Current wisdom assigns CAM in its idling mode importance as a stress-mitigating, maintenance mechanism a state of quiescence rather than dormancy that keeps the mesophyll primed for renewed opportunity, viz. renewed water supply. As stomata close while desiccation progresses and E falls, idling ensues and CAM, now totally dependent on respired CO2, hence diminished overall, continues to provide enough energy to avoid death, or the need to lapse into an inactive condition from which recovery would be slow. Idling also maintains a CO2 source to help protect the light-harvesting apparatus (Maxwell et al. 1992,1994,1995). Photosynthesis for the CAM-idling plant returns to pre-stress levels within hours to a day or two following return to wet weather, much faster than possible for a drought-avoiding shrub, or a similarly deciduous Pitcairnia that likewise must rst regenerate its canopy.
One of the most perplexing facets of CAM concerns certain details of carbon management, particularly the continued prominence of CO2 recycling in recovered foliage and sometimes leaves that never experienced severe drought. Why do apparently well-watered subjects so often depend so heavily on recycled CO2 compared with inputs from the atmosphere? According to Martin (1994), CAM-idling in the strictest sense (recycled CO2 accounts for 100% aH+) has never been recorded for a bromeliad (but see Stiles and Martin 1996). However, many plants examined in situ were processing much more carbon than could be accounted for by gas exchange, and often well above what seemed necessary.
Griffiths et al. (1986) and Griffiths (1988) reported values ranging from 50 to 99%, sometimes even during fairly wet weather, for the diverse taxa included in their survey in Trinidad (Table 4.4). Thoroughly irrigated subjects exposed to a variety of growing conditions have often behaved similarly. Why were these plants gaining carbon so feebly compared with respiration, even while seemingly unstressed? Before trying to answer this question, we need to revisit the relationship between carbon and water in the context of CAM.
The algorithm used to calculate fractions of aH+ attributable to recycled carbon vs. exogenous CO2 employs the stoichiometry of two titratable H+: one malic acid molecule: one CO2 molecule. Internally generated CO2 represents the balance remaining after subtracting from aH+ the amount from outside according to measured gas exchange. Whatever other bene®ts accompany CAM, its capacity to recycle dark-respired CO2 whether in or out of the idling mode, promotes WUE in the same way described earlier for the CAM-cycler (see also Martin et al. 1988). Fetene and Lüttge (1991) proposed using the ratio of moisture saved through recycling to transpiration, which, by substituting A/E for WUE, was reduced to estimate the advantages of CAM to water balance in Bromelia humilis.
Bromelia humilis also demonstrated how cues related to growing conditions affect the carbon budget of a CAM bromeliad. More precisely, Fetene and Lüttge illustrated why well-watered plants sometimes rely so heavily on respired compared with exogenous CO2 ± why, despite adequate irrigation, they so readily reduce g. Respiration always assures some recycling, but only enough to account for a small fraction of H+max while CAM remains robust, i.e., while CO2 reaching PEPc from the atmosphere greatly exceeds the supply from mitochondria. The acidity assignable to recycling by non-stressed CAM types should approximate aH+ in an otherwise comparable CAM-cycler because the stomata of the cycler close at night, trapping endogenous CO2 for nonautotrophic re®xation.
Recall that Fetene et al. (1990) and Fetene and Lüttge (1991) demonstrated how well-fertilized and N-deprived B. humilis pretreated at two exposures gained different amounts of carbon under the same high and low PPFDs (Figs. 4.5, 4.6). They also manipulated drought-stress, leaf-to-air VPD and night-time temperature to note shifting dependency on recycled vs. exogenous CO2. While these data provide no de®nitive answers, they suggest some intriguing possibilities and underscore the complexity of the CAM syndrome and its sometimes dubious utility as an indicator of eco-physiological status (prevailing plant stress). More importantly, their manipulations demonstrate how disparate aspects of the environment, both historic and immediate, can affect the operation of CAM. Bromelia humilis, at least, shifts toward CAM-idling whether challenged by N-de -ciency, drought, high temperature or steep VPD in night air, i.e., the same plant response reduces vulnerability to several threats to water balance and perhaps other essential processes like light harvest.
High temperatures at night (>30 °C) shifted 24-h carbon budgets closer to or into negative territory, and more substantially for —N than for +N plants. Relative reliance on recycled CO2 for phase one increased apace until at 35 °C, contributions from respiration about equaled the amounts of CO2 derived from the atmosphere at 20 °C (30 mmol m—212 h—1 for +N plants and 18 mmol CO2 m—2 12 h—1 for subjects grown on unamended soil). CO2 uptake responded more sensitively to temperature than aH+, and about equal amounts of acid accumulated at 35 °C and 20 °C, perhaps due to an unusually high temperature coefficient (Q10) for dark respiration as Lüttge and Ball (1987) noted for some other CAM bromeliads. Regardless of pretreatment, dark respiration rose exponentially with temperature, but more in —N plants than in better-nourished specimens. Temperature coefficients ranged between 2.3 and 3.0 (10 25 °C) with —N plants, once again exceeding the responses of better-fertilized subjects.
The more elevated of the two applied VPDs (7.46 Pa KPa—1 vs. 15.49 Pa KPa—!) reduced CO2 uptake to different degrees depending on pretreatment. Reliance on recycling was about 2 6-fold greater at the higher VPD. Water saved by recycling as equivalents of E (ratio of recycled CO2 to net nocturnal CO2 assimilation) increased from 0.08 to 0.60 at the lower VPD and from 0.80 to 3.0 at the higher one. Thus, at the lower VPD, amounts of water equal to only 8 60% more than the total transpired remained unexpended, while savings in drier air rose to 80 300%. Less moisture-saturated air had reduced g to just 5 23% of that prevailing when the more humid atmosphere had threatened plant water status less. Ten days of drought almost shut down CO2 uptake and reduced H+max to just 30 40% of pre-stress levels. However, recycling increased proportionally from about 25 35% to near 100%. By day 10, the water saved by recycling amounted to 2 6-fold the quantity that plants had transpired. After 12 days, CO2 uptake almost ceased, indicating that the protection afforded by reducing g developed much faster here than for some nonbromeliads.
Agave deserti, Opuntia ficus-idea and Ferrocactus acanthoides required 11 20 days just to reduce initial rates of CO2 uptake 50% in another study (Nobel 1988). Apparently, CAM serves Bromelia humilis quite well in its highly seasonal, hot and probably often infertile habitats. Rather than an all-or-nothing response, proportional reliance on endogenous CO2 waxes and wanes with uctuations in several aspects of the environment capable of reducing water economy and growth and, if severe enough, of in icting serious plant injury. Sensitivity, if greater here than usual, would mean that this bromeliad anticipates threatening conditions sooner than some other CAM types. Or modest capacitance may simply permit water-stress to develop faster for Bromelia humilis compared with these other xerophytes when subjected to comparable droughts. Viewed either way, an unusually sensitive response to conditions that can suppress phase one of CAM (e.g., high temperature, poor nutrition) or accelerate E (e.g., high temperature, high VPD) mitigates the liability imposed by the low capacitance (for a CAM plant) of this bromeliad, thus promoting its tolerance to diverse kinds of stress.
Sensitivity to VPD allows plants to reduce nonproductive water use, but do responses vary among Bromeliaceae according to other plant characteristics that in uence vulnerability to drought? Dry air reduces g for Tillandsia usneoides (see Lange and Medina 1979; Fig. 4.19), but species with substantial capacity to replace losses from large phytotelmata (e.g., Aechmea nudicaulis, A. aquilega) behave the same way, although perhaps less sensitively. Light constitutes another agency that effects rapid changes in g and accordingly, shifts relative dependence on atmospheric vs. respired CO2 among CAM bromeliads. Tillandsia usneoides recycled proportionally more carbon after transfer to higher PPFD (Martin et al. 1986), whereas Aechmea nudicaulis did so upon relocation into shade (Griffiths et al. 1986). Finally, chronic, pronounced recycling need not seriously limit growth. Cultivated Ananas comosus rivals some C3 crops for the production of dry matter, yet recycling accounted for 45% of aH+ in one analysis involving irrigated specimens (Sale and Neales 1980).
So it seems that a variety of chronic and more transitory stresses, including excessive temperature, nutrient scarcity and suboptimal VPD, promote heavy dependence on recycled CO2 in at least some CAM bromeliads. Signi cantly, all of these challenges from the environment in uence plant water economy and carbon budgets at least indirectly (e.g., N status through its effects on A). Still, drought often appears to act most decisively, although unevenly according to several studies on Type Five Bromeliaceae in the laboratory and eld (see Fig. 4.15 for strong circumstantial evidence). Several of these investigations indicate how drought probably affects recycling for the more notably stress-tolerant epiphytes.
Whereas less than 50% of the titratable acidity present in the well-watered shoots of usually arboreal Tillandsia schiedeana (Type Five) at dawn had come from recycled CO2, 30 days without irrigation in a growth chamber boosted that gure to about 90% (Martin and Adams 1987). Recycling varied more over the year on an absolute than on a proportional basis in Tillandsia flexuosa growing in one of its semiarid coastal Venezuelan habitats (Griffiths et al. 1989). Recycled carbon accounted for 76 vs. 73% of the total acid synthesized from mid-wet to mid-dry season, although H+max diminished 35% as aridity intensi ed. Exogenous CO2 accounted for only 1% of the malic acid accumulated by terrestrial Bromelia plumieri in Trinidad (Griffiths et al. 1986; Table 4.4). Neither moisture-stress nor nutritional de ciencies were mentioned, but readings date from February and March, two especially arid months (<25 mm precipitation) at this strongly seasonal site. On that occasion, no rain had fallen for several weeks.
Thicker-leafed Aechmea fendleri recycled proportionally more CO2 than A. nudicaulis, suggesting that succulence may elevate endogenous CO2 enough to simulate a stress symptom in a relatively well-hydrated subject. However, Griffiths (1988) considered hydrenchyma too inert to account for the difference, and Luttge and Ball (1987) supported his assessment with data from additional species. While achlorophyllous storage tissue comprised 60 75% of the mesophyll of Hechtia glomerata, it accounted for only 9.5% of the CO2 available for recycling. The presence of exceptionally active tissue constitutes another possibility that has some support. Several CAM plants endemic to warm habitats, including three bromeliads (Aechmea fasciata, Ananas comosus, Hechtia glomerata), exhibited dark respiration with Q10s that ranged from 2.13 to 4.09 between 10 and 30 °C. Additionally, all CAM plants require ATP to mediate the massive traffic in malate across the tonoplast. Finally, a biochemical peculiarity also in u-ences how much endogenous CO2 certain CAM plants produce compared with others. Bromeliads may stand out because they consume free hexose, which assures relatively high rates of respiration, rather than the glucans many other CAM plants (e.g., Kalanchoe) employ to drive phase one.
Loeschen et al. (1993) used 12 dry-growing Tillandsia species to rule out nongreen tissue as a major source of CO2 for phase one. Recycling did not correlate with leaf anatomy; in fact only one subject, T. schiedeana, deviated substantially from the 1:1 ratio mandated by the stoichiometry of malic acid production during CAM (Fig. 4.13). Tillandsia schiedeana alone acidi ed beyond what could be explained by the consumption of exogenous CO2. Several other taxa yielded values above one, but less than two. Note that T. schiedeana (30% water-storage tissue) occurs about midway within the range (0 53%) exhibited by their sampling. Tillandsia usneoides produced a modestly positive value despite its undifferentiated mesophyll (Fig. 2.10A), while T. valenzuelana (53%) synthesized less acid than gas exchange predicted. Different degrees of stress supposedly accounted for the mixed results, and this explanation is plausible given the single pretreat-ment provided to all 12 of these ecologically diverse species.
Additional inquiry might pro tably focus on the functions of foliage with anatomically uniform vs. dimorphic mesophyll. Perhaps drought depresses A in a less precipitous fashion among subjects with the second compared with the rst type of leaf structure, i.e., one or the other kind of plant reduces g sooner as water de cits develop. Green cells in T. usneoides presumably lose turgor faster when plants are subjected to drought than those of species featuring hydraulic coupling to collapsible, water-storing parenchyma. Moreover, architectural constraints may oblige a speci c type of leaf anatomy even if another option would grant superior drought-performance. Perhaps the leaves of Spanish moss are simply too small to support a division of labor between water storage and photosynthesis. Finally, what other physiological or structural peculiarities co-occur with an anatomically undifferentiated mesophyll? And what about those exceptionally thin epidermal layers and delicate cuticles illustrated in Fig. 2.10?
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