Photosynthesis and growth reduction with warming are driven by nonstomatal limitations in a Mediterranean semi-arid shrub

Abstract

Whereas warming enhances plant nutrient status and photosynthesis in most terrestrial ecosystems, dryland vegetation is vulnerable to the likely increases in evapotranspiration and reductions in soil moisture caused by elevated temperatures. Any warming-induced declines in plant primary production and cover in drylands would increase erosion, land degradation, and desertification. We conducted a four-year manipulative experiment in a semi-arid Mediterranean ecosystem to evaluate the impacts of a ~2°C warming on the photosynthesis, transpiration, leaf nutrient status, chlorophyll content, isotopic composition, biomass growth, and postsummer survival of the native shrub Helianthemum squamatum. We predicted that warmed plants would show reduced photosynthetic activity and growth, primarily due to the greater stomatal limitation imposed by faster and more severe soil drying under warming. On average, warming reduced net photosynthetic rates by 36% across the study period. Despite this strong response, warming did not affect stomatal conductance and transpiration. The reduction of peak photosynthetic rates with warming was more pronounced in a drought year than in years with near-average rainfall (75% and 25-40% reductions relative to controls, respectively), with no indications of photosynthetic acclimation to warming through time. Warmed plants had lower leaf N and P contents, δ (13)C, and sparser and smaller leaves than control plants. Warming reduced shoot dry mass production by 31%. However, warmed plants were able to cope with large reductions in net photosynthesis, leaf area, and shoot biomass production without changes in postsummer survival rates. Our findings highlight the key role of nonstomatal factors (biochemical and/or nutritional) in reducing net carbon assimilation rates and growth under warming, which has important implications for projections of plant carbon balance under the warmer and drier climatic scenario predicted for drylands worldwide. Projected climate warming over the coming decades could reduce net primary production by about one-third in semi-arid gypsum shrublands dominated by H. squamatum.

Keywords: Climate change; Helianthemum squamatum; dryland ecosystems; leaf trait plasticity; plant nutrient status; plant survival and growth; plant–climate interactions; stable isotopes.

Figure 1

Linear regressions between net photosynthesis rate (A)/stomatal conductance (B) and soil water content in control and warmed plants across measurement dates. Each point represents the mean value of 10–15 replicated plants from separate plots. Vertical and horizontal error bars represent standard errors. Linear regression equations for control and warmed plants are also shown.

Figure 2

Mean net photosynthetic rates (A), stomatal conductance (B), and intrinsic water‐use efficiency values (C) in warmed and control plants at 11 different measurement dates spanning four growing seasons. Data represent means ± SE (n = 10–15).

Figure 3

Linear regressions between mean net photosynthesis rates (A) and mean stomatal conductance (g _s) in control and warmed plants across measurement dates. Each point represents the mean value of 10–15 replicated plants from separate plots. Vertical and horizontal error bars represent standard errors. Fitted linear regressions for control and warmed plants are also shown. Analysis of covariance indicated that the regression lines of control and warmed plants were significantly different (P = 0.001). Data recorded in November 2012 were excluded from the regression analysis, as there were no significant differences in A or g _s between temperature treatments at this time.

Figure 4

Quantum efficiency of photosystem II (A), transpiration rates (B), and instantaneous water‐use efficiency values (C) in warmed and control plants at 10–11 different measurement dates spanning four consecutive growing seasons. Data represent means ± SE (n = 10–15).

Figure 5

Mean leaf δ ¹³C values in control and warmed plants at the peak of the growing season (April) in the 4 years of the study. Data represent means ± SE (n = 10–15).

Figure 6

Negative relationship between leaf areas and C:N ratios at the peak of the growing season (April 2013, 2014, 2015). Green circles represent control plants and orange circles represent warmed plants. N = 10–15 individual plants per treatment × year combination.