survival for Dudleya saxosa, the rock live-forever, growing in small soil volumes

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1 Functional Ecology 2007 Carbon dioxide uptake, water relations and drought Blackwell Publishing Ltd survival for Dudleya saxosa, the rock live-forever, growing in small soil volumes P. S. NOBEL and B. R. ZUTTA Department of Ecology and Evolutionary Biology, University of California, Los Angeles, 621 Charles E. Young Drive South, Los Angeles, CA , USA Summary 1. Although many plants grow in rock crevices and other regions of small soil volume, including over epiphytic and hemi-epiphytic species, analyses of the actual soil volume occupied, the water availability in that soil, the water-storage capacity in the shoots and underground organs, and the photosynthetic pathway utilized have rarely been combined. 2. Dudleya saxosa (M.F. Jones) Britton and Rose (Crassulaceae), growing in the Sonoran Desert, has very shallow roots that occupied soil volumes averaging only m 3 per medium-sized plant. This volume of soil can hold about the same amount of water (10 g) as can be stored in the leaves, corm and roots combined (11 g), but at a sufficiently high water potential for transfer to the plant for less than 1 week after a substantial rainfall. 3. About 80% of the net carbon dioxide uptake by D. saxosa over a 24-h period occurred during the daytime (C 3 ) under wet conditions, the daily total decreasing by 34% and the pattern shifting to nocturnal net CO 2 uptake (CAM) after 46 days drought. Seventy-seven days drought eliminated its daily net CO 2 uptake. 4. Stomatal frequency was only 67 mm 2 on the adaxial (upper) surface and twofold lower on the abaxial surface. The cuticle was thick, 34 µm for the adaxial surface. Leaves had 24 mesophyll cell layers, leading to a high mesophyll cell surface area per unit leaf area of The three leaf anatomical features plus utilization of CAM increased net CO 2 uptake per unit of water transpired, and helped D. saxosa thrive in a small soil volume, with the underground corm being a major supplier of water to the succulent leaves during 2.5 months of drought. The maximum water-holding capacity of the soil explored by the roots closely matched the maximum water-holding capacity of the plant, reflecting the conservative strategy used by D. saxosa in a stressful semi-arid environment. Key-words: corm, Crassulacean acid metabolism, cuticle, stomata, water potential Functional Ecology (2007) doi: /j x Ecological Society Introduction Water uptake is crucial for any plant species, as can be especially apparent for those native to arid and semiarid environments (Nobel 1988; Gibson 1996; Fitter & Hay 2002). Moreover, the presence of exposed rocks and rock outcroppings in deserts worldwide can limit the soil volume, and hence water available to the roots, which can exacerbate the prevailing water stress (Wentworth 1981; Nobel, Miller & Graham 1992; Martre et al. 2002; Schmiedel & Jurgens 2004). In Author to whom correspondence should be addressed. psnobel@biology.ucla.edu addition to geophytes and lithophytes, many arctic and high-elevation plants also have root systems that occupy small soil volumes (Jackson et al. 1996; Kessler, Parris & Kessler 2001; Rundel, Gibson & Sharifi 2005). An analogous situation occurs for the epiphytic and hemi-epiphytic species that are common in the Araceae, Bromeliaceae, Gesneriaceae, Orchidaceae, Piperaceae and Pteridophyta (Winter & Smith 1996; Lüttge 1997; Küper et al. 2004), the roots of which often occupy very limited regions such as tree crotches. Many such species employ Crassulacean acid metabolism (CAM), which increases net CO 2 uptake per unit water lost by three- to eightfold compared with that for sympatric C 3 species (Nobel 1988, 2005; Lüttge 2004). 698

2 699 Dudleya drought survival in small soil volume Dudleya saxosa (M.F. Jones) Britton and Rose (Crassulaceae), one of 45 species of Dudleya occurring in arid and semi-arid regions of the south-western USA and north-western Mexico (Hickman 1993), is a small, succulent perennial herb that favours exposed rocky regions, where it occupies cracks and crevices with limited soil volume (Levin & Mulroy 1985; Marchant et al. 1998). Its short stature is characteristic of plants growing on desert pavement, such as quartz fields in South Africa (Schmiedel & Jurgens 2004). The roots of D. saxosa at three sites in the north-western Sonoran Desert have a mean depth of only 46 mm, and essentially no roots occur below 120 mm (Nobel & Zutta 2007). But the consequences of shallow roots that presumably occupy a small soil volume have not been investigated for any Dudleya species. In that regard, heavily glaucous plants of Dudleya brittonii tend to occupy rock crevices, whereas non-glaucous ones occupy microhabitats with greater soil volume, which has been attributed to the greater longevity of glaucous leaves and thus their availability for water storage when rains eventually interrupt the dry season (Mulroy 1979). Dudleya saxosa occurs predominantly on north-facing slopes between 240 and 2200 m (Hickman 1993). The preference for cooler, north-facing slopes is apparently related to the relatively poor tolerance of its leaves to high temperatures, which is also the reason why it occurs in deserts in quartz fields, with their cooler surface temperatures (Nobel & Zutta 2007). Daytime and night-time rates of net CO 2 uptake were measured for D. saxosa under natural conditions in the field, and under well watered as well as drought conditions in the laboratory, to determine whether it uses the C 3 or the CAM pathway. The results were interpreted in terms of the plant s stomatal frequency, cuticle thickness and mesophyll surface area per unit leaf area (A mes /A). In particular, the stomatal frequency was predicted to be low and the cuticle to be thick to help prevent water loss, and A mes /A was predicted to be high, leading to a high liquid-phase conductance that favours net CO 2 uptake (Gibson 1996; Nobel 1988, 2005). The limited soil volume occupied by the roots of D. saxosa was hypothesized to hold water at a high enough water potential for only brief water uptake by a plant, so D. saxosa should be photosynthetically active for only short periods after substantial rainfall. In this regard, water storage in its succulent leaves, as well as in its relatively large underground corm, were also evaluated. Such measurements and analysis should help our understanding of how this and many other species cope with a limited soil volume. Materials and methods site characteristics Dudleya saxosa, commonly known as the rock liveforever, was studied at Agave Hill in the 6700-ha University of California Natural Reserve System, Philip L. Boyd Deep Canyon Desert Research Center in the north-western Sonoran Desert. Agave Hill (33 38 N latitude, W longitude, mean elevation 825 m) refers to a series of small hills with outcroppings of disintegrating granite and occasional dense surface layers of white, angular quartz stones. Dudleya saxosa can have a frequency of 3 1 plants m 2 where quartz covers >90% of the soil surface, decreasing to 0 3 plants m 2 for 60 90% coverage, and to essentially zero in the immediately surrounding region of similar area with <60% coverage of the ground surface by quartz stones (Nobel & Zutta 2007). Rainfall at Agave Hill averages 220 mm annually, occurring mainly during the late summer and winter/early spring (Nobel 1988; Nobel & Bobich 2002). Field measurements were made during cool to mild, mostly clear days of 3 5 March 2006 (maximum/minimum daily air temperatures averaged 19/6 C) under conditions of relatively dry soil (rainfall at Agave Hill totalled only 34 mm from 1 October March 2006); additional field measurements of soil volume for the root system of D. saxosa were performed on 29 September plant morphology and anatomy Leaves of D. saxosa radiate as a basal rosette from an inconspicuous stem. Its projected leaf area is equal to length width at mid-length, and its total leaf surface area is equal to projected area (concavity of the upper surface + convexity of the lower surface), both summed over all leaves (Nobel & Zutta 2007). The leaves were examined at 100 with a CH-2 phasecontrast light microscope (Olympus, Lake Success, NY, USA) to determine stomatal frequency (based on nail polish impressions), cuticular thickness (at mid-leaf), and cellular dimensions. Transverse and longitudinal sections prepared with double-edged razor blades were used to determine the ratio of mesophyll cell surface area to the corresponding leaf surface area (A mes /A; Nobel 2005), assuming that the palisade cells were cylindrical with flattened ends and that the spongy mesophyll cells were cuboidal; approximately 150 cells were measured for each section. Rectangular parallelepipeds of tissue 6 mm along the leaf axis 4 mm wide 1 5 mm thick were removed near mid-leaf using a razor blade. This was done in the field to calculate tissue density based on the volume and fresh weight of the samples, and in the laboratory to determine leaf water potential. After lightly blotting the surface to remove sap from cut cells, a sliced leaf sample was placed in the stainless-steel chamber of an SC10C TruPsi thermocouple psychrometer (Decagon Devices, Pullman, WA, USA) and equilibrated for 8 h before determining the leaf water potential. Nine plants of D. saxosa were removed in field soil on 3 March 2006 and placed in a glasshouse with daily maximum/minimum air temperatures of 30/20 C, average daily maximum/minimum relative humidities

3 700 P. S. Nobel & B. R. Zutta of 50/30%, and weekly watering with 0 05-strength Hoagland s solution (Epstein & Bloom 2005), which maintained the soil water potential in the root zone above 0 4 MPa (determined with PCT-55 thermocouple psychrometers; Wescor, Logan, UT, USA). Drought was induced by ceasing watering after 8 weeks and was defined as commencing when the soil water potential in the root zone was 0 5 MPa. Under well watered conditions and at 11 weeks drought, plants were excavated and their leaves, roots and corm removed and weighed; the material was then dried for 48 h at 80 C in a 45EM mechanical convection oven (Precision Scientific, Winchester, VA, USA) to determine organ dry weight. Dry weight was also calculated for D. saxosa in the field, using regressions of leaf dry weight vs length. Dudleya saxosa was also excavated on 29 September In both cases the soil was carefully collected within 5 mm of its roots (a reasonable distance for plant water uptake based on the observed inter-root spacing; Caldwell 1976; Taylor & Klepper 1978). The soil was dried at 80 C for 72 h in the mechanical convection oven, weighed, and the volume determined based on the known density of dry soil from Agave Hill (1520 kg m 3 ; Nobel & Geller 1987). tissue acidity and net co 2 exchange Tissue acidity was determined in the field for leaf segments 15 mm long (average fresh mass 0 27 g) centred on mid-leaf. After adding 20 ml distilled water and 0 5 g washed quartz sand, samples were ground and then titrated to ph 7 4 using 5 mm NaOH dispensed in 0 1 ml increments (Nobel, Loik & Meyer 1991); ph was determined with a M140 ph meter (Corning Life Sciences, Corning, NY, USA). Net CO 2 exchange for D. saxosa was measured with a LI-6200 portable infrared photosynthesis system (Li-Cor, Lincoln, NE, USA). The exposed edges of its 250-ml cuvette were covered with a foam-rubber gasket and then pressed against a transparent rectangular acrylic frame (110 mm long 34 mm wide 45 mm tall) placed around a plant; the soil surface was sealed from the cuvette with dental impression material (vinyl polysiloxane). Data are based on projected leaf area. Data are means ± SE (n = number of measurements on different plants) unless indicated otherwise. Significant differences between means were evaluated using Student s t-test or a one-way anova followed by a Tukey test. Results morphology and anatomy Leaf length for medium-sized plants of D. saxosa at Agave Hill averaged 34 1 ± 2 5 mm, and leaf width averaged 7 1 ± 0 4 mm (n = 35 leaves on five plants). Avoiding the two youngest, rather stubby leaves Table 1. Leaf morphology, leaf dry weight and soil rooting volume for medium-sized plants of Dudleya saxosa at Agave Hill Parameter Data Leaves (per plant) Number 8 6 ± 1 2 Total projected area 2130 ± 210 mm 2 Total surface area 6790 ± 530 mm 2 Dry weight 0 49 g Soil volume (per plant) 42 8 ± m 3 Leaf dry weight was calculated from regressions. Data are means ± SE (n = 5 plants, except 10 plants for number of leaves per plant). Table 2. Leaf anatomy for Dudleya saxosa at Agave Hill Parameter Data Stomatal frequency Adaxial (upper) surface 67 ± 3 mm 2 Abaxial (lower) surface 31 ± 3 mm 2 Cuticle thickness Unshaded plants Adaxial surface 34 ± 2 µm Abaxial surface 27 ± 1 µm Shaded plants Adaxial surface 28 ± 1 µm Abaxial surface 26 ± 2 µm Palisade mesophyll layers Adaxial surface 7.0 ± 0.4 Abaxial surface 5.7 ± 0.3 Spongy mesophyll layers 10.8 ± 0.4 A mes /A 142 ± 5 Data are from near mid-leaf on unshaded plants (except where indicated) and are means ± SE (triplicate readings on n = 6 leaves for stomatal and cuticular properties, n = 8 leaves for mesophyll properties). (<5 mm long), the concavity of the upper (adaxial) surface averaged 1 20 ± 0 01, and the convexity of the lower (adaxial) surface averaged 1 98 ± 0 02 (n = 35 leaves on five plants). Based on such properties of individual leaves, the total projected leaf area and total leaf surface area were calculated for each plant (Table 1). Based on regressions of leaf dry weight vs leaf length, mean leaf length and average number of leaves per plant, the total leaf dry weight per plant was estimated to be 0 49 g (Table 1). Five plants of similar size and leaf number were excavated on 29 September 2006, and the soil was collected from each root system and dried. Based on the bulk density for dry soil, the soil volume per plant determined for these roots was m 3 (Table 1). Smaller and larger plants were excavated on 3 5 March 2006; plants with 6 3 ± 1 8 living leaves (n = 3) occupied a soil volume of 30 ± m 3, and plants with 15 3 ± 2 8 living leaves (n = 4) occupied a soil volume of 72 ± m 3 (P < 0 05). Stomatal frequency was more than twofold higher on the adaxial surface, 67 mm 2, compared with the abaxial surface (P < 0 01; Table 2). The length of the stomatal pore was 23 ± 2 µm (triplicate measurements

4 701 Dudleya drought survival in small soil volume Table 3. Organ fresh and dry weights for medium-sized plants of Dudleya saxosa under wet conditions and at 77 days drought in the laboratory Weight (g plant 1 ) Plant part Fresh Dry Leaves Wet conditions 6.00 ± ± days drought 2.14 ± ± 0.04 Roots Wet conditions 2.50 ± ± days drought 0.87 ± ± 0.04 Corm Wet conditions 8.00 ± ± days drought 2.59 ± ± 0.10 Data are means ± SE (n = 4 plants under wet conditions and 5 other similarly sized plants at 77 days drought). on n = 6 leaves). For exposed (unshaded) plants, the cuticle was 26% thicker for the adaxial surface, 34 µm, compared with the abaxial surface (P < 0 05; Table 2). For plants shaded by Agave deserti (Engelm.) Gentry, which is the dominant species at Agave Hill (Nobel 1988; Drennan & Nobel 1997), the adaxial cuticle was about 18% thinner than for the unshaded case (P < 0 05) and was similar in thickness to that for the abaxial surface (Table 2). The isolateral succulent leaves of D. saxosa were thick, averaging 2 8 ± 0 1 mm (n = 10 leaves) near the leaf axis from the leaf base to three-quarters of the way to the tip, after which the leaves became thinner. Near mid-leaf, the leaves had a total of about 13 layers of palisade mesophyll cells on the two sides with 11 layers of spongy mesophyll cells in the centre (Table 2). Because of the many cell layers, the leaves had a large mesophyll surface area per unit leaf area (A mes /A) that averaged 142 at mid-leaf (Table 2), 142 ± 4 at 3 mm from the leaf base and three-quarters of the way to the leaf tip, and 93 ± 8 at 3 mm from the leaf tip (n = 6 leaves). Based on the volume and mass of tissue parallelepipeds removed near mid-leaf in the field, the leaf density was 960 ± 10 kg m 3 (n = 5 leaves). This high density is consistent with the small intercellular air spaces observed microscopically, which were estimated to occupy only 4 5% of the tissue volume. The water potential for such leaf sections in the laboratory averaged 0 22 ± 0 04 MPa under well watered conditions; 0 54 ± 0 06 MPa after 46 days drought; and 0 99 ± 0 07 MPa after 77 days drought (n = 5 plants; P < 0 05). Leaf dry weight per plant was similar for the four plants examined in the laboratory under wet conditions, the five plants examined at 77 days drought (Table 3), and the estimate for field plants (Table 1). During the 77 days drought, the fresh weight of leaves decreased by 3 86 g, presumably primarily representing water loss. The underground organs also decreased in fresh weight during the drought, by 1 63 g for the roots and by 5 41 g for the corm (Table 3). Fig. 1. Fluctuations in tissue acidity (a) and net CO 2 uptake rate (b) for leaves of Dudleya saxosa over a 24-h period in the field in spring (3 4 March 2006). Acidity data for samples from mid-leaf are means ± SE (n = 4 plants). CO 2 -exchange data are averages of duplicate readings on a single plant with six leaves exposed to the cuvette. All data are on a projected leaf-area basis. Open symbols, daytime (between and h); closed symbols and dark bar, night-time (between and h); intermediate symbol, and h. tissue acidity and net co 2 exchange Tissue acidity for leaves of D. saxosa near the spring equinox in the field tended to increase during the night and decrease during the daytime (Fig. 1a). Based on projected leaf area (length of excised segment its mean width), the nocturnal acidity increase was 280 mmol m 2. Concomitantly, net CO 2 exchange was generally negative during the daytime and positive at night, reaching a maximum rate of 4 3 µmol m 2 s 1 at a solar time of h for the plant considered (Fig. 1b). Defining daytime as the period with measurable shortwave irradiation, h (Nobel & Zutta 2007), the daytime net CO 2 exchange was 6 mmol m 2 and the night-time net CO 2 exchange was 95 mmol m 2. Net CO 2 exchange over 24-h periods was also determined for D. saxosa in the laboratory under well watered conditions (Fig. 2a) and after 46 days drought (Fig. 2b). Under wet conditions, the maximal net CO 2 uptake occurred at h, when the rate was 6 1 µmol m 2 s 1 ; net CO 2 exchange was positive at the

5 702 P. S. Nobel & B. R. Zutta Fig. 3. Integrals of net CO 2 uptake for Dudleya saxosa over 12-h periods of daytime ( h; ) or night-time ( ) under wet conditions and during drought. Data are means ± SE (n = 4 plants, as for Fig. 2). Fig. 2. Net CO 2 -uptake rate for Dudleya saxosa over 24-h periods in the laboratory under well watered conditions (a) or after 46 days drought, defined as beginning 5 days after cessation of watering (b). Data are means ± SE (n = 4 plants with six to eight leaves exposed to the cuvette). beginning of the night, but was negative near and just after midnight (Fig. 2a). After 46 days drought, net CO 2 exchange was negative throughout most of the daytime and positive throughout the entire night, reaching a maximum rate of 4 4 µmol m 2 s 1 just after midnight (Fig. 2b). Net CO 2 uptake by D. saxosa during daytime ( h) under wet conditions in the laboratory was 199 mmol m 2 (Fig. 3). Daytime uptake was halved by 25 days drought, and was abolished by 44 days drought. Net CO 2 uptake by D. saxosa at night was 52 mmol m 2 under wet conditions, increased more than threefold at 46 days drought, and then decreased. By 77 days drought, net CO 2 uptake at night was only 10 mmol m 2, and was similar in absolute magnitude to the daytime net CO 2 loss (Fig. 3). Discussion Dudleya saxosa is a facultative CAM species. Specifically, net CO 2 uptake over a 24-h period occurred 80% during the daytime under wet conditions, but mainly at night at 46 days drought, and only at night at 77 days drought. Other Dudleya species also show flexibility in using the C 3 vs the CAM pathway (Troughton et al. 1977); for example, Dudleya farinosa growing along the California coast utilizes the daytime C 3 pathway during the winter rainy season, but switches to nocturnal CO 2 uptake via CAM during the summer drought (Bartholomew 1973). Its maximal net CO 2 uptake rates are 1 9 µmol m 2 s 1 in C 3 mode and 0 9 µmol m 2 s 1 in CAM mode, which average 25% of the maximal rates for D. saxosa, as does its night-time net CO 2 uptake under relatively dry conditions near the spring equinox. Because two protons are involved per CO 2 incorporated into a carbohydrate (Nobel 1988), the nocturnal acidity increase is predicted to be 190 mmol m 2 for D. saxosa, 30% less than was observed, which can be attributed to some internal recycling of CO 2 (Ting 1985). For Dudleya blochmanae, which also grows along the California coast, leaf water potential decreases from 0 2 MPa during the winter rainy season to 0 4 MPa by the dry late spring (Teeri 1984), similar to the decrease in leaf water potential observed for D. saxosa during 46 days drought in the laboratory. For these changes in leaf water potential, the nocturnal increase in acidity for D. blochmanae approximately tripled (Teeri 1984), indicating increased CAM activity, which is consistent with the tripling of nocturnal net CO 2 uptake by D. saxosa observed here during 46 days drought. The stomatal frequencies for D. saxosa, 67 mm 2 for the adaxial leaf surface and 31 mm 2 for the abaxial one, are low for plants in general and for desert plants in particular (Nobel 1988, 2005; Gibson 1996). Moreover, a lower frequency on the lower surface is contrary to the case for most dicots, including desert succulents. The leaf cuticle of D. saxosa was thick, µm, similar to that for the sympatric A. deserti, µm (Nobel 1976). The thicker cuticle observed for D. saxosa exposed to full sunlight vs under the nurse plant A. deserti is consistent with light effects on cuticular thickness for other species (Gibson 1996; Baltzer & Thomas 2005). A mes /A for D. saxosa averaged 142, indicating a large mesophyll surface per unit leaf area.

6 703 Dudleya drought survival in small soil volume For instance, A mes /A for most C 3 species ranges from 10 to 40 on a projected leaf-area basis (Björkman 1981; Nobel 2005), although it is higher for desert succulents such as agaves and cacti, averaging about 100 (Nobel 1988). In any case, the 24 layers of palisade and spongy mesophyll cells for D. saxosa provide a large area for diffusion of CO 2 into the cells, albeit with a relatively small intercellular air space of only 4 5% of leaf volume, the latter hindering internal CO 2 diffusion compared with typical air spaces of about 30% of leaf volume (Nobel 2005). Soil at Agave Hill borders between the textural classes sandy loam and loamy sand, and can hold much water at a relatively high water potential (Nobel 1976, 1988). Specifically, it holds 24% water by volume between 0 01 MPa (field capacity) and 0 99 MPa (Nobel & Geller 1987), the leaf water potential for D. saxosa at 77 days drought, which essentially eliminated its daily net CO 2 uptake. Soil at Agave Hill at a depth of 50 mm, which is in the centre of its root zone, decreases over this water potential range in 4 6 days after a substantial rainfall of 20 mm (Young & Nobel 1986; Nobel 1988), similar to the rate of soil drying observed in the glasshouse. For the mean soil volume occupied by the roots of D. saxosa ( m 3 ), this decrease in soil water content corresponds to 10 g water. For comparison, leaves of an average D. saxosa at Agave Hill can lose 3 9 g water per plant from wet conditions to the leaf water content at 77 days drought. During the 2.5-month drought, the roots lost about 1 6 g FW and the corm lost even more, 5 4 g, for a total decrease in fresh weight that was nearly twice that of the leaves. The relatively slow decline in leaf water potential and in leaf water content for D. saxosa during drought in part reflects its low stomatal frequency and its thick cuticle, not a prolonged period of water uptake from the soil. In particular, the leaf and soil water potentials indicate that water replenishment from the soil is transitory, occurring over <1 week following a substantial rainfall. Moreover, the relatively small volume of soil within the root system can hold about the same amount of water (10 g) as can be stored by the leaves, roots and corm (11 g). Thus the maximum amount of water that can be stored in the soil volume explored by the roots of D. saxosa closely matches the maximum amount of water that can be stored in the plant. Moreover, roots of larger plants occupied a larger soil volume, underscoring the importance of limited available soil volume for plant size. The ecophysiological and morphological adaptations of D. saxosa reflect a generally conservative survival strategy in a semi-arid habitat. Specifically, the extent of the root system allows D. saxosa to persist until the next pulse of rain, which acts as a control in a chronically unproductive environment (Grime 2001; Pierce, Vianelli & Cerabolini 2005). This strategy favours efficient resource use, as opposed to continual resource foraging, even under stress (Tilman 1988). Also, the physiological flexibility of CAM in D. saxosa allows it to resist drought and recover rapidly once resources become available. This plasticity in carbon gain has allowed CAM species to succeed in extremely variable environments, inhabiting wetter habitats as well as those subjected to prolonged drought (Pierce, Winter & Griffiths 2002; Lüttge 2004). Evaluation of the consequences of water availability in the small soil volume occupied by the root stems of epiphytes and various other species suggests the suite of morphological, anatomical and physiological adaptations that are necessary. The roots must explore a sufficient soil volume with a high enough water potential to lead to the requisite water uptake and delivery to the leaves. Once the soil water potential decreases below that in the plant, water will flow out of the roots, a process hindered by their rectification-like behaviour due to decreases in root hydraulic conductivity, the development of root soil air gaps, and especially the rapidly decreasing hydraulic conductivity of soil as its water content decreases (Nobel & Cui 1992; Nobel 2005). The leaves must minimize water loss while still gaining CO 2, with the succulence of leaves, stems and underground organs obviously being advantageous. Dudleya saxosa does this remarkably well, as it gains CO 2 daily during 2 5 months drought, relying on water stored in its leaves, roots and, especially, its corm, while limiting water loss by having low stomatal frequencies and a thick cuticle, and utilizing CAM. In any case, other plants living in rock crevices and epiphytes living in tree crotches, such as bromeliads, orchids and ferns, also predominantly use the waterconserving CAM (Winter & Smith 1996; Lüttge 1997) and presumably have a similarly small root system that matches water availability in the soil to water storage in the plant. Acknowledgements The authors thank the following undergraduate students for contributing to the results presented: Edit Avodian, Mabel Chin, Jorge Heredia, Lucas Johnson, Camille Nakamura and Amanda Wright. We also acknowledge use of facilities and a protected research area of the University of California Natural Reserve System, Philip L. Boyd Deep Canyon Desert Research Center, and thank Mr Mark Fisher for providing climatic data and Dr Allan Muth, director of the Center. Financial support was provided in part by the UCLA Council on Research. References Baltzer, J.L. & Thomas, S.C. (2005) Leaf optical responses to light and soil nutrient availability in temperate deciduous trees. American Journal of Botany 92, Bartholomew, B. (1973) Drought response in the gas exchange of Dudleya farinosa (Crassulaceae) grown under natural conditions. Photosynthetica 7, Björkman, O. (1981) Responses to different quantum flux

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