Dominant plant taxa predict plant productivity responses to CO2 enrichment across precipitation and soil gradients.

The Earth's atmosphere will continue to be enriched with carbon dioxide (CO2) over the coming century. Carbon dioxide enrichment often reduces leaf transpiration, which in water-limited ecosystems may increase soil water content, change species abundances and increase the productivity of plant communities. The effect of increased soil water on community productivity and community change may be greater in ecosystems with lower precipitation, or on coarser-textured soils, but responses are likely absent in deserts. We tested correlations among yearly increases in soil water content, community change and community plant productivity responses to CO2 enrichment in experiments in a mesic grassland with fine- to coarse-textured soils, a semi-arid grassland and a xeric shrubland. We found no correlation between CO2-caused changes in soil water content and changes in biomass of dominant plant taxa or total community aboveground biomass in either grassland type or on any soil in the mesic grassland (P > 0.60). Instead, increases in dominant taxa biomass explained up to 85 % of the increases in total community biomass under CO2 enrichment. The effect of community change on community productivity was stronger in the semi-arid grassland than in the mesic grassland, where community biomass change on one soil was not correlated with the change in either the soil water content or the dominant taxa. No sustained increases in soil water content or community productivity and no change in dominant plant taxa occurred in the xeric shrubland. Thus, community change was a crucial driver of community productivity responses to CO2 enrichment in the grasslands, but effects of soil water change on productivity were not evident in yearly responses to CO2 enrichment. Future research is necessary to isolate and clarify the mechanisms controlling the temporal and spatial variations in the linkages among soil water, community change and plant productivity responses to CO2 enrichment. Published by Oxford University Press on behalf of the Annals of Botany Company 2015. This work is written by (a) US Government employee(s) and is in the public domain in the US.

Introduction

Continued enrichment of the Earth's atmosphere with carbon dioxide (CO2) is certain through the coming century and is expected to alter climate and terrestrial ecosystem structure and function. In water-limited ecosystems, one major mechanism by which CO2 enrichment may cause ecosystem change is by increasing soil water (Morgan ; Nowak ). CO2 enrichment can increase soil water by reducing stomatal conductance and leaf- and canopy-scale transpiration in both C3 and C4 species (Nowak ; Ainsworth and Long 2005). Lower stomatal conductance and plant transpiration under CO2 enrichment in turn decreases soil water depletion, which results in higher soil water and potentially reduced water limitation of ecosystem processes compared with ambient CO2.

Increased soil water with CO2 enrichment generally increases the productivity of water-limited plant communities. Greater productivity increases often occur with lower precipitation across precipitation levels typical of grassland ecosystems (Owensby ; Morgan ; Nowak ; Körner 2006; Polley ), because the increased soil water under CO2 enrichment is more likely to relieve water limitation (Nowak ). However, in severely water-limited systems such as deserts, CO2 enrichment may not increase productivity if reduced leaf transpiration is offset by increased leaf area because soil water may not increase. In addition, slow growth rates in drought-adapted desert plants limit the potential to increase community productivity in the short-term (Nowak ; Newingham ).

Plant community change is another mechanism by which CO2 enrichment may increase community productivity (Bradley and Pregitzer 2007; Gornish and Tylianakis 2013). Community change is most likely to alter community productivity when change involves the dominant plant taxa (Smith and Knapp 2003). Smith suggested that altered resource availability drives the ecosystem change primarily by causing community change. If true, increased soil water with CO2 enrichment would result in changes in dominant taxa abundance, which would in turn increase productivity. However, increased soil water alone can also result in community productivity increases (Fig. 1).

Figure 1.

Model by which increased soil water resulting from atmospheric CO2 enrichment may increase plant community productivity in water-limited ecosystems. The increase in soil water may predict the increase in community productivity, or the effect of soil water increase may be mediated by change in the abundance of dominant plant taxa, which in turn predicts in the increase in community productivity.

The contributions of increased soil water and community change to increased community productivity with CO2 enrichment are also expected to differ with soil texture. At precipitation levels typical of grasslands, soil water will be lower on coarse-textured than fine-textured soils, increasing water limitation of community productivity, and thus the importance of soil water increases in regulating productivity. For example, over 4 years of CO2 enrichment, the increase in plant aboveground biomass was best predicted by soil water on a coarse-textured soil, but increases in biomass were best predicted by the abundance of a dominant grass species on a fine-textured soil (Fay ), which accounted for up to 60 % of the effect of CO2 enrichment (Polley ).

To investigate how water-limited plant communities respond to CO2 enrichment across varying precipitation amounts and soils, we examined soil water, plant community change and plant productivity responses to CO2 enrichment in five multi-year CO2 enrichment experiments from mesic and semi-arid grasslands and in a xeric shrubland in the central and western USA. The experiments span a 6-fold range of mean annual precipitation (MAP), which provides a test of variation in CO2 responses with precipitation. The mesic grassland experiment contained fine and coarse-textured soils, providing a test of texture effects on CO2 responses. Interannual variability in precipitation is often high in water-limited systems, and so yearly community productivity increases from CO2 enrichment were correlated with increases in soil water and community change.

Methods

Sites and experiments

Mesic grassland

Two CO2 enrichment experiments were conducted at Temple, TX, USA, in the southern portion of the North American tallgrass prairie, a region of humid subtropical climate with warm summers and abundant precipitation (Table 1). The Prairie CO2 Gradient (PCG, Fig. 2A, Johnson ) experiment manipulated CO2 using two chambers (1 m tall, 1 m wide and 60 m long) placed on an intact formerly grazed pasture. The C4 perennial grass Bothriochloa ischaemum accounted for 51 % of aboveground biomass, accompanied by C3 perennial forbs, primarily Solanum dimidiatum and Ratibida columnaris (Polley ). In one chamber, CO2-enriched air was introduced at the chamber entrance, and photosynthesis by the enclosed vegetation depleted the air of CO2 as it transited the length of the chamber. Air flow rates were controlled to create a 550–350 µmol mol−1 gradient in CO2. Similarly, ambient air was supplied to the second chamber, which was controlled to create a 365–200 µmol mol−1 gradient. The chambers were divided into 5 m sections, and air was cooled and dehumidified in each section to maintain air temperature and vapour pressure deficit near ambient conditions. The CO2 gradients were maintained during the growing seasons of 1997–2000.

Table 1.

Location, climate and CO2 treatments for the four experiments. MAP, mean annual precipitation; MAT, mean annual temperature.

Experiment	CO2 treatments (µmol mol−1)	Location, lat., long.	Elevation (m)	MAP (mm)	MAT (max, °C)	MAT (min, °C)
PCG	200–550	Texas, USA; 31°05′, −97°20′	186	914	35	3
LYCOG	250–500	Texas, USA; 31°05′, −97°20′	186	914	35	3
OTC	360 and 720	Colorado, USA; 40°40′, −104°45′	1555	320	16	0.5
PHACE	385 and 600	Wyoming, USA; 41°11′, −104°54′	1930	384	18	−3
NDFF	375 and 550	Nevada, USA; 36°46′, −115°57′	970	148	38	−5

Figure 2.

CO2 manipulation experiments included in the study. (A) Carbon dioxide gradient chambers used in PCG and LYCOG experiments in mesic grassland (Photo: P. Fay, USDA-ARS). (B) Open-top chambers used in short-grass steppe experiment (Photo: S. Cox, USDA-ARS). (C) Free-air CO2 enrichment technology used in mixed-grass prairie PHACE experiment (Photo: S. Cox, USDA-ARS). (D) FACE plot used in xeric shrubland experiment (L. Fenstermaker, Desert Research Institute).

The Lysimeter CO2 Gradient (LYCOG) experiment was the successor to the PCG experiment and adapted the PCG chambers to enclose 60 intact soil monoliths (1.5 m3) from a silty clay, a sandy loam and a heavy clay soil, arranged in a stratified random design along the two chambers (Fig. 2A; Polley ; Fay ). The monoliths supported well-established, constructed communities of native prairie. The C4 grasses Sorghastrum nutans, Bouteloua curtipendula, Schizachyrium scoparium and Tridens albescens accounted for 80 % of total aboveground biomass. The remainder was C3 forbs (Solidago canadensis, Salvia azurea) and one legume (Desmanthus illinoensis; Fay ; Polley ). Other species were regularly removed by hand or selective glyphosate application. Air temperature and vapour pressure deficit were controlled as for PCG; CO2 concentration was maintained at 500–380 and 380–250 µmol mol−1 during 2006–10. In both experiments, irrigation regimes were representative of average growing season precipitation for the site.

Semi-arid grassland

Two CO2 enrichment experiments were conducted in a cold semi-arid steppe region of northeastern Colorado and southeastern Wyoming, characterized by cooler summers than the other sites (Table 1). Semi-arid grasslands are more water-limited than mesic grasslands, are dominated by a different, more drought tolerant assemblage of species and are predicted to be more responsive in plant productivity to CO2 enrichment than mesic grasslands (Morgan ). An open-top chamber (OTC, Fig. 2B) experiment was conducted during 1996–2001 in short-grass steppe near Fort Collins, Colorado. Basal cover of the vegetation was ∼25 %. Two perennial C3 grasses Pascopyrum smithii and Hesperostipa comata accounted for 60 % of aboveground biomass, accompanied by a C4 grass, Bouteloua gracilis, and forbs (Morgan , 2004). Six circular plots of 15.5 m2 were fitted with OTCs which were randomly assigned to maintain an ambient CO2 level of 360 µmol mol−1 or an elevated CO2 level of 720 µmol mol−1 during the growing season.

The Prairie Heating and CO2 Experiment (PHACE, Fig. 2C) was conducted in a northern mixed prairie near Cheyenne, Wyoming (Parton ). Cool-season C3 grasses, mostly P. smithii and H. comata, account for 75 % of aboveground biomass. C4 grasses, almost exclusively B. gracilis, and sedges, forbs and small shrubs account for the rest (Morgan ). PHACE treatments were factorial combinations of two levels of CO2; ambient = 385 µmol mol−1 and elevated = 600 µmol mol−1 achieved using Free-Air CO2 Enrichment (FACE) technology, and ambient or warmed temperature regimes (+1.5/3.0 day/night), with five replications each. Treatments were randomly assigned to twenty 3.3 m diameter circular plots. Here we consider data from 2006 to 2009 from ambient temperature treatments.

Xeric shrubland

The Nevada Desert FACE Facility (NDFF, Fig. 2D) was located in the Mojave Desert in southern Nevada, USA, on the Nevada National Security Site, formerly the Nevada Test Site. The climate is mid-latitude desert with the lowest annual precipitation of the sites (Table 1) and was thus predicted to be the least responsive to CO2 enrichment due to severe water limitation. Most precipitation occurs during the winter. The NDFF used the FACE technology with three ambient plots averaging 375 µmol mol−1, three elevated plots averaging 550 µmol mol−1 CO2 and three non-blower control plots without FACE infrastructure; all plots were 23 m in diameter. The NDFF experiment was conducted from April 1997 to June 2007. Experimental plots were in a Larrea tridentata—Ambrosia dumosa desert scrub community, which consisted of C3 shrubs, forbs, annuals and a C4 bunchgrass (Jordan ).

Sampling and data analysis

We used previously published data on soil water content, and dominant taxa and total community aboveground biomass to estimate soil water change, community change and community productivity change in each year of CO2 enrichment. All sites measured vertical profiles of volumetric soil water content (Nelson ; Nowak ; Parton ; Fay ). In LYCOG soil water potential was calculated from soil water content using soil water characteristic curves for each soil (Fay ). At the grassland sites, dominant taxa and community biomass were estimated annually from the dry mass of current-year standing aboveground biomass. Aboveground biomass in the xeric shrubland experiment was determined by a single harvest of standing aboveground biomass after 10 years of CO2 enrichment (Newingham ), and responses of dominant species were determined as in Newingham .

The response ratio β (Amthor and Koch 1996; eq. 1) was computed from the dominant taxa biomass, community biomass, and growing season mean volumetric soil water content at enriched (CE) and ambient (CA) CO2 each year.

The calculation of β standardizes the responses for different levels of CO2 used among the experiments.

Soil water content β was calculated for the soil depth that best predicted aboveground biomass: 0–135 cm (PCG), 0–40 cm (LYCOG), 70–100 cm (OTC) and 5–25 cm (PHACE). We calculated β in the mesic grassland CO2 gradients from values of biomass and soil water content at 500 and 390 µL L−1 CO2. These values were estimated from linear regressions of biomass and soil water content against CO2 for each year. In LYCOG, regressions were fit across all three soils and for each soil separately. The β values were not calculated for the xeric shrubland because there were no responses to CO2 enrichment in growing season soil water content and no on-going responses in total or dominant taxa aboveground biomass. Correlations among the β for community biomass, soil water content and dominant taxa were tested with linear regression analysis. The magnitude of community biomass β with no community change was estimated from the y-intercept of community biomass β/dominant taxa β regressions.

Results

Precipitation gradient

Mean community biomass β was 0.52 in PCG and 1.19 in LYCOG (Fig. 3A), corresponding to community biomass increases with CO2 enrichment of 15 and 29 %, respectively. Mean soil water content β was 0.37 for PCG and 0.43 for LYCOG (Fig. 3A, inset), corresponding to 9–10 % increases in soil water content.

Figure 3.

Relationships among community aboveground biomass, MAP, dominant plant taxa biomass and soil water content (SWC) responses to CO2 enrichment in xeric shrubland, mesic grassland and semi-arid grassland CO2 enrichment experiments. (A) Community biomass β, mean ± SE across all years of CO2 manipulation for each experiment, plotted by site MAP. Inset is the corresponding mean ± SE soil water content β. (B) Relationship between annual values of β for community biomass and dominant plant taxa, with linear regressions fit separately to mesic grassland and semi-arid grassland experiments. (C and D) Relationships of community biomass β and dominant plant taxa β to soil water content β.

Carbon dioxide enrichment altered the abundance of dominant grasses in both mesic grassland CO2 experiments. In LYCOG, C4 grass β ranged from −0.9 to 1.2. In PCG, C4 grass β ranged from −0.23 to 1.0 (Fig. 3B), corresponding to −20 to 90 % changes in C4 grass biomass. Across both experiments, community biomass β increased with the C4 grass β (R2 = 0.43, P = 0.03, Fig. 3B). The community biomass β at the y-intercept was 0.6, equating to a 15 % increase in community biomass with CO2 enrichment in the absence of change in C4 grass biomass. The values of β for community and C4 grass biomass were not correlated with soil water content β (P > 0.69, Fig. 3C and D).

Mean community biomass β was 0.51 in OTC and 0.73 in PHACE (Fig. 3A), corresponding to 31 and 35 % increases, respectively, in community biomass under CO2 enrichment. Mean soil water content β averaged 0.26 for OTC and 0.39 for PHACE (Fig. 3A, inset), corresponding to 17–18 % increases in soil water content.

Carbon dioxide enrichment increased the abundance of the dominant plant taxa in both semi-arid grassland experiments. C3 grass β averaged 0.65 in the OTC experiment and 0.30 in the PHACE experiment (Fig. 3B), corresponding to 30–50 % increases with CO2 enrichment. Community biomass β strongly increased with the C3 grass β (slope = 0.90, R2 = 0.81, P = 0.0002, Fig. 3B), with a slope nearly twice that of the community–C4 grass β relationship for mesic grassland (slope = 0.50, Figs 3B and 4). The community biomass β at the y-intercept was 0, indicating that there was no community biomass increase with CO2 enrichment in the absence of change in C3 grass biomass. As in the mesic grassland, β values for community biomass and C3 grass biomass were not correlated with soil water content β across the two experiments (P > 0.59, Figs 3C and D and 4).

Figure 4.

Summary of correlations among changes in soil water, abundance of dominant plant taxa and plant community biomass increases with CO2 enrichment in mesic grassland, semi-arid grassland and xeric shrubland. Solid arrows denote positive correlations among variables, and thicker lines denote stronger relationships. Grey boxes indicate no significant CO2 enrichment effects, and grey lines indicate no correlations.

The xeric shrubland responses to CO2 enrichment were a dramatic departure from those of the mesic and semi-arid grasslands. Carbon dioxide enrichment at the NDFF had no effect on soil water content (Nowak ) or on cumulative total aboveground and belowground biomass (Newingham ) and productivity of dominant annual plant taxa (Smith ; Fig. 4) following 10 years of CO2 enrichment. Thus, there was no basis for testing correlations among β values for soil water content, dominant taxa and aboveground biomass in this system.

Soils gradient

The total community biomass increase resulting from CO2 enrichment varied considerably among soil types in the LYCOG experiment. Mean community biomass β was 1.0 on the fine-textured clay soil and 1.4 on the silty clay and sandy loam soils (Fig. 5A), corresponding to 23–35 % increases in aboveground biomass with CO2 enrichment. Soil water content mean β was 0.1–0.2 (range 0.03–0.31) in the clay and silty clay soils, increasing to 0.85 (range 0.50–1.04) on the sandy loam soil (Fig. 5A), which also had the highest mean soil water potential (Fig. 5A, inset). These values of β corresponded to 1–26 % increases in soil water content with CO2 enrichment. Community biomass β was not correlated with soil water content β on any soil individually (0.06 < P < 0.41, Figs 5A and 6) or across all soils (P = 0.09).

Figure 5.

Relationships among community aboveground biomass, dominant plant taxa biomass and soil water content responses to CO2 enrichment in the three soils in the LYCOG experiment in mesic grassland. (A) Community biomass β, mean ± SE across all years of CO2 manipulation in relation to soil water content β. Large symbols denote means ± SEs across years for each soil. Inset is the corresponding mean ± SE soil water potential for each soil type. (B) Community biomass β relationship to C4 grass β, with linear regressions fit to silty clay and sandy loam soils. (C) C4 grass β relationship to soil water content β.

Figure 6.

Summary of correlations among changes in soil water, abundance of dominant plant taxa and plant community biomass increases with CO2 enrichment on three soils in mesic grassland. Solid arrows denote positive correlations among variables, and thicker lines denote stronger relationships. Grey boxes indicate no significant CO2 enrichment effects, and grey lines indicate no correlations.

The value of β for C4 grasses ranged from −1.0 to 2.0 across all soils (Fig. 5B), corresponding to −41 to 130 % changes in C4 biomass with CO2 enrichment. The community biomass β increased with C4 grass β on the silty clay and sandy loam soils (slope = 0.52, R2 = 0.90, P = <0.0001). The community biomass β on these two soils was 0.9 at the y-intercept for C4 grass β, equating to a 2 % increase in community biomass with CO2 enrichment in the absence of change in C4 grass biomass. Community biomass β was not correlated with C4 grass β on the clay soil (P = 0.31, Fig. 5B). Dominant grass β was not correlated with soil water content β for any soil (0.28 < P < 0.58; Figs 5C and 6).

Discussion

Carbon dioxide enrichment can increase the productivity of communities solely by increasing soil water or by mediating community change. Soil water increases were expected to cause larger community productivity responses with lower precipitation and on coarser-textured soils in the grasslands, but responses were expected to decline sharply in the extreme aridity of the xeric shrubland. Our findings indicate that in the grasslands, yearly soil water content increases never predicted community change or community productivity. Instead, community change caused a larger community productivity response in semi-arid than that in mesic grasslands, and the predicted sharp decline in responsiveness to CO2 was supported in the xeric shrubland.

The absence of cumulative increases in community productivity with CO2 enrichment in the xeric shrubland may be explained by the absence of increased soil water and community change. There was no sustained increase in soil water content (Nowak ) because CO2 enrichment only increased photosynthesis and water-use efficiency and decreased stomatal conductance in occasional wet years (Nowak ; Naumburg ; Housman ; Aranjuelo ). There was also no sustained community change because the dominant perennial species were unaffected by CO2 enrichment (Newingham ), and responses were confined to native and exotic annuals which transiently increased with CO2 enrichment only during high rainfall years (Smith , 2014). Thus, the mechanisms proposed as the fundamental drivers of productivity increases with CO2 enrichment in water-limited ecosystems were largely absent in this arid ecosystem.

In the grasslands, the absent correlations between soil water content change, community change and community productivity increases suggests that effects of increased soil water on plant productivity were not well represented by the growing season mean soil moisture response. Increased soil water content may not always translate into greater plant growth because plant growth exhibits a threshold response to soil water (Lambers ). Soil water variability, such as an increased duration or severity of soil water deficit, in current or previous years may lower community productivity (Polley ; Fay , 2011; Heisler-White ; Hovenden ; Reichmann and Sala 2014), and the CO2 effect on soil water during drought periods may be a better predictor of productivity responses than the mean response in soil water over the growing season.

The lack of correlation between yearly soil water change and community responses differs from previous findings. Averaged over multiple years of CO2 enrichment, increased community productivity occurred in part because of increased soil water in these grassland experiments (Polley ; Nelson ; Morgan ; Fay ). The importance of soil water increases averaged over multiple years but not in any given year suggests that predictors of community change or productivity responses at one temporal scale may not apply at other scales in these grasslands (Peters ).

Community change was a stronger predictor of community productivity increases in the drier semi-arid grassland compared with the mesic grassland. The weaker relationship to community change in mesic grassland stemmed from 2 years when CO2 enrichment increased plant productivity but decreased the dominant taxa (Fig. 3B), indicating that productivity of other species in these mesic grassland communities increased with CO2 enrichment enough to offset decreases in the dominants. In contrast, the dominant taxa never decreased in the semi-arid grassland. Offsetting responses within communities may dampen the productivity response to CO2 in mesic grassland (Hooper ), and both dominant and sub-dominant taxa can contribute to community productivity responses to CO2 enrichment.

Two other factors may have contributed to the stronger community change effect on community productivity increases in the semi-arid grassland. First, lower MAP and higher mean soil water content increases with CO2 enrichment may have resulted in release from water limitation for all community members in the semi-arid grassland compared with the mesic grassland. Second, in the mesic grassland, there was no community change effect on community productivity on the clay soil. The strong community change/productivity responses occurred on the two soils with high mean soil water potential (Fay ), suggesting that the overall availability of soil water, not the increase in soil water content, determines community and productivity responses to CO2 enrichment.

In the semi-arid grassland during years with no community change, there was no increase in community biomass, suggesting that yearly increases in community productivity were almost completely explained by community change. Although community change was a weaker predictor of community productivity change in mesic grassland, it still predicted ∼80 % of the productivity response. These results suggest that, in years with no community change, community productivity increased by 15–22 % from other potential causes, such as direct effects of CO2 enrichment on carbon gain or plant water status (Ainsworth and Long 2005).

Conclusions

Community change predicted most of the changes in community productivity in the grasslands and better predicted community productivity responses in the drier grassland and on soils with higher plant availability of soil water in the mesic grassland. The xeric shrubland makes clear that in the absence of increased soil water or community change, increased community productivity is unlikely. The linkage of community change and productivity to yearly changes in soil water with CO2 enrichment remains unclear, but it may depend more on the temporal variability in soil water than on the size of the increase. Future research needs to isolate and clarify the temporal and spatial mechanisms controlling the linkages among soil water, community change and plant productivity responses to CO2 enrichment.

Sources of Funding

Mesic grassland experiments: USDA-ARS Climate Change, Soils & Emissions and Pasture, Forage and Rangeland Systems Programs. Semi-arid grassland experiments: NSF-TECO (IBN-9524068), NSF (DEB-9708596, 1021559), the NSF LTER (DEB-9350273), USDA-ARS Climate Change, Soils & Emissions Program, USDA-CSREES (2008-35107-18655), the US DOE NICCR (DE-SC0006973). Xeric shrubland experiments: US DOE (DE-FG02-03ER63651), NSF (DEB-0212812) and the Nevada Agricultural Experiment Station. Opinions, findings and conclusions or recommendations expressed in this material are those of the authors and do not necessarily reflect the views of the National Science Foundation. USDA is an Equal Opportunity Employer.

Contributions by the Authors

P.A.F. and B.A.N. conceived the manuscript and led the writing, P.A.F. analysed the data and the remaining authors contributed data, edited the manuscript and approved the submission.

Conflict of Interest Statement

None declared.