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. 2004 Nov 26;95(2):363–369. doi: 10.1093/aob/mci034

Young Daughter Cladodes Affect CO2 Uptake by Mother Cladodes of Opuntia ficus-indica

EULOGIO PIMIENTA-BARRIOS 1,*, JULIA ZAÑUDO-HERNANDEZ 1, VERONICA C ROSAS-ESPINOZA 1, AMARANTA VALENZUELA-TAPIA 1, PARK S NOBEL 2
PMCID: PMC4246837  PMID: 15567805

Abstract

• Background and Aims Drought damages cultivated C3, C4 and CAM plants in the semi-arid lands of central Mexico. Drought damage to Opuntia is common when mother cladodes, planted during the dry spring season, develop young daughter cladodes that behave like C3 plants, with daytime stomatal opening and water loss. In contrast, wild Opuntia are less affected because daughter cladodes do not develop on them under extreme drought conditions. The main objective of this work is to evaluate the effects of the number of daughter cladodes on gas exchange parameters of mother cladodes of Opuntia ficus-indica exposed to varying soil water contents.

• Methods Rates of net CO2 uptake, stomatal conductance, intercellular CO2 concentration, chlorophyll content and relative water content were measured in mature mother cladodes with a variable number of daughter cladodes growing in spring under dry and wet conditions.

• Key Results Daily carbon gain by mother cladodes was reduced as the number of daughter cladodes increased to eight, especially during drought. This was accompanied by decreased mother cladode relative water content, suggesting movement of water from mother to daughter cladodes. CO2 assimilation was most affected in phase IV of CAM (late afternoon net CO2 uptake) by the combined effects of daughter cladodes and drought. Rainfall raised the soil water content, decreasing the effects of daughter cladodes on net CO2 uptake by mother cladodes.

• Conclusions Daughter cladodes significantly hasten the effects of drought on mother cladodes by competition for the water supply and thus decrease daily carbon gain by mother cladodes, mainly by inhibiting phase IV of CAM.

Keywords: Chlorophyll, Crassulacean acid metabolism, drought, gas exchange, net CO2 uptake, Opuntia ficus-indica

INTRODUCTION

The semi-arid lands of central north-western Mexico experienced an unusually dry period during the last part of the 20th century, with annual rainfall below 400 mm (Pimienta-Barrios et al., 2002). Such prolonged drought causes severe damage not only to cultivated C3 and C4 crops, but also to cultivated CAM species (Pimienta-Barrios, 1990). The greatest damage by drought to cultivated species of Opuntia is caused to mother cladodes from which young cladodes develop during spring. In contrast to cultivated opuntias, wild opuntias generally do not develop young cladodes when extreme drought conditions prevail; this has been considered an avoidance strategy to prevent water loss (Pimienta-Barrios et al., 2002, 2003). During the early stages of development, daughter cladodes exhibit C3 photosynthesis with daytime stomatal opening (Osmond, 1978; Acevedo et al., 1983) and require water import from the mother cladodes (Nobel et al., 1994a; N. Wang et al., 1997). Classically, CAM plants endure drought by maintaining night-time CO2 uptake, together with morphological succulence and anatomical modifications such as thick cuticles and low stomatal frequency (Nobel, 1985). Their photosynthetic plasticity in response to drought has received less attention (Mattos et al., 1999; Cushman, 2001; Dodd et al., 2002; Keeley and Rundel, 2003).

Sink strength can affect the strength of the source, as the removal of actively growing sinks (e.g. tubers, seeds, and young leaves; Gifford and Evans, 1981; Salisbury and Ross, 1992) generally decreases photosynthesis. These observations are essentially only from studies of domesticated C3 and C4 plants (Loomis and Connor, 1992; Z. Wang et al., 1997), while studies relating source and sink for CAM plants are rare. The main objective of the present study was to evaluate the physiological effects of daughter cladodes on the physiology of mature mother cladodes of Opuntia ficus-indica under both wet and dry conditions. An increase in sink strength (greater number of daughter cladodes that develop on a mother cladode) was hypothesized to reduce the photosynthetic capacity of the mother cladodes, especially during drought, because daughter cladodes import water and organic matter from the mother cladodes.

MATERIALS AND METHODS

Site description, plant material and experimental design

The study was performed during spring 2003 at an experimental field of the Departamento de Ecología of the Universidad de Guadalajara. The site is in central Jalisco, Mexico, at 20°5′N, 103°32′W, and 1420 m above sea level. The climate is temperate-subtropical. Daily air temperature and rainfall were obtained from a weather station maintained at the Fifth Military Base of the Mexican Air Force. On the dates of gas exchange measurement, the photosynthetic photon flux (PPF, wavelengths of 400–700 nm) on a horizontal plane was recorded hourly from sunrise to sunset with a LI-250 quantum sensor (LI-COR, Lincoln, NE, USA) and then integrated to get the total daily PPF. Air temperature was recorded every hour using a mercury thermometer. Air relative humidity was recorded hourly using a digital humidity gauge (63–101, RadioShack, Los Angeles, CA, USA).

Mature 12-month-old cladodes (flattened stem segments) of Opuntia ficus-indica (L). Miller (Cactaceae) averaging 35 cm long, 19 cm wide and 1·8 cm thick were harvested from a cultivated population at Nextipac, Jalisco, Mexico. They were planted on 13 March 2003 in plastic pots (19 L) filled with a vermiculite/sand mixture (1 : 1, v : v) and watered weekly with 3 L per pot to promote the sprouting of young cladodes at the beginning of the spring. Daughter cladodes were allowed to develop freely on the mature cladodes; 32 d after planting (15 April 2003) young cladodes were selectively removed, leading to zero, one, two, four or eight daughter cladodes per mother cladode. Each of these five treatments was replicated 16 times, within a completely randomized design. Watering was suspended, allowing the soil around the mother cladode to dry at a rate determined by the conditions prevailing at the study site in the spring. Total rainfall before the last gas exchange measurement on 20–21 June was 110 mm. The length of daughter cladodes was measured weekly using a ruler with the base of the cladode as reference.

Gas exchange measurements

Instantaneous net CO2 uptake, stomatal conductance and intercellular CO2 concentration were measured on all mother cladodes every 2 h over 24-h periods on 9–10 May, 30–31 May, and 20–21 June 2003 with a LI-COR LI-6200 portable photosynthesis system (Li-Cor, Lincoln, NE, USA). A 0·25-L leaf chamber was modified by replacing the distal half-cylinder with a narrowed opening (2 cm × 4 cm) lined with a closed-pore foam gasket that was firmly pressed against an approximately southwest-facing surface of the cladodes.

Chlorophyll content

Five samples for determination of chlorophyll content were removed, using a cork borer 1 cm in diameter, from the centre of mother cladodes in each treatment on the dates on which gas exchange was measured. Chlorophyll was extracted by homogenizing frozen material in cold acetone (80 %). The homogenates were centrifuged for 10 min at 12 000 g at 4 °C; the insoluble material was re-extracted and re-centrifuged. Chlorophyll content (µg cm−2) was calculated from spectophotometric measurements at 645 and 663 nm (Bruinsma, 1961).

Soil water potential, soil water content and cladode relative water content

Soil water potential was determined with a WP4 dew-point potentiometer (Decagon Devices, Pullman, WA, USA) using five samples removed from the centre of the root zone (a depth of 10–15 cm) on the same dates as measurement of gas exchange. Soil water content from the centre of the root zone was also determined for ten soil samples dried at 105 °C to constant mass (generally within 72 h); data are expressed as percentage water content: [(fresh mass − dry mass)/dry mass] × 100 (Torres, 1984). The relative water content (RWC) for mother cladodes was determined between 1000 h and 1100 h for five segments (3 cm × 3 cm) by immediately determining their fresh mass and then oven drying at 80 °C to constant mass. RWC was then calculated (Koide et al., 2000). RWC was also determined for daughter cladodes on 30–31 May and 20–21 June only.

Statistical analysis

Data were analysed using a hierarchical ANOVA (Zar, 1999); means were separated by a least significant difference (LSD) test (Little and Hill, 1975). Data are presented as means ± s.e. (with n = number of measurements).

RESULTS

For 2003, the total daily PPF was higher on 9–10 May (57 mol m−2 d−1) and 30–31 May (55 mol m−2 d−1) than on 20–21 June (50 mol m−2 d−1). Mean day/night temperatures varied little between the three dates: 26/18 °C for 9–10 May, 25/18 °C for 30–31 May, and 24/19 °C for 20–21 June. Day/night relative humidity was highest on 20–21 June (51/57 %), lowest on 9–10 May (31/45 %), and intermediate on 30–31 May (40/68 %).

Elongation of daughter cladodes started in early May 2003, and was slow (0·10 cm d−1) during the first and second weeks; rates increased substantially (0·45 cm d−1) from the third week of May to the end of the first week of June before rainfall started. Once rain fell, daughter cladode growth rate decreased (0·31 cm d−1) (Fig. 1A, B). Rainfall was 91 mm during the second week of June, 56 mm during the third week, and 105 mm during the fourth week, totalling 252 mm for June (Fig. 1B). Both soil water content and soil water potential decreased substantially from the first week to the fourth week of May, but because of rainfall, soil water content increased six-fold and soil water potential increased by over 29 MPa from 30–31 May to 20–21 June (Fig. 1C, D).

Fig. 1.

Fig. 1.

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(A) Elongation of developing daughter cladodes of Opuntia ficus-indica, (B) rainfall, (C) soil water content, and (D) soil water potential. Arrows indicate dates of measurement of gas exchange. Data are means ± s.e. (n = 32 cladodes, eight from each treatment for cladode growth; n = 10 samples for both soil water content and soil water potential).

The first measurement of photosynthesis, RWC and chlorophyll coincided with the initial stages of daughter cladode growth, when the spring dry period started. The second was at the beginning of the linear phase of cladode growth, at the time of the smallest soil water content, soil water potential and RWC in mother cladodes that had developing daughter cladodes (Fig. 1A, C, D; Table 1). The third measurement occurred 10 d after the first noteworthy rainfall, when RWC increased substantially in mother cladodes with and without daughter cladodes. A less pronounced increase in RWC was observed for daughter cladodes (Table 1).

Table 1.

Relationships between number of daughter cladodes and relative water content and chlorophyll content for Opuntia ficus-indica on dates of gas exchange measurement

Date
 Number of daughter cladodes
 Mother cladode RWC (%)
 Daughter cladode RWC (%)
 Mother cladode chlorophyll content (µg cm−2)
9–10 May 2003 0 97a 79a
1 90b 69b
2 84c 55c
4 69d 52c
8 59e 53c
30–31 May 2003 0 84a 69a
1 73b 93a 46b
2 67c 88b 39c
4 61d 81c 42c
8 58d 80c 42c
20–21 June 2003 0 90a 32a
1 85b 89b 34a
2 83b 91a 25a
4 93a 88b 29a
8 91a 88b 32a
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Values within columns for a particular date followed by different letters are significantly different at P < 0·05.

As the number of daughter cladodes increased, the RWC of the mother cladodes decreased progressively and substantially on 9–10 and 30–31 May (Table 1); it was lower, particularly with no or few daughter cladodes, on 30–31 May than on 9–10 May (P < 0·05). Once rainfall occurred, the RWC increased for all the treatments on 20–21 June, but the increase was statistically greater in mother cladodes with zero, four and eight cladodes (Table 1). On 30–31 May the RWC for daughter cladodes was lower when four or eight cladodes grew on mother cladodes, compared with no or fewer daughter cladodes. The RWC for daughter cladodes increased on 20–21 June, but only with two, four and eight daughter cladodes (Table 1).

The chlorophyll content of mother cladodes decreased progressively from zero to two cladodes, but it did not decrease further with four and eight cladodes on 9–10 and 30–31 May (Table 1); such mother cladodes showed yellowing and visible symptoms of dehydration. On 20–21 June the chlorophyll content was lower than in May and was not statistically different between treatments (Table 1).

Gas exchange patterns of mother cladodes varied with the measurement date and the number of daughter cladodes (Fig. 2). For all treatments, positive net CO2 uptake began earlier in the afternoon (phase IV for CAM plants; Osmond, 1978) and lasted about 4 h for the wettest conditions (20–21 June) and was shortest during drought (30–31 May) when, indeed, CO2 uptake became substantially positive in the late afternoon for mother cladodes with no daughter cladodes (Fig. 2A), but only early in the night with one daughter cladode (Fig. 2B), at midnight with two or four daughter cladodes (Fig. 2C, D), and not until after midnight with eight daughter cladodes (Fig. 2E). The treatment with no daughter cladodes tended to have the highest rates of net CO2 uptake, while the lowest night-time rates (phase I) occurred during drought for the mother cladodes with the greatest number of daughter cladodes (Fig. 2E).

Fig. 2.

Fig. 2.

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Net CO2 uptake rates over 24-h periods for mature mother cladodes of O. ficus-indica with (A) no daughter cladodes, (B) one daughter cladode, (C) two daughter cladodes, (D) four daughter cladodes, and (E) eight daughter cladodes. Hatched bars on the axis indicate night-time. Data are means ± s.e. (n = 16 plants).

Carbon gain during phase I for mother cladodes on 9–10 May depended only slightly on the number of daughter cladodes (Table 2). In contrast, during drought (30–31 May) carbon gain sharply decreased with the increase in the number of daughter cladodes (Table 2). For 20–21 June, carbon gain in phase I was lowest with eight daughter cladodes. Phase II (early morning net CO2 uptake) did not vary significantly with the number of daughter cladodes on 9–10 May. On 30–31 May carbon gain was smallest with eight cladodes. On 20–21 June carbon gain during phase II was lower than in May. Phase III (daytime period of net CO2 release) was little affected by the number of daughter cladodes or the measurement date. Carbon gain in phase IV in mother cladodes did not vary significantly in relation to the number of daughter cladodes on 9–10 May, and was absent during drought (30–31 May) when daughter cladodes were present. On 20–21 June after rainfall, carbon gain increased considerably, with no statistical differences between treatments (Table 2).

Table 2.

Total net CO2 uptake during CAM phases, highest rates of CO2 uptake, total daily net CO2 uptake and mean night-time intercellular CO2 mole fraction for mother cladodes in response to number of daughter cladodes on different dates

Date Number ofdaughter cladodes Total net CO2 uptake for indicated phases (mmol m−2)
 Highest rates of CO2 uptake (µmol m−2 s−1) Total daily net CO2 uptake (mmol m−2 d−1) Mean night-time intercellular CO2 mole fraction (µmol mol −1)
I
 II
 III
 IV
9–10 May 2003 0 430b 143a −36a 28a 15a 565a 222a
1 439b 139a −31a 35a 14a 582a 233a
2 472a 104a −23a 34a 16a 589a 223a
4 447ab 126a −29a 36a 14a 580a 224a
8 383b 117a −25a 20a 13a 495b 245a
30–31 May 2003 0 559a 132a −25a 50a 23a 716a 184b
1 364b 100a −27a 0b 17ab 437b 237ab
2 289bc 124a −59a 0b 14b 354bc 313ab
4 208c 117a −51a 0b 12b 274bc 328ab
8 86d 78b −30a 0b 7c 134c 430a
20–21 June 2003 0 432a 29a −29a 122a 18a 554a 308a
1 426a 3b −26a 130a 17a 533a 305a
2 414a 27a −26a 155a 17a 570a 298a
4 394a 25a −32a 148a 16a 535a 315a
8 291b 4b −26a 152a 13b 421a 333a
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Data are means (n = 16 plants). Values within columns for a particular date followed by different letters are significantly different at P < 0·05.

Total daily carbon gain was reduced significantly only by eight daughter cladodes on 9–10 May. On 30–31 May total daily carbon gain progressive decreased as the number of daughter cladodes increased, and was reduced by 81 % with eight daughter cladodes compared with no daughter cladodes. The maximum rates of net CO2 uptake (Fig. 2) tended to decrease as the number of daughter cladodes increased on 30–31 May only. On 20–21 June the lowest maximal rate of net CO2 uptake was with eight cladodes. The average night-time intercellular CO2 mole fraction was the same among treatments for 9–10 May and 20–21 June; on 30–31 May, it increased with the number of daughter cladodes (P < 0·05; Table 2).

Stomatal conductance of mother cladodes during phase I was not significantly different with the number of daughter cladodes on 9–10 May and 20–21 June, although on 30–31 May the treatment with eight daughter cladodes had the greatest stomatal conductance. For all treatments stomatal conductance did not vary significantly during phase II on 30–31 May and 20–21 June, but on 9–10 May the treatments with two and eight daughter cladodes were largest. Stomata conductance in phase III did not vary significantly on 9–10 May and 30–31 May among treatments, but it was greatest without daughter cladodes on 20–21 June. Phase IV did not vary significantly on 9–10 May and 20–21 June, but it was highest with zero daughter cladodes on 30–31 May. The largest stomatal conductance occurred in phase II for the three dates of measurement, and smallest on 9–10 May during phase III, and in phase IV when soil was driest (30–31 May), especially for mother cladodes with daughter cladodes (Table 3).

Table 3.

Stomatal conductance during CAM phases for mother cladodes in response to number of daughter cladodes on different dates

Date
 Number of daughter cladodes
 Conductance for indicated phases (mol m−2 s−1)
I
 II
 III
 IV
9–10 May 2003 0 0·160a 0·452b 0·005a 0·048a
1 0·187a 0·573ab 0·007a 0·018a
2 0·196a 0·661a 0·004a 0·017a
4 0·193a 0·571ab 0·006a 0·012a
8 0·188a 0·617a 0·006a 0·035a
30–31 May 2003 0 0·280ab 1·744a 0·019a 0·053a
1 0·258ab 1·303a 0·012a 0·016b
2 0·192b 0·836a 0·012a 0·007b
4 0·278ab 0·897a 0·013a 0·003b
8 0·328a 1·326a 0·015a 0·004b
20–21 June 2003 0 0·305a 0·576a 0·022a 0·090a
1 0·288a 0·897a 0·011b 0·096a
2 0·364a 0·764a 0·005b 0·093a
4 0·387a 0·983a 0·008b 0·087a
8 0·387a 1·562a 0·015b 0·093a
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Data are means (n = 16 plants). Values within columns for a particular date followed by different letters are significantly different at P < 0·05.

DISCUSSION

The total daily carbon gain for mother cladodes of O. ficus-indica with daughter cladodes was significantly reduced during drought. The RWC of the mother cladodes decreased in parallel with the reduction in daily net CO2 uptake, suggesting that water moved from them to the developing daughter cladodes (Barcikowski and Nobel, 1984; Nobel et al., 1994a; Herrera et al., 2000; Rabas and Martin, 2003). This observation is supported by the fact that mother cladodes with four or eight cladodes showed the greatest yellowing and most dehydration (RWC of about 60 % on 30–31 May versus 80 % for their daughter cladodes). Actually, measurements on 30–31 May coincided with the onset of growth of daughter cladodes and their increased demand for assimilates (N. Wang et al., 1997, 1998). Near the beginning of the experiment (9–10 May) a gradual decrease in RWC of mother cladodes correlated with the increase in the number of daughter cladodes. Hence in addition to importing assimilates, daughter cladodes also import large volumes of water from mother cladodes (in a dilute phloem solution; Nobel et al., 1994a), causing a physiological drought condition in mother cladodes that was hastened by decreased soil water availability. These observations suggested that an ontogenic factor (daughter cladodes) acts in synergism with the abiotic drought with respect to the mother cladodes.

As indicated, daughter cladodes in the early stages of development import significant volumes of water from mother cladodes. Interestingly, the progressive reduction in RWC of mother cladodes was less during drought (30–31 May) than earlier, suggesting that mother cladodes had reached a RWC at which water is tightly held by matric potentials, particularly from mucilage and the apoplast (Barcikowski and Nobel, 1984; Goldstein et al., 1991; Nobel et al., 1992), and most of the available stored water in the mother stems was exhausted by both transpiration of mother cladodes and by daughter cladodes. After rainfall had begun (measurement date of 20–21 June), the RWC of daughter cladodes increased, but it was less pronounced than for mother cladodes. Also, daughter cladodes of O. ficus-indica exhibited C3 photosynthesis with daytime stomatal opening, leading to a large demand for water from mother cladodes (Ting, 1985; Nobel et al., 1994a; N. Wang et al., 1997). Such a redistribution of water is considered an adaptive response to drought stress (Herrera et al., 2000; Rabas and Martin, 2003). The presence of daughter cladodes hastened the effects of drought, even under the moderate day/night temperatures during the measurements. Indeed, mother cladodes of some cultivated varieties of O. ficus-indica suffer excessive dehydration and yellowing—and may even die—if daughter cladodes develop on them during extreme drought, which regularly occurs in the semi-arid lands of central Mexico (Pimienta-Barrios, 1990; Pimienta-Barrios et al., 2002).

In addition to water availability, the relative expression of the four CAM phases (Osmond, 1978) is governed by genotypic, ontogenic and environmental factors, such as light intensity and relative humidity (Borland and Griffiths, 1996; Mattos et al., 1999; Cushman, 2001). Because water availability is often most crucial, the flexibility of CAM phases is commonly related to changes from wet to dry conditions or vice versa, either artificially or under natural conditions (Nobel, 1995; Mattos et al., 1999; Dodd et al., 2002; Nobel et al., 2002; Keeley and Rundel, 2003). The flexibility of the expression of CAM phases for mother cladodes of O. ficus-indica also depended on the presence of daughter cladodes, an example of photosynthetic plasticity in response to an ontogenic factor (Cushman, 2001). Photosynthetic plasticity through the regulation of CAM phases allowed O. ficus-indica to increase its net CO2 uptake under favourable conditions, and to maintain carbon gains in mother cladodes when they were stressed by the combined effects of daughter cladodes and drought, as cultivated opuntias do not stop forming daughter cladodes but wild opuntias do (Pimienta-Barrios et al., 2002, 2003).

Cultivated O. ficus-indica has specific traits that maximize yield under optimum conditions and reduce the capacity to cope with environmental stresses, so making them more sensitive to biotic and abiotic stressors than are wild opuntias (Pimienta-Barrios, 1990), which have developed physiological and morphological traits by adaptation, acclimation and genetic selection/speciation that allow them to withstand various biotic and abiotic stresses by tolerance and avoidance mechanisms (Orcutt and Nilsen, 2000; Grime, 2001; Pimienta-Barrios et al., 2002).

The greater sensitivity of phase IV during the dry period was mainly because it occurs in the late afternoon (Dood et al., 2002; Black and Osmond, 2003), coinciding with higher temperatures and irradiance that favour photorespiration (Osmond, 1978; Maxwell et al., 1997; Takeba and Kozaki, 1997; Lambers et al., 1998). Frequently severe drought stress in CAM plants lead to loss of phase IV and reduction of phase II (Nobel, 1985; Mattos et al., 1999; Griffiths, et al., 2002). In O. ficus-indica during phase II, both CO2 uptake and stomatal aperture were maintained by mother cladodes with daughter cladodes, even during prolonged drought. In contrast phase IV was curtailed, coinciding with smallest conductance. Regularly when dehydration of photosynthetic tissue is well advanced, as on 30–31 May, the zero point for gas exchange is determined by the total or near-total closure of stomata (Larcher, 2003). However, there is evidence that drought stress affects photosynthetic metabolism in addition to stomatal aperture (Tezara et al., 2003).

The stress on mother cladodes of O. ficus-indica caused by drought and exacerbated by daughter cladodes apparently increased night-time respiration and reduced the activity of PEP carboxylase, leading to higher intercellular CO2 mole fractions (Maxwell et al., 1997). The increase in intercellular CO2 under water stress indicates mesophyll (non-stomatal) limitation to photosynthesis (Srinivasa-Rao et al., 2000). The largest intercellular CO2 mole fraction (399 µmol mol−1) for mature plants of O. ficus-indica and other CAM plants in the field is observed in spring when soil moisture is extremely low and day/night air temperatures are high (Pimienta-Barrios et al., 2000; Nobel et al., 2002). Large intercellular CO2 mole fractions during drought can help prevent damage by photo-oxidation in CAM plants (Pieters et al., 2003). Intense irradiance occurred at the study site, particularly during the driest period. The simultaneous occurrence of high irradiance and drought stress increase photodamage in addition to reducing carbon gain (Long et al., 1994), explaining in part the physiological significance of increased intercellular CO2 concentration observed for mother cladodes with four and eight cladodes on 30–31 May.

Daily net CO2 uptake was reduced because daughter cladodes and drought shortened the periods of positive net CO2 uptake and reduced the maximum rates of CO2 uptake, which became more pronounced as the number of daughter cladodes increased to eight, causing the highest rates of net CO2 uptake to occur late in the night when temperatures were low and the relative humidity high. This pattern reflects an avoidance strategy to maintain carbon gain with reduced water loss and shows physiological plasticity, which is also observed for O. robusta in the field during the driest months (Pimienta-Barrios et al., 2002, 2003) and for unrooted cladodes of O. ficus-indica 8 weeks after detachment (Raveh and Nobel, 1999). Under wet conditions and without daughter cladodes, carbon gain during the day for mature cladodes of O. ficus-indica contributed 27 % of the total daily net CO2 uptake. Indeed, the flexibility of CAM phases in mature cladodes of O. ficus-indica, such as stomatal opening in the daytime during wet periods with moderate temperatures (Cushman, 2001; Pimienta-Barrios et al., 2001), can extend carbon gain daily and seasonally, leading to more efficient use of resources (Nobel, 1995; Mattos and Lüttge, 2001; Pimienta-Barrios et al., 2001).

The chlorophyll content of photosynthetic tissue can be an important indicator of its photosynthetic integrity. In this regard, the synthesis of chlorophyll is affected by small reductions in tissue water potential (Hsiao, 1973); perhaps this reduced daily net CO2 uptake by the mother cladodes, and decreased susceptibility to photodamage (Horton, 2000), an effect exacerbated by the presence of daughter cladodes. The average thickness of chlorenchyma tissue in cultivated CAM plants such as Opuntia varies from 3 to 6 mm (Nobel et al., 1994b; Nobel et al., 2002), while in C3 and C4 it varies from 100 to 300 µm (Nobel, 1999); as a consequence, the chlorophyll content per unit area is significantly higher in CAM plants (Cui et al., 1993) than in C3 plants (Larcher, 2003). Apparently, the relatively small chlorophyll content of mother cladodes after rainfall in June was still sufficient to support CO2 fixation and carbon gain by O. ficus-indica. In Hedera canariensis a 60 % reduction of chlorophyll content only decreased leaf absorptance by 10–13 %. Therefore, a change in chlorophyll content per unit area is not always a major factor in regulating light interception (Björkman and Demmig-Adams, 1995), particularly for species with a thick chlorencyhma such as O. ficus-indica.

Consistent with the hypothesis, the increase in the number of daughter cladodes decreased the photosynthetic activity of the mother cladodes. Indeed, the substantial decrease in the RWC of the mother cladodes and maintenance of large RWC in daughter cladodes suggests that water moves from mother to daughter cladodes of O. ficus-indica (N. Wang et al., 1997, 1998). After drought stress had been alleviated by rainfall, the mother cladodes became rehydrated and substantial daily net CO2 uptake and stomatal conductance occurred in phase IV.

Supplementary Material

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Acknowledgments

We thank Alejandro Muñoz-Urias and numerous undergraduate students of Plant Physiology courses for help with the fieldwork, and the officials of the meteorological station of the Fifth Military Base of the Mexican Air Force who provided the weather data. This project was financed by the Universidad de Guadalajara and the UCLA Council of Research.

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