The Aspen FACE project has provided a unique experimental platform for investigating forest ecosystem responses to the rising concentrations of atmospheric CO2 and tropospheric O3. A hallmark of the experiment is the consistency of response of many ecosystem properties to the atmospheric treatments (Karnosky et al., 2003, 2005), including growth (Isebrands et al., 2001; Percy et al., 2002; Karnosky et al., 2005); leaf physiology (Noormets et al., 2001; Takeuchi et al., 2001); soil respiration and soil C cycling (King et al., 2001, 2004; Loya et al., 2003; Karberg et al., 2005); and soil N transformations and microbial dynamics (Larson et al., 2002; Holmes et al., 2003; Zak et al., 2003). The primary driver of many of these ecosystem-level responses to the experimental treatments is NPP. We hypothesized that NPP would be stimulated by elevated atmospheric CO2 and decreased by tropospheric O3. Combined fumigation was expected to result in NPP similar to that of the control. This analysis of 7 yr of NPP data largely supports these hypotheses.
Allometric modeling of biomass and NPP
Growth of the experimental forest communities of the Aspen FACE project compares well with growth of stands of similar age reported from sites in north-central Wisconsin, Minnesota and Alaska. After 7 yr growth, control stands of pure aspen at our site had total above-ground (wood + foliage) and below-ground (coarse + fine roots) biomass of 2758 and 591 g m−2, respectively. Ruark & Bockheim (1988) reported above- and below-ground biomass in naturally regenerated 8-yr-old aspen stands in north-central Wisconsin of 2500 and 1380 g m−2, respectively. The discrepancy in below-ground biomass was probably caused by residual root biomass from the previous stand in the study of Ruark & Bockheim (1988), whereas in our study cuttings were planted in root-free soil.
Alban & Perala (1990) reported average above-ground biomass of 2376 g m−2 from a series of sites 5 yr after harvest in northern Michigan and Minnesota. Paré & Van Cleve (1993) reported above-ground biomass of naturally regenerated aspen 14 yr after harvest near Fairbanks, Alaska of c. 5000 g m−2, roughly twice the age and biomass of our study. The agreement between our study and these published reports gives confidence that the Aspen FACE stands are representative of natural forests, and supports our allometric approach to estimating biomass.
Applying species- and site-specific biomass regressions to annual nondestructive measurements of all trees in the experimental plots at Aspen FACE will be valid for estimating biomass and NPP of wood and coarse roots for some time to come (perhaps with some additional destructive harvesting). However, the utility of the allometric approach for fine roots may be limited. There has been difficulty in developing stand-level scaling relationships between above-ground plant parts and soil core estimates of fine root biomass (Kurz et al., 1996; King et al., 1999). This is because of high spatial variation in root distributions, and extremely plastic fine root responses to differences in environmental conditions (Nadelhoffer, 2000; King et al., 2002; Pregitzer, 2002). In the current study, we partitioned a fraction of heart root biomass (determined allometrically) to fine roots based on measured root biomass partitioning from the destructive harvests in 2000 and 2002, of which the fine root sampling was much more rigorous in 2002. The fraction of total root biomass partitioned to fine roots varies with seasonal changes in fine root standing crop (Hendrick & Pregitzer, 1996; King et al., 2002) and stage of stand development (King et al., 1999). Hence, fine root biomass determined from our ‘static’ partitioning may or may not accurately reflect standing fine root biomass at a given point in time, and does not capture fine root production and turnover.
Similarly, allometric modeling of foliage biomass (NPP) at Aspen FACE has been valid for the early stage of stand development, but its utility will be limited in the future. Comparison of allometric estimates of stand-level foliage production (this study) with litter-trap estimates of litter production showed good agreement (R2 = 0.89) for the years 2001–3 (C. P. Giardina, unpublished). However, foliage biomass becomes ‘uncoupled’ from stem growth after canopy closure in young stands, and is inversely related to it in older forests (Ovington, 1957; Ford, 1984; Cannell, 1985; Gower et al., 1994; Miller, 1995). Collection of annual foliar litter production suggests the aspen and aspen–birch stands are approaching canopy closure; that is, the annual increment in litter production is decreasing (C.P.G., unpublished data). Therefore future stem growth may not be accompanied by proportional increments in foliage biomass, compromising the allometric approach.
Stimulation of NPP by elevated CO2
This analysis of 7 yr of growth data supports our first hypothesis, that elevated atmospheric CO2 (c. 550 ppm by volume) will cause sustained enhancement of forest NPP and biomass accumulation. This is consistent with the thousands of studies conducted at smaller spatial and temporal scales and across a wide variety of plant species over the past several decades (Strain & Bazzaz, 1983; Eamus & Jarvis, 1989; Ceulemans & Mousseau, 1994; Strain & Cure, 1994; Amthor, 1995; Curtis & Wang, 1998; Norby et al., 1999). Stimulation of total biomass accumulation by elevated atmospheric CO2 at Aspen FACE averaged 43% for all communities, although this response developed over time (significant CO2 × time interaction). This is higher than the average 25% growth enhancement reported for other forest FACE experiments (DeLucia et al., 1999; Hamilton et al., 2002; Norby et al., 2002; Calfapietra et al., 2003), and the average 31% stimulation from a meta-analysis of the earlier elevated CO2 literature (Curtis & Wang, 1998).
The large, sustained CO2 enhancement of NPP at Aspen FACE could have several causes. Because of the relatively high latitude of the site (45°40′ N), the soil is of recent glacial origin, with good chemical and physical properties for forest growth (Dickson et al., 2000). Analysis of soil N cycling from 1999 to 2003 (Holmes et al., 2003, 2005) suggests that soil N availability is not constraining growth responses to elevated CO2 at the Aspen FACE experiment. The north-temperate climate is mesic, with favorable site water balance for most of the year, because of low evaporative demand (calculated by King et al., 2001). A large fraction of the global forest C sink occurs in recently glaciated north-temperate and boreal forest ecosystems, where long-term C storage in soils is especially important (Schlesinger, 1997; Myneni et al., 2001). Therefore the nutrient limitation to sustained CO2 enhancement of forest NPP, as reported from low-latitude forests on highly weathered soils (Oren et al., 2001), may be less of a constraint at higher latitudes.
Additionally, the experimental stands at Aspen FACE are dominated by early successional species in the early stage of stand development, which confers greater growing space (less intertree competition) and greater productivity relative to older stands (Pregitzer & Euskirchen, 2004). This could provide the capacity for greater stimulation of NPP and other ecosystem properties in response to elevated CO2 relative to older, closed-canopy forests (King et al., 2004).
The stimulation of total biomass production at Aspen FACE was caused by proportional increases in all plant parts: roots, wood and foliage. Averaged across community type from 1997 to 2003, elevated CO2 caused 42, 45 and 41% increases in foliage, wood and coarse root biomass, respectively. Allometric analyses on an individual tree basis, using the harvest data from 2000 and 2002 and at the stand level, showed that elevated CO2 did not change biomass partitioning among plant parts (data not shown). This is consistent with our understanding of tree biomass partitioning responses to elevated atmospheric CO2 (Gebauer et al., 1996; King et al., 1996; Norby et al., 1999).
There were important differences in the magnitude of CO2 enhancement of component and total plant biomass production between communities, however. The order of relative response was generally pure aspen < aspen–paper birch < aspen–sugar maple; however, the order of absolute stand-level biomass production has been pure aspen > aspen–paper birch > aspen–sugar maple. In the pure aspen community, it is possible that intraspecific competition has constrained the potential stand-level relative growth enhancement in response to elevated atmospheric CO2. Interspecific competition in the aspen–birch community could possibly have allowed a greater overall growth response to elevated CO2. The aspen–maple community started out with smaller trees and therefore less intertree competition (intra- and interspecific competition was reduced), hence there was a greater capacity to respond to elevated atmospheric CO2.
McDonald et al. (2002) provide evidence that competitively advantaged trees in the pure aspen community at Aspen FACE show a greater relative growth response to elevated CO2 compared with competitively disadvantaged trees in an autoregressive manner (‘the big get bigger faster’). These results apparently scale to the level of the stand. It will be interesting to see how relative growth responses to the treatments change as the stands proceed through canopy closure, and intertree competition and mortality become more significant. More growing space in the young stands could contribute to the greater relative CO2 growth enhancement at Aspen FACE compared with the Duke (DeLucia et al., 1999; Hamilton et al., 2002) and Oak Ridge National Laboratory (Norby et al., 2002) experiments, which both have older, closed canopy forests. This is consistent with a recent synthesis of soil respiration results from the four forest FACE experiments, which found that the relative stimulation of soil respiration caused by elevated CO2 was greater in young, open-canopy forests compared with older, closed-canopy forests (King et al., 2004).
Decreased forest NPP from tropospheric O3
Our second hypothesis was that elevated tropospheric O3 (c. 1.5 × ) would decrease forest NPP, which was again supported by this analysis of 7 yr of growth data from the Aspen FACE experiment. This result is largely consistent with the literature but, importantly, we feel provides realistic quantification of the magnitude of the response for an important forest type in north-temperate and boreal forest ecosystems. Our understanding of O3 effects on vegetation is largely based on studies of crops or small trees grown in highly controlled environments for short periods (reviewed by Heck et al., 1984; Pye, 1988; Samuelson & Kelly, 2001; Andersen, 2003). These studies show that, in a wide range of plant species, tropospheric O3 causes almost universal reductions in crop yield or biomass production, but the magnitude of response has been highly dependent on experimental conditions. High variation in experimental results and uncertain correlation between visible foliar injury and yield reduction have led to considerable efforts to compare seedling responses with those of mature trees to determine appropriate factors for scaling O3 responses to the landscape (Chappelka & Samuelson, 1998; Matyssek & Innes, 1999; Samuelson & Kelly, 2001).
At Aspen FACE, chronic exposure to moderately elevated tropospheric O3 (c. 1.5×) has resulted in an average reduction in biomass production of 22, 12 and 16% in the pure aspen, aspen–birch and aspen–maple communities, respectively. These results are comparable with the average 23% decrease in tree seedling growth reported in the review of Pye (1988), but higher than the 2.6–6.8% decrease in annual NPP in the USA during the late 1980s to early 1990s from the modeling study of Felzer et al. (2004). Importantly, the response to O3 was modified by both community composition and time (significant O3 × community × time interaction). The pure aspen community was the most sensitive to O3 and maintained this sensitivity over time. The aspen–birch and aspen maple communities, however, appear to be losing sensitivity to O3 relative to the control.
Differences in community response could be caused by compensatory growth of less-O3-sensitive species (Pye, 1988; Broadmeadow & Jackson, 2000) in the mixed communities, or changes in O3 responsiveness induced by competition (McDonald et al., 2002; Liu et al., 2004). In the aspen–maple community, sugar maple comprises c. 9% of wood biomass, whereas in the aspen–birch community the two species are more evenly represented with no clear dominance of one over the other (data not shown). Hence compensatory growth of less-O3-sensitive species is unlikely to be the cause of the increased productivity over time. In a 2-yr phytotron study, Liu et al. (2004) observed that European beech experienced no reduction in total biomass production caused by elevated O3 when grown in monoculture. However, when grown in mixed culture with Norway spruce O3 caused a 32% reduction in beech biomass, and the spruce benefited (+13%) from the weak performance of its competitor. These results underscore the important fact that monospecific responses to O3 are not simply additive, and more realistic experimental designs are required to determine long-term ecosystem responses to the changing atmosphere. An important aspect of the Aspen FACE experiment will be to see if the mixed communities fully regain productive capacity under elevated O3.
As with elevated CO2, growth under tropospheric O3 does not appear to have altered biomass partitioning among the major plant parts, as there were no statistically significant shifts in root : shoot, foliage : branch or wood : coarse root ratios (data not shown). This finding apparently contradicts many earlier studies that show relative decreases in root growth under O3, which is thought to aid in the repair of damaged photosynthetic structures by increased C allocation above ground (Karnosky et al., 1996; Andersen, 2003). In our study, all plant parts became proportionally smaller under elevated O3. The exception to this is fine roots in the pure aspen section, which showed an average 44% stimulation in biomass. Possible causes include (i) spurious values among the three replicates for each treatment; (ii) confounding by abundant fine roots from herbaceous species that proliferated under the open canopies of the elevated O3 treatment; or (iii) it is a real effect. Fine root (<1-mm-diameter) biomass values for each replicate of the 2002 harvest upon which the static partitioning was based were 50.4, 48.1 and 34.0 g m−2, compared with an average 31.7 g m−2 for control plots at that time. If herbaceous roots were accidentally included in our estimates, the static partitioning used here would propagate the error through each year of biomass estimation. This is unlikely as all communities were harvested and processed at the same time using the same method. Sampling error could also have biased towards high root biomass estimates, but this is unlikely as 10 cores of 15 cm diameter × 25 cm deep were used in each split-plot FACE ring section. The only other fine root harvest at the site performed in 1999 did not detect significant effects of O3 on fine root biomass (King et al., 2001). In any case, this finding is highly counterintuitive, and requires further study before we can conclude that elevated O3 increases fine root biomass in young aspen ecosystems.
Tropospheric O3 compromises stimulation of NPP caused by elevated CO2
Our final hypothesis was that chronic exposure to elevated CO2 and elevated tropospheric O3 (+CO2, +O3) would result in forest NPP similar to that of the control. A putative ‘protective effect’ of elevated CO2 has been discussed (Allen, 1990; Wustman et al., 2003), in that decreased stomatal conductance under elevated CO2 might decrease the flux of O3 into the plant; there may be other protective mechanisms, such as responses of antioxidant enzymes (Rao et al., 1995). Our analysis partially supports this hypothesis. For total and component biomass production, the interaction between CO2 and O3 was never statistically significant. Thus elevated CO2 provided comparable stimulation to NPP at both levels of the O3 treatment in all communities over time. Because of the sensitivity of the aspen community to O3, however, total biomass production in this community was depressed for the first 3 yr of growth, after which it did not differ from the control. The aspen–birch and aspen–maple communities exhibited an average stimulation of total biomass production of 8 and 24%, respectively, under combined fumigation. Thus the large stimulation in biomass production all three communities experienced in response to elevated CO2 was completely annulled or greatly reduced by concurrent exposure to moderate levels of tropospheric O3.
Experiments using long-term exposure of trees to combined CO2 and O3 fumigation are beginning to show that responses to both gases are variable, depending on species/clone and provenance. However, the antagonistic effects on growth of elevated CO2 and tropospheric O3 have generally been observed in these experiments. Dickson et al. (1998) exposed five hybrid poplar genotypes to factorial treatments of CO2 and O3 in open-top chambers (OTC) for 1 yr, and found that plants exposed to combined fumigation (+CO2, +O3) had biomass similar to the control. Broadmeadow & Jackson (2000) grew seedlings of oak, ash and pine under factorial CO2 and O3 treatments in OTC for 3 yr. Elevated CO2 enhanced growth; O3 decreased it; and combined fumigation provided some protection from O3 in the order of species responsiveness: oak > pine > ash. In a 5-yr OTC experiment, Rebbeck & Scherzer (2002) found that yellow poplar growth was insensitive to O3 alone, but increased 60% with combined fumigation (+CO2, +O3) relative to the control, but not until the fifth season. Similarly, Riikonen et al. (2004) found that growth of two clones of silver birch responded negatively to O3, but only at ambient CO2. Tree growth increased under elevated CO2 and combined fumigation (+CO2, +O3) treatments. Together with our results these studies show that, in the long run, elevated CO2 provides some protection from exposure to phytotoxic concentrations of tropospheric O3 for a variety of forest tree species. However, this also means that gains in NPP that could be achieved under elevated CO2 are being compromised by tropospheric O3 pollution, and this has had continent-scale implications for C sequestration for some time (Felzer et al., 2004).
Because CO2 is chemically inert in the atmosphere, and human population growth and fossil energy consumption continue to increase, the concentration of atmospheric CO2 will continue to rise for the foreseeable future. Tropospheric O3 is highly reactive and was historically considered a regional pollutant. However, it is becoming apparent that the cumulative impact of industrialization around the globe is also raising the background concentration of this pollutant along with CO2. Our analysis of 7 yr of growth data at the Aspen FACE project, and decades of earlier research, indicate that the concentration of atmospheric CO2 expected for the year 2050 has the capacity to stimulate forest NPP. At least for young northern forests on glacial soils, this response does not appear to be constrained by nutrient or water limitations. However, the concurrent global rise in tropospheric O3 is damaging forest physiology and growth to the point that potential gains in terrestrial C sequestration caused by rising CO2 are partially or completely annulled. We conclude, therefore, that global monitoring of ambient O3 exposure of vegetation should become an important part of government environmental protection programs. Moving forward with technologies that remove important anthropogenic precursors to photochemical O3 formation (mainly oxidized forms of nitrogen) from automobile and industrial emissions would help to decrease concentrations of tropospheric O3 because of its short half-life in the atmosphere, decreasing at least one constraint on the capacity of forest ecosystems to sequester atmospheric C.