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Physiology and Biochemistry |
Departamento de Biología Evolutiva, Instituto de Ecología, A. C., Apartado 63, 91000, Xalapa, Veracruz, Mexico
Received for publication February 9, 2006. Accepted for publication June 20, 2007.
ABSTRACT
Columnar cacti have been traditionally classified as crassulacean acid metabolism (CAM) plants, though recent research indicates some cactus seedlings employ the C3 pathway. To verify this last result, we measured acidity fluctuations for five columnar and one globular cactus species in seedlings from 1 to 48 d old after experimental exposure to 60% and 30% full sunlight, and in adult plants in the field. Using light-response curves of chlorophyll fluorescence, we determined photosynthetic efficiency (
F/Fm'), maximum electron transport rate (ETRmax) and saturating photosynthetically active photon flux density (PPFDsat). All seedlings used the CAM pathway from their first day of development, and increases in nocturnal acidity depended on species, light treatment, and age. The CAM pathway was also found in adult plants. Cactus seedlings were able to acclimatize to light conditions by making photochemical adjustments, mainly by modifying the level of light at which photosystem II is saturated (PPFDsat). The presence of CAM in the seedlings of columnar cacti increases water-use efficiency and reduces the risk of photoinhibition. This could favor survival in the highly variable light levels characteristic of the desert environments of columnar cacti.
Key Words: Cactaceae • cactus seedlings • chlorophyll fluorescence • crassulacean acid metabolism • fluctuation in acidity • instant light-response curves • Tehuacán, Mexico
The family Cactaceae possesses several adaptations to drought (such as a leaf reduction or loss, succulence, and photosynthetic stems) that allow them to survive in the semiarid environments where they reach their greatest diversity. One physiological adaptation is the crassulacean acid metabolism (CAM), which increases water-use efficiency (Nobel, 1988
) because the stomata open at night and CO2 is fixed when the air temperatures are lower and the relative humidity is higher, reducing water loss (Winter and Smith, 1996
; Roberts et al., 1997
; Lüttge, 2002
). Thus CAM is typically, but not exclusively, associated with plants that inhabit semiarid regions with seasonal water availability (Cushman, 2001
).
The magnitude of CAM's contribution to total carbon fixation is highly variable and depends on both genotypic and ontogenetic factors that affect the expression of biochemical and physiological plant attributes (Cushman, 2001
; Dodd et al., 2002
; Keeley and Rundel, 2003
), likewise it depends on environmental conditions (Winter and Smith, 1996
; Lüttge, 2002
), such as temperature and light intensity (Nobel and Hartsock, 1983
), and the plant's water status (Dodd et al., 2002
). The quantity of light that a CAM plant receives greatly affects the balance between CO2 fixation and the accumulation of organic acids (Nobel, 1981
; Nobel and Hartsock, 1983
; Barker and Adams, 1997
; Lüttge, 2004
), the opening of stomata (Nobel and Hartsock, 1983
), and in some facultative CAM species, the switch from the C3 photosynthesis pathway to CAM in response to photoperiod (Winter and Smith, 1996
; De Mattos et al., 1999
). Also, the ability to switch the photosynthetic pathway is related to water deficit (Dodd et al., 2002
), to habitat and life form depending on environmental conditions, and even to evolutionary relationships (Griffiths and Smith, 1983
; Kluge and Brulfert, 1996
; Martin and Wallace, 2000
).
Even though cacti are emblematic CAM plants, some researches have documented that in their early stages cactus seedlings depend on C3 photosynthesis rather than CAM. Particularly in columnar cacti, CAM has been reported for all the studied species, and not a single case of C3 has been documented (Nobel, 2002
). However, Altesor et al. (1992)
found that some Cactaceae seedlings are typically C3 during their first days of development and later switch to CAM, although it is unclear whether this is due to stress, a programmed developmental change, or both (Keeley and Rundel, 2003
). Unfortunately, these experiments and those of Loza-Cornejo et al. (2003)
and Ayala-Cordero et al. (2006)
, who also documented a C3-CAM change in columnar cactus seedlings, used seedlings growing at a low light level not found in their natural environment and apparently much lower than their light compensation point (Nobel and Hartsock, 1983
).
Some cactus species establish below the canopies of shrubs and woody species, benefiting from the protection against direct sunlight, high temperatures, water deficit, and herbivores, and from the increased nutrient availability (Sosa and Fleming, 2002
; Flores and Jurado, 2003
). However, given the seasonal variation in the phenology of the species under which the cacti grow, the photosynthetic photon flux density (PPFD) that plants receive can change considerably throughout the year. Hence, plants would be growing between the necessary light for photosynthesis and the excessive light, which could be damaging. To acclimatize to environments with high light, CAM plants must be able to optimize their photosynthetic efficiency to decarboxylate malate and to mitigate photoinhibition, thus avoiding over-energizing photosystem II (PSII) (Griffiths and Smith, 1983
; Adams et al., 1987
; Barker and Adams, 1997
; De Mattos et al., 1997
; Lüttge, 2004
). Photorespiration, the xanthophyll cycle, energy dissipation via zeaxanthin, and D1-protein turnover are protective mechanisms for energy dissipation in CAM plants (Lüttge, 2000
; Nobel and Bobich, 2002
).
Chlorophyll fluorescence has become a standard method for measuring photosynthetic capacity in intact leaves (Maxwell and Johnson, 2000
) and can be estimated under field conditions during phase III of CAM when the stomata are closed (Winter and Smith, 1996
; White and Critchley, 1999
). Differences in photosynthetic efficiency, measured by chlorophyll fluorescence, describe species- and genotype-specific differences in photosynthetic reduction and can be used to detect physiological changes resulting from environmental conditions such as excess light, extreme temperature, or drought (Nippert et al., 2004
).
In this study, we investigated whether columnar cacti seedlings express CAM photosynthesis at the earliest stages of development. We evaluated the effect of light intensity on the presumed switch from C3 to CAM and the photochemistry of photosynthesis (chlorophyll fluorescence) during the ontogeny of five species of columnar cacti and one globular cactus. Two light conditions similar to those during establishment of the seedlings were used. Rapid light curves were calculated for chlorophyll fluorescence in 1-wk-old seedlings of each species. Furthermore, we evaluated the acid concentration and chlorophyll fluorescence in adults of these species in the field. We hypothesized that (1) columnar cacti can use the CAM photosynthetic pathway during early development; (2) the acid concentration of the tissue in CAM plants is determined by the light received the previous day; (3) the photochemical efficiency of the plants depends on the environmental conditions; and (4) species differ in acid concentration and photochemical efficiency.
MATERIALS AND METHODS
Plant species
Five species of columnar cactus from the tribe Pachycereeae were selected: Neobuxbaumia tetetzo (Coulter) Backeberg, Pachycereus weberi (Coulter) Buxbaum, Stenocereus stellatus (Pfeiffer) Riccobono, Escontria chiotilla (Weber) Rose, and Myrtillocactus geometrizans (Martius) Console. The study also included one globular cactus belonging to tribe Echinocacteae, Ferocactus recurvus (Miller) Lindsay. Both taxonomic groups belong to the subfamily Cactoideae (Cactaceae). Seeds used for the experiments were extracted from fruit collected in Venta Salada, on the Valle de Tehuacán-Cuicatlán Biosphere Reserve in the state of Puebla, Mexico (18°16' N, 97°9' W at 1000 m a.s.l.).
Shade-house experiment
This study was carried out from June to August 2003. Two shade houses were used, one with high light intensity (HL; 60% of full sunlight) and the other with low light intensity (LL; 30% of full sunlight). These two treatments correspond to mean values determined in the field under a xerophytic shrub canopy (in the middle and two thirds of the way into the canopy) during the rainy season when the cacti germinate. Seedlings of columnar cacti establish more frequently under the shade of plants (Valiente-Banuet et al., 1991
). One thousand seeds were sown per species in 20 x 10 cm trays containing soil from the field site mixed with sand. For each species, there were three trays in each treatment. The shade house was covered throughout the experiment, and we added water to maintain soil moisture at field capacity, which ensured high soil humidity. Cacti seeds seem to be adapted to germinate at high soil humidity, but not necessarily at field capacity (Flores and Briones, 2001
). Some facultative CAM species switch from CAM to C3 in response to watering; by growing our seedlings at high soil humidity, we favored the expression of C3 rather than CAM.
Air temperature and the PPFD were determined using Li-Cor (Lincoln, Nebraska, USA) 1000–15 and Li-Cor LI-190SA sensors every 3 h from 22 June to 18 August 2003. Relative humidity was recorded every 3 h using a Vaisala (Oyj, Finland) HMP45A sensor on a sunny day. The sensors were connected to a Li-Cor LI-1000 data logger.
Acid level measurements
Germination was considered to have occurred when the radicle emerged, and on the following day we began to measure organic acid levels in the seedlings. Samples were collected every 3 h for 24 h, with three replicates per species in each treatment. Samples were put into 60% ethyl alcohol and immediately frozen. The concentration of organic acids was determined following a modified version of the Zotz and Andrade (1998)
protocol. Samples were brought up to 20 mL with 60% ethyl alcohol, boiled for 5 min, and titrated with 0.015 N NaOH. The results were expressed as total acid concentration in millimoles of H+ per gram of fresh tissue. We assumed that fluctuations in titratable acidity would reflect the nocturnal accumulation and subsequent diurnal consumption of malic acid (Winter and Smith, 1996
). Indeed, a diurnal oscillation pattern in titratable acidity was detected from the start, including the first and second days after germination, in all species; we subsequently collected and titrated tissue samples only in the morning (0600 hours) and in the evening (1800 hours) when the plants were 7 and 48 d old.
Rapid light curves for chlorophyll fluorescence
Rapid light curves (RLC) for chlorophyll fluorescence were produced using a portable fluorometer (Mini-PAM, Walz, Effeltrich, Germany). Seedlings were held in a leaf clip (Leaf-Clip Holder 2030-B), and the RLC were produced using two scales of the Mini-PAM light curve program to obtain a sequence of 0 to 2000 µmol of PPFD ·m–2·s–1. The light source was a halogen lamp inside the instrument. The intensity of actinic light was increased every 30 s for 8 min. The photosynthetic efficiency of PSII (F/Fm') was calculated as (Fm' – F)/Fm', where F is the fluorescence of the sample adapted to the light and Fm' is the maximum fluorescence of the sample adapted to the light when a saturation pulse of actinic light is applied.
The rate of electron transport for PSII (ETR) was calculated as ETR = F/Fm' x PPFD x 0.5 x 0.84, where PPFD is the photosynthetic photon flux density recorded by the sensor in the leaf clip. According to Rascher et al. (2000)
, only 79% of the recorded PPFD can be considered effective on the leaf surface given the distance between the leaf plane and the diffuser disc of the quantum sensor. The required reflection factor is 0.5 for both photosystems to absorb photons (Roberts et al., 1996
), and 0.84 is the estimated mean proportion of incident light absorbed by the photosystems (Ehleringer, 1981
). The dissipation of thermal energy was calculated as NPQ = (Fm – Fm')/Fm', where Fm is the maximum fluorescence at the beginning of the RLC.
For each species, the data for F/Fm' and ETR against PPFD were adjusted according to the statistical models proposed by Rascher et al. (2000)
. With the adjusted ETR vs. PPFD curve, the cardinal points were determined: maximum apparent electron transport rate (ETRmax) and saturating photosynthetically active photon flux density for PSII (PPFDsat), determined to 0.9 of ETRmax. The RLC were made when the seedlings were 1 wk old, at 1200 hours. There were three replicates per species in each treatment.
Field measurements
Tissue samples were collected in the field to determine the photosynthetic pathway in the mature or adult stage of the species studied and to compare this with the information for the shade-house seedlings. With the exception of N. tetetzo, which is not found in Venta Salada, total acidity was determined in five adult plants for each of the five other species at 0600 and 1800 hours in the rainy season (summer, July 2003). To ensure a similar interception of PPFD throughout the day in all of the columnar cacti, we selected branches with a height of 1.50 m that were oriented toward the east (Nobel, 1982
; Barker and Adams, 1997
). For the globular cactus, F. recurvus, we also collected tissue from the east side of the plant. Tissue samples were excised with an aluminum cork borer, 0.5 cm in diameter. The samples were frozen and transported to the laboratory. The chlorenchyma of each sample was titrated using the same method applied to the seedlings. Acid concentration was expressed in mmol H+ per surface area of tissue. On the same day, we determined the photosynthetic efficiency (F/Fm') at 1200 hours under ambient light with the portable fluorometer. On the day the samples were collected, the air temperature, relative humidity, and PPFD were measured.
Statistical analysis
For determining any cyclic variation in the concentration of organic acids over 24 h in the seedlings (characteristic of CAM plants), our statistical approach was to fit a sinusoidal function to the daily acid data under the hypothesis that a nonsignificant difference between diurnal and nocturnal tissue proton concentration would result in a nonsignificant fitting of this function. The data were adjusted to the function y = b(sin x) + a, where the sampling hour is the independent variable expressed in radians, the constant a is the mean concentration of acids, and the slope b is the amplitude of the periodic variation in acid concentration (Altesor et al., 1992
). Nonlinear regression models were employed to test the statistical significance of the sinusoidal function.
Two-way analyses of variance (ANOVA) were used to detect differences between light treatments and between the species of seedlings for each variable. Differences in maximum acid accumulation between light treatments for each species were determined using Tukey's multiple range tests. The field data for the adult plants were analyzed using a one-way ANOVA to determine whether species differed in their maximum value of acid accumulation. Differences between seedlings and adult plants in F/Fm' at midday were evaluated using a one-way ANOVA. The data were analyzed using the Statistica 6 program (Statsoft, Tulsa, Oklahoma, USA), and the critical value for all analyses was 0.05.
RESULTS
The environmental conditions at the beginning of the experiment were the same for all species in each treatment; however, owing to the variation in the germination time of the seeds, the total amount of light that the seedlings received during their development was different (Fig. 1). Although the different species germinated at different times, each species germinated the same day in both light treatments, and plants within a species, therefore, were exposed to the same variations of light conditions during the experiment. Acid accumulated nocturnally in seedlings of all six species under both light conditions (HL and LL) starting on the day after germination and also fluctuated diurnally as is typical of CAM plants. On adjusting the diurnal oscillation in acidity over 24 h cycles with the sine function, we detected a significant periodicity in the acid accumulation during the first (Fig. 2, Table 1) and second day (data not presented) after germination. All regression coefficients were significantly different from zero (P < 0.01), which indicates that the periodicity of the titratable acidity followed a sinusoidal function in all species and light treatments. However, M. geometrizans did not germinate in the HL treatment, and under LL the number of seedlings was not sufficient on the second day of sampling. Maximum acidity values were recorded early in the day (0600 hours), and the lowest values were recorded before sunset (1800 hours) (Fig. 2).
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F/Fm') of 1-wk-old seedlings differed significantly in response to the light treatments for only two species (Table 2); the photosynthetic efficiency of P. weberi and E. chiotilla was higher in the LL than in the HL treatment. Values of F/Fm' were similar in the seedlings and adults of S. stellatus, M. geometrizans, and F. recurvus (F/Fm' = 0.61 on average), even though the PPFD was >2000 µmol·m–2·s–1 in the field and 1500 or 750 µmol·m–2·s–1 under HL or LL in the shade house. In contrast, adult plants of P. weberi and E. chiotilla had high F/Fm' (0.68 on average) in the field, while their seedlings had lower values (F/Fm' = 0.52 on average) in the shade house (Table 2).
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CAM photosynthesis has been reported for 23 species of columnar cacti, and as far as we know, C3 metabolism has not been reported for the adult plants of these taxa (Nobel, 2002
). However, Altesor et al. (1992)
and Loza-Cornejo et al. (2003)
indicated that some species of cactus may use the C3 pathway during the first weeks of development, after which they change to CAM.
The columnar and globular cactus seedlings we studied use the CAM photosynthetic pathway from their first day of development; the fluctuation in their organic acids coincides with the definition proposed for CAM. The organic acid fluctuation is characterized by an increase in organic acids during the night and a decrease during the day (Winter and Smith, 1996
; Roberts et al., 1997
; Lüttge, 2002
, 2004
). Our experiment differs from those in previous studies, which used only low light intensity. The capacity for nocturnal absorption of CO2 is related to the intensity of light that the plants receive (Nobel and Hartsock, 1983
; Adams et al., 1987
). According to Nobel and Hartsock (1983)
and Nobel (1988), cacti and agave plants require more than 4 mol·m–2·d–1 (an instantaneous value of 93 µmol·m–2·s–1 for a 12-h photoperiod) to fix CO2 at night and therefore to accumulate organic acids. Altesor et al. (1992)
reported that, during the 10 to 20 wk after germination, the cacti that they studied (including N. tetetzo and F. recurvus from the current study) used C3 photosynthesis because the concentration of organic acids did not fluctuate nocturnally. Irregular fluctuations in the concentration of titratable acids during early ontogeny and until 1 yr of age were reported for S. queretaroensis (Loza-Cornejo et al., 2003
) and until 9 mo of age for S. beneckei (Ayala-Cordero et al., 2006
). In these three previously reported experiments, the seedlings received 70 µmol·m–2·s–1 or less with a photoperiod of 12 h. In our experiment, the light levels received by the seedlings (60% and 30% of full sunlight) corresponded to values measured in the field under plant canopies during the rain season (when the cacti germinate). The daily amount of light received by the seedlings was always greater than 185 µmol·m–2·s–1, and organic acids accumulated from the beginning of seedling development. This evidence suggests that in the previously mentioned experiments (Altesor et al., 1992
; Loza-Cornejo et al., 2003
; Ayala-Cordero et al., 2006
), the plants were under light stress. In other words, the light level used was much lower than their light compensation point (Nobel and Hartsock, 1986
; Nobel, 1988
). However, CAM metabolism in itself is not disadvantageous for growth in low-light environments, as evidenced by the growth of terrestrial CAM species in the understory of tropical forests (Skillman et al., 1999
). Aechmea magdalenae is a neotropical shade-tolerant CAM plant with high photosynthetic capacity and with relatively high values of nocturnal acidification (Skillman et al., 2005
).
Because the species in this study germinated on different days, they were exposed to different sequences of daily light conditions (Fig. 1) and consequently the organic acids accumulated differently over time under both light treatments (Fig. 3). The degree to which CAM contributes to total carbon gain is highly variable and depends on environmental conditions such as temperature and quantity of light (Winter and Smith, 1996
). In adult plants of S. queretaroensis, the assimilation of CO2 increased linearly with the increase in photosynthetically active light, with maximum CO2 fixation at 20 mol·m–2·d–1 (Nobel, 2002
). In addition, in CAM plants the quantity of organic acids that accumulates during the night is determined by the light received during the previous day (Nobel and Hartsock, 1983
; Adams et al., 1987
; Adams and Demmig-Adams, 1996
; Lüttge, 2004
). This pattern has also been observed for rainforest shade-tolerant CAM species (Winter et al., 1986
; Skillman et al., 1999
). On the one hand, our results support this tendency, as in the case of F. recurvus and E. chiotilla, which accumulate less organic acids when they receive less light (Fig. 3). However, S. stellatus (Fig. 3) increased in acidity in spite of the decrease in light, while accumulation of organic acids for N. tetetzo and P. weberi was independent of the quantity of light received (Fig. 3). Our results agree with those of Winter and Smith (1996)
and show that species vary greatly in the pattern of acid accumulation and that they respond to the environment in different ways. This is possible because of the great plasticity that the CAM metabolic pathway allows (Cushman, 2001
; Dodd et al., 2002
). Our data also suggest that the level of accumulated acids increases with seedling age (Fig. 3).
Some species can change from the CAM photosynthetic pathway to C3 if water is available (Lüttge, 1996
; Dodd et al., 2002
). However, the adult cacti in this study did not have this physiological plasticity in spite of being collected during the rainy season when soil water was abundant. Acid accumulation in these species was characteristic of CAM (Nobel, 1988
), and we also observed significant interspecific differences in the quantity of organic acids accumulated even when all were growing under the same environmental conditions in the field. In light of this and in agreement with Cushman (2001)
, we think that this variation is the result of genotypic factors intrinsic to the species.
All the species in this study accumulated acidity in the morning. Such accumulation makes high quantities of internal CO2 available at midday for the decarboxylation of organic acids during phase III of CAM (Barker and Adams, 1997
; De Mattos et al., 1999
; Lüttge, 2002
). This leads us to propose that the high photosynthetic efficiency (F/Fm') in all the species—both the seedlings under seminatural conditions and the adult plants in the field—and the seedling's low values for the dissipation of thermal energy (NPQ) (data not presented) indicate that these plants use a great proportion of the light that they absorb for photosynthesis. These high quantities of internally generated CO2 give them the advantage of being able to tolerate levels of PPFD close to 2000 µmol·m–2·s–1, thus reducing the risk of photoinhibition (Adams et al., 1987
; Barker and Adams, 1997
; Barker et al., 1998
). In Opuntia macrorhiza, a CAM cactus species, values of F/Fm' = 0.02 were recorded when these plants were exposed to high light levels in the field (Barker and Adams, 1997
), while the values of (F/Fm') determined for all the species in the current study were never lower than 0.4.
For seedlings, we determined the cardinal points from the light response curves. The light level at which PSII becomes saturated (PPFDsat) is related to acclimatization to the light environment in which the seedlings grew (Nobel, 1988
; Einhorn et al., 2004
), and this is supported by our results. That is, PSII is saturated at lower light levels in the seedlings that grew under LL conditions, with the exception of E. chiotilla (Fig. 5). For ETRmax, we found differences between species that are probably related to their capacity to store malic acid, which, as proposed by De Mattos and Lüttge (2001)
, is determined by the size of the vacuole. Malic acid is also required as a source of CO2 to maintain a high level of electron transport (Barker and Adams, 1997
). It is worth mentioning that the photosynthetic efficiency of the young seedlings (7 d old) is comparable to that of the adult plants and that the saturating light levels for ETR (PPFDsat ranges from 231 to 631 µmol·m–2·s–1) of the seedlings are close to the saturating light levels (500 µmol·m–2·s–1) for nocturnal CO2 uptake and maximal nocturnal acid accumulation of agaves and cacti (Nobel 1988
). The response of photosynthetic efficiency and ETR to increasing PPDF could indicate that there was no immaturity in the photosynthetic apparatus of the seedlings, as Loza-Cornejo et al. (2003)
inferred.
Our results, however, suggest that the photosynthetic response is species specific because P. weberi and E. chiotilla are the only species with decreased photosynthetic efficiency under HL; photosynthetic efficiency and the cardinal points (ETRmax and PPFDsat) actually increased in N. tetetzo under more intense solar radiation. In contrast, the photosynthetic efficiency of F. recurvus and S. stellatus was the same under the two light treatments, though there were differences in their cardinal points (Fig. 5). This leads us to propose that by adjusting their photochemical capacity these plants can acclimatize to light environments as variable as those under which they grew, as suggested by Adams and Demmig-Adams (1996)
. The photosynthetic parameters determined in the RLCs offer a clearer view of the response of species to the light environment, indicating that these responses are not only related to momentary light conditions, but also to the level of physiological plasticity of the species (Rascher et al., 2000
). Cactus seedlings require shade or a nurse plant to establish (Franco and Nobel, 1989
; Valiente-Banuet et al., 1991
), but our results suggest that these seedlings can adapt and survive high light levels when water is available because they can use the CAM pathway and thereby photosynthesize as efficiently as an adult plant.
Conclusions
Our results indicate that all columnar cacti species in this study underwent CAM immediately after germination, refuting earlier assertions to the contrary. We can state that all species can be classified as CAM plants, both in the seedling and adult stage. The quantity of stored organic acids varies widely between species and depends on the quantity of light received and the photosynthetic efficiency for acid remobilization. The seedlings had a great ability to acclimatize to the light conditions in which they had developed; they could use and remobilize organic acids within a 24-h cycle as a result of their photosynthetic efficiency, ETRmax, and the level of light required to saturate PSII (PPFDsat). Therefore, the presence of CAM in cactus seedlings confers the capacity to use photosynthetically active light to fix CO2 and to increase water-use efficiency, both of which favor their establishment in deserts.
FOOTNOTES
1 The authors thank J. García-Cruz and J. Aké for their help in the field and J. L. Andrade for valuable discussions. Anonymous reviewers and B. E. Hazen helped improve the document. This research was fully supported by a CONACYT graduate scholarship (no. 159293) to O.H.-G. and a CONACYT grant (no. 36642-V) to O.B. 
2 Author for correspondence (oscar.briones{at}inecol.edu.mx
; phone: 52 (228) 842-1800, ext. 3008; fax: 52 (228) 818-7809
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= low light; 
= high light). (A, B) Neobuxbaumia tetetzo; (C, D) Pachycereus weberi; (E, F) Ferocactus recurvus; (G, H) Steneocereus stellatus; (I, J) Escontria chiotilla; and (K) Myrtillocactus geometrizans. The periodicity of titratable acidity followed a statistically significant sinusoidal function in all species and light treatments (N = 3). Degrees of freedom and F and P values are in 
= low light, LL; 
= high light, HL). Total light received by the seedlings 1 d before titratable acidity was determined (
