Crassulacean acid metabolism (CAM) species show an average increase in biomass productivity of 35% in response to a doubled atmospheric CO₂ concentration. Daily net CO₂ uptake is similarly enhanced, reflecting in part an increase in chlorenchyma thickness and accompanied by an even greater increase in water-use efficiency. The responses of net CO₂ uptake in CAM species to increasing atmospheric CO₂ concentrations are similar to those for C₃ species and much greater than those for C₄ species. Increases in net daily CO₂ uptake by CAM plants under elevated atmospheric CO₂ concentrations reflect increases in both Rubisco-mediated daytime CO₂ uptake and phosphoenolpyruvate carboxylase (PEPCase)-mediated night-time CO₂ uptake, the latter resulting in increased nocturnal malate accumulation. Chlorophyll contents and the activities of Rubisco and PEPCase decrease under elevated atmospheric CO₂, but the activated percentage for Rubisco increases and the K_M(HCO₃⁻) for PEPCase decreases, resulting in more efficient photosynthesis. Increases in root:shoot ratios and the formation of additional photosynthetic organs, together with increases in sucrose-Pi synthase and starch synthase activity in these organs under elevated atmospheric CO₂ concentrations, decrease the potential feedback inhibition of photosynthesis. Longer-term studies for several CAM species show no downward acclimatization of photosynthesis in response to elevated atmospheric CO₂ concentrations. With increasing temperature and drought duration, the percentage enhancement of daily net CO₂ uptake caused by elevated atmospheric CO₂ concentrations increases. Thus net CO₂ uptake, productivity, and the potential area for cultivation of CAM species will be enhanced by the increasing atmospheric CO₂ concentrations and the increasing temperatures associated with global climate change.

INTRODUCTION

Crassulacean acid metabolism (CAM) is one of three photosynthetic types used by vascular plants. Nocturnal CO₂ fixation by the cytosolic enzyme phosphoenolpyruvate carboxylase (PEPCase) results in the formation of malate, which is stored in the vacuole of cells in the chlorenchyma. Daytime decarboxylation of the accumulated malic acid releases CO₂, which is assimilated into carbohydrates using 1,5-ribulosebisphosphate carboxylase/oxygenase (Rubisco) and the C₃ photosynthetic carbon reduction cycle ( Winter & Smith 1996a). As is the case for the C₄ type of photosynthesis, primary fixation of CO₂ by PEPCase concentrates CO₂ at the site of Rubisco in CAM plants, thereby suppressing the oxygenase activity of this enzyme ( Taiz & Zeiger 1998). Daytime stomatal closure in CAM species reduces CO₂ leakage from the site of the C₃ cycle and effectively decouples the internal CO₂ pool from that of the atmosphere ( Monson 1989).

For both C₄ and CAM plants, the CO₂-concentrating mechanism potentially leads to higher optimal temperatures for photosynthesis ( Monson 1989). Moreover, the lower tissue temperatures accompanying the predominantly nocturnal stomatal opening of CAM plants compared with daytime stomatal opening for C₃ and C₄ plants generally result in a three- to five-fold higher water-use efficiency (WUE) for CAM plants than for C₃ or C₄ plants under comparable environmental conditions ( Nobel 1996, 1999). The higher WUE reflects the nearly exponential increase in the saturation water vapour content of air as the temperature rises, so stomatal opening during the daytime leads to a much higher transpiration rate than for the same degree of stomatal opening at night when tissue temperatures at the water evaporation sites average 10–12 °C lower.

CAM plants show considerable plasticity, varying in response to environmental conditions and with developmental state ( Winter & Smith 1996a; Cushman & Bohnert 1999). Many constitutive CAM species fix CO₂ almost exclusively at night (phase I, Fig. 1; Osmond 1978), even when well-watered, e.g. stem succulents such as Opuntia ficus-indica ( Nobel 1988). For other species, e.g. Agave deserti ( Nobel 1988), CO₂ uptake extends into the early morning (phase II, Fig. 1), and also occurs in the late afternoon (phase IV, Fig. 1), when uptake of atmospheric CO₂ involves binding of CO₂ by Rubisco ( Winter & Smith 1996a). The high intercellular CO₂ concentrations associated with malate decarboxylation suppress stomatal opening during the middle of the day (phase III, Fig. 1). Most facultative C₃–CAM intermediates switch between C₃ and CAM in response to changes in environmental factors, especially soil water availability. Reduced water availability favours expression of CAM in the C₃–CAM intermediates of the tropical tree genus Clusia ( Lüttge 1996). However, for species of Peperomia, the expression of CAM in older leaves is independent of environmental signals, although water stress, light and temperature modify the extent of CAM ( Ting et al. 1996 ). For some C₃–CAM intermediates, e.g. Mesembryanthemum crystallinum, environmental stimuli such as drought, soil salinity and low temperature elicit the CAM response only in mature plants ( Adams et al. 1998 ). CO₂ uptake patterns in facultative CAM plants may also be regulated by day length ( Brulfert et al. 1982 ) and season ( Guralnick, Rorabaugh & Hanscom 1984).

The daily cycle of net CO₂ (solid line) uptake and malic acid accumulation (dotted line) for a typical CAM plant, illustrating the four phases of CAM ( Osmond 1978).

For some CAM species, predominantly daytime net CO₂ uptake is accompanied by ‘CAM cycling.’ This means that, despite nocturnal stomatal closure, malate levels increase during this period as respiratory CO₂ is captured via PEPCase activity, leading to a reduction in daytime stomatal aperture ( Martin, Higley, & Wang 1988). For other species, ‘CAM idling’ occurs during severe drought. Stomatal closure during both day and night then results in no net CO₂ assimilation. A diel cycle in malic acid accumulation during CAM idling, associated with respiration followed by the re-fixation of respiratory CO₂, apparently keeps the various steps functioning, allowing rapid recovery of carbon assimilation upon rehydration ( Bastide et al. 1993 ).

The majority of the approximately 300 000 species of vascular plants utilize the C₃ pathway; about 2–3% are C₄, including many agriculturally important species such as maize, sorghum and sugar cane, and 6–7% are CAM ( Nobel 1991; Winter & Smith 1996a). CAM has independently evolved many times and occurs in over 30 taxonomically diverse families ( Ehleringer & Monson 1993; Smith & Winter 1996). The terrestrial environments and micro-environments favouring CAM are generally characterized by water shortage ( Taiz & Zeiger 1998). Seven of the major CAM families – the Agavaceae, Asphodelaceae, Aizoaceae, Asclepiadaceae, Cactaceae, Crassulaceae (the family for which the type is named) and Euphorbiaceae – occur in arid regions or climates of seasonal water shortage. CAM species in the other two major CAM families, the Bromeliaceae and the Orchidaceae, are predominantly tropical epiphytes whose soil-depauperate substrate has a low water-holding capacity ( Winter & Smith 1996a). For epiphytic species of the Bromeliaceae, the proportion of CAM species increases with increasing habitat aridity, indicating a competitive advantage of CAM in water-limited environments ( Griffiths & Smith 1983; Smith 1989). The succulent morphology of many CAM species provides a high shoot water-storage capacity ( Nobel 1988), and large vacuoles facilitate appreciable storage of the nocturnally accumulated malic acid ( Winter & Smith 1996a). The degree of leaf succulence correlates positively with the occurrence of CAM for both the Crassulaceae ( Teeri, Tonsor & Turner 1981) and the Orchidaceae ( Winter et al. 1983 ), the latter family containing nearly half of the known CAM species ( Winter & Smith 1996a).

The pre-industrial atmospheric CO₂ concentration of approximately 280 μmol mol⁻¹ is predicted to double by the middle of the 21st century due to the effects of deforestation, other land-use changes, and especially the burning of fossil fuels ( Neftel et al. 1985 ; Schimel et al. 1996 ). Such observations have resulted in extensive research into the effects of atmospheric CO₂ concentration on the photosynthesis of C₃ plants. For most C₃ species, photosynthesis increases at elevated atmospheric CO₂ concentrations and the accompanying increases in intercellular CO₂ concentration, which suppress the oxygenase activity of Rubisco and thereby reduce photorespiratory loss of carbon. Because the specificity of Rubisco for CO₂ relative to O₂ declines with increasing temperature, the stimulation of net CO₂ uptake by elevated atmospheric CO₂ concentrations is potentially greater at higher temperatures ( Morison & Lawlor 1999). Long-term enhancement of photosynthesis is often limited by feedback inhibition of Rubisco activity or by environmental stresses, such as low nitrogen availability or extreme temperatures ( Morison & Lawlor 1999; Stitt & Krapp 1999). Increased growth and photosynthesis under elevated atmospheric CO₂ concentrations have been measured for some C₄ species ( Poorter 1993; Lecain & Morgan 1998). However, photosynthesis by C₄ species is more readily saturated as atmospheric CO₂ concentrations rise, reflecting the relative insensitivity of PEPCase to the CO₂:O₂ ratio because of lack of binding of O₂ to the catalytic site ( Lawlor & Mitchell 1991).

From a biochemical point of view, obligate CAM species could respond similarly to C₄ species if PEPCase were saturated at close to the current atmospheric CO₂ concentration ( Ting 1994; Winter & Smith 1996b). Nonetheless, facultative CAM plants might respond more to elevated atmospheric CO₂ concentrations ( Ting 1994). Compared with C₃ and C₄ species, relatively few studies have been conducted on the effects of elevated atmospheric CO₂ concentrations on CAM plants (studies are summarized in Table 1). Most of the CAM species investigated show increased productivity, although the effects of elevated CO₂ on the patterns of gas exchange differ. For most species, nocturnal CO₂ uptake is enhanced, while for others, daytime CO₂ uptake is increased with a concomitant decrease in the proportion of nocturnal CO₂ fixation ( Table 1). Additionally, a number of changes occur in the morphology, anatomy, and biochemistry of CAM species under elevated atmospheric CO₂ concentrations (summarized in Table 1), which may contribute to their higher net CO₂ uptake rates and the increased biomass productivity as the atmospheric CO₂ concentration increases.

Table 1. Responses of CAM species to elevated atmospheric CO₂ concentrations

Family/species	Productivity	Morphological changes	CO₂ uptake	Enzymes
Monocotyledons
Agavaceae
Agave deserti	Increased (1)	Leaves thicker (1), leaves longer (1), chlorenchyma thicker (1), root cell length increased (2)	Afternoon and night-time uptake increased (1, 3), WUE increased (1)	PEPCase decreased (1), Rubisco decreased but activated in vivo% increased (1)
Agave salmiana	Increased (4)		Afternoon and night-time uptake increased (4, 5)	PEPCase decreased (4), Rubisco decreased but activated in vivo% increased (4), PEPCase K_M decreased (4)
Agave vilmoriniana	Increased (6)		Night-time uptake increased (7)
Yucca schidigera ^a			Increased (8)
Orchidaceae
Mokara Yellow ^b	Increased (9–11)	Root : shoot ratio increased (9, 10)	Nocturnal malate accumulation increased (9)	PEPCase decreased (9), Rubisco decreased (9)
Bromeliaceae
Aechmea magdalenae	Increased (12)
Ananas comosus	Increased (13–15)	Root : shoot ratio increased (13), leaf thickness increased (13)	Increased morning and night-time uptake (13–16), WUE increased (15)
Tillandsia ionantha			Nocturnal malate accumulation increased (17)
Dicotyledons
Aizoaceae
Mesembryanthemum crystallinum ^c
Cactaceae
Ferocactus acanthodes	Increased (3)		Increased (3)
Hylocereus undatus		Chlorenchyma cell volume increased (18)	Increased (18)
Opuntia ficus-indica	Increased (4, 19–23)	Specific cladode mass increased (19, 20, 24), cladodes thicker (19, 21, 24, 25), chlorenchyma thicker (19, 25), stomatal frequency decreased (24), root : shoot ratio increased (4, 21, 22), root cell length increased (26), chlorenchyma cell length increased (20)	Afternoon, night-time and early-morning uptake increased (20–23, 27), WUE increased (21, 23)	PEPCase decreased (4, 27, 28), Rubisco decreased but activated in vivo% increased (4, 27, 28), PEPCase K_M decreased (4)
Stenocereus queretaroensis			Afternoon and night-time uptake increased (5)
Clusiaceae
Clusia uvitana ^c			Night-time uptake decreased (29)
Portulacaceae
Portulacaria afra ^c			Night-time uptake decreased (30)
Crassulaceae
Crassula arborescens			Nocturnal malate accumulation increased (17)
Kalanchoë blossfeldiana ^c	Increased (31)
Kalanchoë daigremontanum			Unchanged (32, 33)
Kalanchoë pinnata	Increased (34)		Daytime uptake increased (34)

^a Seedlings of Yucca schidigera as used in this investigation are possibly facultatively C ₃ ( Huxman et al. 1998 ).
^b Arachnis hookeriana×Ascocenda Madame Kenny.
^c C ₃–CAM intermediate.
References: (1) Graham & Nobel (1996), (2) Drennan & Nobel (1996), (3) Nobel & Hartsock (1986), (4) Nobel, Israel & Wang (1996), (5) Nobel (1996), (6) Idso et al. (1986) , (7) Szarek, Holthe & Ting (1987), (8) Huxman et al. (1998) , (9) Gouk, Yong & Hew (1997), (10) Gouk, He & Hew (1999), (11) Hew et al. (1995) , (12) Ziska et al. (1991) , (13) Zhu, Bartholomew & Goldstein (1997a), (14) Zhu, Bartholomew & Goldstein (1997b), (15) Zhu, Goldstein & Bartholomew (1999), (16) Crewes, Vines & Black (1975), (17) Nowak & Martin (1995), (18) Raveh, Gersani & Nobel (1995), (19) Luo & Nobel (1993), (20) Nobel & Israel (1994), (21) Nobel et al. (1994b) , (22) Cui, Miller & Nobel (1993), (23) Cui & Nobel (1994), (24) North, Moore & Nobel (1995), (25) Wang & Nobel (1996), (26) Drennan & Nobel (1998), (27) Israel & Nobel (1994), (28) Nobel, Cui & Israel (1994a), (29) Winter et al. (1992) , (30) Huerta & Ting (1988), (31) Mortensen & Moe (1992), (32) Holtum, O’Leary & Osmond (1983), (33) Osmond & Björkman (1975), (34) Winter et al. (1997) .

GROWTH AND BIOMASS

Biomass accumulation is enhanced by elevated atmospheric CO₂ concentrations for all CAM species investigated ( Tables 1 and 2). Most of these studies are relatively short-term compared with the life span of CAM species. Nonetheless, dry matter increases averaging approximately 35% are achieved within 3 months at elevated atmospheric CO₂ concentrations of 650–750 μmol mol⁻¹. These increases are similar to the 33% increase averaged for some 430 C₃ crop species when the atmospheric CO₂ concentration is doubled ( Kimball 1983). However, they exceed the approximately 10% increase in dry matter production for C₄ plants with a doubling in the atmospheric CO₂ concentration ( Kimball 1983; Lawlor & Mitchell 1991; Poorter 1993), despite the similarity in initial fixation of CO₂ by PEPCase for both C₄ plants during the daytime and CAM plants at night. Thus the response to elevated atmospheric CO₂ concentrations cannot be predicted on the basis of the initial carboxylating enzyme alone, nor is the response saturated at atmospheric CO₂ concentrations that are slightly above the current value ( Table 2), as would be likely if the response of CAM plants were mediated solely by CO₂ saturation of PEPCase.

Table 2. Response of biomass of CAM plants to long-term (> 1 month) exposure to elevated atmospheric CO₂ concentrations as a percentage increase over controls maintained under ambient atmospheric CO₂ concentrations for the same period

Species	Biomass (% increase)	CO₂ (μmol mol⁻¹) ^a	Duration (months)	Reference
Agave deserti	30	350–650	12	Nobel & Hartsock (1986)
	31	370–750	17	Graham & Nobel (1996)
Agave salmiana	17	370–730	4	Nobel et al. (1996)
Agave vilmoriniana	28	300–600	6	Idso et al. (1986)
Orchid ‘Mokara Yellow’	80	350–10 000	2	Gouk et al. (1997)
	170	350–10 000	3	Gouk et al. (1997)
Aechmea magdalenae	36	354–712	3	Ziska et al. (1991)
Ananas comosus	−10	354–712	3	Ziska et al. (1991)
	23	330–730	4	Zhu et al. (1997a)
Ferrocactus acanthodes	30	350–650	12	Nobel & Hartsock (1986)
Opuntia ficus-indica	32	370–750	3	Cui & Nobel (1994)
	21	370–520	4·5	Cui et al. (1993)
	55	370–720	4·5	Cui et al. (1993)
	40	360–720	12	Nobel & Israel (1994)
Kalanchoë blossfeldiana	37	350–700	1·4	Mortensen & Moe (1992)
Kalanchoë pinnata	51	350/400–700/800	1·9	Winter et al. (1997)
	42	350/400–700/800	2·2	Winter et al. (1997)

a Conversion to concentration approximate; the biomass increase occurs from the first concentration to the second concentration.

For Opuntia ficus-indica, the most-studied CAM plant with respect to the effect of elevated atmospheric CO₂ concentrations, stimulation of biomass accumulation also occurs as the atmospheric CO₂ concentration is increased from 520 to 720 μmol mol⁻¹ ( Cui et al. 1993 ). Similarly, increasing the atmospheric CO₂ concentration from 675 to 885 μmol mol⁻¹ results in a 13% increase in growth rate for Agave vilmoriniana ( Idso et al. 1986 ). Although a doubling of the atmospheric CO₂ concentration results in a 28% increase in biomass for A. vilmoriniana under dry soil conditions ( Table 2), a lack of biomass response to elevated atmospheric CO₂ concentrations may occur for A. vilmoriniana ( Idso et al. 1986 ) and Ananas comosus ( Ziska et al. 1991 ) when they are heavily watered. For A. comosus, such reduced CAM activity and growth under elevated CO₂ concentrations are attributed to water-logging of the soil ( Zhu, Goldstein & Bartholomew 1999).

Acclimatization to elevated atmospheric CO₂ concentrations occurs for some C₃ species and has been attributed to a feedback inhibition by increased carbohydrate levels ( Heineke et al. 1999 ) that decreases the expression of photosynthetic genes ( Moore et al. 1999 ) and affects the activated form of Rubisco ( Bowes 1991). Root restriction due to small soil volumes may also result in acclimatization ( Arp 1991). For O. ficus-indica, dry weight gains under elevated atmospheric CO₂ concentrations are not different from dry weight gains under the current atmospheric CO₂ concentration after 4·5 months of exposure when the root volume is significantly restricted ( Nobel et al. 1994b ). The reduced biomass stimulation that occurs with increasing time of CO₂ enrichment for Kalanchoë pinnata ( Table 2) may reflect an increase in CAM expression with increasing leaf age, with its associated biochemical changes ( Winter et al. 1997 ).

The enhancement of growth by elevated atmospheric CO₂ concentrations decreases with plant age for some C₃ species ( Bazzaz et al. 1989 ), and elevated CO₂ concentrations may also accelerate ontogenesis ( Loehle 1995; Miller et al. 1997 ). For A. vilmoriniana, small, younger plants show a greater response to elevated atmospheric CO₂ concentrations than do larger, older plants ( Idso et al. 1986 ). Similarly, the maximum relative growth rate for cladodes of O. ficus-indica, in addition to being higher, is achieved earlier under a doubled atmospheric CO₂ concentration, but the growth rate subsequently decreases to levels similar to those for cladodes under the current atmospheric CO₂ concentration ( Luo & Nobel 1993; North et al. 1995 ). The number of areoles per cladode for O. ficus-indica under different atmospheric CO₂ concentrations is similar ( North et al. 1995 ), although cladode thickness is greater under elevated atmospheric CO₂ concentrations ( Table 1). Nevertheless, the acceleration of development caused by elevated atmospheric CO₂ concentrations increases biomass productivity for O. ficus-indica by allowing earlier formation of new cladodes ( Nobel & Israel 1994). Similarly, increases in biomass accumulation and leaf thickness for A. comosus and Agave deserti ( Table 1) are also associated with increased leaf production, which is sustained for at least 17 months by A. deserti ( Table 2; Graham & Nobel 1996).

The increased productivity for highly productive CAM plants under elevated atmospheric CO₂ concentrations may have important ecosystem and especially agricultural consequences ( Nobel 1996). In particular, the CAM plants Agave mapisaga, Agave salmiana, Opuntia amyclaea and O. ficus-indica may have an average annual dry mass productivity of 43 tons per hectare per year under the current CO₂ atmospheric concentration ( Nobel 1991). This productivity exceeds the average annual above-ground dry-mass productivity of essentially all C₃ plants, and is exceeded by that of only a few C₄ species, notably Saccharum officinarum (sugar cane). Based on studies using plants in a field plot that received free-air CO₂ enrichment, the dry mass productivity of O. ficus-indica when the plants are closely spaced may be 47 tons per hectare per year at 360 μmol mol⁻¹, increasing to 65 tons per hectare per year when the atmospheric CO₂ concentration is doubled ( Nobel & Israel 1994), which has major implications for this widely cultivated species as the atmospheric CO₂ concentration increases.

MORPHOLOGY AND ANATOMY

Changes in the morphology and anatomy of photosynthetic organs caused by increasing atmospheric CO₂ concentrations influence the photosynthetic characteristics of CAM species, such as gas exchange, reflectance and light absorption ( Nobel et al. 1994a ). Changes in plant morphology reflect changes in carbon allocation patterns, which alter the interaction of the plant with both its abiotic and its biotic environment ( Rogers, Runion & Krupa 1994). For the few CAM species whose morphology and anatomy have been studied under elevated atmospheric CO₂ concentrations ( Table 1), a consistent effect of the higher atmospheric CO₂ concentrations is an increase in thickness of the photosynthetic organs. For O. ficus-indica, exposure to a doubled atmospheric CO₂ concentration results in increases in cladode thickness of 19% for basal cladodes, 14% for the new daughter cladodes initiated on the basal cladode (first-order daughter cladodes) and 11% for second-order daughter cladodes (initiated on first-order daughter cladodes; Cui, Miller & Nobel 1993; Nobel & Israel 1994; Nobel et al. 1994a ; North et al. 1995 ). Differences in thickness became apparent within 2 weeks of exposure to the elevated atmospheric CO₂ concentration ( Nobel et al. 1994b ) and were maintained even after these determinate organs had stopped growing ( North et al. 1995 ). Similarly, the leaves of both Agave deserti and Ananas comosus are 11% thicker under approximately twice the current atmospheric CO₂ concentration ( Graham & Nobel 1996; Zhu et al. 1997a ).

More than 65% of the increase in thickness of the leaves of A. deserti ( Graham & Nobel 1996) and of second-order daughter cladodes of O. ficus-indica ( Cui et al. 1993 ; Nobel et al. 1994a ) is accounted for by an approximately 20% increase in the thickness of the chlorenchyma. For O. ficus-indica, increases in both the length of chlorenchyma cells and the number of cell layers contributes to the increased tissue thickness ( North et al. 1995 ), as can also occur for C₃ species ( Thomas & Harvey 1983). An increase in chlorenchyma thickness under elevated atmospheric CO₂ concentrations may be related to a higher CO₂ concentration deeper in the leaf ( Powles, Chapman & Osmond 1980). For the CAM species Crassula argentea, gradients of increasing δ¹³C with increasing distance from the upper epidermis are consistent with a diffusion limitation on CO₂ uptake in these succulent tissues ( Robinson, Osmond & Giles 1993). For O. ficus-indica, the contribution of increased chlorenchyma thickness to overall cladode thickness decreases from 66% for young, second-order daughter cladodes to 16% for two-year-old basal cladodes ( Cui et al. 1993 ). Thus increased storage tissue must contribute significantly to the increased thickness for the older cladodes. For A. comosus, the ratio of stem mass to total plant mass increases under elevated atmospheric CO₂ concentrations ( Zhu et al. 1997a ). The associated increase in stem dry matter suggests that starch levels are increased under elevated atmospheric CO₂ concentrations, as stem dry matter is positively correlated with starch content for this species ( Bartholomew & Paull 1986).

The increase in chlorenchyma thickness with rising atmospheric CO₂ concentrations increases the amount of photosynthetic tissue and the chlorenchyma cell surface area per unit leaf area for A. deserti and per unit cladode area for O. ficus-indica, thus potentially increasing net CO₂ uptake and WUE ( Nobel 1999). The uptake of CO₂ and the water vapour conductance are also influenced by stomatal frequency, which decreases by 20% for O. ficus-indica under elevated CO₂ concentrations, although stomatal pore length is unchanged ( North et al. 1995 ). Stomatal frequency is lower under elevated CO₂ for some, but not all C₃ and C₄ species ( Thomas & Harvey 1983; Rogers et al. 1994 ). A general decrease in stomatal frequency has accompanied the global rise in atmospheric CO₂ concentration and is suggested to lead to a higher WUE ( Beerling & Woodward 1993; Beerling, McElwain & Osborne 1998). In particular, a decrease in stomatal area per unit leaf area decreases transpiration more than photosynthesis ( Nobel 1999). Epicuticular wax increases 60% and the cuticle thickness increases 30% for O. ficus-indica under a doubled CO₂ concentration ( North et al. 1995 ). Cladode reflectance is higher from 400–700 nm but lower from 740–1000 nm for O. ficus-indica growing at elevated atmospheric CO₂ concentrations ( Nobel et al. 1994a ). On the other hand, epicuticular wax decreases by 40% for A. deserti under elevated atmospheric CO₂ concentrations, which decreases the reflectance of the photosynthetic photon flux from 400–700 nm ( Graham & Nobel 1996).

CAM plants typically have extremely low root:shoot ratios of about 0·08–0·14, consistent with their low rates of transpiration and high WUE ( Nobel 1988; Nobel & North 1996). Increases in the root:shoot ratio of 33% and 45% have been measured for A. comosus and the hybrid orchid ‘Mokara Yellow’, respectively, under two to three times the current atmospheric CO₂ concentration ( Zhu et al. 1997a ; Gouk et al. 1997 ). Increases of up to 100% in root:shoot ratio occur for O. ficus-indica under a doubled atmospheric CO₂ concentration ( Cui et al. 1993 ), although the magnitude of the increase may be limited by small soil volumes ( Nobel et al. 1994b ). Not all CAM species show increases in root:shoot ratios under elevated atmospheric CO₂ concentrations; for example, ratios for Ferocactus acanthodes, A. deserti and Agave salmiana are similar under current and doubled CO₂ concentrations ( Nobel & Hartsock 1986; Graham & Nobel 1996; Nobel et al. 1996 ). Similar variability in the responses of root:shoot ratios has been reported for C₃ and C₄ species ( Rogers et al. 1996 ), and may be the result of interactions of experimental and environmental factors, such as soil volume and temperature, with the response to atmospheric CO₂ concentration ( Rogers et al. 1994 ; Morison & Lawlor 1999). Root architecture, especially root diameter and the number of lateral roots, does not change under elevated atmospheric CO₂ concentrations for A. salmiana or O. ficus-indica ( Nobel et al. 1996 ; Drennan & Nobel 1998), although root cell length increases for A. deserti and O. ficus-indica ( Drennan & Nobel 1996, 1998). For these typically shallow-rooting drought-adapted species, root architecture may respond more to water availability, which also will change as the atmospheric CO₂ concentration increases.

GAS EXCHANGE

The net daily CO₂ uptake for most CAM species is enhanced at elevated atmospheric CO₂ concentrations ( Table 1, Fig. 2). The percentage stimulation for plants representing a range of morphologies (i.e. epiphytes, stem succulents and leaf succulents) and maintained at elevated atmospheric CO₂ concentrations for at least several weeks averages 35% ( Table 3), which is consistent with the average biomass increase for these species under elevated atmospheric CO₂ concentrations ( Table 2). For example, the biomass enhancement for Ananas comosus caused by doubling the atmospheric CO₂ concentration is 23% ( Zhu et al. 1997b ), and the increase in net daily CO₂ uptake is 15% ( Fig. 2; Zhu et al. 1999 ). Agave salmiana shows a 59% increase in daily net CO₂ uptake under doubled atmospheric CO₂ and a concomitant 55% increase in biomass ( Nobel et al. 1996 ).

Daily time-courses of the net CO₂ uptake rate under the current atmospheric CO₂ concentration (dotted line) and, unless otherwise indicated, after acclimatization to a doubled atmospheric CO₂ concentration (solid line) under wet conditions for: (a) Agave deserti, 350 and 650 μmol mol⁻¹ CO₂ (instantaneous increase), day/night air temperatures of 25/15 °C, PPF of 26 mol m⁻² d⁻¹ ( Nobel & Hartsock 1986); (b) A. deserti, 370 and 750 μmol mol⁻¹ CO₂, day/night air temperatures of 25/20 °C, PPF of 15 mol m⁻² d⁻¹ ( Graham & Nobel 1996); (c) Agave salmiana, 360 and 720 μmol mol⁻¹ CO₂, day/night air temperatures of 25/15 °C, PPF of 22 mol m⁻² d⁻¹ ( Nobel 1996); (d) Agave vilmoriniana, 370 and 750 μmol mol⁻¹ CO₂ ( Szarek et al. 1987 ); (e) Ananas comosus, 350 and 700 μmol mol⁻¹ CO₂, day/night air temperatures of 30/20 °C, PPF of 17 mol m⁻² d⁻¹ ( Zhu et al. 1999 ); (f) Ferocactus acanthodes, 350 and 650 μmol mol⁻¹ CO₂ (instantaneous increase), day/night air temperatures of 25/15 °C, PPF of 26 mol m⁻² d⁻¹ ( Nobel & Hartsock 1986); (g) Hylocereus undatus, 370 and 740 μmol mol⁻¹ CO₂, day/night air temperatures of 25/15 °C, PPF of 10 mol m⁻² d⁻¹ ( Raveh et al. 1995 ); (h) H. undatus, 370 and 740 μmol mol⁻¹ CO₂, day/night air temperatures of 25/15 °C, PPF of 10 mol m⁻² d⁻¹, after 24 d of drought ( Raveh et al. 1995 ); (i) H. undatus, 370 and 740 μmol mol⁻¹ CO₂, day/night air temperatures of 45/35 °C, PPF of 10 mol m⁻² d⁻¹ ( Raveh et al. 1995 ); (j) Kalanchoë pinnata, 340 and 680 μmol mol⁻¹ CO₂ (instantaneous increase), day/night air temperatures of 25/20 °C, PPF of 22 mol m⁻² d⁻¹ ( Winter & Engelbrecht 1994); (k) Opuntia ficus-indica, 370, 520 (dashed line), and 750 μmol mol⁻¹ CO₂ ( Cui et al. 1993 ); and (l) Stenocereus queretaroensis, 360 and 720 μmol mol⁻¹ CO₂, day/night air temperatures of 25/15 °C, PPF of 22 mol m⁻² d⁻¹ ( Nobel 1996).

Table 3. Percentage increase in total daily net CO₂ uptake under elevated atmospheric CO₂ concentrations and percentage contribution of daytime CO₂ uptake to total daily net CO₂ uptake for CAM plants under ambient (340–370 μmol mol⁻¹) and elevated (680–750 μmol mol⁻¹) atmospheric CO₂ concentrations

Species	Increase in total daily net CO₂ uptake (%)	Daytime net CO₂ uptake (% of total)		Reference
Species	Increase in total daily net CO₂ uptake (%)	Ambient CO₂	Elevated CO₂	Reference
Agave deserti	2	22	38	Nobel & Hartsock (1986)
	49	17	24	Graham & Nobel (1996)
Agave salmiana	36	15	23	Nobel (1996), Nobel et al. (1996)
Ananas comosus	15	19	33	Zhu et al. (1999)
Hylocereus undatus	34	24	35	Raveh et al. (1995)
Opuntia ficus-indica
basal cladodes	41–152	−4	17	Cui et al. (1993)
daughter cladodes	41–61	8	15	Cui et al. (1993)
Stenocereus queretaroensis	36	7	16	Nobel (1996)

The enhancement of daily net CO₂ uptake is maintained in the long term (8–17 months) for those species investigated, i.e. Agave deserti ( Graham & Nobel 1996), A. comosus ( Zhu et al. 1997b ) and O. ficus-indica ( Nobel & Israel 1994). For A. deserti, a small (approximately 10%) decrease in daily net CO₂ uptake may occur over 17 months for both current and doubled atmospheric CO₂ concentrations, and is suggested to be due to the effects of limited soil volume on growth ( Nobel et al. 1994b ; Graham & Nobel 1996). However, the enhancement of CO₂ uptake by elevated atmospheric CO₂ concentrations remains high. Similarly, total net daily CO₂ uptake for O. ficus-indica is still 35% higher after 1 year under doubled versus the current atmospheric CO₂ concentration ( Nobel & Israel 1994). Thus for the species studied, acclimatization of CO₂ uptake to elevated atmospheric CO₂ concentrations does not seem to occur. Immediate exposure to a doubled atmospheric CO₂ concentration results in only a 2% increase in daily net CO₂ uptake the next day for A. deserti ( Fig. 2a) and Ferocactus acanthodes ( Fig. 2f; Nobel & Hartsock 1986). The difference in percentage increase for A. deserti for instantaneous versus long-term exposure suggests that the response to elevated atmospheric CO₂ concentrations is maximized once certain physiological and/or morphological changes occur, such as the thickening of the chlorenchyma.

The daily pattern of CO₂ uptake is also altered under elevated atmospheric CO₂ concentrations ( Fig. 2). For most species, afternoon (phase IV, Fig. 1) CO₂ uptake increases under elevated atmospheric CO₂ concentrations. Uptake may be initiated earlier in the afternoon, e.g. for A. salmiana and Stenocereus queroetaroensis ( Fig. 2a,l; Nobel 1996); for those species whose stomatal opening typically occurs in the afternoon at the current atmospheric CO₂ concentration, a marked increase in the maximum rate of CO₂ uptake occurs during this period. For example, for A. comosus, the maximum rate of CO₂ uptake in the afternoon is 85% greater under a doubled atmospheric CO₂ concentration, and similar effects occur during phase II ( Fig. 2e; Zhu et al. 1999 ).

Increases in the duration and the rate of daytime net CO₂ uptake result in an increase in the percentage contribution of daytime CO₂ uptake to the total daily net CO₂ uptake for CAM species under elevated atmospheric CO₂ concentrations ( Table 3). Such responses are consistent with the effect of higher cellular CO₂ concentrations leading to increased saturation of Rubisco, the carboxylating enzyme mediating phases II and IV ( Fig. 1) of the CAM cycle ( Winter & Smith 1996a), and with the responses of most C₃ species to elevated atmospheric CO₂ concentrations ( Kimball 1983; Poorter 1993; Rogers et al. 1994 ). Indeed, the higher carbon-isotope discrimination values for leaves of A. comosus grown under a doubled atmospheric CO₂ concentration are indicative of increased Rubisco-mediated CO₂ uptake during the daytime ( Zhu et al. 1999 ).

Less expected for CAM species is the increase in PEPCase-mediated uptake of CO₂ at night (phase I, Fig. 2) under elevated atmospheric CO₂ concentrations. PEPCase may be carbon-saturated at current atmospheric CO₂ concentrations ( Ting 1994), and elevated atmospheric CO₂ concentrations minimally affect net CO₂ uptake by C₄ plants for which the initial carboxylating enzyme is also PEPCase ( Lawlor & Mitchell 1991; Bowes 1993). However, even for those species that achieve relatively high rates of net daytime CO₂ uptake and have large contributions of daytime uptake to overall carbon gain, e.g. Hylocereus undatus ( Table 3), the observed stimulation of biomass ( Table 2) and the enhancement of total carbon gain cannot be sustained by the observed increases in daytime CO₂ uptake alone ( Table 3). The most extreme example of this occurs for O. ficus-indica, which has very low rates of daytime net CO₂ uptake under the current atmospheric CO₂ concentration ( Table 3) and may even have net daytime losses ( Cui et al. 1993 ). Under a doubled atmospheric CO₂ concentration, the contribution of daytime to total daily uptake rarely exceeds 17%, whereas this species can show a 100% increase in daily net CO₂ uptake ( Table 3) and biomass increases of approximately 40% ( Table 2). Indeed, the maximal rate of nocturnal CO₂ uptake for daughter cladodes was 43% higher at an atmospheric CO₂ concentration of 520 μmol mol⁻¹ and 96% higher at 720 μmol mol⁻¹ CO₂ compared with uptake rates at 360 μmol mol⁻¹ CO₂ ( Fig. 2), indicating that night-time uptake of CO₂ is far from being saturated at the current atmospheric CO₂ concentration for this CAM species. Lack of saturation of PEPCase at the current atmospheric CO₂ concentration possibly results from low diffusion conductances leading to low internal CO₂ concentrations ( Nobel 1999). However, for some CAM species, e.g. A. comosus, enhanced night-time CO₂ uptake under a doubled atmospheric CO₂ concentration occurs only when day/night temperatures are increased ( Zhu et al. 1999 ).

For several species, e.g. A. salmiana ( Fig. 2c), O. ficus-indica ( Fig. 2k) and S. queretaroensis ( Fig. 2l), increased CO₂ uptake under a doubled atmospheric concentration is most pronounced in the first half of the night. A similar pattern is apparent for A. deserti and F. acanthodes subjected to an instantaneous increase in atmospheric CO₂ concentration ( Fig. 2a,f), which increases the maximum rate of CO₂ uptake by approximately 50%. However, this stimulation for the latter two species is sustained for only about 6 h, after which the rate drops below that for plants exposed to the current CO₂ concentration, resulting in only small net gains in total daily net CO₂ uptake. Such patterns are probably associated with the insufficiency of a CO₂ acceptor or a filled malate pool in plants that have not fully adapted to the elevated atmospheric CO₂ concentration through longer-term exposure. For some species, e.g. Clusia uvitana and Portulacaria afra, decreases in nocturnal net CO₂ uptake occur in response to short-term exposure to elevated atmospheric CO₂ concentrations ( Huerta & Ting 1988; Winter et al. 1992 ). Both species are C₃–CAM intermediates that exhibit extensive daytime net CO₂ uptake. For Mesembryanthemum crystallinum and P. afra, the switch to CAM photosynthesis cannot be induced by manipulating the atmospheric CO₂ concentration but readily occurs in response to water stress ( Huerta & Ting 1988; Winter 1979). For C. uvitana, which also shows increased CAM activity in response to water stress, nocturnal CO₂ uptake may be a function of the net carbon gain during the light period, with daytime decreases resulting in an increase in nocturnal uptake ( Winter et al. 1992 ).

The enhancement of daily net CO₂ uptake by elevated atmospheric CO₂ concentrations is influenced by environmental factors, especially photosynthetic photon flux (PPF, 400–700 nm), drought, and day/night air temperatures ( Nobel & Israel 1994; Raveh et al. 1995 ; Graham & Nobel 1996; Zhu et al. 1999 ). For A. deserti, H. undatus and O. ficus-indica, daily net CO₂ uptake increases as the PPF increases from 5 to 20 mol m⁻² d⁻¹ under both current and doubled atmospheric CO₂ concentrations. For these three species, the enhancement of CO₂ uptake by elevated atmospheric CO₂ concentrations is greatest for 10–20 mol m⁻² d⁻¹, a PPF range that may allow maximal response of both daytime and night-time CO₂ uptake to the elevated atmospheric CO₂ concentration. When CAM plants are exposed to water stress or high temperatures, net CO₂ uptake is generally depressed more during the daytime than at night ( Nobel 1988). For the shade plant H. undatus, which shows saturation of net CO₂ uptake at only 10–20 mol m⁻² d⁻¹ under the current atmospheric CO₂ concentration, increasing photoinhibition of C₃ photosynthesis with increasing PPF and a concomitant decrease in daytime CO₂ uptake is partially offset by the enhancement of CO₂ uptake by the elevated CO₂ concentration ( Raveh et al. 1995 ).

For A. deserti, H. undatus and O. ficus-indica, total daily net CO₂ uptake decreases with increasing duration of drought under both current and elevated atmospheric CO₂ concentrations ( Nobel & Israel 1994; Raveh et al. 1995 ; Graham & Nobel 1996). However, the rate of decrease is greater under the current atmospheric CO₂ concentration, e.g. for O. ficus-indica, 25, 50 and 75% decreases in total daily net CO₂ uptake occur at 17, 23 and 33 d of drought, respectively, under the current atmospheric CO₂ concentration and at 23, 31 and 40 d, respectively, under a doubled CO₂ concentration. Concomitantly, the percentage enhancement of daily net CO₂ uptake under elevated atmospheric CO₂ concentrations increases as the drought progresses, e.g. for A. deserti, H. undatus ( Fig. 2h) and O. ficus-indica, the percentage enhancements under a doubled atmospheric CO₂ concentration after 25 d are 300, 340 and 200%, respectively. For O. ficus-indica, positive carbon gain is eliminated by 50 d of drought under the current atmospheric CO₂ concentration but still occurs under a doubled atmospheric CO₂ concentration ( Nobel & Israel 1994).

The increased ability to withstand drought for CAM species under elevated atmospheric CO₂ concentrations is associated with an increased WUE ( Table 4), as has been found for C₃ and C₄ species ( Eamus 1991; Ham et al. 1995 ; Jarvis, Mansfield & Davies 1999). The enhancement under a doubled CO₂ concentration occurs despite the greater contribution of daytime CO₂ uptake, which is less water-use efficient, to the total net daily CO₂ uptake. For A. deserti, A. comosus and O. ficus-indica, the increase in WUE is due both to increased daily net CO₂ uptake at elevated atmospheric CO₂ concentrations and also to decreases in stomatal conductance ( Cui et al. 1993 ; Graham & Nobel 1996; Zhu et al. 1999 ). Water vapour conductance for A. deserti decreases 24% under elevated atmospheric CO₂ concentrations, and most water loss occurs at night. The higher plant water content associated with the increased WUE for these succulent species allows for net CO₂ uptake to occur for longer periods during drought ( Raveh et al. 1995 ; Graham & Nobel 1996).

Table 4. Water-use efficiencies (WUE) for CAM plants under ambient (350–370 μmol mol⁻¹) and elevated (700–750 μmol mol⁻¹) atmospheric CO₂ concentrations

Species	WUE (mmol CO₂ mol⁻¹ H₂O)		Reference
Species	Ambient CO₂	Elevated CO₂	Reference
Agave deserti	20	42	Graham & Nobel (1996)
Ananas comosus	9·5	13	Zhu et al. (1999)
Opuntia ficus-indica
basal cladodes	4	7	Cui et al. (1993)
daughter cladodes	10	16	Cui et al. (1993)

For both current and elevated atmospheric CO₂ concentrations, maximum daily net CO₂ uptake for many CAM species occurs at day/night air temperatures of approximately 25/15 °C, reflecting the optimal night-time temperature for carboxylation by PEPCase ( Winter 1985; Nobel 1988). Increasing or decreasing the day/night air temperatures from the optimum reduces the daily uptake of CO₂, but the reduction is generally greater at current than at elevated atmospheric CO₂ concentrations. For H. undatus ( Fig. 2i), daytime net CO₂ uptake becomes negative at a day/night air temperature of 45/35 °C ( Raveh et al. 1995 ), the latter reflecting the sensitivity of C₃ photosynthesis to high temperatures. Increases in leaf temperature increase the O₂:CO₂ ratio at the site of CO₂ fixation via Rubisco, thus increasing photorespiration ( Taiz & Zeiger 1998). Elevated atmospheric CO₂ concentrations can offset this increase and may thus contribute to the large percentage enhancement in total daily net CO₂ uptake that occurs under elevated temperatures for several CAM species, such as A. deserti, O. ficus-indica, H. undatus and A. comosus ( Nobel & Israel 1994; Raveh et al. 1995 ; Graham & Nobel 1996; Zhu et al. 1999 ). The enhancement of total daily net CO₂ uptake at high temperatures for CAM species is likely to be important under a changing global climate that may result in average annual temperature increases of 2–4 °C associated with a doubled concentration of atmospheric CO₂ and increases in other greenhouse gases ( Kattenberg et al. 1996 ).

For CAM species at the current atmospheric CO₂ concentration, respiration becomes more important at high temperatures ( Kluge & Ting 1978). Relatively little is known about the effect of elevated atmospheric CO₂ concentrations on their respiration. In any case, elevated atmospheric CO₂ concentrations may reduce mitochondrial/dark respiration, as occurs for C₃ species ( Amthor 1991; Drake et al. 1999 ).

CELLULAR ASPECTS OF PHOTOSYNTHESIS

Chlorophyll

The chlorophyll content for A. deserti, A. vilmoriniana and O. ficus-indica is approximately 20% less under doubled compared with the current atmospheric CO₂ concentration ( Table 5; Szarek et al. 1987 ; Nobel et al. 1994a ; Graham & Nobel 1996). Similar decreases occur in C₃ species and suggest increased photosynthetic efficiency ( Wullschleger, Norby & Hendrix 1992; Moore et al. 1998 ). For O. ficus-indica, the chlorophyll a:b ratio is 9% lower under a doubled CO₂ concentration ( Table 5; Nobel et al. 1994a ), indicating an increase in light-harvesting chlorophyll b and photosystem II activity, as found for shade versus sun leaves ( Nobel 1999). In contrast the chlorophyll a:b ratio increases approximately 12% with a doubling of the atmospheric CO₂ concentration for A. deserti and A. vilmoriniana ( Table 5; Szarek et al. 1987 ; Graham & Nobel 1996). The different responses of the chlorophyll a:b ratio may reflect changes in light penetration to the mesophyll resulting from different responses of the photosynthetic surfaces to elevated atmospheric CO₂ concentrations. In particular, increased cuticular thickness and decreased transmission of PPF occur for O. ficus-indica as the atmospheric CO₂ concentration is raised ( Nobel et al. 1994a ), but decreased cuticular thickness and increased PPF transmission occur for A. deserti ( Graham & Nobel 1996).

Table 5. Chlorophyll and carboxylation enzyme properties under current (370 μmol mol⁻¹) and doubled (720–750 μmol mol⁻¹) atmospheric CO₂ concentrations

Species	Current CO₂	Doubled CO₂	Reference
Chlorophyll content
Agave deserti (g m⁻²)	0·80	0·64	Graham & Nobel (1996)
Agave vilmoriniana (μg g⁻¹ FW)	132	116	Szarek et al. (1987)
Opuntia ficus-indica (g m⁻²)	0·65	0·52	Nobel et al. (1994a)
O. ficus-indica (μg g⁻¹ FW)	320	280	Nobel et al. (1994a)
Chlorophyll a:b
A. deserti	2·3	2·6	Graham & Nobel (1996)
A. vilmoriniana	2·5	2·8	Szarek et al. (1987)
O. ficus-indica	3·2	2·9	Nobel et al. (1994a)
PEPCase (μmol m⁻² s⁻¹)
A. deserti	55	37	Graham & Nobel (1996)
O. ficus-indica	32	20	Nobel et al. (1994a)
Rubisco (μmol m⁻² s⁻¹)
A. deserti	40	35	Graham & Nobel (1996)
Agave salmiana	28	23	Nobel et al. (1996)
O. ficus-indica	41	29	Nobel et al. (1994a)
O. ficus-indica	34	29	Nobel et al. (1996)
Activated:total Rubisco (% of total)
A. desert	59	74	Graham & Nobel (1996)
A. salmiana	54	89	Nobel et al. (1996)
O. ficus-indica	53	88	Nobel et al. (1996)
K _M for PEPCase (mol m⁻³ HCO₃⁻)
A. salmiana	0·39	0·33	Nobel et al. (1996)
O. ficus-indica	0·48	0·27	Nobel et al. (1996)
K _M for Rubisco (mmol m⁻³ CO₂)
A. salmiana	25	26	Nobel et al. (1996)
O. ficus-indica	23	25	Nobel et al. (1996)

Enzymes

Carboxylation activities for the enzymes PEPCase and Rubisco decrease in response to a doubled atmospheric CO₂ concentration for the few CAM species that have been studied ( Table 5; Nobel et al. 1994a ; Graham & Nobel 1996; Nobel et al. 1996 ). Decreases in PEPCase and Rubisco activities also occur for the orchid ‘Mokara Yellow’ under 1 and 5% atmospheric CO₂ concentrations in photosynthetic shoots and roots ( Gouk et al. 1997 ). Many C₃ species show decreases in Rubisco content or activities in response to elevated atmospheric CO₂ concentrations ( Drake, Gonzàlez-Meler & Long 1997), potentially resulting in acclimatization to the higher CO₂ concentrations ( Bowes 1993; Moore et al. 1999 ). However, transforming the C₃Nicotiana tabacum such that Rubisco production is decreased approximately 15% reduces net carbon uptake at the current but not at a doubled atmospheric CO₂ concentration, indicating a reduced requirement for Rubisco at elevated atmospheric CO₂ concentrations ( Masle, Hudson & Badger 1993). Furthermore, as CO₂ is an activator as well as a substrate for Rubisco ( Lorimer, Badger & Andrews 1976), increases in internal CO₂ concentrations in response to elevated atmospheric CO₂ concentrations can result in increases in the enzyme activation state, thus compensating for decreases in total activity. Indeed, for A. deserti, Agave salmiana and O. ficus-indica, decreases in Rubisco carboxylation activity of 15–30% are compensated for by 25–65% increases in the ratio of the activated to total Rubisco ( Table 5), leading to increases in Rubisco- mediated daytime CO₂ uptake.

For A. deserti and O. ficus-indica, the decreases in PEPCase activity under a doubled atmospheric CO₂ concentration are greater than those for Rubisco ( Table 5; Nobel et al. 1994a ; Graham & Nobel 1996), and possibly reflect a relatively decreased requirement for this initial carboxylating enzyme as the substrate becomes more abundant. Furthermore, a doubling of the atmospheric CO₂ concentration results in 15 and 44% decreases in the apparent K_M(HCO₃⁻) for PEPCase for A. salmiana and O. ficus-indica, respectively ( Table 5). In this regard, the K_M(HCO₃⁻) for PEPCase from Zea mays decreases with decreasing pH ( O’Leary 1982).

The K_M(CO₂) for Rubisco does not change for A. salmiana or O. ficus-indica in response to a doubling of the atmospheric CO₂ concentration ( Table 5; Nobel et al. 1996 ). This is consistent with results for Gossypium hirsutum (C₃) and Z. mays (C₄), whose K_M(CO₂) for Rubisco is similar for plants grown from seed at 330 and 640 μmol mol⁻¹ CO₂ ( Yeoh, Badger & Watson 1981). The K_M(CO₂) for Rubisco is unchanged by CO₂ enrichment for other C₃ species as well ( Campbell, Allen & Bowes 1988). The K_M(CO₂) for Rubisco for A. salmiana and O. ficus-indica is in the upper part of the range for C₃ and CAM species (12–25 mmol m⁻³; Yeoh et al. 1981 ), but less than values for C₄ species (28–34 mmol m⁻³; Yeoh et al. 1981 ). The difference in K_M(CO₂) between the C₃ and C₄ species may reflect the strong CO₂-concentrating mechanism of the C₄ type ( Yeoh et al. 1981 ). The lower K_M(CO₂) for Rubisco from CAM species may indicate a lower CO₂ concentration at the site of the enzyme than for C₄ species, which may in part explain why CAM species show a greater response to elevated atmospheric CO₂ concentrations than do C₄ species. Indeed, Kalanchoë pinnata, whose stimulated growth under elevated atmospheric CO₂ concentrations is attributed to increases in daytime CO₂ uptake ( Winter et al. 1997 ), has a K_M(CO₂) for Rubisco of 15 mmol m⁻³ ( Yeoh et al. 1981 ).

Malate

The majority of CAM species subjected to elevated atmospheric CO₂ concentrations for extended periods show a night-time increase in titratable acidity or malate accumulation ( Table 6). This indicates increased night-time CO₂ fixation ( Griffiths 1988) and is consistent with the increase in phase I CO₂ uptake ( Fig. 1) and lack of saturation of phase I at the current atmospheric CO₂ concentration. The lack of response of malic acid accumulation in K. pinnata to elevated atmospheric CO₂ concentrations possibly reflects the fact that biomass enhancement for this species is due to increased daytime net CO₂ uptake ( Winter et al. 1997 ). Although Kalanchoë daigremontiana shows similar nocturnal malate accumulation at 300 μmol mol⁻¹ CO₂ and in response to a short-term exposure to 1000 μmol mol⁻¹ CO₂, the rate of accumulation is faster at the elevated atmospheric CO₂ concentration. This results in a decreased period of accumulation, suggesting that the extent of malate accumulation is limited by factors other than the atmospheric CO₂ concentration ( Holtum et al. 1983 ). Plants subjected to short-term increases in atmospheric CO₂ concentration may lack anatomical and biochemical changes to support increased malate accumulation, e.g. sufficient carbohydrates for increased synthesis of the acceptor. Interestingly, Tillandsia ionantha and Crassula arborescens both show increased malic acid accumulation in response to short-term exposure to elevated atmospheric CO₂ concentrations, although whether these plants had become acclimatized to the higher CO₂ concentrations in their greenhouse environment is not known ( Nowak & Martin 1995).

Table 6. Nocturnal acidity increases for CAM species in response to short-term (< 1 week) and long-term (> 1 month) exposure to elevated atmospheric CO₂ concentrations as a percentage increase over controls maintained under the current atmospheric CO₂ concentration for the same period

Species	Elevated CO₂ concentration (μmol mol⁻¹)	Duration of treatment	Nocturnal acidityv(% increase)	Reference
Agave vilmoriniana	752	Long-term	7·5 to 12	Szarek et al. (1987)
Ananas comosus	730	Long-term	34	Zhu et al. (1997a)
Orchid “Mokara Yellow”	10 000	Long-term	23 to 100	Gouk et al. (1997)
Tillandsia ionantha	800	Short-term	50	Nowak & Martin (1995)
Opuntia ficus-indica	750	Long-term	22	Wang & Nobel (1996)
Portulacaria afra	950	Short-term	0	Huerta & Ting (1988)
Crassula arborescens	920	Short-term	50	Nowak & Martin (1995)
Kalanchoë daigremontiana	1000	Short-term	0 to −25	Holtum et al. (1983)
Kalanchoë pinnata	750	Long-term	−8 to −11	Winter et al. (1997)

Sugars and photosynthate partitioning

Acclimatization to elevated atmospheric CO₂ concentrations, as is observed for many species and especially for C₃ annuals, is usually attributed to altered source–sink relationships, with excess soluble sugars and starch accumulation resulting in feedback inhibition of photosynthesis ( Arp 1991; Stitt 1991; Bowes 1993; Moore et al. 1999 ). Feedback inhibition may reflect inhibition of photophosphorylation resulting from depletion of Pi pools, as sugar phosphates build up, reflecting reduced rates of starch and sucrose synthesis ( Stitt 1991). Additionally, a build-up of sugars may suppress Rubisco, resulting in a lowered photosynthetic rate ( Bowes 1993; Moore et al. 1999 ). For O. ficus-indica, the synthesis of glucomannan, a probable carbon reserve for PEP, increases 170% under a doubled atmospheric CO₂ concentration ( Wang & Nobel 1995), which may help explain the large stimulatory effect of a doubled atmospheric CO₂ concentration on its net CO₂ uptake. Increases in soluble sugar and starch content of more than 60% also occur for O. ficus-indica in response to long-term exposure to elevated atmospheric CO₂ concentrations, but do not result in down-regulation of photosynthesis ( Cui et al. 1993 ; Nobel & Israel 1994).

In the basal cladodes of O. ficus-indica, increases in starch accumulation during the daytime and at elevated atmospheric CO₂ concentrations do not lower the photosynthetic rates, as occurs for some C₃ species ( Servaites et al. 1989 ), indicating that starch accumulation is not limiting its photosynthesis ( Wang & Nobel 1996). Similarly, starch accumulation induced by girdling the petioles of mature leaves of some starch-storing C₃ species also does not directly cause feedback inhibition of photosynthesis ( Goldschmidt & Huber 1992). The sucrose content and its daily change in cladodes are similar under current and doubled atmospheric CO₂ concentrations, despite 146% increases in the activity of sucrose-Pi synthase under a doubled atmospheric CO₂ concentration ( Wang & Nobel 1996). However, increases in phloem transport to developing daughter cladodes (sinks) under a doubled atmospheric CO₂ concentration ensure that sucrose levels do not increase in the basal cladodes (sources) leading to feedback inhibition ( Wang & Nobel 1995, 1996). Sink strength, as evidenced by increases in the activities of sucrose-Pi synthase and soluble starch synthase for daughter cladodes, also increases for O. ficus-indica under a doubled atmospheric CO₂ concentration ( Black 1993; Jenner & Hawker 1993; Wang & Nobel 1996). Furthermore, the increase in glucose and malate in the sink regions under a doubled atmospheric CO₂ concentration may increase the osmolality of the sink cells and thus decrease the turgor pressure of the phloem in the sink region ( Ho 1988), resulting in a more rapid movement of photoassimilate into the daughter cladodes ( Wang & Nobel 1996). Thus some of the excess carbohydrate produced in the basal cladodes of O. ficus-indica at elevated atmospheric CO₂ concentrations sustains growth of the daughter cladodes.

Despite a 175% increase in glucose levels in the basal cladodes under a doubled atmospheric CO₂ concentration, the concentrations of glucose (1 mol m⁻³) and sucrose (5 mol m⁻³) in the chlorenchyma of O. ficus-indica are 10 and 60 times less, respectively, than those needed to suppress gene expression in annual crops ( Sheen 1994). Furthermore, for C₃ species, the occurrence of strong end-product inhibition appears correlated with high acid invertase activity ( Goldschmidt & Huber 1992) and an increased hexose flux through hexokinase ( Moore et al. 1999 ). In this regard, the activity of invertase is extremely low in basal cladodes of O. ficus-indica under both current and elevated atmospheric CO₂ concentrations, and the activity of hexokinase is slightly decreased under a doubled atmospheric CO₂ concentration ( Wang & Nobel 1996). The cellular contents of O. ficus-indica in particular and CAM species in general are relatively dilute, as indicated by high relative tissue water contents and high water potentials ( Nobel 1988). Indeed, the succulence of many CAM species, which buffers fluctuations in the daily supply of water and photoassimilates available for growth ( Nobel 1988; Wardlaw 1990), may represent a photosynthetic type that can accommodate increases in carbohydrate levels in response to elevated atmospheric CO₂ concentrations without acclimatization of photosynthesis.

CONCLUSIONS

Predicting the response of CAM species to elevated atmospheric CO₂ concentrations on the basis of the initial carboxylating enzyme fails to consider the complexity of this photosynthetic type. Indeed, although generalizations may be more applicable to C₃ and C₄ species, variation of response also occurs for these photosynthetic types ( Lawlor & Mitchell 1991; Poorter 1993). Doubling the atmospheric CO₂ concentration greatly stimulates net CO₂ uptake by the CAM species studied ( Tables 1 and 3), despite the suggestion that the predominant initial fixation of CO₂ by PEPCase in CAM plants might be saturated at the current atmospheric CO₂ concentration ( Ting 1994; Winter & Engelbrecht 1994). The accompanying biomass increase, which reflects increases in both daytime and night-time net CO₂ uptake, averages about 35% for these CAM species ( Table 2), including 40% for the highly productive and widely cultivated O. ficus-indica over a one-year period ( Nobel & Israel 1994). Decreases in Rubisco activity that occur for CAM species in response to elevated atmospheric CO₂ concentrations are compensated for by increases in the fraction of the enzyme in the activated state ( Table 5), thus maintaining photosynthetic performance, as occurs for C₃ species. However, unlike some C₃ species, especially annuals, there is little evidence of acclimatization to elevated atmospheric CO₂ concentrations with time of exposure for most of the CAM species studied. The lack of acclimatization is possibly associated with the succulence of CAM species, which can accommodate large increases in chlorenchyma thickness and accumulation of photosynthate without feedback inhibition.

Such conclusions, however, are based on the study of relatively few species with no study exceeding 18 months, a relatively short time period in the life span of species such as A. deserti and O. ficus-indica. Although remarkable similarity in response to elevated atmospheric CO₂ concentrations occurs for the species investigated, only one species, O. ficus-indica, has been studied in depth. Thus comprehensive studies of a greater number of CAM species from different families and environments would be valuable. In particular, focusing on PEPCase-mediated night-time CO₂ uptake may contribute to an understanding of why that process is not limited at close to the current atmospheric CO₂ concentration. Whether the K_M(HCO₃⁻) for PEPCase decreases in other CAM species exposed to elevated atmospheric CO₂ concentrations and the basis for the decrease need to be investigated. Studies of carbohydrate partitioning in CAM species may explain the lack of acclimatization. Longer-term exposure to elevated atmospheric CO₂ concentrations could establish whether acclimatization occurs after years, as well as whether effects on reproduction occur. Furthermore, the response of C₃– CAM intermediates to elevated atmospheric CO₂ concentrations has been little investigated, beyond the apparent insensitivity to atmospheric CO₂ concentrations of the switch from C₃ to CAM. The variable CAM response of such intermediates may present an opportunity to determine specific contributions, for example of anatomical changes, to the enhancement of net CO₂ uptake and of productivity in response to elevated atmospheric CO₂ concentrations.

Observations of significant biomass increases and lack of acclimatization, coupled with the increasing air temperatures accompanying global climate change that may extend the range of cultivation for freezing-sensitive CAM species ( Nobel & Garcia de Cortázar 1991; Nobel 1996), could affect land-use practices with regard to mitigating rising atmospheric CO₂ concentrations. In particular, the international protocol discussed in Kyoto, Japan, in December 1997 pledges countries to work towards a stabilization of atmospheric CO₂ concentrations. The high WUE of CAM plants ( Table 4) together with the large biomass productivity of selected CAM crops, both of which should increase under elevated atmospheric CO₂ concentrations, suggests their consideration with regard to terrestrial sequestration of atmospheric CO₂ in arid and semi-arid regions. Such regions, which are poorly suited to C₃ and C₄ crops without irrigation, occupy about 30% of the earth’s land area. Moreover, the substantial biomass increases for CAM species under elevated atmospheric CO₂ concentrations could enhance the importance of such native plants in ecosystems worldwide.

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Citing Literature

Volume23, Issue8

August 2000

Pages 767-781

Responses of CAM species to increasing atmospheric CO₂ concentrations

ABSTRACT

INTRODUCTION

GROWTH AND BIOMASS

MORPHOLOGY AND ANATOMY

GAS EXCHANGE

CELLULAR ASPECTS OF PHOTOSYNTHESIS

Chlorophyll

Enzymes

Malate

Sugars and photosynthate partitioning

CONCLUSIONS

REFERENCES

Citing Literature

Figures

References

Information

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Responses of CAM species to increasing atmospheric CO2 concentrations

ABSTRACT

INTRODUCTION

GROWTH AND BIOMASS

MORPHOLOGY AND ANATOMY

GAS EXCHANGE

CELLULAR ASPECTS OF PHOTOSYNTHESIS

Chlorophyll

Enzymes

Malate

Sugars and photosynthate partitioning

CONCLUSIONS

REFERENCES

Citing Literature

Figures

References

Related

Information

Responses of CAM species to increasing atmospheric CO₂ concentrations