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Although crown wetting events can increase plant water status, leaf wetting is thought to negatively affect plant carbon balance by depressing photosynthesis and growth. We investigated the influence of crown fog interception on the water and carbon relations of juvenile and mature Sequoia sempervirens trees. Field observations of mature trees indicated that fog interception increased leaf water potential above that of leaves sheltered from fog. Furthermore, observed increases in leaf water potential exceeded the maximum water potential predicted if soil water was the only available water source. Because field observations were limited to two mature trees, we conducted a greenhouse experiment to investigate how fog interception influences plant water status and photosynthesis. Pre-dawn and midday branchlet water potential, leaf gas exchange and chlorophyll fluorescence were measured on S. sempervirens saplings exposed to increasing soil water deficit, with and without overnight canopy fog interception. Sapling fog interception increased leaf water potential and photosynthesis above the control and soil water deficit treatments despite similar dark-acclimated leaf chlorophyll fluorescence. The field observations and greenhouse experiment show that fog interception represents an overlooked flux into the soil–plant–atmosphere continuum that temporarily, but significantly, decouples leaf-level water and carbon relations from soil water availability.
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The degree to which whole plant water status approaches equilibrium with ΨSoil is influenced by several different mechanisms (Donovan et al. 2001, 2003). Night-time transpiration (EN) is one physiologically important mechanism that has previously been shown to prevent the overnight equilibration between ΨL and ΨSoil for many distantly related tree species (Sellin 1999; Donovan et al. 2001; Dawson et al. 2007). Heterogeneity of soil moisture within the rhizosphere is another factor that can impede night-time equilibration through hydraulic redistribution between rhizosphere compartments with different ΨSoil (Brooks et al. 2006; Warren et al. 2007). Apoplastic solutes also contribute to pre-dawn disequilibrium between leaf and soil through extremely low osmotic potentials for a given turgor pressure (Donovan et al. 2001, 2003). Additionally, for tall trees like S. sempervirens, ΨL is expected to differ from ΨSoil even during periods of no EN, due to the gravitational component ρGh∼ −0.01 MPa m−1. Together, these mechanisms are expected to constrain plant water content and maximum ΨL to an upper limit set by ΨSoil and soil-to-root hydraulic conductance (kS-Rt) as described by the following unidirectional SPAC mass balance model:
where ΔΨSoil-Rt is the water potential difference from soil to root; CRt, CSt and CL are root, stem-wood and leaf-specific capacitances defined as the change in tissue water content per unit change in water potential; ΨRt, ΨSt and ΨL are root, stem-wood and leaf water potential, respectively; and EN is night-time transpiration (Dawson et al. 2007).
where kAtm-L is the efficiency of foliar uptake and ΔΨAtm-L is the water potential gradient between the intercepted crown water and the leaf. A bidirectional (i.e. leaf to root) SPAC mass balance framework suggests that ΨL is more directly related to rates of foliar uptake (i.e. kAtm-LΔΨAtm-L) when plant crowns are wet.
Although crown interception can positively influence plant water relations through direct foliar uptake, leaf wetting events are often viewed as having a negative effect on photosynthesis and, eventually, growth. This is because atmospheric water that condenses on leaf surfaces physically reduces the transport of CO2 to the sites of carboxylation and may result in significant degradation of the photosynthetic enzyme ribulose 1·5-bisphosphate carboxylase/oxygenase (Rubisco), depending upon the duration of canopy interception, the time of day and the overall wettability of the leaf surface (Brewer & Smith 1994; Ishibashi & Terashima 1995; Hanba et al. 2004). However, previous work has focused on the responses of plants grown in wet soils and did not evaluate the potential benefits of foliar uptake on leaf level gas exchange for plants exposed to soil water deficit. If crown interception and subsequent foliar uptake increases leaf water content and ΨL to values greater than those obtained through root water uptake, the temporary cost of leaf wetting on CO2 diffusion and Rubisco may be outweighed by greater leaf level gas exchange for a given level of soil water deficit or ΨSoil.
We chose the California Coast Redwood (Sequoia sempervirens D. Don) for testing how well ΨL and leaf level gas exchange are coupled to variation in soil water availability when exposed to crown fog interception. The current distribution of S. sempervirens is largely constrained to areas characterized by the regular occurrence of summertime coastal fog (Marotz & Lahey 1975; Dawson 1998). Fog is considered to play an important role in the ecology and hydrology of S. sempervirens forests because fog frequency is greatest in the summer when drying soils coincide with otherwise low humidity conditions (Means 1927; Byers 1953; Oberlander 1956; Dawson 1998; Burgess & Dawson 2004; Ewing et al. 2009). The presence of fog during this annual summertime drought has previously been shown to: (1) reduce transpiration by decreasing the vapour pressure deficit (VPD) between leaves and the atmosphere (Burgess & Dawson 2004); (2) increase soil water content through fog drip from canopy to soil, also known as occult precipitation (Azevedo & Morgan 1974; Dawson 1998; Ewing et al. 2009); and (3) contribute to whole plant hydration through direct uptake of fog water deposited on leaf surfaces (Burgess & Dawson 2004). However, the overall effect of fog interception on S. sempervirens photosynthesis has not been measured, nor has the influence of fog interception on water potential gradients been explored.
Because fog water deposited on S. sempervirens canopies is available for water use through direct foliar uptake (Burgess & Dawson 2004), we predicted that overnight canopy fog interception would: (1) increase crown water status above that maintained by night-time rehydration via root water uptake, resulting in a decoupling between ΨL and ΨSoil, and (2) minimize the negative effect of increasing soil water deficit on leaf level gas exchange.
MATERIALS AND METHODS
Field observations were made at The Grove of the Old Trees, an 11 ha ridge-top parcel (300 m altitude) of old growth redwood forest in Sonoma County, California (38°24′N, 122°59′W) approximately 8 km from the Pacific Ocean. Within canopy variation in branchlet water potential was measured on two trees of similar height, but contrasting exposure to the marine fog; one is a 70-m-tall tree (Tree 1) that grew near the forest edge, while the other is a 63-m-tall tree (Tree 2) that grew in the interior of the stand. Previous research at The Grove of Old Trees has demonstrated a decrease in annual occult precipitation from the forest edge to the interior due to less fog interception by interior tree crowns (Ewing et al. 2009). On 10 August 2005, diurnal trends in branchlet xylem water potential (ΨL) were measured at three heights in the two trees on the southwest side of the crown (Tree 1 at 40, 53.8 and 60.3 m and Tree 2 at 32.9, 55.5 and 67.5 m). For the purposes of the data presented here, we define branchlet as a leafy shoot comprised of one small diameter photosynthetic stem with either needle- or scale-like leaves attached in such a manner that it is difficult to separate stem from leaf tissue. The measurements were made every 2 h over the course of a 14-h period, beginning pre-dawn (0540 h). Branchlets were cut and immediately sealed in plastic bags placed in the dark and transported to the base of the tree for determination of ΨL using a Scholander pressure chamber (Model 1000, PMS Instruments, Corvallis, OR, USA). Balancing pressure was recorded when xylem exudates reached the cut stem surface as verified by a dissecting scope at 25× magnification. Previous studies on conifers have reported similar ΨL between measurements made immediately after excision and by this procedure (Kaufmann & Thor 1982; Kolb et al. 1998).
Unexpectedly, during our field observations, a moist front of marine air carrying fog entered the forest at approximately 0600 h. It initially penetrated the forest at the ground level and was only a few meters thick but then pushed upwards through the forest canopy and into the tree crowns until much of the forest canopy was enveloped in fog. The fog then dissipated shortly after 1200 h. At ∼0700 h in the lower crown (32.9 m) and ∼0800 h in the mid and upper crown (55.5 and 67.5 m) of the exposed 70-m-tall tree, the branchlets intercepted the fog water resulting in a thin film of water being deposited on the branchlet surface that lasted until ∼1300 h. Although the fog reached the crown of the interior 63-m-tall tree (Tree 2), presumably increasing relative humidity (RH) and lowering temperature, branchlets on the interior tree never intercepted the fog water and, thus, the branchlets on this tree remained dry. Therefore, the two trees we measured were exposed to very different fog treatments. We continued with our water potential measurements during this period despite the fog, but these measurements were made on branchlets that were thoroughly dried using paper towels after the fog water was shaken off the entire branchlet before using the Scholander pressure chamber (PMS Instruments; following the methods of Burgess & Dawson 2004). Based on these unexpected but informative field observations, we initiated the detailed greenhouse investigation outlined below.
Study plants and experimental design
We measured the effect of experimental crown fog interception on leaf level carbon and water relations of redwood saplings in a greenhouse. Twelve 1.6-m-tall S. sempervirens saplings of the Santa Cruz variety were obtained from a local nursery. Saplings were repotted in 60 L pots and allowed to equilibrate to ambient greenhouse conditions for 3 weeks before the start of the treatment period. RH in the greenhouse ranged from 36 to 70% and air temperature (Ta) ranged from 15 to 23 °C. Greenhouse RH and Ta reflected August conditions at The Grove of Old Trees when fog was not present (30.2 to 87.4% RH and 11.6 to 29.4 °C). The influence of fog on redwood leaf carbon and water relations was investigated over a 32-d treatment period (7 March to 7 April 2006). Saplings were randomly assigned to one of the three treatment groups: (1) well watered (control); (2) water withheld from soil (dry-down); and (3) water withheld from soil, plus crown interception of fog water (fog). After the experiment began, trees in the control treatment were watered daily to saturation (between 1900 and 2000 h), while the other treatments received no soil water additions. We rotated pots every 3 d throughout the experiment to remove potential microclimate effects.
Fog was generated for the fog treatment nightly between 2000 and 0800 h by an ultrasonic water atomizer (Chaoneng Electronics, Nanhai, Guangdong, China) placed in a water reservoir, similar to the method of Burgess & Dawson (2004). Fog was generated and contained inside a clear polyvinyl chloride (PVC) chamber that was large enough to accommodate one 2-m-tall S. sempervirens sapling. Two small electric waterproof computer fans (Adda AQ series, Brea, CA, USA) were used to circulate the fog throughout each chamber. After each nightly fog event, the sides of the PVC chamber were removed and the trees were taken out of the chamber. Extreme care was taken to prevent fog water from reaching the soil through fog drip by placing PVC lids on each pot and sealing the tree bole to the lid with a waterproof putty (Terrastat IX, Henkel Technologies, Germany). Using these methods, fog exposure was confined to the canopy. This meant that during fog events, the only means of fog water use was through aboveground structures.
We measured ΨL at pre-dawn (between 0400 and 0600 h) and midday (between 1100 and 1400 h) on two branchlets from each tree. Pre-dawn water potential (ΨPd) measurements were taken 1 and 4 d before treatment to insure that trees in all treatment groups were at similar levels of canopy water status at the start of the experiment. All water potential measurements were made 4, 7, 14 and 21 d after the start of the treatment. Midday water potential (ΨMd) was measured on branchlets after gas exchange measurements were taken.
Soil water availability
In order to evaluate the water potential components along the SPAC among the treatment plants, we estimated ΨSoil by measuring ΨPd and volumetric soil water content on treatment days 14, 21, and 28. Soil water content was measured using a handheld soil moisture sensor (Hydrosense, Campbell Scientific, Logan, UT, USA). The relationship between ΨPd and volumetric soil water content provides an estimate of ΨSoil in the root zone, assuming that no mechanisms of pre-dawn disequilibrium, such as night-time transpiration or heterogeneity in soil water content, are observed (see Introduction for further discussion). Equilibration between ΨPd and ΨSoil is a common assumption when night-time transpiration is minimal or absent, and is widely used for calculating whole plant and leaf-specific hydraulic conductance (Irvine et al. 1998; Hubbard, Bond & Ryan 1999; Ryan et al. 2000; Fischer, Kolb & Dewald 2002; Phillips et al. 2003; Simonin et al. 2006). We did not detect night-time transpiration or heterogeneity in soil water content. Therefore, we assumed overnight equilibration between ΨPd and ΨSoil and used volumetric soil water content measurements and ΨPd to generate a soil water-release curve. Soil water-release curves typically use a power function to describe variation in soil water potential with soil water content (Campbell 1998). The power function describing variation between ΨPd and soil water content for the control and dry-down treatment trees was used to model pre-dawn ΨSoil for all the treatment groups (y = −77.9x−1.8; r2 = 0.83; P < 0.01).
Leaf gas exchange and chlorophyll fluorescence
Maximum rates of midday net CO2 assimilation (Aarea) and stomatal conductance (gs) per unit leaf area were measured between 1100 and 1400 h, 3 h after the fog treatment when the leaf surfaces were dry. The leaf level gas exchange measurements were made on treatment days 4, 7, 14 and 21 using an infrared gas analyser (6400, Li-Cor, Biosciences Inc., Lincoln, NE, USA). Three mature branchlets, from the same cohort per individual tree, were measured at 400 µmol mol−1 CO2 (slightly higher than ambient CO2 concentration), with 1000 µmol m−2 s−1 photosynthetic photon flux density provided by a cool red-blue light source (6400-02B SI-710, Li-Cor, Inc.). The light level used in the gas exchange cuvette was chosen based on the response of Aarea to variation in light availability measured for understorey saplings at The Grove of Old Trees field site during the spring of 2005 when soil water availability was not limiting. The light saturation point for understorey tree saplings at our field site occurs between 0800 and 1100 µmol m−2 s−1. Leaf temperature was allowed to vary naturally and ranged from 24 to 30 °C, with leaf-to-air VPDs ranging from 1.87 to 3.28 kPa. Gas exchange measurements represent the maximum values that saplings in each treatment achieve given the light level, CO2 concentration in the cuvette, and water status of the leaf. Leaf area was measured with a leaf area meter (LI-3100, Li-Cor, Inc.), in order to express midday maximum photosynthesis on a leaf area basis.
Chlorophyll fluorescence was measured between 0400 and 0600 h on 10 dark-acclimated leaves per tree on treatment days 4, 7, 14 and 21 with a pulse amplitude modulated fluorometer (MINI-PAM, H. Walz GmbH, Effeltrich, Germany). To maintain a constant distance and angle (60°) relative to the leaf plane, the fibre optic probe that delivered the measuring beam and saturating pulse was mounted above the leaf with a leaf clip holder (Model 2030-B, H. Walz GmbH).
Greenhouse treatment comparisons were made using a repeated measures analysis of variance to test for within-subject (days since water was withheld) and between-subject (water regime) effects on all tree response variables. Repeated measures analyses were performed using the JMP (version 5.0.1, SAS Institute, Cary, NC, USA) statistical software package. Linear and non-linear regressions were used to test for correlation between tree response variables measured in the field (Sigma Plot, version 8, Systat Software Inc., San Jose, CA, USA).
Diurnal variation in ΨL is expected to follow a sinusoidal pattern where ΨL begins at a maximum value at or near pre-dawn, declines steadily to a midday minimum and then recovers in the afternoon. This sinusoidal pattern has been shown in many distantly related woody and herbaceous species (Jarvis 1976; Batten, McConchie & Lloyd 1994; Gallego et al. 1994; Prior et al. 1997; Sellin 1999). When immersed in fog, diurnal variation in S. sempervirens ΨL followed the opposite pattern than expected (Fig. 1a,b) for these mature trees. As fog pushed up off of the ground through the tree crowns (bottom to top), ΨL approached, but did not exceed, ΨPd for all three canopy heights (Fig. 1a). When fog finally condensed on leaf surfaces of the exposed tree (∼0700 h for the lower crown and ∼0800 for mid and upper crown), ΨL increased above ΨPd and stayed above ΨPd across all three heights until the fog dissipated and leaf surfaces were dry (Fig. 1b).
For both trees, ΨPd followed the expected gravitation water potential gradient of approximately −0.01 MPa m−1 across all three canopy heights (Fig. 2a; r2 = 0.99, a = −0.011 ± 0.0004, y0 = −0.336 ± 0.02). In accordance with a unidirectional SPAC model, the vertical gradient in ΨL was below the ΨSoil + ρGh gradient during periods of no fog (Fig. 2a; r2 = 0.86, a = −0.029 ± 0.0059, y0 = 0.273 ± 0.317; Fig. 2c; r2 = 0.93, a = −0.025 ± 0.0035, y0 = 0.079 ± 0.186) and approached, but did not exceed, the ΨSoil + ρGh gradient during the foggy period when the leaves were dry and the driving gradient for E was at a minimum (Fig. 2b; r2 = 0.53, a = −0.0046 ± 0.0043, y0 = −0.797 ± 0.228). Contrary to a unidirectional SPAC model, at mid-morning after leaves of the exposed tree were wetted by intercepted fog (1120 h), ΨL was well above the ΨSoil + ρGh gradient, such that a positive ΨSoil was predicted from fitting a linear regression to ΨL versus height (Fig. 2b; r2 = 0.99, a = 0.127 ± 0.010, y0 = −0.013 ± 0.0002).
Soil water availability and leaf water potential
We found no significant difference in ΨPd between treatment groups before the start of the experimental dry-down (Table 1, Fig. 3a). However, we observed a significant effect of both watering regime and the interaction of the watering regime with time on post-treatment ΨPd and ΨMd (Table 1, Fig. 3a,b). After withholding water for more than 4 d, trees in the control treatment had greater ΨPd and ΨMd than trees in either of the drought or fog treatment groups. At 4 d post-treatment, ΨPd was highest for the fog treatment (−0.10 ± 0.08 MPa), followed by control (−0.21 ± 0.02 MPa) and drought (−0.23 ± 0.08 MPa) treatment groups. Control trees maintained ΨPd around −0.20 MPa for the entire 28-d treatment period. ΨPd of trees in the fog treatment never dropped below −0.70 MPa, while trees in the drought treatment dropped below −1.1 MPa (Fig. 3a). When ΨPd was compared to soil water content, trees in the fog treatment maintained greater ΨPd than trees in the drought and control treatments for a given soil water content (Fig. 4a,b). When comparing the log values of ΨPd and soil moisture, a distinct separation between the trees exposed to, and withheld from, overnight fog events occurred during periods of low soil moisture (Fig. 4b).
Table 1. Repeated measures analyses for the effect of water regime (between-subject variation) through time (within-subject variation) on pre-dawn and midday leaf water potential (ΨP and ΨM, MPa), photosynthesis (Aarea, µmol m−2 s-1), stomatal conductance (gs, mol m−2 s−1) and chlorophyll fluorescence (fv/fm)
Tree response variable
P > F
P-values in bold are significant at α = 0.05.
Water regime × time
Leaf gas exchange and chlorophyll fluorescence
The watering regime and the interaction of watering regime with time had a significant effect on Aarea (P = 0.015 and 0.007, respectively, Table 1) and a marginally significant effect on gs (P = 0.07 and 0.075, Table 1). As expected, Aarea was relatively constant for trees in the control treatment (4.06 ± 0.92 µmol m−2 s−1, Fig. 3c). Trees in the dry-down treatment showed a strong decline in Aarea after water was withheld. Withholding water resulted in a 23% decline in Aarea at day 7, a 72% decline at day 14 and a 67% decline at day 21 (Fig. 3c). In contrast to the dry-down treatment, trees in the fog treatment maintained Aarea similar to that of control, 4.39 ± 0.86 µmol m−2 s−1, up to 14 d post-treatment. After day 14, Aarea decreased by 63% to 1.89 ± 0.51 µmol m−2 s−1 (Fig. 3c).
Variation in gs showed a similar pattern to variation in Aarea across all the three treatment groups. Trees in the control treatment maintained relatively stable gs at 0.03 ± 0.004 mol m−2 s−1, whereas trees in the dry-down treatment showed a strong decline in gs after water was withheld (Fig. 3d). Withholding water resulted in a 43% decline in gs at day 7, a 61% decline at day 14 and a 70% decline at day 21 (Fig. 3d). The pattern of gs for trees in the fog treatment was similar to the control treatment up to day 14. But after 21 d, gs for the fog trees decreased by 65%.
Maximum midday leaf gas exchange was highly correlated with changes in water availability as assessed by ΨPd for both the dry-down and fog water regimes (Fig. 5a,b; Aarear2 = 0.72 P < 0.0001; gsr2 = 0.63; P < 0.0001). Both Aarea and gs were sensitive to changes in ΨPd between −0.2 and −0.6 MPa for trees in the dry-down and fog water regimes. Any further drop in ΨPd, between −0.6 and −1.5 MPa, had a minor effect on Aarea and gs (Fig. 5a,b). Although Aarea and gs were strongly correlated to variation in ΨPd, the sensitivity of Aarea and gs to variation in ΨMd was less pronounced (Aarear2 = 0.28 g, r2 = 0.31; data not shown). The weaker correlation between leaf gas exchange and ΨMd can be attributed to the large variation in ΨMd for a given ΨPd. For example, ΨMd varied between −0.50 and −1.28 MPa when ΨPd was greater than −0.24 and less than −0.15 MPa (Fig. 3). This suggests that for S. sempervirens saplings, the ΨL associated with the onset of stomatal closure is strongly influenced both by water availability, as assessed by our ΨPd measurements, and demand, as assessed by ΨMd. Taken together, the strong decline in gs on day 21, for trees in the fog treatment, was associated with either ΨPd less than −0.38 MPa and/or ΨMd less than −1.3 MPa (Figs 3 & 5).
Additionally, we observed no effect of water regime or the interaction of water regime with time on leaf chlorophyll fluorescence (P = 0.810 and 0.924, respectively) and, therefore, no correlation between chlorophyll fluorescence and variation in ΨPd. The lack of change between treatments in chlorophyll fluorescence and the strong correlation between Aarea and gs across all the three treatment groups (r2 = 0.86; P < 0.0001; Fig. 6) suggest that the relationship between Aarea and changes in ΨPd was largely attributed to variation in gs, and not the result of damage to photosystem II. When leaf level gas exchange was plotted against modelled ΨSoil, a large amount of variation was observed between fog and dry-down treatment responses. Both Aarea and gs for trees in the fog treatment were less sensitive to variation in modelled ΨSoil when compared to trees in the dry-down treatment (Fig. 5c,d; Aarear2 = 0.44; P = 0.04, gSr2 = 0.51 P = 0.03).
Fog interception and leaf water relations
Our field observations showed that daytime crown fog interception resulted in ΨL that exceeded the predicted maximum ΨL if soil water was the only readily available water source (Fig. 2b). Interestingly, we found that tree crown fog interception resulted in complete compensation for the negative effect of gravity with increasing height (i.e. ΨSoil + ρGh) on ΨL for leaves in the lower crown (32.9 m), with only partial compensation observed at the mid (55.5 m) and upper (67.5 m) crown positions. Furthermore, fog interception by lower crown foliage maintained ΨL above that predicted by soil water availability throughout the entire day (Fig. 2b). If fog condensation on leaves and stems had simply eliminated transpiration, a unidirectional SPAC model would predict equilibration between ΨL and ΨSoil and a vertical ΨL gradient with y-intercept (y0) or ΨSoil < 0. In contrast, the vertical ΨL gradient observed in the field predicted a ΨSoil > 0 when the crown was wet (Fig. 2; y0 = 0.127 ± 0.010). Interestingly, when foliage at each height in the exposed tree was covered in a film of water, the water potential gradient was steeper than the gravitational gradient of −0.01 MPa m−1. The lower slope observed during crown wetting events could come about in response to within-canopy variation in the capacity for foliar uptake (i.e. kAtm-LΔΨAtm-L; from Eqn 2) and/or the time course of water potential changes in leaves and stems; this is what we call their rehydration kinetics [e.g. CL(dΨL/dt) ≠ CSt(dΨSt/dt)]. Differences in the timing of canopy exposure to fog could also contribute to the observed slope of −0.013 MPa m−1. Additionally, using the mass balance framework described in Eqn 2, we can see that the impact of foliar uptake on whole plant water relations is ultimately dependent on both the rate of foliar uptake (i.e. kAtm-LΔΨAtm-L), and the rate of root water loss to the soil (i.e. kRt-SΔΨRt-Soil). It is also likely that water uptake by roots and leaves could have occurred at the same time. Concurrent water uptake by the crown and the roots is most likely to occur when transpiration is interrupted by a crown wetting event, similar to the conditions seen during the field observations. Under this scenario, stem water potential (ΨSt) would be initially less than ΨL and ΨRt as both leaves and roots would have direct access to water. Thus, from a mass balance perspective (Eqn 2), the impact of foliar uptake on plant water status and the ΨSoil + ρGh is a function of both leaf and root water relations.
Although the field observations of crown fog interception and ΨL were limited to two mature redwood trees, the results from the greenhouse experiment provided further and more definitive evidence that fog interception can result in a decoupling between maximum ΨL and ΨSoil. We found that crown fog interception increased ΨPd above that maintained by night-time rehydration via root water uptake only (Fig. 4a,b). Taken together, the field observations and results from the greenhouse experiment indicate that leaf and stem water absorption alter the generalized unidirectional model of the SPAC, as foliar uptake provides an additional water source that can decouple plant crown water relations from soil water availability to the point where ΨL can exceed ΨSoil + ρGh. In light of our results, we propose that the SPAC model is best viewed as a true ‘continuum’ among all potential water sources, not simply unidirectional.
Increased leaf water content associated with crown water interception, during periods of soil water stress, has the potential to influence many other aspects of plant form and function. For example, a unidirectional SPAC model would predict a strong influence of ΨSoil + ρGh on the upper limit of tree height via constraints on ΨL, turgor pressure and cell expansion (Koch et al. 2004; Woodruff, Bond & Meinzer 2004; Ishii et al. 2008). If ΨSoil + ρGh does limit maximum tree height via constraints on maximum ΨL, it is likely that increased ΨL associated with crown water interception and direct foliar uptake could provide for greater potential cell growth and expansion through increased turgor pressure or CL(dΨL/dt) for a given ΨSoil + pGh. Overall, our data, when combined with previous research, suggests that a unidirectional SPAC model is unable to describe whole plant water relations and growth in response to variation in soil water availability.
Fog interception and leaf gas exchange
Our results suggest that fog interception by tree crowns provides a significant water subsidy that can have a positive influence on leaf level gas exchange when plants are exposed to an otherwise desiccating environment. Leaf level gas exchange is influenced by several environmental factors that either directly or indirectly influence variation in ΨL (Dewar 2002; Buckley, Mott & Farquhar 2003; Tuzet, Perrier & Leuning 2003). Because maximum ΨL is thought to approach but not exceed ΨSoil, both Aarea and gs are considered strongly coupled to variation in soil water availability as measured by ΨSoil (Sperry et al. 1998; Tuzet et al. 2003). In our study, Aarea and gs were positively correlated to modelled pre-dawn ΨSoil for S. sempervirens trees in the dry-down treatment but less so for trees in the fog treatment. Saplings in the dry down treatment showed an immediate decrease in leaf level gas exchange when exposed to minor soil water stress, whereas saplings exposed to fog interception showed a more gradual decrease in leaf level gas exchange, and maintained greater Aarea and gs for a given ΨSoil (Fig. 5c,d). The observed increase in midday Aarea and gs suggests that fog water subsidies, via crown interception and subsequent foliar uptake, are not short-lived but are in fact great enough to impact leaf gas exchange throughout a majority of the day. Thus, our results show that foliar uptake of intercepted water can increase ΨL and improve photosynthetic carbon assimilation during periods of mild soil water stress. In this way, fog, rain or dew intercepted by plant crowns can be viewed as alternative water sources for leaves that have a positive influence on leaf carbon gain.
Although crown wetting events via fog, rain or dew have previously been shown to increase leaf water content for many distantly related plant species, the potential benefits of crown interception on photosynthesis and growth is generally ignored or even dismissed. Instead, previous research has focused on the negative effects of leaf wetting events on plant performance (Ishibashi & Terashima 1995) and the adaptive response of plants with an emphasis on morphological features that reduce leaf wettability and water retention (e.g. leaf drip tips, stomatal plugs; Lightbody 1985; Feild et al. 1998; Ivey & DeSilva 2001). The increased rates of leaf level gas exchange observed in our study suggest that a cost/benefit analysis is necessary to fully understand the potential adaptive outcomes of crown wetting events on leaf form and function. Although leaf wetting can reduce the rate of CO2 uptake by leaves, this temporary reduction can lead to increased gas exchange after leaf surfaces have dried due to the positive effects of leaf wetting on ΨL. To the best of our knowledge, only three previous studies have shown a significant positive effect of crown water interception on leaf level gas exchange (Grammatikopoulos & Manetas 1994; Munné-Bosch & Alegre 1999; Martin & Willert 2000). Unlike these previous studies, however, our study was conducted on whole plants, not individual leaves, and occurred over an extended period of time spanning a large range of soil water availability. Our research and the previous works cited above suggest that leaf wettability and the frequency of leaf wetting events are likely to be a strong selective pressure on leaf form and function during periods of mild soil water stress. For redwoods, the finely divided and closely arranged needles lead to a great deal of water retention in tree crowns, particularly when compared with other tree species with long needle (e.g. Pinus) or elongated (e.g. Eucalyptus) leaf shapes (T. Dawson, personal communication). Thus, variation in leaf shape, wettability and water retention may be particularly important not only for crown water uptake but also for other aspects of a species' ecophysiology within the same community where some species may shed water from leaf surfaces much more quickly and therefore may not accrue the same benefits as redwood does.
Researchers and naturalists alike have long noted that the distribution of S. sempervirens along the California coast strongly coincides with the frequent occurrence of summer fog. However, most descriptions have generally focused on the enhanced soil, and therefore root water availability resulting from summer fog inputs as an explanation for this unique range distribution. Our results illustrate how crown water interception and uptake of fog can provide another readily available water source that contributes to greater ΨL, resulting in greater midday gas exchange for a given soil water availability. The increased carbon gain associated with foliar water uptake may ultimately translate into increased fitness in these foggy coastal sites. Furthermore, we demonstrate that foliar uptake of intercepted fog water can decouple plant water status from soil water availability. In doing so, foliar uptake can result in ΨL that is greater than the ΨSoil + ρGh potential gradient such that maximum ΨL may actually exceed ΨSoil. The importance of leaf wetting for the carbon gain of other tree species is unknown, yet, given the frequency of rain, fog and dew events in most forested ecosystems, it seems likely that similar effects are more widespread than generally acknowledged. This work and the research cited herein suggest that crown wetting events often represent an overlooked aspect of plant water relations that can have a dramatic and positive effect on whole plant and ecosystem water and carbon balance (e.g. Díaz & Granadillo 2005; Gabriel & Jauze 2008; Johnson & Smith 2008; Williams et al. 2008; Ewing et al. 2009).
We would like to thank Vanessa Boukili, Emily Limm and Anna Simonin for their help with the field investigation; Anthony Ambrose for establishing tree crown access at the Grove of Old Trees; Crystal Richie for the help in maintaining the greenhouse treatments; and the Dawson and Santiago labs and three anonymous reviewers for comments on an earlier draft of this paper. Partial financial support was provided by NSF grant 0310103 to L.S.S.