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Ecology |
2Natural Science Division, Pepperdine University, Malibu, California 90263-4321 USA; 3Department of Botany and Plant Pathology, Michigan State University, East Lansing, Michigan 48823-1312 USA; 4Department of Biology, University of Utah, Salt Lake City, Utah 84112 USA
Received for publication June 29, 2001. Accepted for publication November 13, 2001.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: Ceanothus • chaparral • water relations • xylem cavitation
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). However, there were no external symptoms of fungal disease, dieback occurred after nearly 9 mo without rain, and mean midday xylem pressure was as low as –11.2 MPa. This suggested an alternate possibility, that branchlet death was caused by water-stress-induced failure of water transport via xylem cavitation and soil drying (Tyree and Sperry, 1988
; Sperry et al., 1998
). In chaparral shrubs, to maintain the evergreen habit, it is particularly vital that water is continuously delivered to the evergreen foliage. This is especially true for shallow rooted, nonsprouting species, such as C. crassifolius (Davis et al., 1999
). Such species do not have a root crown or a mechanism of shoot replacement after damage by drought and other disturbances such as wildfire (Thomas and Davis, 1989
) or wind (Wagner, Ewers, and Davis, 1998
).
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; Hacke et al., 2000
). The model determined the steady-state carrying capacity of the continuum based on measurements of the vulnerability of roots and stems to xylem cavitation, soil texture, and bulk soil water potential. |
MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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. Annual precipitation was recorded at a meteorological station 4 km from our study site (Malibu Beach-Dunne Station, Number 1025, Los Angeles Flood Control District). Precipitation in the rain season of 1995–1996 was 305 mm and in 1996–1997, 329 mm. This was 76% and 82%, respectively, of the 100-yr mean.
Seasonal changes in xylem pressure and assessment of branchlet dieback
We estimated seasonal changes in predawn and midday leaf xylem pressure (PL) on 12 C. crassifolius individuals between November 1995 and June 1998, using a pressure chamber (model 1001, PMS Instrument Company, Corvallis, Oregon, USA), on terminal branchlets, following the methods of Scholander et al. (1965)
. Our pressure chamber was custom designed to measure water potentials down to –14 MPa. A wildfire in October of 1996 consumed our 12 original plants, at which time we switched to 12 auxiliary plants within 100 m of the original stand. In November of 1997, we sampled 22 additional plants that suffered extreme dehydration and branchlet dieback, about 200 m from the original stand. On the 12 individuals plus the 22 new individuals in November, we counted the number of recently discolored branchlets (leaves yellow in color; Fig. 1B) between 8 August and 9 December 1997, before the onset of winter rains.
Fungal isolation experiments
In October of 1995, 100 peripheral branchlets, 30–50 cm in length, one from each of 100 individuals of C. crassifolius, were collected in the field. Samples were selected that had some, but not all, of their twigs containing discolored leaves. They were individually wrapped in wax paper to avoid moisture condensation or contamination and shipped by overnight mail to the Plant Pathology Laboratory at Michigan State University, where they were processed within 24 h. There were no signs of fruiting bodies, symptoms of necrosis on young leaves or petioles, nor evidence of canker on stems. From these samples, stem segments were taken both from healthy-appearing tissue within 1 cm of discolored (brown) tissue and also from discolored tissue. In July of 1997, 280 peripheral, green, healthy-appearing branchlets were sampled, one from each of 280 individual shrubs. These were processed in the same manner as for the discolored samples mentioned above. For each branchlet, a segment 2 cm in length was surface sterilized for 1 min in 70% ethanol and then for 10 min in 10% chlorine bleach (0.05% sodium hyperchlorite). Excess bleach on stem surfaces was blotted dry between sterile paper towels. The stem segments were subdivided by cutting with a flame-sterilized scalpel both transversely and longitudinally to achieve segments that included both xylem and phloem tissues, of final dimensions 0.5 x 0.25 x 0.25 cm. Petri plates were filled with 20 mL Difco PDA (potato dextrose agar) plus one drop of 25% lactic acid. The final stem segments were pushed into the agar with sterile forceps and incubated in the dark at room temperature for 9 d.
Three species of fungi isolated from discolored branchlets were: (1) Botryosphaeria dothidea, which was found in all 100 branchlets (primary fungus), (2) Botryosphaeria sp. (undetermined species, secondary fungus) isolated from about ten branchlets, (3) Sclerophoma sp. (rare undetermined species, tertiary fungus) isolated from only a few branchlets. The three isolates (Fig. 1C) were then used for inoculation experiments into healthy-appearing branches in the field (see below).
Inoculation experiments
The three cultures isolated above were inoculated on 3 January 1997 into three branches of 15 individuals of C. crassifolius growing at our study site. The inoculum consisted of a 0.5 cm diameter agar plug from the margin on a 10–15-d culture on PDA. The culture plug was held in place on the stem and protected from drying with parafilm wrap. Also a fourth branch was inoculated with sterile agar (sterile control) and a fifth was not inoculated but sawed through near its base (severed control) and supported in its normal position in the canopy with duct tape. Subsequently, xylem pressure, variable fluorescence (Fv/Fm, after a 15-min dark adaptation; Model OS5-FL, Modulated Fluorometer, Opti-Science, Tyngsboro, Massachusetts, USA), and a color index of leaves were measured every few days at first, then at progressively longer intervals until 27 July 1997 (204 d). Our color index ranged from 1 to 9 with low values representing green leaves, intermediate values representing yellow leaves, and high values representing brown leaves (Fig. 1B). These numbers corresponded to Munsell Color Standards for Plant Tissues (Munsell Color, Kollmorgen Instruments, Baltimore, Maryland, USA). Our numbers with their corresponding Munsell Colors are as follows: 1 = 5 GY 3/4; 2 = 5 GY 4/4; 3 = 5 GY 5/8; 4 = 2.5 GY 5/6; 5 = 2.5 GY 7/8; 6 = 5 y 6/8; 7 = 7.5 YR 6/8; 8 = 5 YR 5/8; 9 = 5 YR 3/4.
Xylem-notching experiments
During the summer of 1997, we greatly reduced hydraulic supply by basal stems to terminal branchlets by using a saw to aseptically cut stems (surface disinfected with 70% ETOH) about halfway through, five times, at a 1-cm spacing, spiraling at 90° angles with each successive cut (Fig. 1F). Sawed branches were reinforced with a metal splint (two aluminum scapulas held together around the sawed portion of the stem with duct tape). Uncut branches on the same individuals served as a control. Xylem pressure and color index (Munsell Color Standards for Plant Tissues) were measured periodically over a 25-d period.
Vulnerability curves
We determined the susceptibility of stem and root xylem to water-stress-induced embolism using the centrifuge method of Alder et al. (1997)
. Bowen (1999)
has established that the centrifuge method of constructing vulnerability curves matches closely the dehydration and air injection methods of constructing vulnerability curves for chaparral shrubs (cf. Jarbeau, Ewers, and Davis, 1995
). Stems were measured in the spring of 1997. One stem segment was cut from each of 12 individuals in our C. crassifolius population. Branches were wrapped in plastic and sent by overnight mail to the University of Utah. Branch segments were trimmed underwater to produce an unbranched length of 257 mm with a diameter of 4–7 mm. Segments were inserted in a tubing manifold and flushed for 1 h at 100 kPa with a 0.1 mol/L solution of HCl in distilled water, which had been degassed and passed through a 0.1-µm mesh diameter filter. We found that HCl or water or KCl produced the same curves (Alder, Sperry, and Pockman, 1996
). Now we use water plus 10 mmol KCl. After flushing to remove embolism, the hydraulic conductivity (Kh, in meters to the fourth power per megaPascal per second) was measured with the aid of an analytical balance connected to a computer that calculated Kh as
 | (1) |
P/x is the pressure gradient (in megaPascals per meter) and q the net volume flow rate (in cubic meters per second) caused by the applied pressure (background flow at P/x = 0 subtracted). The applied pressure (P) was kept below 5 kPa to avoid the displacement of embolism during the conductivity measurements. Following the initial flush and measurement of Kh, segments were then removed and spun in a centrifuge rotor designed to accommodate woody stems and roots (cf. Alder, Sperry, and Pockman, 1997
). The spinning induces a negative pressure profile in the segment that is a function of segment length and the rotation rate. The duration of the spin treatment was 5 min, after which Kh was measured, and the percentage loss from the initial Kh was calculated (percentage of embolism). The procedure was repeated using progressively higher rotation rates (corresponding to decreasing xylem pressure). The relationship between percentage of embolism and xylem pressure gave the vulnerability curve to water-stress-induced embolism. Root segments were measured during the summer of 1999 at Pepperdine University using the same technique as above. Lateral roots of 5–12 mm diameter were collected at 20–40 cm depth from the same population sampled for the stem measurements. One root segment was collected from each of 16 individual plants.
Estimation of critical xylem pressure (PLcrit) and maximum transpiration rate (Ecrit)
We used a water transport model (Sperry et al., 1998
; Hacke et al., 2000
) to estimate the most negative leaf xylem pressure (PLcrit) associated with the maximum possible steady-state transpiration rate (Ecrit) for the canopy. The model calculated the relationship between E and Px at any bulk soil water potential, taking into account the decreases in hydraulic conductance in the rhizosphere and xylem associated with transpiration. Any leaf xylem pressure more negative than PLcrit (or E greater than Ecrit) would cause essentially the complete loss of hydraulic conductance from soil to leaf by the drying of soil in the rhizosphere and the cavitation of the xylem.
The major inputs for the model were (a) the vulnerability curves of root and stem xylem, (b) soil texture in terms of percentage of sand, silt, and clay particles, (c) bulk soil water potential, and (d) the ratio of absorbing root area to transpiring leaf area (AR/AL). Stem and root vulnerability curves were used to predict how the hydraulic conductance (kp) of plant components declined with xylem pressure (Px) based on a Weibull function curve fit to vulnerability data (Neufeld et al., 1992
)
 | (2) |
), in the present analysis we were only interested in relative changes in kp, and we assigned ksat to give a maximum whole-plant conductance of 1 mmol · s–1 · MPa–1. The arbitrary assignation for ksat does not affect the model predictions of Px, but causes the corresponding predictions of E to be valid in relative, rather than absolute, units. We also expressed E on a plant, rather than leaf area basis, to avoid complications of changing leaf area per plant during the season. The whole-plant ksat was divided equally between root and shoot components as is typical of many woody plants (Sperry et al., 1998
). The root component was divided equally into minor vs. major roots, and the shoot component into minor vs. major stems, with each being given the same kp(Px) function. A sensitivity analysis indicated that ±20% variation in ksat assignments had little influence on predictions. The model was most sensitive to the kp(Px) function.
The hydraulic conductance of the rhizosphere (kr), as a function of soil water potential (
s, assuming a negligible osmotic component), was calculated as
 | (3) |
e is the soil air entry potential, b is the exponent of the moisture release equation, and X is a "conductance factor," which converts soil conductivity to rhizosphere conductance based on the cylindrical geometry of water uptake by a root (Sperry et al., 1998
). Equation 3 was discretized to represent concentric rhizosphere layers as explained in Sperry et al. (1998)
. The soil parameters ksat, e, and b were estimated from the percentage of sand, silt, and clay particles measured at the site according to Campbell (1985)
. Six soil samples were taken at 15–20 cm depth from the study site and analyzed by the hydrometer method (Soil Analytical Laboratory, Logan, Utah, USA). Soil texture and derived parameters are given in Table 1. Ceanothus crassifolius is a relatively shallow-rooted shrub, so we represented the bulk soil water potential of the rooting zone by a single value equal to the predawn leaf xylem pressure.
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) and estimated for a desert shrub (Kolb and Sperry, 1999
).
For any given bulk soil s and transpiration rate E, the model calculated the corresponding leaf xylem pressure for steady-state conditions. By incrementing E until there was no longer any significant hydraulic conductance in the continuum, the critical values of E and PL were estimated. We used an E increment equal to 1% of the maximum predicted E under wet soil conditions. The k in Eqs. 2 and 3 closely approach but never reach zero for any finite Px, and in actuality there should always be some limited hydraulic conductance associated with molecular films of water on soil particles and within cell wall nanopores, regardless of how negative Px or s may become. For this reason, the predictions of Ecrit and Pcrit are not points of complete hydraulic failure, but rather conservative estimates of the limits to transport capacity necessary to sustain any biologically meaningful gas exchange (Sperry et al., 1998
).
Statistical tests
Statistical comparisons between paired treatments were made by unpaired Student's t tests at P < 0.05.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Ceanothus crassifolius inoculated with three species of indigenous fungi (Fig. 1C) in January 1996 did not decline in PL, experience branchlet dieback, or show a decline in variable fluorescence (Fv/Fm) over a 30-d period (Fig. 4A, B); the opposite was the case for branches detached from the plant to show the effect of dehydration on these parameters. Furthermore, inoculated branches did not increase in their Munsell Color Index over a 204-d period, unlike detached branches (Fig. 4C). Branches that remained on the plant, but whose hydraulic conductance was diminished by the xylem-notching treatment, showed a decrease in PL to a minimum mean value of –14 MPa and increased in Munsell Color Index to a maximum mean value of 5 over a 15-d period (Figs. 1F, 5).
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The soil texture data and vulnerability curves were used in the transport model to predict PLcrit over a range of bulk s for the C. crassifolius population. Using mean soil texture and mean vulnerability curves, the corresponding average PLcrit was near –12 MPa, varying only slightly with bulk soil s (Fig. 7A). The corresponding values of mean Ecrit vs. s show Ecrit declining to near zero as s approaches PLcrit (Fig. 7B). Recall that the modeled E values were arbitrary (because of the arbitrary choice of ksat in Eqs. 2) and expressed on a per plant basis. Plotting them shows the relative decline in allowable plant water use as s declines.
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s (Fig. 7A). The corresponding minimum Ecrit shows a decline to near zero as s declines to –10 MPa and beyond (Fig. 7B, dotted curve). Conversely, minimum PLcrit based on the finer soil (B) and the most resistant vulnerability curves was near –13 MPa (Fig. 7A).
Safety margins from hydraulic failure were evaluated by comparing actual midday PL with PLcrit as predawn PL (a proxy for s) became more negative during drought (Fig. 7A). As can be seen from the convergence of midday P to within the PLcrit range, safety margins were predicted to reach zero for worst-case scenarios where the most vulnerable xylem is combined with the coarsest soils. This indicates that hydraulic failure was a distinct possibility within the population and was likely a contributing cause of the observed dieback.
As the drought progressed, midday and predawn PL converged to a 1 : 1 correspondence (Fig. 7A: dashed line vs. solid line) showing the progressive reduction in midday Px from bulk soil to leaf to zero as E per plant was reduced to zero. The predicted reduction in E with soil drought is plotted along with Ecrit in Fig. 7B (Epred), which allows safety margins to be viewed in terms of E rather than Px as in Fig. 7A. There is no new information contained in such a plot, because the Epred values were deduced from the PL data. However, a more realistic view of the safety margin from hydraulic failure is obtained. It can be seen that safety margins from Ecrit are diminished more rapidly with drought than safety margins from PLcrit. For example, plants at –8 MPa have what appears to be a comfortable 2-MPa safety margin from a PLcrit of –10 MPa (Fig. 7A). However, at the same time their Epred is very close to Ecrit (Fig. 7B). The difference in safety margins occurs because when Px in the continuum is approaching negative values near the tail ends of the soil drying or xylem vulnerability curve, a small increment in E translates into a disproportionately large drop in Px. Thus, as hydraulic failure is approached, Px would be expected to drop rather abruptly prior to dieback. This may be the explanation for the relative scarcity of data below –8 MPa for green shoots: plants or branches in this range are close to hydraulic failure and could be in a rapid transition to dieback.
The model predicted which component of the soil-root-shoot system, i.e., rhizosphere, minor and major roots, or major and minor branches, was most hydraulically limiting at the critical point where Px = PLcrit and E = Ecrit (Fig. 8). When soil was either very wet (s > –2) or very dry (s < –10), the greatest resistance was in the minor branch component as a result of xylem cavitation. However, at intermediate s, the greatest resistance was within the rhizosphere as a result of soil drying around the root during transpirational uptake (Fig. 8). This basic pattern was obtained regardless of whether mean or extreme values of soil texture and xylem vulnerability were used in the model, or if AR/AL was doubled from 10 to 20. It was also not sensitive to ±20% changes in how the maximum soil-canopy conductance was partitioned between the four plant components. In the relevant s range below –8 MPa, where hydraulic failure was likely to have occurred for our population (Fig. 7), the limiting component was transitional between rhizosphere and minor branch xylem. Predicted percentage of embolism in branches at PLcrit under these circumstances was >95%.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Apparently endophytic fungi were widely present, occurring in at least half of the healthy stems. However, upon death of the branchlets, they proliferated and were present in 100% of dead branchlets. By Occam's razor, drought-induced embolism of branchlets is sufficient to explain all the dieback symptoms. Therefore, contrary to interpretations by Brooks and Ferrin (1991)
and Riggan et al. (1994)
, perhaps the endophytic fungi should be viewed in this case as well-positioned saprophytes rather than latent parasites.
During the peak of drought, the green, healthy-appearing branchlets had water potentials of about –8.4 MPa, whereas adjacent branchlets on the same branch, but with discolored leaves, always had measured water potentials below the limits of our pressure chamber (less than –14.0 MPa). This is consistent with air blockage as the cause of branchlet dieback. Once branchlets are 100% embolized, it would be difficult to force water out of the severed end of branchlets with a pressure chamber.
The patchy nature of the dieback within single plants (Fig. 1A, E) suggests that the reduction in hydraulic conductance by water stress was not equal to all branchlets. This would result from intraplant variation in the parameters that determine the point of hydraulic failure. These parameters include the predrought soil-to-leaf hydraulic conductance, the vulnerability of individual leaves, branchlets, and rootlets to cavitation, the depth of the roots that preferentially supply different zones of the crown, and the soil properties in their rooting zones. While we only assessed interplant variation in this study and thus analyzed hydraulic limitations implicitly on a whole-plant basis, the range of intraplant variation is likely to be similar if previous work on other species is representative (Zimmermann, 1978
; Tyree and Sperry, 1988
; Sperry and Saliendra, 1994
; Cochard et al., 1997
). As recognized and demonstrated previously (Zimmermann, 1983
; Tyree and Sperry, 1988
), patchy dieback within the crown under water-stressed conditions would act to improve the hydraulic conductance and water status to remaining foliage, acting as a last-ditch mechanism to avoid whole-plant mortality (Rood et al., 2000
).
The patchy nature of the dieback also implies that the point of greatest hydraulic restriction was not in the major transport arteries—otherwise the whole crown would be equally affected. Consistent with this observation, the model indicated that the greatest restrictions were in the peripheral parts of the flow path—in the rhizosphere component and in the minor branches (Fig. 8). Importantly, even if failure was initiated belowground in the rhizosphere, it would also trigger failure in the distal branches downstream. In addition to promoting a patchy dieback pattern, localizing hydraulic restrictions to peripheral units also facilitates recovery from the drought. In the case of the rhizosphere restriction, rewetting of soil would be the only requirement for restoring conductivity. Dead branchlets could be replaced by axillary buds on the surviving stems.
If whole branches were to die back to ground level, which was not observed for any individual in our population, replacement would be improbable. This is because C. crassifolius is a nonsprouter after wildfire and does not produce a root crown (lignotuber) with adventitious buds and carbon stores to facilitate whole-branch regrowth (James, 1984
; Davis et al., 1999
). This is in contrast to chaparral species that are sprouters after wildfire. Such species are known to undergo whole-branch replacement after dieback by wildfire (DeSouza, Silka, and Davis, 1986
; Thomas and Davis, 1989
; Stoddard and Davis, 1990
), dieback by freezing (Langan, Ewers, and Davis, 1997
), and breakage by wind (Wagner, Ewers, and Davis, 1998
).
It should be noted that the branchlet death in the outer canopy of our shrubs was not due to natural pruning as reported in the literature (Mahall and Wilson, 1986
; Keeley, 1975, 1992, 1999
). Natural pruning is associated with low light levels in combination with water stress. In our study, peripheral branchlet dieback was associated with drought, not shade. Furthermore, we did not observe whole-plant mortality during our investigation, only dieback of outer canopy branchlets.
Our results are consistent with the findings of Schlesinger and his colleagues for the closely related non-sprouting species, Ceanothus megacarpus (Schlesinger and Gill, 1978, 1980
; Schlesinger et al., 1982
). They found whole-plant mortality to be restricted to a thinning stage between years 5 and 15 with little mortality thereafter. The primary cause of plant death was attributed to water stress. The lowest seasonal water potential that they observed was –12 MPa, in 6-yr-old pure stands of C. megacarpus. Mortality approximated 50% of the individuals by year 15 and did not significantly increase in stands up to at least 54 yr old. Our stands of C. crassifolius were 25 yr old at the initiation of our study. Therefore, whole-plant death due to thinning would not expected.
Specht (1969)
estimated the percentage of dead to live biomass in stands of C. crassifolius to be 58% at 9 yr, 64% at 18 yr, and 70% at 37 yr. If one included natural pruning of lower branches in deep shade (Mahall and Wilson, 1986
) and water-stress-induced dieback of small peripheral branchlets observed in this study, the 12% increase in dead biomass between years 9 and 37 would be expected. Likewise, Hanes (1971)
found the number of live to dead shrubs of C. crassifolius in a 40-yr stand to be a little over 50%. Taken together, it appears that the percentage of dead to live biomass in mature Ceanothus stands frequently achieves 50%, with whole-plant mortality restricted to a thinning stage. However, the age of thinning probably depends on extreme drought events, which may occur later in stand development as recorded by Horton and Kraebel (1955)
. They found nearly 50% mortality of C. crassifolius shrubs between the 20th and 25th yr as a result of severe drought.
It is possible that the branchlet dieback we observed in this study represents a mechanism to reduce overall transpiration rate, conserving water and reducing the incidence of whole-plant mortality. This process would be adaptive considering the relatively shallow rooting depth of C. crassifolius and the inability of these species to sprout from a root crown after major branch death. This is in contrast to sprouting species of chaparral that have been shown to continue major branch replacement throughout their life span (Keeley, 1992
).
Our results differ from previous analyses of hydraulic limitations in some other species that have predicted the major hydraulic restriction developing in the minor roots as a result of extensive root cavitation (Alder, Sperry, and Pockman [1996]
for Acer grandidentatum; Kolb and Sperry [1999]
for Artemisia tridentata; Hacke et al. [2000]
for Pinus taeda; Mencuccini and Comstock [1997]
for Hymenoclea salsola and Ambrosia dumosa). There were three reasons why cavitation in C. crassifolius roots was not a limiting factor in our study, whereas rhizosphere drying was important (Fig. 8). First, the vulnerability of roots to cavitation was not significantly different from shoots (Fig. 6) in C. crassifolius, whereas in the other study species, roots were considerably more vulnerable than shoots. Equal vulnerability of roots and shoots ensures that hydraulic restrictions will develop either in the rhizosphere or peripheral branches. Second, the overall resistance of C. crassifolius xylem to cavitation was much greater than previous study species. In fact, the vulnerability curves in Fig. 6 are among the most resistant known, together with curves for Juniperus monosperma, Larrea tridentata, and Ambrosia dumosa of the Sonoran and Mojave deserts (Mencuccini and Comstock, 1997
; Pockman and Sperry, 2000
). The more resistant the xylem is to cavitation, the more likely hydraulic failure will occur in the rhizosphere rather than in the xylem unless the greater cavitation resistance is accompanied by an AR/AL large enough to avoid a rhizosphere restriction (Hacke et al., 2000
). Third, significant rhizosphere restriction is unavoidable when cavitation-resistant xylem is combined with a relatively coarse soil as was the case for our C. crassifolius population. In this circumstance, significant hydraulic resistance will be predicted in the rhizosphere regardless of how high the AR/AL (Sperry et al., 1998
).
Aside from the obvious advantage of protecting the major transport arteries, the adaptive significance of localizing the peripheral hydraulic restrictions specifically to rhizosphere vs. minor roots vs. minor branch components is unknown. A better understanding would require analysis of the costs of cavitation resistance and investment in roots vs. the benefits of enhanced water extraction in a given life-history, environmental, and competitive context. It may be that plants where roots are significantly more vulnerable than shoots are also plants with relatively deep root systems such that failure in vulnerable (= cheap) shallow roots acts to shift water use to progressively deeper layers. Ceanothus crassifolius is relatively shallowly rooted, and it may require very cavitation-resistant roots to more effectively mine the shallow soil water. It is known that within the chaparral community, deeper rooted plants are correspondingly more vulnerable to shoot cavitation at particular xylem pressures (Jarbeau, Ewers, and Davis, 1995
; Davis, Kolb, and Barton, 1998
; Davis et al., 1999
), and there is some recent evidence that deep-rooted species have much lower cavitation resistance of roots than stems (Crocker, 1999
; McElwain, 2001
).
The natural dieback we observed in C. crassifolius is one of the few examples of mortality in a natural setting that can be linked to hydraulic limitations on plant gas exchange. While a variety of studies have demonstrated how an observed reduction of gas exchange during drought protects plants from hydraulic failure (e.g., Cochard, Breda, and Granier, 1996
; Lu et al., 1996
; Hacke et al., 2000
), it is rare to observe extreme natural drought events where plants have been forced to their limits. This is presumably more common at the vulnerable seedling stage, where previous studies in the chaparral have shown a correlation between increasing embolism and seedling mortality (Williams, Davis, and Portwood, 1997
). Thomas and Davis (1989)
reported a minimum water potential less than –10 MPa (the limit of their pressure chamber) for seedlings of Ceanothus megacarpus, about 4 km from our study site, and Schlesinger et al. (1982)
recorded water potentials as low as –12.0 MPa for seedlings of C. megacarpus in the Santa Ynez Mountains near Santa Barbara, California. The lowering of water tables in riparian areas as a result of altered stream flows has been linked to cavitation and branch dieback in adult cottonwood (Populus deltoides, P. fremontii) trees (Tyree et al., 1994
; Rood et al., 2000
). It seems likely that future work will provide more examples of hydraulic limits "in action" as they are more widely recognized as a potential cause of mortality (cf. Sparks and Black, 1999
).
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FOOTNOTES |
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5 Author for reprint requests (davis{at}pepperdine.edu
)
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Alder N. N. J. S. Sperry W. T. Pockman 1996 Root and stem xylem embolism, stomatal conductance, and leaf turgor in Acer grandidentatum populations along a soil moisture gradient. Oecologia 105: 293-301[CrossRef][ISI]
Bowen T. J. 1999 Interactive effects of water-stress and freezing on xylem embolism in Ceanothus chaparral. Thesis, Pepperdine University, Malibu, California, USA
Brooks F. D. Ferrin 1991 Interim report for Cooperative Agreement PSW-90-045CA. USDA Forest Service, Pacific Southwest Forest and Range Experiment Station, Riverside, California, USA
Campbell G. S. 1985 Soil physics with BASIC. Elsevier, New York, New York, USA
Cochard H. N. Breda A. Granier 1996 Whole tree hydraulic conductance and water loss regulation in Quercus during drought: evidence for stomatal control of embolism?. Annales des Sciences Forestières 53: 197-206[CrossRef]
Cochard H. M. Peiffer K. Le Gall A. Granier 1997 Developmental control of xylem hydraulic resistances and vulnerability to embolism in Fraxinus excelsior L.: impacts on water relations. Journal of Experimental Botany 48: 655-663
Crocker M. 1999 In the chaparral shrub Heteromeles arbutifolia, which is more susceptible to water stress: leaf tissue or stem xylem?. Thesis, Pepperdine University, Malibu, California, USA
Davis S. D. F. W. Ewers J. Wood J. J. Reeves K. J. Kolb 1999 Differential susceptibility to xylem cavitation among three pairs of Ceanothus species in the Transverse Mountain Ranges of Southern California. Ecoscience 6: 180-186[ISI]
Davis S. D. K. J. Kolb K. P. Barton 1998 Ecophysiological processes and demographic patterns in the structuring of California chaparral. In P. W. Rundel, G. Montenegro, and F. Jaksic [eds.], Landscape disturbance and biodiversity in Mediterranean-type ecosystems, 297–310. Springer Verlag, Berlin, Germany
DeSouza J. P. A. Silka S. D. Davis 1986 Comparative physiology of burned and unburned Rhus laurina after chaparral wildfire. Oecologia 71: 63-68[CrossRef][ISI]
Hacke U. G. J. S. Sperry B. E. Ewers D. S. Ellsworth K. V. R. Schäfer R. Oren 2000 Influence of soil porosity on water use in Pinus taeda. Oecologia 124: 495-505[CrossRef][ISI]
Hanes T. L. 1971 Succession after fire in the chaparral of southern California. Ecological Monographs 41: 27-52[CrossRef]
Hickman J. C. 1993 The Jepson manual: higher plants of California. University of California Press, Berkeley, California, USA
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