone growth. Given this, the predictions of plant defense theories might best be fulfilled during those times of the year when growth and defense are in competition for resources.
This paper explores the roles that nitrogen availability and phenology play in monoterpene concentrations, and the relationship between concentrations and emissions in 3-yr-old Douglas-fir (Pseudotsuga menziesii Fran), a coniferous tree. Nitrogen is examined because its availability constrains growth in many coniferous forest ecosystems.
MATERIALS AND METHODS
Seedlings of Douglas-fir were planted in 4-L pots with a soil-free mixture (1:1:1 by volume) of mont-morillonite clay, Turface, and Perlite. When plants were 2 yr old, they were transplanted into 10-L pots to minimize root binding. Plants were grown in greenhouses with controlled temperature (15 [degrees]-20 [degrees] C days, 10 [degrees]-15 [degrees] nights), under natural lighting and daily watering.
Three nitrogen fertilization levels were applied to the seedlings. All plants received a common, half-strength, modified Hoagland’s nitrogen-free fertilizer solution three times weekly; ammonium nitrate was added to the solution to result in 1, 5, and 16 mmol/L concentrations. The 4-L pots received 250 mL of nutrient solution, and the 10-L pots received 625 mL. Plants were arranged in the greenhouse in a completely randomized design and were re-randomized each week. The fertilizer treatments were applied for 2 yr, and all measures were made on fully expanded needles that had expanded under the nitrogen treatment.
Measurements of monoterpene tissue concentration, monoterpene emission, foliar nitrogen, and photosynthesis were made at four times of the year during distinct phenological stages: (1) March, pre-budbreak in the spring, PBB; (2) May, during leaf expansion, LE; (3) September, when new needles were fully expanded and assimilating carbon, AC; (4) December, when plants in the field were predicted to be in winter dormancy, WD. At each phenological stage, except for leaf expansion, all measures were made within 5 d of each other and the order of plants measured was randomly determined. During leaf expansion, the high-nitrogen plants broke bud first and so were measured first, followed by intermediate-nitrogen plants, and then low-nitrogen plants.
Photosynthesis was measured on branches enclosed in a cuvette with a flow-through gas exchange system as described in Monson and Fall (1989). Leaves were enclosed in the cuvette, temperature was held constant at 30 [degrees], and light levels were stepped from 1100 [[micro]mol][center dot][m.sup.-2][center dot][s.sup.-1] down to 50 [[micro]mol][center dot][m.sup.-2][center dot][s.sup.-1]. Leaves were maintained at each light level until photosynthetic rates had stabilized. Leaf areas were determined using a Delta-T leaf area meter. Photosynthetic rates could then be expressed on a unit leaf area basis because the needles of Douglas-fir are essentially flat and projected in a planar manner.
Nitrogen concentration was determined for tissue dried at 60 [degrees]. Samples were digested with a block digestion using a sulfuric acid-mercuric oxide catalyst. The digests were then analyzed on an Alpkem (Clackamas, Oregon) auto-analyzer with Alpkem method A303-d071-00 REV. B and N.I.S.T. certified pine standards used for calibration.
Tissue monoterpene concentrations were determined by collecting the tissues from which the emission measures had been made, freezing at -70 [degrees], grinding under liquid nitrogen, and extracting in pentane (Hall and Langenheim 1986). Extracts were stored at 4 [degrees] for 1-3 wk and then analyzed by gas chromatography using a flame-ionization detector. Chromatographic analysis was performed with a Shimadzu-14 (Shimadzu Corporation, Tokyo, Japan) gas chromatograph with a fused silica capillary column (SE-54 (Alltech, Deerfield, Illinois), 30 m x 0.25 mm inside diameter). Helium was used as a carrier gas at a linear velocity of 25 cm/min. The oven temperature was 70 [degrees] isothermal for 5 min, increased by 6 [degrees]/min to 220 [degrees]C. The injector was at 200 [degrees] and the detector at 250 [degrees]. Concentrations were determined by adding a known amount of an internal standard, tri-decane, during the extraction process. Peaks were identified by comparison to reagent-grade authentic external standards (from Sigma Chemicals, St. Louis, Missouri) and gc-ms (gas chromatography-mass spectrometry), using identical chromatographic techniques and a quadrupole mass spectrometer at 70 eV ionizing potential.
Monoterpene emissions were measured by enclosing branches in a temperature- and light-controlled cuvette with a flow-through gas exchange system (modified from Monson and Fall 1989). The modifications involved using a water-jacketed cuvette, rather than a peltier plate, for temperature control and an incandescent, rather than a metal halide, lamp as a light source. All measures were made at 30 [degrees] and a light intensity of 350 [[micro]mol][center dot][m.sup.-2][center dot][s.sup.-1]. Hydrocarbon-free air was passed through the cuvette and water was removed from the exiting air stream using a cold trap at -40 [degrees]. The exiting air was then passed through a Teflon loop immersed in liquid nitrogen to trap monoterpenes cryogenically. The resulting preconcentrated sample was flash-heated at 100 [degrees] and automatically injected onto a 30 m x 0.25 mm interior diameter polyethylene glycol stationary phase column (DBTM-Wax, J & W Scientific, Folsom, California). Chromatographic analysis was performed with a model 5790A gas chromatograph (Hewlett-Packard, Palo Alto, California) with hydrogen as a carrier gas. Analyses were performed isothermally at 60 [degrees] with the injector at 200 [degrees] and the detector at 250 [degrees]. Peak areas were related to monoterpene quantities by injecting known quantities of hydrocarbons onto the column. Peak identifications were made by comparison to authentic external standards (Sigma Chemicals, St. Louis, Missouri).
Statistical analyses were done using a two-way ANOVA [nitrogen treatment x sample time] with N = 60 [three nitrogen levels x four sampling times x five replicates], calculating the minimum significant difference, and using Tukey’s honestly significant difference method (Sokal and Rohlf 1981:242-247) to determine significant differences (at the 0.05 level) between means. All analyses were performed using SYSTAT 5 for Windows.
Maximum photosynthetic rate (Amax) increased with nitrogen fertilization [ILLUSTRATION FOR FIGURE 1 OMITTED]. The nitrogen effect on photosynthetic rate was evident at all sampling periods; each fertilization treatment showed significantly different photosynthetic rates at light levels [greater than]700 [micro]mol[center dot][m.sup.-2][center dot][s.sup.-1]. Photosynthetic rates did not vary significantly within a treatment or among sampling times. Nitrogen concentration in the needles also followed the fertilization pattern. The high-N plants always had higher N concentrations than did the low-N plants, but the intermediate-N plants showed more variability [ILLUSTRATION FOR FIGURE 2 OMITTED]. There was no consistent variation in nitrogen concentration among seasonal samplings [ILLUSTRATION FOR FIGURE 2 OMITTED].
Eleven different monoterpenes were found consistently in tissue extracts: camphene, tricyclene, [Alpha]-pinene, [Beta]-pinene, sabinene, [Delta]-carene, myrcene, limonene, [Beta]-phellandrene, [Gamma]-terpinene, and terpinolene. For all plants studied, however, [Beta]-pinene, [Alpha]-pinene, and [Delta]-carene composed [greater than]80% of the monoterpene pool and 95% of the emissions; thus, only results for these three compounds will be presented.
Tissue monoterpene concentrations varied both seasonally and with nitrogen fertilization level, with significant interactions between nitrogen level and season (F = 6.88 summed for all compounds, P [less than] 0.01; Fig. 3). Within a fertility treatment and across sampling periods, the low-nitrogen plants had significantly lower concentrations during the pre-budbreak measures and then were relatively constant at all other seasons (P [less than] 0.05 for each compound, Tukey’s hsd). The high-nitrogen plants, in contrast, decreased significantly from the pre-budbreak to the leaf expansion period and then returned to near their pre-budbreak levels for the rest of the year (P [less than] 0.05 for each compound, Tukey’s hsd). The intermediate-nitrogen plants did not show seasonal changes in monoterpene concentrations (P [greater than] 0.1 for each compound, Tukey’s hsd).
As a result of these seasonal variations, the effects of leaf nitrogen concentration on monoterpene concentrations depended upon the phenological stage in which the plants were measured. Before budbreak in the spring, concentration of foliar nitrogen was directly related to monoterpene concentration ([r.sup.2] = 0.96; Fig. 3). During leaf expansion, however, the high-nitrogen plant had significantly (P [less than] 0.05 for each compound, Tukey’s hsd) lower monoterpene concentrations than did the medium or low nitrogen. In the late summer, after leaf expansion, the high-nitrogen plants had significantly higher monoterpene concentrations than the low- or medium-nitrogen plants (P [less than] 0.05 for each compound, Tukey’s hsd). For the winter sampling, there was no relationship between nitrogen availability and monoterpene concentration (P [greater than] 0.1 for each compound, Tukey’s hsd).
There was a direct relationship between monoterpene foliar concentrations and emission rates ([r.sup.2] [greater than] 0.65 for each compound; Fig. 4). This relationship suggests that, for any one plant at any one time, basal emission rate (emission rate at a prescribed temperature) was determined by the foliar monoterpene concentration.
Furthermore, monoterpene emissions followed seasonal and nutritional effects similar to those shown by monoterpene concentrations (F = 7.03 summed for all compounds, P [less than] 0.01; Fig. 5). Low-nitrogen plants had their lowest emissions during the pre-budbreak measures and then were relatively constant at all other seasons (P [less than] 0.05 for each compound, Tukey’s hsd). The high-nitrogen plants decreased from the pre-budbreak to the leaf expansion period and then returned to near their pre-budbreak levels for the rest of the year (P [less than] 0.05 for each compound, Tukey’s hsd). The intermediate-nitrogen plants did not show seasonal changes in monoterpene emissions (P [greater than] 0.1 for each compound, Tukey’s hsd). When leaves were not expanding, nitrogen fertilization was directly related to monoterpene emissions ([r.sup.2] = 0.94; Fig. 5). During leaf expansion, however, the high-nitrogen plants had significantly lower emission rates than the low- and medium-nitrogen plants (P [less than] 0.05 for each compound, Tukey’s hsd; [ILLUSTRATION FOR FIGURE 5 OMITTED]).
Resource availability and monoterpene concentration
The results reported here demonstrate that monoterpene concentrations in fully expanded needles in Douglas-fir can show large seasonal changes, as has been shown in Picea (Schonwitz et al. 1990) and sequoia (Hall and Langenheim 1986). High-nitrogen plants show a decline in monoterpene concentrations during leaf expansion; low-N plants show an increase in concentrations, and intermediate-N plants show little change in monoterpene concentrations. After the cessation of leaf expansion, monoterpene concentrations in all plants return to the pre-budbreak levels. We conclude that these patterns of monoterpene concentration are controlled by an interaction between resource availability and seasonal changes in plant growth demand.
This study agrees with the predictions of the plant defense theories discussed earlier (the resource availability hypothesis and the growth-differentiation balance hypothesis), when seasonal changes in plant demand are taken into account. Perennial plants that exhibit growth during a restricted time frame following budbreak might be expected to show an inverse relationship between nitrogen availability and allocation to mobile carbon-based defenses only during periods of growth. At other times of the growing season, growth demands for carbon and nitrogen would not be strong enough to influence patterns of monoterpene synthesis and associated pool size. Plants such as annuals that grow throughout most of their lifetimes, on the other hand, would be expected to generate continuous demands on carbon and nitrogen resources; these plants probably fit within the G.D.B.H. and C.N.B.H. for all or almost all of their lifetimes.
Our results suggest that growth demand for carbon may be linked to nitrogen availability; low-N plants would have reduced carbon demand because of N limitations. This would obviate the need to mobilize carbon that is stored in the monoterpene pool and may be the reason that we see a decrease in monoterpene concentrations after budbreak only in the high-N trees. Thus, we find that when the C.N.B.H. and G.D.B.H. are considered in the light of growth demand, they serve to predict changes in concentrations of monoterpenes.
The positive relationship between monoterpene concentration and emission suggests that variations in emissions at a constant temperature are due to concentration-induced variations in monoterpene vapor pressure gradients from the leaf to the atmosphere. The results of this study do not distinguish between the effect of concentration on partial pressure in the vapor phase and the effect of concentration on liquid phase diffusion of monoterpenes within the needles. Both possibilities would be expected to generate a positive relationship between concentration and emission. This relationship suggests that knowledge of concentration is sufficient to predict relative emissions rates, thus simplifying the development of emissions inventories (Lamb et al. 1993). The impact of concentration upon emission does not preclude other biological parameters from affecting emissions as well. For example, leaf or needle structure could affect the diffusive resistance to monoterpene flux, and is possibly an important emission control parameter.
The nitrogen availability-phenology-concentration relationship and the concentration-emission relationship come together to generate predictable nutritional and temporal patterns of emissions. High-nitrogen sites should have plants with higher monoterpene concentrations for most of the year (except during the period of leaf expansion). These differences in concentrations, particularly during the warm summer months when most emissions occur, should result in higher monoterpene emissions and could underlie the variations in emissions found in previous studies (Fehsenfeld et al. 1992). Most recent studies on monoterpene emissions have focused on the influence of temperature upon emissions (Tingey et al. 1981, 1991, Lamb et al. 1985, Guenther et al. 1991, 1993, Janson 1993), but they have not examined the sources of variation in emissions at constant temperatures. We suggest that such variations in baseline emissions rates result from differences in concentrations that reflect variations in nutrient availability and plant function.
An additional consequence of variation in nitrogen availability that must be considered in estimating monoterpene emissions on a stand level is the effect of N on foliar biomass. Many coniferous forests are N-limited in their growth, and increases in N availability often lead to increases in foliar biomass (Turner and Olson 1976, Miller 1981). Increases in foliar biomass will lead to higher emissions on a per unit ground area basis. This study indicates that during times of the year when leaves are not expanding, this effect will be compounded by the effect of N on monoterpene concentrations.
This conceptual framework for viewing monoterpene emissions should aid in understanding and estimating emissions in several ways. First, it provides an approach for estimating regional variations in emissions that result from variations in N availability related to soil and climatic characteristics, and should thus aid in the development of ecologically-based budgets and models (Matson and Vitousek 1987). Secondly, it provides a basis for examining the potential effects of anthropogenic changes in nitrogen fertilization on monoterpene emission. For example, inadvertent deposition of anthropogenic nitrogen adds up to 20 Tg N/yr globally, with large potential effects on terrestrial and aquatic ecosystems (Lovett and Kinsman 1990, Aber 1992, Vitousek and Matson 1993). These nitrogen additions may affect the amount of biomass that produces monoterpenes (Turner and Olson 1976, Aber et al. 1993) as well as the concentration of monoterpenes in foliage, and, hence, the baseline emission rates per unit of biomass. Nitrogen fertilization of terrestrial ecosystems could thus be causing compounded increases in monoterpene emissions, with consequences for regional tropospheric photochemistry and the atmospheric lifetime of methane. Global databases on soil nitrogen exist and have been recently used in ecosystem models of carbon gain (Post et al. 1985, Potter et al. 1993). These models could be modified to incorporate the emissions-nitrogen relationships explored here and the climate-emissions relationships, as developed by Guenther et al. (1993), to reduce the uncertainty in current emissions estimates. An ecological approach to the study of monoterpene emissions may allow both better understanding of regional variations in emissions and prediction of how monoterpene emissions will change as ecosystems respond to environmental perturbations.
We thank Larry Cool, Jim Greenberg, Doug Turner, Bob MacDonald, and Pat Zimmerman for assistance and advice in sample analyses. Zoe Cardon, Chris Field, Jon Gershenzon, Hal Mooney, Peter Vitousek, and three reviewers provided helpful comments on earlier drafts. Sean Craig assisted with the statistical analyses. We were supported during this research by NSF and NASA pre doctoral fellowships (M. Lerdau), by a NASA Ames/Stanford dissertation improvement grant (M. Lerdau), and by NSF grant ATM-9312153 (R. Fall).
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