Synergistic Effects of Elevated CO2 and Fertilization on Net CO2 Uptake and Growth of the CAM Plant Hylocereus undatus

in Journal of the American Society for Horticultural Science
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  • 1 Department of Life Sciences, Ben-Gurion University of the Negev, Beer-Sheva 84105, Israel
  • | 2 Gilat Research Center, Mobile Post Negev 85280, Agricultural Research Organization, Ministry of Agriculture, Israel

This study examined the response of the crassulacean acid metabolism (CAM) vine-cactus fruit crop species Hylocereus undatus to two CO2 regimes [enrichment (1000 μmol·mol−1) vs. ambient control (380 μmol·mol−1)] and to two fertilization regimes [0.5- vs. 0.1-strength Hoagland's solution (designated high and low, respectively)]. CO2 enrichment increased total daily net CO2 uptake, nocturnal acid accumulation, shoot elongation, and total dry mass by 39%, 24%, 14%, and 6% (averaging the two fertilization regimes) versus ambient CO2 treatment, respectively. Plants exposed to high fertilization demonstrated 36%, 21%, 198%, and 79% (averaging the two CO2 regimes) increases versus those receiving the low fertilization regime in total daily net CO2 uptake, nocturnal acid accumulation, stem elongation, and total dry mass, respectively. Plants exposed to high fertilization and elevated CO2 demonstrated 108%, 77%, 264%, and 111% increases versus those receiving the low fertilization regime at the ambient CO2 concentration in total daily net CO2 uptake, nocturnal acid accumulation, stem elongation, and total dry mass, respectively. This response was 25% to 71% higher than the summed effects of the separate responses to each factor, indicating a synergistic effect of elevated CO2 and high fertilization. Thus, it is apparent that H. undatus crops grown under a high-fertilization agromanagement regime may benefit from elevated CO2 to a greater extent than those grown with low fertilization.

Abstract

This study examined the response of the crassulacean acid metabolism (CAM) vine-cactus fruit crop species Hylocereus undatus to two CO2 regimes [enrichment (1000 μmol·mol−1) vs. ambient control (380 μmol·mol−1)] and to two fertilization regimes [0.5- vs. 0.1-strength Hoagland's solution (designated high and low, respectively)]. CO2 enrichment increased total daily net CO2 uptake, nocturnal acid accumulation, shoot elongation, and total dry mass by 39%, 24%, 14%, and 6% (averaging the two fertilization regimes) versus ambient CO2 treatment, respectively. Plants exposed to high fertilization demonstrated 36%, 21%, 198%, and 79% (averaging the two CO2 regimes) increases versus those receiving the low fertilization regime in total daily net CO2 uptake, nocturnal acid accumulation, stem elongation, and total dry mass, respectively. Plants exposed to high fertilization and elevated CO2 demonstrated 108%, 77%, 264%, and 111% increases versus those receiving the low fertilization regime at the ambient CO2 concentration in total daily net CO2 uptake, nocturnal acid accumulation, stem elongation, and total dry mass, respectively. This response was 25% to 71% higher than the summed effects of the separate responses to each factor, indicating a synergistic effect of elevated CO2 and high fertilization. Thus, it is apparent that H. undatus crops grown under a high-fertilization agromanagement regime may benefit from elevated CO2 to a greater extent than those grown with low fertilization.

Most studies on the physiological responses of plants to increasing CO2 concentrations have focused on C3 and C4 photosynthetic pathway plants. It has been found that CO2 enrichment enhances net CO2 uptake and growth of C3 plants by 30% to 40% (Kimball, 1983), whereas in C4 photosynthetic pathway plants, the effect is less marked, being about 10% (Newton, 1991). Studies on the response of CAM plants to elevated CO2 are far more limited than those on C3 and C4 plants (Poorter and Navas, 2003). Among the CAM species that have been studied, the findings are not uniform: some reports found no significant change in CO2 uptake and growth in response to elevated CO2 levels (Holtum et al., 1983; Szarek et al., 1987), whereas other studies reported an increase in these parameters (Drennan and Nobel, 2000; Raveh et al., 1995).

In C3 and C4 plants, a sustained positive response to CO2 enrichment may be attenuated by environmental conditions such as irradiance [including ultraviolet (UV)-B], temperature, ambient ozone concentrations, and the availability of water and nutrients. These factors, alone or in combination, could lead to acclimation during long-term exposure to elevated CO2 concentrations (Poorter, 1993). In particular, it has been found that high nutrient concentrations usually amplify the response of plants to CO2 enrichment (Poorter and Perez-Soba, 2001; Reich et al., 2006). Most of the studies on the response of CAM plants to elevated CO2 were conducted under conditions of low fertilization [0.1- to 0.3-strength Hoagland's solution (Drennan and Nobel, 2000)], but there have been no systematic studies of the effect of high-fertilization regimes on the response of CAM plants to CO2 enrichment.

A small number of studies have investigated the response to CO2 of the CAM species H. undatus (commonly known as pitahaya or dragon fruit), a vine cactus that is indigenous to the tropical and subtropical regions of Central America and that is grown as a crop in a number of countries, including Mexico, some countries of Southeast Asia, and currently in Israel (Mizrahi et al., 1997). Raveh et al. (1995) showed that CO2 enrichment of H. undatus resulted in a 34% increase in total daily net CO2 uptake, which enabled the plants to overcome various abiotic stresses. Nobel and De la Barrera (2002) reported stimulation of CO2 uptake by H. undatus grown at high N concentrations and ambient CO2: maximal nocturnal net CO2 uptake rates were 2.5 and 9.8 μmol·m−2·s−1 at 0.16 and 16 mm N, respectively.

The specific objective of this study was to test the hypothesis that increased levels of fertilization amplifies the effect of CO2 enrichment on net CO2 uptake and growth in H. undatus.

Materials and Methods

Plant material.

Rooted shoot cuttings of H. undatus were used in this study. Shoots of uniform size (60 ± 2 cm in length) were planted (positioned at random) in 10-L pots, placed 60 cm apart, and filled with volcanic gravel (Tuff Merom Golan, Merom Golan, Israel). These conditions were chosen to ensure that rooting volume did not limit growth (Mizrahi et al., 2007).

Experimental design.

The experiments were conducted in Beer-Sheva, northern Negev Desert, Israel (lat. 31°15′N, long. 34°48′E, 315 m above sea level). Plants (n = 10 for each treatment) were grown for 1 year, from Aug. 2006 to Aug. 2007, under conditions of ambient CO2 [380 ± 10 (se) μmol·mol−1] or elevated CO2 [1000 ± 70 (se) μmol·mol−1]. The plants were grown in a cooled greenhouse in two vented chambers (each 220 cm high, 120 cm wide, and 1000 cm long), one for each CO2 concentration. Each chamber contained plants receiving two different fertilization regimes, as described below. The locations of the pots and the chambers were changed three times during the experiment to reduce the effect of location. For the chamber with the enriched CO2 atmosphere, pure CO2 (cylinders of compressed CO2; Maxima, Beer-Sheva, Israel) was supplied through a flow meter that controlled the flow rate at about 0.8 L·min−1. Ambient air entered each chamber through a port in the lower panel of the chamber wall opposite to the wall with the vent. The chamber air was changed three times per hour, with the air being vented via a duct to the outside by means of a centrifugal fan. The CO2 concentration inside each chamber was monitored at 30-min intervals with an automatic four-channel monitoring system (IRGA PTM-48M; PhyTech, Rehovot, Israel). A detailed description of the system is given in Weiss et al. (2009) and references therein.

Plants were fertigated twice a week via a drip irrigation system (8 L·h−1; one dripper per plant) with 2 L of 0.5-strength Hoagland's solution [high (120 mg·L−1 N, 50 mg·L−1 P, and 90 mg·L−1 K)] or 0.1-strength Hoagland's solution [low (24 mg·L−1 N, 10 mg·L−1 P, and 18 mg·L−1 K)]. The N:P:K ratio was the same for high and low nutrient treatments to control for negative physiological responses caused by interaction of the nutrient elements (Zhang et al., 2006).The high nutrient treatment was the same as that giving maximum stimulation of CO2 uptake observed by Nobel and De la Barrera (2002) under ambient CO2 conditions. It is also the nutrient treatment recommended in commercial fields. The low values were the same as those used in most of the studies previously performed on CAM plants (Drennan and Nobel, 2000).

Air temperatures at the midplant height in the chambers were monitored at 30-min intervals with a data logger (MicroLog™ EC650; Fourier Systems, New Albany, IN). Average values for monthly maximum and minimum air temperatures were similar for the two chambers and were therefore combined in the graphs shown in Fig. 1A. The monthly maximum/minimum air temperature averages for the coldest season (December–February) were 19/7 °C, and those for the hottest season (May–September) were 32/19 °C (Fig. 1A). The experiment was conducted under natural photoperiod. The instantaneous photosynthetic photon flux (PPF) inside the chambers was measured at wavelengths of 400 to 700 nm with a TIR-4 quantum sensor (PhyTech) connected to an IRGA PTM-48M system. Monthly average values for total daily PPF were similar for the two chambers and were therefore combined in the graphs shown in Fig. 1B. The monthly average of total daily PPF for the coldest season was 13 mol·m−2·d−1, and the average for the hottest season was 20 mol·m−2·d−1 (Fig. 1B), the latter value being the optimal total daily net CO2 uptake for H. undatus (Raveh et al., 1995).

Fig. 1.
Fig. 1.

Monthly averages of (A) maximum [Tmax (○)], mean [Tmean (Δ)], and minimum [Tmin (□)] daily air temperature and (B) total daily instantaneous PPF (◇) in the growth chambers situated in a cooled greenhouse during the period 15 Aug. 2006 to 15 Aug. 2007. Values are means ± se.

Citation: Journal of the American Society for Horticultural Science J. Amer. Soc. Hort. Sci. 134, 3; 10.21273/JASHS.134.3.364

Gas exchange measurements.

Gas exchange was measured, starting from day 212 of the experiment, on third-order shoots (n = eight for each treatment) with an IRGA PTM-48M monitoring system. Measurements were taken over a period of 4 d (15–18 Mar. 2007) and were recorded throughout the day and night at 30-min intervals. To measure net gas exchange of the shoot, the original chamber of the IRGA PTM-48M, which is suitable for measuring flat leaves, was replaced with a chamber enclosing 20 cm2 (2 × 10 cm) of shoot surface area. The chamber, which was made of 0.2-cm-thick polyethylene, had a volume of 4 cm3; the airflow through the chamber was 11.6 cm3·s−1. The chamber was attached directly to the shoot with two pieces of cellophane tape. The air, which entered the chamber through two identical openings, one on each side of the chamber, was pumped through the center of the chamber via a 0.4-cm-diameter tube to the IRGA PTM-48M. This set-up created a constant turbulent flow that minimized leaf boundary resistance and permitted a restricted amount of air to be drawn into the chamber. A detailed description of the chamber and the gas exchange calculation is given in Weiss et al. (2009).

Nocturnal acidity assay.

Nocturnal acid accumulation (ΔH+), a measure that reflects nighttime CO2 uptake in CAM plants (Osmond, 1978), was determined 90 d (n = five for each treatment) and 150 d (data not shown) after the beginning of the experiment. Shoot tissue was sampled with a cork borer (0.9 cm in diameter) at dusk [1800 hr (H+ dusk)] and at dawn [0530 hr (H+ dawn)]. All tissue samples were frozen immediately in liquid N2 and stored at –20 °C for subsequent analysis. For acid analysis, the shoot tissue was homogenized with 10 mL of double-distilled water with an ice-cold pestle and mortar. The homogenate was titrated against 0.01 N NaOH to pH 7.4. ΔH+ was then estimated as ΔH+ = H+ dawn – H+ dusk (Nobel and Israel, 1994).

Shoot nutrient assay.

Third-order shoots (n = eight for each treatment) were selected at random at the end of the experiment. Samples were washed with doubly distilled water and were then oven dried at 70 °C to constant mass (48–72 h). The dry mass was ground in a grinder to a fine powder, which was used for further analyses. Samples were acid digested (with concentrated H2SO4) and analyzed for reduced nitrogen content by the Kjeldahl method (Bradstreet, 1965). Phosphorus and potassium concentrations were assayed by coupled plasma atomic emission spectrometry (ICP-AES Optima 3000; Perkin Elmer, Norwalk, CT).

Measurements of growth and biomass.

Total shoot lengths were measured with a measuring tape on 17 Sept. 2006, 27 Nov. 2006, 3 Feb. 2007, and 15 Aug. 2007. At the end of the experiment, the plants were harvested, and shoots and roots were separated. Roots were washed gently to remove soil and were blotted (n = 10 for each treatment). To determine root dry mass, roots were oven dried at 70 °C to constant mass (48–72 h). Shoot dry mass was determined by multiplying total shoot length by the average percentage of dry mass to length ratio of six shoot segments (each 30 cm long) sampled from each of the measured plants.

Statistical analysis.

Statistical analyses were performed with JMP IN 5.0 ® software (SAS Institute, Cary, NC), using analysis of variance (ANOVA) and Tukey's honest significant difference (hsd) test, with significance set at P < 0.05. Statistical analyses of the effect of CO2 and fertilization and their interaction are summarized in Table 1.

Table 1.

Probability values of analysis of variance and Tukey's honestly significant difference test for the effects of CO2, nutrient and their interactions on total daily net CO2 uptake, maximal net CO2 uptake rate, nocturnal acid accumulation, shoot nutrient concentration (N, P, and K), total shoot length, shoot dry mass, root dry mass, total dry mass, and root/shoot dry mass ratio of Hylocereus undatus plants grown at elevated and ambient CO2 (1000 and 380 μmol·mol−1, respectively) under high and low nutrient concentrations (0.5- and 0.1-strength Hoagland's solution, respectively).

Table 1.

Results

Net CO2 uptake.

For H. undatus, CO2 uptake occurred mostly at night (Fig. 2). At the high nutrient concentration, net CO2 uptake rate peaked earlier in the night under the elevated CO2 concentration than under the ambient concentration (2200 vs. 0100 hr). For the low nutrient treatment, maximal CO2 uptake rate was recorded earlier in the night (at 2000 hr), regardless of the CO2 treatment. However, for these plants, CO2 uptake rate toward the end of the night (0330–0800 hr) was higher in plants exposed to the ambient CO2 concentration than in those grown with CO2 enrichment (Fig. 2). High nutrient treatment significantly increased the total daily net CO2 uptake by 36% and 49% under the ambient and elevated CO2 treatments, respectively (Fig. 3A, Table 1). CO2 enrichment significantly increased the total daily net CO2 uptake by 39% and 52% under the low and high nutrient treatments, respectively. Under CO2 enrichment, the maximal values of net CO2 uptake rates were 5.2 and 10.2 μmol·m−2·s−1 at low and high nutrient treatments, respectively (Fig. 3B). Under the ambient CO2 concentration, maximal net CO2 uptake rate was 3.0 and 4.8 μmol·m−2·s−1 at low and high nutrient treatments, respectively. The elevated CO2/high nutrient combination raised the total daily net CO2 uptake by 108% in comparison with the ambient CO2/low nutrient combination (Fig. 3A, Table 1). There was a significant synergistic effect (CO2 × nutrient interaction; Table 1) of the elevated CO2/high nutrient combination on total daily net CO2 uptake. There was no significant effect of the elevated CO2/high nutrient combination on maximal net CO2 uptake rate (Fig. 3B, Table 1).

Fig. 2.
Fig. 2.

Daily course of rates of net CO2 uptake in Hylocereus undatus plants grown for 212 d at elevated CO2 [1000 μmol·mol−1 (●)] and ambient CO2 [380 μmol·mol−1 (○)] under high (A) and low (B) nutrient concentrations (0.5- and 0.1-strength Hoagland's solution, respectively). Measurements were taken every 30 min over a period of 4 d (15–18 Mar. 2007). Average day/night air temperature was 25/13 °C, and total daily instantaneous PPF was 18 mol·m−2·d−1. The shaded area at the bottom of the figure represents the nighttime hours. Values are means ± se (n = eight plants).

Citation: Journal of the American Society for Horticultural Science J. Amer. Soc. Hort. Sci. 134, 3; 10.21273/JASHS.134.3.364

Fig. 3.
Fig. 3.

Total daily net CO2 uptake (A) and maximal net CO2 uptake rate (B) in Hylocereus undatus plants grown for 212 d at elevated and ambient CO2 (1000 and 380 μmol·mol−1, respectively) under high and low nutrient concentrations (0.5- and 0.1-strength Hoagland's solution, respectively). Values are means ± se (n = eight plants). Total daily net CO2 uptake data were obtained by integrating the instantaneous rates in Fig. 2. Different letters represent significant differences between treatments at P < 0.05 (analysis of variance and Tukey's honestly significant difference test).

Citation: Journal of the American Society for Horticultural Science J. Amer. Soc. Hort. Sci. 134, 3; 10.21273/JASHS.134.3.364

Nocturnal acid accumulation.

High nutrient treatment increased the total nocturnal acid accumulation by 21% and 42% under the ambient and the elevated CO2 treatments, respectively (Fig. 4). CO2 enrichment increased the nocturnal acid accumulation by 24% and 46% under the low and high nutrient treatments, respectively. The elevated CO2/high nutrient combination raised nocturnal acid accumulation by 77% in comparison with the ambient CO2/low nutrient combination (Fig. 4, Table 1). After 90 d, there was a significant synergistic effect of the elevated CO2/high nutrient combination on nocturnal acid accumulation (Fig. 4, Table 1). Similar results were obtained for the 150-d measurement (data not shown).

Fig. 4.
Fig. 4.

Effect of elevated CO2 on the nocturnal acid accumulation of Hylocereus undatus plants grown for 90 d at elevated and ambient CO2 (1000 and 380 μmol·mol−1, respectively) under high and low nutrient concentrations (0.5- and 0.1-strength Hoagland's solution, respectively). Values are means ± se (n = five plants). Different letters represent significant differences between treatments at P < 0.05 (analysis of variance and Tukey's honestly significant difference test).

Citation: Journal of the American Society for Horticultural Science J. Amer. Soc. Hort. Sci. 134, 3; 10.21273/JASHS.134.3.364

Shoot nutrient concentration.

High nutrient treatment significantly increased shoot N concentration in comparison with low nutrient treatment (by 171% for the ambient CO2 group and by 105% for the elevated CO2 treatment). At the low nutrient concentration, elevated CO2 did not have any significant effect on shoot N concentration, whereas at the high nutrient concentration, elevated CO2 caused a significant reduction of as much as 41% in shoot N concentration (Fig. 5A). The elevated CO2 treatment in combination with the high nutrient treatment significantly increased shoot P concentration by 50% to 102% in comparison with plants grown under ambient and low nutrient conditions (Fig. 5B). Thus, the nature of the elevated CO2/high nutrient combination had a significant effect on shoot N and P concentration. There was, however, no significant effect of either factor, alone or in combination, on shoot K concentration (Fig. 5C, Table 1).

Fig. 5.
Fig. 5.

Mean shoot N (A), P (B), and K (C) concentrations (% of dry mass) of Hylocereus undatus plants grown for 1 year at elevated and ambient CO2 (1000 and 380 μmol·mol−1, respectively) under high and low nutrient concentrations (0.5- and 0.1-strength Hoagland's solution, respectively). Values are means ± se (n = five plants). Different letters represent significant differences between treatments at P < 0.05 (analysis of variance and Tukey's honestly significant difference test).

Citation: Journal of the American Society for Horticultural Science J. Amer. Soc. Hort. Sci. 134, 3; 10.21273/JASHS.134.3.364

Shoot length.

Total shoot length was significantly increased by high nutrient treatment at ambient and elevated CO2 concentrations for all the sampling dates (Fig. 6). At the end of the experiment, total shoot length under the high nutrient treatment had increased by 198% at ambient CO2 and by 218% at elevated CO2 (Fig. 6, Table 1) in comparison with the values for low nutrient treatment. Total shoot length was significantly increased (22%) by elevated CO2 only under the high nutrient regime (e.g., in February and Aug. 2007). The elevated CO2/high nutrient combination increased total shoot length by 224% and 264% in Feb. 2007 and Aug. 2007, respectively, in comparison with the ambient CO2/low nutrient combination (Fig. 6, Table 1). These effects were found to be synergistic (Table 1). During January/February, the response of shoot elongation to elevated CO2 was about 3-fold higher for the high nutrient treatment than for low nutrient treatment [increases of 49% vs. 18%, respectively (Fig. 6, Table 1)].

Fig. 6.
Fig. 6.

Effect of elevated CO2 on total shoot length of Hylocereus undatus plants grown for 1 year at elevated CO2 [1000 μmol·mol−1 (solid symbols)] and ambient CO2 [380 μmol·mol−1 (open symbols)] CO2 and under high [0.5-strength Hoagland's solution (circles)] and low [0.1-strength Hoagland's solution (triangles)] nutrient concentrations. Values are means ± se (n = 10 plants). Different letters represent significant differences between treatments within a specific sampling date at P < 0.05 (analysis of variance and Tukey's honestly significant difference test).

Citation: Journal of the American Society for Horticultural Science J. Amer. Soc. Hort. Sci. 134, 3; 10.21273/JASHS.134.3.364

Biomass.

High nutrient treatment promoted significant increases in total dry mass and shoot dry mass under ambient and elevated CO2 treatments (Fig. 7, A and C). The effect of nutrient treatment on dry mass was more marked than the effect of CO2 treatment. For example, at elevated CO2, the total dry mass increased by 197% at high nutrient versus low nutrient concentrations. However, only under the high nutrient treatment did elevated CO2 significantly increase total dry mass (18% at elevated CO2 vs. ambient CO2) and shoot dry mass (Fig. 7, A and C; Table 1).

Fig. 7.
Fig. 7.

Effect of elevated CO2 on the shoot dry mass (A), root dry mass (B), total dry mass (C) and root/stem dry mass ratio (D) of Hylocereus undatus plants grown for 1 year at elevated and ambient CO2 (1000 and 380 μmol·mol−1, respectively) under high and low nutrient concentrations (0.5- and 0.1-strength Hoagland's solution, respectively). Values are means ± se (n = 10 plants). Different letters represent significant differences between treatments at P < 0.05 (analysis of variance and Tukey's honestly significant difference test).

Citation: Journal of the American Society for Horticultural Science J. Amer. Soc. Hort. Sci. 134, 3; 10.21273/JASHS.134.3.364

Root dry mass was significantly increased (by 56%) under elevated CO2 compared with ambient CO2, but only for the high nutrient treatment (Fig. 7B, Table 1). There was no significant effect of elevated CO2 or high nutrient treatment on root/shoot dry mass ratios (Fig. 7D, Table 1). The elevated CO2/high nutrient combination caused shoot dry mass, root dry mass, and total dry mass to increase by 110%, 100%, and 111%, respectively, in comparison with the ambient CO2/low nutrient combination (Fig. 7, Table 1). These effects were characterized by a synergistic pattern (Table 1).

Discussion

The findings described above support the hypothesis that the response of H. undatus to CO2 enrichment increases as nutrient availability increases. The results of this study on a CAM species are consistent with those of earlier studies on C3 and C4 plants (Coleman et al., 1991; Ghannoum et al., 2000; Poorter and Perez-Soba, 2001): A comparison of the summed relative effect of CO2 and nutrient on each of the measured parameters (predicted values, calculated from Figs. 3, 4, 6, and 7, A–C) with their observed relative effect showed a synergistic effect of CO2 and nutrient in most of the measured parameters (Fig. 8). For example, the increases in shoot dry mass in response to elevated CO2 alone (elevated CO2/low nutrient vs. ambient CO2/low nutrient) and to high nutrient alone (ambient CO2/low nutrient vs. ambient CO2/high nutrient) were 6% and 79%, respectively, leading to a predicted sum effect of 85%. The measured effect of both treatments (elevated CO2/high nutrient vs. ambient CO2/low nutrient) demonstrated an increase of 110%. The difference between the measured and predicted values (25% higher than the predicted sum effect) reflect the percentages of synergism.

Fig. 8.
Fig. 8.

Observed and predicted relative effects of the interaction between CO2 and nutrient treatments on total daily net CO2 uptake (A), maximal net CO2 uptake rate (B), nocturnal acid accumulation (C), total shoot length (D, E, F, and G measured in Sept. 2006, Nov. 2006, Feb. 2007, and Aug. 2007, respectively), total dry mass (H), root dry mass (I), and shoot dry mass (J) of Hylocereus undatus plants grown for 1 year at elevated and ambient CO2 (1000 and 380 μmol·mol−1, respectively) under high and low nutrient concentrations (0.5- and 0.1-strength Hoagland's solution, respectively). Predicted values are the summed effects of the separate responses to each factor (CO2 and nutrient treatments). Points above the 1:1 line demonstrate a positive synergistic effect of CO2 and nutrient treatments. Asterisks represent significant interaction between treatments at P < 0.05 (analysis of variance and Tukey's honestly significant difference test; Table 1).

Citation: Journal of the American Society for Horticultural Science J. Amer. Soc. Hort. Sci. 134, 3; 10.21273/JASHS.134.3.364

Similar results were found previously for C3 plants (Zhang et al., 2006). The mechanism behind those interactions could be attributed to the fact that elevated CO2 is expected to enhance photosynthesis, which in turn increases growth, resulting in increased nutrient demand. Therefore, increased nutrient availability can support synergistic increases in plant growth and biomass production at elevated CO2, as was previously demonstrated (Poorter and Perez-Soba, 2001; Reich et al., 2006). In our study, the nutrient effect on shoot growth was more than 10 times higher than the effect of elevated CO2, as was found previously for C3 and C4 plants (Coleman et al., 1991; Newman et al., 2006). In contrast, the nutrient effect on root growth (Fig. 7B) was significant only under elevated CO2, as has also been reported for C3 and C4 plants (Carswell et al., 2000; Kim et al., 2001). Increase in root/shoot dry mass ratio in response to elevated CO2 was previously found in C3 plants (Carswell et al., 2000), and a similar (P > 0.05) trend was also demonstrated in the current study (Fig. 7D, Table 1), probably due to high within-treatment variation. The magnitude of the increase in biomass due to elevated CO2 for H. undatus was in the same range as that found in nine species of CAM plants by Poorter and Navas (2003). These findings demonstrate a CO2-unsaturated photosynthetic process in CAM plants exposed to ambient CO2.

For the low nutrient treatment groups, the lack or attenuation of the stimulation of biomass production and total shoot length in response to elevated CO2, as observed here (Figs. 6 and 7) and in previous studies on C3 and C4 plants, was originally explained by a downward acclimation of photosynthesis to elevated CO2, which is known to be more marked under nutrient deficiency (Reich et al., 2006). Yet this downward acclimation of photosynthesis was not evident in our net CO2 uptake and nocturnal acid accumulation measurements (Figs. 2, 3, and 4). Therefore, the “downward acclimation” hypothesis was not applicable to the findings of the present study. Thus, it is necessary to obtain multiple measurements over time to assess possible acclimation. In other studies, the lack of response to elevated CO2 was explained by the limited level of sink strength in the low nutrient treatment, as was also found by Mandre et al. (1995).

Under high nutrient conditions, shoot N, P, and K levels were similar to those of CAM plants in a commercial orchard (Nobel, 1988). Values for shoot N, P, and K concentrations for the at low nutrient/ambient CO2 combination (Fig. 5) were similar to the shoot N, P, and K levels of other CAM plants growing in their natural habitats (Nobel and Pimienta-Barrios, 1995). The values for shoot N concentration for the low nutrient treatment and ambient CO2 were half of those of Nobel and De la Barrera (2002) for H. undatus fertilized with 24 mg·L−1 N, but our study was characterized by a chronically longer nutrient-deficient period (52 vs. 22 weeks). The findings in our study that elevated CO2 significantly decreased shoot N concentration (Fig. 5A) under conditions of high nutrient supply are in keeping with those for C3 and C4 plants grown under a wide range of nitrogen concentrations (Coleman et al., 1991; Hocking and Meyer, 1985; Larigauderie and Oechel, 1988). Our findings may be explained by a dilution of N concentration as a result of the increase in biomass (Ma et al., 2007). In contrast to this N reduction, our study revealed an elevation of shoot P (Fig. 5B) for elevated CO2/high nutrient conditions, as was previously found for C3 plants (Ma et al., 2007). The lack of response of shoot K concentrations to the different treatments (Fig. 5C) may indicate that K availability remained the same for all treatments, and this indicates that the amount of K in the low nutrient treatment was adequate for the needs of the vplants.

In general, total daily net CO2 uptake was significantly increased by elevated CO2 and high nutrient concentrations, as was found previously for H. undatus by Raveh et al. (1995) and Nobel and De la Barrera (2002), respectively. During the second half of the night, there was a reduction in the stimulation of CO2 uptake rates by elevated CO2, but only at low nutrient concentrations (Fig. 2B). Such a pattern was also demonstrated in other CAM species growing under low nutrient conditions and reflects the earlier cessation of acid accumulation (Nobel and Hartsock, 1986). The response to elevated CO2 measured in terms of net CO2 uptake and nocturnal acid accumulation was higher than that measured as an increase in total biomass. However, it should be remembered that the biomass measurement reflects the accumulative response, while net CO2 uptake and nocturnal acid accumulation reflect the effect of CO2 enrichment during a particular measured period.

In contradiction to the assumption that the predominant initial fixation of CO2 by phosphoenolpyruvate carboxylase (PEPCase) in CAM plants is saturated under ambient atmospheric CO2 (Long et al., 2006), our results indicated that most of the stimulation of CO2 uptake by elevated CO2 occurred during the nighttime [phase I: (Osmond, 1978); Fig. 2, A and B] when the uptake of atmospheric CO2 involves the binding of CO2 by PEPCase. Our findings, together with the recently published similar results of Nogues et al. (2008), indicate the presence of a factor restricting CO2 uptake during phase I under ambient conditions.

In conclusion, highly fertilized CAM crops may benefit from elevated atmospheric CO2 to a greater extent than CAM plants grown under low fertilization regimes due to the synergistic effect of high nutrition and elevated CO2. These results pave the way for testing the effect of CO2 enrichment and high fertilization regimes for optimal fruit production. Our findings may be of particular importance in subtropical areas such as Israel, where pitahayas are grown under netting to prevent photoinhibition damage (Raveh et al., 1996; 1998). In this context, it should be noted that stretching a plastic film over the supporting structure during the night to enable enrichment with CO2 should involve only a minimum extra cost, while making a substantial contribution to increasing fruit yield.

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  • Kim, H.Y., Lieffering, M., Miura, S., Kobayashi, K. & Okada, M. 2001 Growth and nitrogen uptake of CO2-enriched rice under field conditions New Phytol. 150 223 229

    • Search Google Scholar
    • Export Citation
  • Kimball, B.A. 1983 Carbon dioxide and agricultural yield: An assemblage and analysis of 430 prior observations Agron. J. 75 779 788

  • Larigauderie, A.D.W.H. & Oechel, W.C. 1988 Effect of CO2 enrichment and nitrogen availability on resource acquisition and resource-allocation in a grass, Bromus mollis Oecologia 77 544 549

    • Search Google Scholar
    • Export Citation
  • Long, S.P., Ainsworth, E.A., Leakey, A.D.B., Nosberger, J. & Ort, D.R. 2006 Food for thought: Lower than expected crop yield stimulation with rising CO2 concentrations Science 312 1918 1921

    • Search Google Scholar
    • Export Citation
  • Ma, H.L., Zhu, J.G., Xie, Z.B., Liu, G., Zeng, Q. & Han, Y. 2007 Responses of rice and winter wheat to free-air CO2 enrichment (China FACE) at rice/wheat rotation system Plant Soil 294 137 146

    • Search Google Scholar
    • Export Citation
  • Mandre, O., Rieger, M., Myers, S.C., Seversen, R. & Regnard, J.L. 1995 Interaction of root confinement and fruiting in peach J. Amer. Soc. Hort. Sci. 120 228 234

    • Search Google Scholar
    • Export Citation
  • Mizrahi, Y., Nerd, A. & Nobel, P.S. 1997 Cacti as crops Hort. Rev. (Amer. Soc. Hort. Sci.) 18 321 346

  • Mizrahi, Y., Raveh, E., Yossov, E., Nerd, A. & Ben-Asher, J. 2007 New fruit crops with high water use efficiency 216 222 Janick J. & Whipkey A. Creating markets for economic development of new crops and new uses ASHS Press Alexandria VA

    • Search Google Scholar
    • Export Citation
  • Newman, Y.C., Sollenberger, L.E., Boote, K.J., Allen L.H. Jr, Thomas, J.M. & Littell, R.C. 2006 Nitrogen fertilization affects bahiagrass responses to elevated atmospheric carbon dioxide Agron. J. 98 382 387

    • Search Google Scholar
    • Export Citation
  • Newton, P.C.D. 1991 Direct effects of increasing carbon dioxide on pasture plants and communities N.Z. J. Agr. Res. 34 1 24

  • Nobel, P.S. 1988 Environmental biology of agaves and cacti Cambridge University Press New York

  • Nobel, P.S. & Israel, A.A. 1994 Cladode development, environmental responses of CO2 uptake, and productivity for Opuntia ficus-indica under elevated CO2 J. Expt. Bot. 45 295 303

    • Search Google Scholar
    • Export Citation
  • Nobel, P.S. & De la Barrera, E. 2002 Nitrogen relations for net CO2 uptake by the cultivated hemiepiphytic cactus, Hylocereus undatus Scientia Hort. 96 281 292

    • Search Google Scholar
    • Export Citation
  • Nobel, P.S. & Hartsock, T.L. 1986 Short-term and long-term responses of crassulacean acid metabolism plants to elevated CO2 Plant Physiol. 82 604 606

    • Search Google Scholar
    • Export Citation
  • Nobel, P.S. & Pimienta-Barrios, E. 1995 Monthly stem elongation for Stenocereus queretaroensis: Relationships to environmental conditions, net CO2 uptake and seasonal variations in sugar content Environ. Exp. Bot. 35 17 24

    • Search Google Scholar
    • Export Citation
  • Nobel, P.S., Cui, M. & Israel, A.A. 1994 Light, chlorophyll, carboxylase activity and CO2 fixation at various depths in the chlorenchyma of Opuntia ficus-indica (L.) Miller under current and elevated CO2 New Phytol. 128 315 322

    • Search Google Scholar
    • Export Citation
  • Nogues, S., Aranjuelo, I., Pardo, A. & Azcon-Bieto, J. 2008 Assessing the stable carbon isotopic composition of intercellular CO2 in a CAM plant using gas chromatography-combustion-isotope ratio mass spectrometry Rapid Commun. Mass Spectrom. 22 1017 1022

    • Search Google Scholar
    • Export Citation
  • Osmond, C.B. 1978 Crassulacean acid metabolism: Curiosity in context Annu. Rev. Plant Physiol. Plant Mol. Biol. 29 379 414

  • Poorter, H. 1993 Interspecific variation in the growth-response of plants to an elevated ambient CO2 concentration Plant Ecol. 104-105 77 97

  • Poorter, H. & Navas, M.L. 2003 Plant growth and competition at elevated CO2: On winners, losers and functional groups New Phytol. 157 175 198

  • Poorter, H. & Perez-Soba, M. 2001 The growth response of plants to elevated CO2 under non-optimal environmental conditions Oecologia 129 1 20

  • Raveh, E., Nerd, A. & Mizrahi, Y. 1996 Responses of climbing cacti to different levels of shade and to carbon dioxide enrichment Acta Hort. 434 271 278

    • Search Google Scholar
    • Export Citation
  • Raveh, E., Nerd, A. & Mizrahi, Y. 1998 Responses of two hemiepiphytic fruit crop cacti to different degrees of shade Scientia Hort. 73 151 164

  • Raveh, E., Gersani, M. & Nobel, P.S. 1995 CO2 uptake and fluorescence responses for a shade-tolerant cactus Hylocereus undatus under current and doubled CO2 concentrations Physiol. Plant. 93 505 511

    • Search Google Scholar
    • Export Citation
  • Reich, P.B., Hobbie, S.E., Lee, T., Ellsworth, D.S., West, J.B., Tilman, D., Knops, J.M.H., Naeem, S. & Trost, J. 2006 Nitrogen limitation constrains sustainability of ecosystem response to CO2 Nature 440 922 925

    • Search Google Scholar
    • Export Citation
  • Szarek, S.R., Holthe, P.A. & Ting, I.P. 1987 Minor physiological response to elevated CO2 by the CAM plant Agave vilmoriniana Plant Physiol. 83 938 940

    • Search Google Scholar
    • Export Citation
  • Weiss, I., Mizrahi, Y. & Raveh, E. 2009 Chamber response time: A neglected issue in gas exchange measurements Photosynthetica 47 121 124

  • Zhang, S.R., Dang, Q.L. & Yu, X.G. 2006 Nutrient and CO2 elevation had synergistic effects on biomass production but not on biomass allocation of white birch seedlings For. Ecol. Mgt. 234 238 244

    • Search Google Scholar
    • Export Citation

Contributor Notes

Corresponding author. E-mail: eran@agri.gov.il.

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    Monthly averages of (A) maximum [Tmax (○)], mean [Tmean (Δ)], and minimum [Tmin (□)] daily air temperature and (B) total daily instantaneous PPF (◇) in the growth chambers situated in a cooled greenhouse during the period 15 Aug. 2006 to 15 Aug. 2007. Values are means ± se.

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    Daily course of rates of net CO2 uptake in Hylocereus undatus plants grown for 212 d at elevated CO2 [1000 μmol·mol−1 (●)] and ambient CO2 [380 μmol·mol−1 (○)] under high (A) and low (B) nutrient concentrations (0.5- and 0.1-strength Hoagland's solution, respectively). Measurements were taken every 30 min over a period of 4 d (15–18 Mar. 2007). Average day/night air temperature was 25/13 °C, and total daily instantaneous PPF was 18 mol·m−2·d−1. The shaded area at the bottom of the figure represents the nighttime hours. Values are means ± se (n = eight plants).

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    Total daily net CO2 uptake (A) and maximal net CO2 uptake rate (B) in Hylocereus undatus plants grown for 212 d at elevated and ambient CO2 (1000 and 380 μmol·mol−1, respectively) under high and low nutrient concentrations (0.5- and 0.1-strength Hoagland's solution, respectively). Values are means ± se (n = eight plants). Total daily net CO2 uptake data were obtained by integrating the instantaneous rates in Fig. 2. Different letters represent significant differences between treatments at P < 0.05 (analysis of variance and Tukey's honestly significant difference test).

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    Effect of elevated CO2 on the nocturnal acid accumulation of Hylocereus undatus plants grown for 90 d at elevated and ambient CO2 (1000 and 380 μmol·mol−1, respectively) under high and low nutrient concentrations (0.5- and 0.1-strength Hoagland's solution, respectively). Values are means ± se (n = five plants). Different letters represent significant differences between treatments at P < 0.05 (analysis of variance and Tukey's honestly significant difference test).

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    Mean shoot N (A), P (B), and K (C) concentrations (% of dry mass) of Hylocereus undatus plants grown for 1 year at elevated and ambient CO2 (1000 and 380 μmol·mol−1, respectively) under high and low nutrient concentrations (0.5- and 0.1-strength Hoagland's solution, respectively). Values are means ± se (n = five plants). Different letters represent significant differences between treatments at P < 0.05 (analysis of variance and Tukey's honestly significant difference test).

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    Effect of elevated CO2 on total shoot length of Hylocereus undatus plants grown for 1 year at elevated CO2 [1000 μmol·mol−1 (solid symbols)] and ambient CO2 [380 μmol·mol−1 (open symbols)] CO2 and under high [0.5-strength Hoagland's solution (circles)] and low [0.1-strength Hoagland's solution (triangles)] nutrient concentrations. Values are means ± se (n = 10 plants). Different letters represent significant differences between treatments within a specific sampling date at P < 0.05 (analysis of variance and Tukey's honestly significant difference test).

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    Effect of elevated CO2 on the shoot dry mass (A), root dry mass (B), total dry mass (C) and root/stem dry mass ratio (D) of Hylocereus undatus plants grown for 1 year at elevated and ambient CO2 (1000 and 380 μmol·mol−1, respectively) under high and low nutrient concentrations (0.5- and 0.1-strength Hoagland's solution, respectively). Values are means ± se (n = 10 plants). Different letters represent significant differences between treatments at P < 0.05 (analysis of variance and Tukey's honestly significant difference test).

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    Observed and predicted relative effects of the interaction between CO2 and nutrient treatments on total daily net CO2 uptake (A), maximal net CO2 uptake rate (B), nocturnal acid accumulation (C), total shoot length (D, E, F, and G measured in Sept. 2006, Nov. 2006, Feb. 2007, and Aug. 2007, respectively), total dry mass (H), root dry mass (I), and shoot dry mass (J) of Hylocereus undatus plants grown for 1 year at elevated and ambient CO2 (1000 and 380 μmol·mol−1, respectively) under high and low nutrient concentrations (0.5- and 0.1-strength Hoagland's solution, respectively). Predicted values are the summed effects of the separate responses to each factor (CO2 and nutrient treatments). Points above the 1:1 line demonstrate a positive synergistic effect of CO2 and nutrient treatments. Asterisks represent significant interaction between treatments at P < 0.05 (analysis of variance and Tukey's honestly significant difference test; Table 1).

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  • Coleman, J.S., Rochefort, L., Bazzaz, F.A. & Woodward, F.I. 1991 Atmospheric CO2, plant nitrogen status and the susceptibility of plants to an acute increase in temperature Plant Cell Environ. 14 667 674

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  • Drennan, P.M. & Nobel, P.S. 2000 Responses of CAM species to increasing atmospheric CO2 concentrations Plant Cell Environ. 23 767 781

  • Ghannoum, O., Von Caemmerer, S., Ziska, L.H. & Conroy, J.P. 2000 The growth response of C4 plants to rising atmospheric CO2 partial pressure: A reassessment Plant Cell Environ. 23 931 942

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  • Hocking, P.J. & Meyer, C.P. 1985 Responses of noogoora burr (Xanthium occidentale Bertol.) to nitrogen supply and carbon-dioxide enrichment Ann. Bot. (Lond.) 55 835 844

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  • Holtum, J.A.M., Oleary, M.H. & Osmond, C.B. 1983 Effect of varying CO2 partial-pressure on photosynthesis and on carbon isotope composition of carbon-4 of malate from the crassulacean acid metabolism plant Kalanchoe daigremontiana Hamet et Perr Plant Physiol. 71 602 609

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    • Export Citation
  • Kim, H.Y., Lieffering, M., Miura, S., Kobayashi, K. & Okada, M. 2001 Growth and nitrogen uptake of CO2-enriched rice under field conditions New Phytol. 150 223 229

    • Search Google Scholar
    • Export Citation
  • Kimball, B.A. 1983 Carbon dioxide and agricultural yield: An assemblage and analysis of 430 prior observations Agron. J. 75 779 788

  • Larigauderie, A.D.W.H. & Oechel, W.C. 1988 Effect of CO2 enrichment and nitrogen availability on resource acquisition and resource-allocation in a grass, Bromus mollis Oecologia 77 544 549

    • Search Google Scholar
    • Export Citation
  • Long, S.P., Ainsworth, E.A., Leakey, A.D.B., Nosberger, J. & Ort, D.R. 2006 Food for thought: Lower than expected crop yield stimulation with rising CO2 concentrations Science 312 1918 1921

    • Search Google Scholar
    • Export Citation
  • Ma, H.L., Zhu, J.G., Xie, Z.B., Liu, G., Zeng, Q. & Han, Y. 2007 Responses of rice and winter wheat to free-air CO2 enrichment (China FACE) at rice/wheat rotation system Plant Soil 294 137 146

    • Search Google Scholar
    • Export Citation
  • Mandre, O., Rieger, M., Myers, S.C., Seversen, R. & Regnard, J.L. 1995 Interaction of root confinement and fruiting in peach J. Amer. Soc. Hort. Sci. 120 228 234

    • Search Google Scholar
    • Export Citation
  • Mizrahi, Y., Nerd, A. & Nobel, P.S. 1997 Cacti as crops Hort. Rev. (Amer. Soc. Hort. Sci.) 18 321 346

  • Mizrahi, Y., Raveh, E., Yossov, E., Nerd, A. & Ben-Asher, J. 2007 New fruit crops with high water use efficiency 216 222 Janick J. & Whipkey A. Creating markets for economic development of new crops and new uses ASHS Press Alexandria VA

    • Search Google Scholar
    • Export Citation
  • Newman, Y.C., Sollenberger, L.E., Boote, K.J., Allen L.H. Jr, Thomas, J.M. & Littell, R.C. 2006 Nitrogen fertilization affects bahiagrass responses to elevated atmospheric carbon dioxide Agron. J. 98 382 387

    • Search Google Scholar
    • Export Citation
  • Newton, P.C.D. 1991 Direct effects of increasing carbon dioxide on pasture plants and communities N.Z. J. Agr. Res. 34 1 24

  • Nobel, P.S. 1988 Environmental biology of agaves and cacti Cambridge University Press New York

  • Nobel, P.S. & Israel, A.A. 1994 Cladode development, environmental responses of CO2 uptake, and productivity for Opuntia ficus-indica under elevated CO2 J. Expt. Bot. 45 295 303

    • Search Google Scholar
    • Export Citation
  • Nobel, P.S. & De la Barrera, E. 2002 Nitrogen relations for net CO2 uptake by the cultivated hemiepiphytic cactus, Hylocereus undatus Scientia Hort. 96 281 292

    • Search Google Scholar
    • Export Citation
  • Nobel, P.S. & Hartsock, T.L. 1986 Short-term and long-term responses of crassulacean acid metabolism plants to elevated CO2 Plant Physiol. 82 604 606

    • Search Google Scholar
    • Export Citation
  • Nobel, P.S. & Pimienta-Barrios, E. 1995 Monthly stem elongation for Stenocereus queretaroensis: Relationships to environmental conditions, net CO2 uptake and seasonal variations in sugar content Environ. Exp. Bot. 35 17 24

    • Search Google Scholar
    • Export Citation
  • Nobel, P.S., Cui, M. & Israel, A.A. 1994 Light, chlorophyll, carboxylase activity and CO2 fixation at various depths in the chlorenchyma of Opuntia ficus-indica (L.) Miller under current and elevated CO2 New Phytol. 128 315 322

    • Search Google Scholar
    • Export Citation
  • Nogues, S., Aranjuelo, I., Pardo, A. & Azcon-Bieto, J. 2008 Assessing the stable carbon isotopic composition of intercellular CO2 in a CAM plant using gas chromatography-combustion-isotope ratio mass spectrometry Rapid Commun. Mass Spectrom. 22 1017 1022

    • Search Google Scholar
    • Export Citation
  • Osmond, C.B. 1978 Crassulacean acid metabolism: Curiosity in context Annu. Rev. Plant Physiol. Plant Mol. Biol. 29 379 414

  • Poorter, H. 1993 Interspecific variation in the growth-response of plants to an elevated ambient CO2 concentration Plant Ecol. 104-105 77 97

  • Poorter, H. & Navas, M.L. 2003 Plant growth and competition at elevated CO2: On winners, losers and functional groups New Phytol. 157 175 198

  • Poorter, H. & Perez-Soba, M. 2001 The growth response of plants to elevated CO2 under non-optimal environmental conditions Oecologia 129 1 20

  • Raveh, E., Nerd, A. & Mizrahi, Y. 1996 Responses of climbing cacti to different levels of shade and to carbon dioxide enrichment Acta Hort. 434 271 278

    • Search Google Scholar
    • Export Citation
  • Raveh, E., Nerd, A. & Mizrahi, Y. 1998 Responses of two hemiepiphytic fruit crop cacti to different degrees of shade Scientia Hort. 73 151 164

  • Raveh, E., Gersani, M. & Nobel, P.S. 1995 CO2 uptake and fluorescence responses for a shade-tolerant cactus Hylocereus undatus under current and doubled CO2 concentrations Physiol. Plant. 93 505 511

    • Search Google Scholar
    • Export Citation
  • Reich, P.B., Hobbie, S.E., Lee, T., Ellsworth, D.S., West, J.B., Tilman, D., Knops, J.M.H., Naeem, S. & Trost, J. 2006 Nitrogen limitation constrains sustainability of ecosystem response to CO2 Nature 440 922 925

    • Search Google Scholar
    • Export Citation
  • Szarek, S.R., Holthe, P.A. & Ting, I.P. 1987 Minor physiological response to elevated CO2 by the CAM plant Agave vilmoriniana Plant Physiol. 83 938 940

    • Search Google Scholar
    • Export Citation
  • Weiss, I., Mizrahi, Y. & Raveh, E. 2009 Chamber response time: A neglected issue in gas exchange measurements Photosynthetica 47 121 124

  • Zhang, S.R., Dang, Q.L. & Yu, X.G. 2006 Nutrient and CO2 elevation had synergistic effects on biomass production but not on biomass allocation of white birch seedlings For. Ecol. Mgt. 234 238 244

    • Search Google Scholar
    • Export Citation
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