1. Department of Biological Sciences, University of Nevada, Las Vegas, Nevada 89154-4004 , USA
2. Department of Biochemistry, University of Nevada, Reno, Nevada 89557, USA
3. Division of Earth and Ecosystem Sciences, Desert Research Institute, Reno, Nevada 89512 , USA
4. Division of Earth and Ecosystem Sciences, Desert Research Institute, Las Vegas, Nevada 89119, USA
5. Department of Environmental and Resource Sciences, University of Nevada, Reno, Nevada 89557, USA
6. Present address: Department of Environmental, Population, and Organismal Biology, University of Colorado, Boulder , CO, 80309, USA.

Correspondence to: Stanley D. Smith¹ Correspondence and requests for materials should be addressed to S.D.S. (e-mail: Email: ssmith@ccmail.nevada.edu).

The well documented increase in atmospheric CO₂ concentration ([CO₂]) acts to increase photosynthesis, plant biomass and plant water-use efficiency in many plant species⁵. Primary production in deserts is strongly limited by water and nitrogen resources³. Conceptual models predict that desert ecosystems will be the most responsive to increased [CO₂] because the strong response of water-use efficiency in plants alleviates water limitations to primary production^{1, 2}. In addition, differences among species in their response to elevated [CO ₂] can modify competitive interactions, potentially changing community composition. For example, the dominance of the exotic grass species Bromus tectorum (cheatgrass), which has invaded many thousand hectares in western North America, may be enhanced by elevated [CO₂] and thus alter competitive balance and the fire cycle in semi-arid shrub-steppe environments^{6, 7, 8}. If these predictions are realized, biodiversity in arid and semi-arid ecosystems could be significantly reduced, which in turn might alter ecosystem processes such as primary production, nutrient dynamics and landscape water balance⁹.

To examine the response of a desert ecosystem to elevated [CO₂], we established the Nevada Desert FACE (free-air CO₂ enrichment¹⁰) Facility (NDFF) in an undisturbed Mojave Desert ecosystem within the Nevada Test Site of southern Nevada, USA⁴. The climate is arid, with most precipitation occurring as rain during winter months. The NDFF is located within a desert scrub community (< 20% total perennial cover) dominated by the evergreen shrub Larrea tridentata (creosote bush) and several species of deciduous shrubs. Perennial grasses are also common on the site, and dense stands of winter annuals occur in response to significant winter rains.

We have continuously maintained [CO₂] at a 550 mol mol ^-1 (p.p.m.) set point in three 23-m diameter experimental plots since April 1997, while maintaining three other plots at ambient [CO₂] and three control plots without the FACE apparatus. Elevated CO₂ treatment occurs 24 h d^-1, except during high winds (5-min average wind speed > 8 m s^-1) or at low air temperature (< 3 °C)⁴. CO ₂ treatment occurred 93% of the time when air temperature exceeded 3 °C, and mean [CO₂] averaged 537  41 and 375  18 mol mol^-1 in the elevated and ambient [CO₂] plots, respectively.

In the 1997–1998 hydrologic year (October to September) corresponding to the 1998 growing season (typically March to September for perennials; March to June for annuals), the southwestern United States experienced a pronounced El Niño cycle during which the NDFF received 309 mm of rain, which was 2.4-fold higher than the long-term average for the area. In contrast, the 1998–1999 hydrologic year was a dry La Niña cycle in which 107 mm of rain fell, and only 17 mm occurred before the onset of the growing season.

For the dominant perennial shrubs of the NDFF, we measured above-ground production during the 1998 and 1999 growing seasons. The cumulative increase in new-shoot biomass for L. tridentata was significantly higher (roughly double) at elevated [CO₂] than at ambient [CO₂] in 1998 (P < 0.01), but no difference in new shoot production occurred between CO₂ treatments in the dry year of 1999 (P  = 0.26) (Fig. 1). In addition, no differences in shrub production occurred between the two types of control plots, and thus the FACE apparatus did not influence these production measurements. We also monitored new root production with minirhizotrons during the same growth period (data not shown) and saw no evidence that plants shifted to new root production in the dry year. Results from the deciduous shrubs at the NDFF, primarily Ambrosia dumosa and Lycium andersonii, also showed substantially enhanced new shoot production at elevated [CO₂] in 1998, but not in 1999 (data not shown).

Figure 1: New shoot production of Larrea tridentata at ambient and elevated [CO₂] at the Nevada Desert FACE Facility in 1998 (a) and 1999 (b) (n = 27 for each CO₂ treatment).

High resolution image and legend (36K)

In response to the anomalous 1997–1998 wet cycle, a large number of annual plants germinated at the NDFF during the winter months. Four species of annuals, Bromus madritensis ssp. rubens, Eriogonum trichopes , Lepidium lasiocarpum and Vulpia octoflora, constituted over 70% of the total density of annuals in the plots and so were selected for above-ground harvests throughout the growth cycle. Bromus (red brome) is an exotic annual grass that has invaded many areas of the Mojave and Sonoran Deserts¹¹; the other three taxa are native annuals. Because of the pronounced spatial variation in soil nutrients that occurs in desert ecosystems¹², two primary microsites were chosen for harvest locations: (1) open interspaces between perennial plants; and (2) beneath or within the canopy of perennial plants. Results from the NDFF confirmed this 'fertile island' effect—soils beneath deciduous and evergreen shrubs have similar concentrations of inorganic nitrogen in the surface 10-cm layer (15 p.p.m. NO₃-N; 3 p.p.m. NH ₄-N), and these concentrations are three- to fivefold higher than in the open interspaces (3 p.p.m. NO₃-N; 1 p.p.m. NH ₄-N).

Total density of the native annuals (Eriogonum, Lepidium and Vulpia) at peak biomass (May) in 1998 was 42% lower (P < 0.01) and total above-ground biomass was 40% higher at elevated [CO₂] (P < 0.1) than at ambient [CO₂] (Fig. 2a). The net result was that individual plants were 2.4-times larger at elevated [CO₂] (0.94 g per plant) than at ambient [CO₂] (0.39 g per plant) (P < 0.01). For Bromus, both plant density and biomass increased at elevated [CO ₂] (Fig. 2a). The 2.3-fold increase in Bromus above-ground biomass at elevated [CO₂] (P < 0.05) was due to a 50% increase in density coupled with a 53% increase in individual plant biomass. Early in the growth season (March), plant density did not differ among elevated [CO₂] and both types of control plots (data not shown), and thus the differences at peak biomass were not caused by differences in seed germination or in seed banks. Because none of the measured parameters differed significantly between the two types of control plots throughout the growing season, the FACE apparatus did not influence these results. Therefore, we conclude that as annual populations exhibited natural self-thinning from germination to peak biomass, both native annuals and Bromus responded to elevated [CO₂] with larger plants, but Bromus became a higher proportion of total plant density at elevated [CO₂]. In the dry winter–spring of 1999, there was no germination of annual plants and therefore no production in either the ambient or elevated [CO₂] plots.

Figure 2: The relative ratio (elevated CO₂/ambient CO₂) of plant density (left), above-ground plant biomass (centre) and seed rain (total seed production; right) per unit area at the Nevada Desert FACE Facility in May, 1998.

a, Native annuals (open bars) and Bromus madritensis spp. rubens (solid bars). b, Bromus madritensis ssp. rubens in open interspaces (open bars) and in 'fertile island' (solid bars) microsites. Note the dashed baseline at a ratio of 1; above the line plants at elevated CO₂ are greater than at ambient CO₂ for that parameter; below the line plants at ambient CO₂ are greater.

High resolution image and legend (36K)

Bromus exhibited a threefold higher total seed rain at the plot level at elevated [CO₂] (Fig. 2a). Although seed rain across the whole plot by native annuals was not significantly increased by elevated [CO₂] (Fig. 2a), [CO₂] effects occurred at an individual plant level. For example, individuals of Bromus and Lepidium produced greater numbers of seeds at elevated than at ambient [CO₂], regardless of microsite location (Table 1). In contrast, Vulpia showed an enhancement in seed production only in fertile island microsites. As Bromus and Lepidium showed no changes in seed production per unit leaf surface area (LSA) and Vulpia showed a slight decrease per LSA, the increases in seed number occurred as a result of larger plants at elevated [CO₂]. However, individual seed mass decreased at elevated [CO₂] in Bromus, a phenomenon that did not occur for the native species (Table 1). Bromus seeds at elevated [CO₂] also have lower N content¹³, and the reduction in seed quality for Bromus at elevated [CO₂] results in a 20% reduction in growth rate of subsequent seedlings¹⁴. However, Bromus produces so many more seeds at elevated [CO₂] that it potentially compensates for reduced seed quality. This phenomenon might have important implications for population structure and competitive relationships between Bromus and native annuals, as well as affect consumers in an ecological system in which granivores have a fundamental role¹⁵.

Table 1: Seed number and mean seed mass for three annual species and two microsites at ambient and elevated [CO₂] in May, 1998 at the Nevada Desert FACE Facility

Full table

Using Bromus, we found an interactive effect of elevated [CO ₂] and microsite on plant density, biomass and seed rain (P  < 0.01) (Fig. 2b). Elevated [CO₂ ] increased Bromus biomass in open interspaces by 76% but by twice that in fertile island microsites (160%). The stimulation of Bromus seed rain by elevated [CO₂] in fertile islands (3.5-fold) was also greater than in interspaces (2.5-fold). In addition, we observed [CO₂]-by-microsite interactions for the native annuals (data not shown). This interactive effect is consistent with predictions that desert annuals will show their strongest response to elevated [CO₂] on sites with moderate to high soil fertility, whereas plant production on low-fertility desert soils is much less responsive to elevated [CO₂]^{1, 3}.

These results have several important implications for the structure and function of desert ecosystems. First, total ecosystem above-ground primary production (both annuals and perennials) during an anomalously wet year for this arid region was substantially higher at elevated [CO₂]. Desert ecosystems have been predicted to exhibit a 50% increase in primary production with a doubling of [CO₂], an increase that would be higher than for any other global biome type². Results from our FACE study exceeded this prediction in a wet year (a roughly 50% increase in native annual plant production, a doubling of new shoot production in the dominant shrub and a 2.3-fold increase in production of an exotic annual grass occurred with a 50% increase in [CO₂]). This also exceeds a roughly 25% increase in primary production observed in a young, rapidly growing pine forest in North Carolina using a similar FACE experimental design¹⁶. However, elevated [CO₂] did not enhance productivity at the NDFF in a drought year. Apparently, plant physiological processes are sufficiently constrained by water stress during dry years in the desert such that plant production is minimal at both [CO₂]. Indeed, our plant gas-exchange results indicate increased photosynthesis and reduced stomatal conductance (and therefore transpiration) at elevated [CO₂] in Larrea during wet seasons, but not during drought^{17, 18}. By enhancing water-use efficiency in plants to the greatest extent when soil moisture is most abundant in this water-limited system, elevated [CO₂] stimulates an already high rate of production in a wet year, but not in a dry year. Desert ecosystems have extremely high temporal variability in rainfall and primary production¹⁹, and our observations of a wet–dry cycle in the Mojave Desert suggest that elevated [CO₂] will increase temporal variability of ecosystem production cycles.

Second, an invasive exotic annual grass showed significantly higher plant density, biomass and seed rain at elevated [CO₂] than did several species of native annuals. The growth of a closely related exotic Bromus (B. tectorum) is also particularly responsive to elevated [CO ₂]⁶. The greater response of exotic Bromus species to elevated [CO₂] relative to native species could enhance the success of a group of highly invasive species in western North America. B. tectorum has invaded many thousands of hectares in this region²⁰, which has increased fire frequency²¹ and has converted large expanses of sagebrush-steppe vegetation to a fire-controlled annual grassland²². Post-fire competitive superiority of Bromus seedlings then precludes the reestablishment of perennial species²³. Bromus madritensis ssp. rubens has initiated a similar invasion cycle in the Mojave and Sonoran Deserts¹¹, although not yet to the extent as the invasion of B. tectorum farther north. The results from this study, showing both higher total biomass and seed rain in Bromus than in native annuals, confirm experimentally in an intact ecosystem that elevated [CO₂] may enhance the invasive success of Bromus spp. in arid ecosystems. Enhanced success of Bromus spp. would expose these deserts to an accelerated fire cycle to which they are not adapted, and thus convert long-lived shrublands to annual grasslands dominated by exotic grasses throughout the region.

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Acknowledgements

We thank D. Jordan, E. Knight, G. Hendrey and the Brookhaven National Laboratory for technical support; C. Biggart, L. DeFalco, C. Grant, E. Hamerlynck, M. Hargrove, K. Hightower, K. Huxman, F. Landau, D. Pataki, K. Salsman, T. Shiver, D. Stortz-Lintz, and M. Taub for field and laboratory assistance; and J. Titus for soil nitrogen data. Financial support was provided by the DOE- and NSF-EPSCoR programs and panel grants from NSF/TECO and DOE/TCP, and additional support was provided by the NAES. We also thank the DOE/Nevada Operations Office and Bechtel Nevada for site operations support.