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Reversing cavitation in tracheids of Pinus sylvestris L. under negative water potentials
Abstract
Xylem cavitation is a frequent event, but since resistance to flow does not generally increase in vivo, reversal must also occur even under negative potentials. We demonstrated that this can occur in excised wood. Our results suggest that refilling of cavitated tracheids at negative water potentials may result from a change in equilibrium between gas concentrations, water potential and surface tension at the embolism interface. Excised branch-wood specimens from small trees of Pinus sylvestris were dried on the bench to a range of relative water contents and then rehydrated in a permeability apparatus using ultra-filtered, de-aerated water as permeant. Water inflow and outflow were measured gravimetrically by recording the gain or loss from two reservoirs held on balances. Flow was induced through the specimen by holding the balances at different levels, while an overall negative water potential could be imposed by raising the specimen above the inflow/outflow reservoirs. Changes in water content of the specimen were calculated as the difference between inflow and outflow. The time-course data for both relative water content and permeability were fitted to an exponential function to give initial and final estimates and a time constant. Rehydration occurred at all imposed water potentials, but the speed of recovery was affected at lower potentials. Where drying of the specimen was more protracted, permeability was initially lower but also recovered during permeation. Both flow and de-aeration were necessary for complete rehydration. A model requiring new information on gas concentrations and transport coefficients is suggested.
... (3) Does the hydraulic resistance in the soil--vegetation--atmosphere system increase during drought, and can it recover when drought ceases? The question of whether recovery occurs is important, because refilling of embolized tracheids is believed to occur only when tension in the water columns approaches zero (Borghetti et al. 1991, Edwards et al. 1994. ...
... Needle water potential never fell below below −1.5 MPa (Table 2) and thus prevented the development of substantial xylem embolism (Figure 7) that would have resulted in an increase in the hydraulic resistance of the woody tissue. This view is consistent with the fact that no one has identified a mechanism by which refilling of embolized xylem can occur under significant tensions (Borghetti et al. 1991, Edwards et al. 1994). Thus, unlike some broad-leaved Figure 8. Seasonal changes in tree growth for the drought (᭺) and control treatments (᭹) during 1995 (the drought period) and the following year. ...
We investigated the impact of drought on the physiology of 41-year-old Scots pine (Pinus sylvestris L.) in central Scotland. Measurements were made of the seasonal course of transpiration, canopy stomatal conductance, needle water potential, xylem water content, soil-to-needle hydraulic resistance, and growth. Comparison was made between drought-treated plots and those receiving average precipitation. In response to drought, transpiration rate declined once volu-metric water content (VWC) over the top 20 cm of soil reached a threshold value of 12%. Thereafter, transpiration was a near linear function of soil water content. As the soil water deficit developed, the hydraulic resistance between soil and needles increased by a factor of three as predawn needle water potential declined from −0.54 to −0.71 MPa. A small but significant increase in xylem embolism was detected in 1-year-old shoots. Stomatal control of transpiration prevented needle water potential from declining below −1.5 MPa. Basal area, and shoot and needle growth were significantly reduced in the drought treatment. In the year following the drought, canopy stomatal conductance and soil-to-needle hydraulic resistance recovered. Current-year needle extension recovered, but a significant reduction in basal area increment was evident one year after the drought. The results suggest that, in response to soil water deficit, mature Scots pine closes its stomata sufficiently to prevent the development of substantial xylem embolism. Reduced growth in the year after a severe soil water deficit is most likely to be the result of reduced assimilation in the year of the drought, rather than to any residual embolism carried over from one year to the next.
... The capillary effect of traces of water left in the end of tracheids is thought to reduce the water potential below that of adjacent cells thus creating a pressure differential between adjacent cells. The increased pressure as a consequence of menisci at the air-water interface will also contribute to dissolving the air in the xylem (Tyree and Yang, 1992 ; Yang and Tyree, 1992 ; Edwards et al., 1994). Most of the recent research on desiccation tolerance in resurrection plants has been conducted on leaf tissue and has been focused at the biochemical and molecular level (see Bewley, 1995 ; Ingram and Bartels, 1996 ; Oliver and Bewley, 1997 for recent reviews). ...
... During the refilling experiments water uptake by both ends of the twig occurred. This has been reported previously by Borghetti et al. (1991) and Edwards et al. (1994) for Pinus sylestris, but it is not known how common this is. During these experiments, the weight loss from the upper balance always exceeded the weight gain by the lower balance. ...
Myrothamnus flabellifoliusWelw. is a desiccation-tolerant (‘resurrection’) plant with a woody stem. Xylem vessels are narrow (14 μm mean diameter) and
perforation plates are reticulate. This leads to specific and leaf specific hydraulic conductivities that are amongst the
lowest recorded for angiosperms (ks0.87 kg m−1MPa−1s−1; kl3.28×10−5kg m−1MPa−1s−1, stem diameter 3 mm). Hydraulic conductivities decrease with increasing pressure gradient. Transpiration rates in well watered
plants were moderate to low, generating xylem water potentials of -1 to -2 MPa. Acoustic emissions indicated extensive cavitation
events that were initiated at xylem water potentials of -2 to -3 MPa. The desiccation-tolerant nature of the tissue permits
this species to survive this interruption of the water supply. On rewatering the roots pressures that were developed were
low (2.4 kPa). However capillary forces were demonstrated to be adequate to account for the refilling of xylem vessels and
re-establishment of hydraulic continuity even when water was under a tension of -8 kPa. During dehydration and rehydration
cycles stems showed considerable shrinking and swelling. Unusual knob-like structures of unknown chemical composition were
observed on the outer surface of xylem vessels. These may be related to the ability of the stem to withstand the mechanical
stresses associated with this shrinkage and swelling.Copyright 1998 Annals of Botany Company
... The occurrence and importance of cavitation in response to water stress and winter freezing in a wide range of plants have been well documented (Sperry & Tyree 1990; LoGullo & Salleo 1993; Sperry & Saliendra 1994; Tognetti & Borghetti 1994; Franks, Gibson & Bachelard 1995; Hacke & Sauter 1995; Jackson, Irvine & Grace 1995; Tognetti et al. 1996; Langan, Ewers & Davis 1997; Pockman & Sperry 1997). In contrast, the role of embolism repair in maintaining a functional water transport system has received little attention (Salleo & LoGullo 1989; Sobrado, Grace & Jarvis 1992; Yang & Tyree 1992; Edwards et al. 1994; Lewis, Harnden & Tyree 1994 ). Factors contributing to this omission include a tendency to view the xylem solely as a domain of non-living cells, difficulties in reconciling repair mechanisms with the existence of tension in the xylem, and technical limitations in the ability to resolve cavitation repair. ...
... How refilling under tension occurs is not known. A mechanism for bubble dissolution under negative pressure was presented and tested for Pinus sylvestris L. (Sobrado et al. 1992; Edwards et al. 1994). The authors conclude that refilling may occur at pressures as low as –46 kPa, although this process requires up to 16 h. ...
Xylem hydraulic conductivity and percentage loss of conductivity (PLC) were measured on a ring-porous (Fraxinus americana L., white ash), a diffuse porous (Acer rubrum L., red maple) and a coniferous (Picea rubens Sarg., red spruce) tree species in a temperate deciduous forest in central Massachusetts, USA. Measurements were made on current and 1-year-old branch segments in the afternoon and on the following morning. Afternoon PLC was 45 to 70% for the current year's extension growth in both white ash and red maple. Morning PLC was significantly lower (10–40%). Conductivity also varied diurnally suggesting, on average, a 50% recovery from cavitation overnight. Red spruce showed lower PLC and conductivity and a less pronounced night-time recovery. Diurnal variation in hydraulic conductivity and PLC suggests that embolism removal occurred in all three species despite the existence of tension within the xylem. Further evidence for embolism removal was observed with an in situ double-staining experiment in which dyes were fed to a transpiring branch during the late afternoon and the following morning. Examination of stem cross-sections showed that a larger number of vessels were conductive in the morning than on the preceding afternoon. Results of this study suggest that hydraulic capacity is highly dynamic and that conductivity measurements reflect a balance between two processes: cavitation and embolism removal.
... Possibly, the increase in K was caused by new sapwood development (Brodribb & Cochard 2009 ). However, there has been evidence of cavitation reversal in conifer tracheids under negative pressure (Borghetti et al. 1991; Sobrado, Grace & Jarvis 1992; Edwards et al. 1994; Zwieniecki & Holbrook 1998). When temperatures drop, gas solubility increases allowing gas dissolution into adjacent functional xylem (Schenk & Espino 2010). ...
... When temperatures drop, gas solubility increases allowing gas dissolution into adjacent functional xylem (Schenk & Espino 2010). If transpiration also occurs, there may be embolism repair (Edwards et al. 1994). Earlier, Burgess & Dawson (2004 reported significant night-time transpiration in natural redwood forests driven by very high D. We suggest that coast redwood might have benefited from colder night-time temperatures coupled with high D conditions to refill cavitated tracheids under negative pressure. ...
Trees planted in urban landscapes in southern California are often exposed to an unusual combination of high atmospheric evaporative demand and moist soil conditions caused by irrigation. The water relations of species transplanted into these conditions are uncertain. We investigated the water relations of coast redwood (Sequoia sempervirens) planted in the urbanized semi-arid Los Angeles Basin, where it often experiences leaf chlorosis and senescence. We measured the sap flux (J(O)) and hydraulic properties of irrigated trees at three sites in the Los Angeles region. We observed relatively strong stomatal regulation in response to atmospheric vapour pressure deficit (D; J(O) saturated at D < 1 kPa), and a linear response of J(O) to photosynthetically active radiation. Total tree water use by coast redwood was relatively low, with plot-level transpiration rates below 1 mm d(-1) . There was some evidence of xylem cavitation during the summer, which appeared to be reversed in fall and early winter. We conclude that water stress was not a direct factor in causing leaf chlorosis and senescence as has been proposed. Instead, the relatively strong stomatal control that is adaptive in the native habitat of coast redwood may lead to carbon limitation and other stresses in semi-arid, irrigated habitats.
... Acoustic events can now be recorded for extended periods of time on various plant organs [20] and have been used as an index of plant water stress [1,6,16]. Cavitation leads to significant loss of water-conducting tissue and concomitant declines in hydraulic conductivity [24], and recovery (in gymnosperms) may be slow or incomplete [1,9,21,37,47]. ...
... The mechanism of refilling is still unclear. In Pinus sylvestris studies have demonstrated embolism reversal in the laboratory [2,9] and recovery of stem water content over winter has been demonstrated in the field [44]. The refilling of embolized vessels may be by osmotic pressure of the xylem sap from the adjoining parenchyma, the so called "vitalistic theory", first purported by Grace [10] and given weight by the results of Salleo et al. [33]. ...
Mature Scots pine (Pinus sylvestris L.) were subjected to an 11 month imposed soil drought, from November 1994. Control plots received rainfall plus irrigation. The extent of cavitation in the xylem of branches and boles was compared using ultrasonic acoustic emission (UAE) measurements. Supporting measurements of the relative water content (Rw) of the bole and shoot were recorded. Acoustic emissions were detected in both treatments. An effect of water-stress, in both boles and branches, at the height of the drought, was noted. Differences in vulnerability were found and suggest a reduced vulnerability to cavitation of remaining functional conduits, after loss of the most vulnerable conduits, in the water-stressed trees. Bole Rw was lower than branch Rw. In 1-year-old shoots of droughted trees a significant increase in xylem embolism was found. Seasonal changes in shoot Rw were interpreted as the occurrence and recovery (refilling) of emboli in xylem tissues: an active role of precipitation is hypothesised. It was estimated that 15% of tracheids were cavitated without affecting above-ground hydraulic resistances. It is suggested that runaway cavitation was avoided through stomatal closure maintaining leaf water potential (indicative of xylem tension) below the cavitation threshold, and thereby little effect of drought was evident in above ground tissues.
... However, the Cohesion theory is not a comprehensive theory of water movement in trees. For example, it does not explain why time lags occur in the movement of sap between the top and base of the tree (Martin et al., 1997;Schulze et al., 1985); what causes cavitation; how decreases in saturation decrease the hydraulic conductivity of the sapwood (Magnani & Borghetti, 1995;Sellin, 1991;Edwards et al., 1994;Tyree et al., 1999); or why the water content in the sapwood of conifers decreases during summer and increases during fall (Waring & Running, 1978;Markstrom & Hann, 1972). ...
... The explanatory power of the theory proposed depends on whether models, such as the one presented in this paper, can actually meet basic assessment criteria such as explaining the lag in flow (Martin et al., 1997;Schulze et al., 1985), the changing saturation (Waring & Running, 1978;Markstron & Hann, 1972) and the changing hydraulic conductivity observed in trees (Magnani & Borghetti, 1995;Sellin, 1991;Edwards et al., 1994;Tyree et al., 1999). If models built from the proposed theory can explain such behaviors, then this theory gains in explanatory power. ...
The electric circuit analogy has had a profound influence on how tree physiologists measure, model and think about tree water flow. For example, previous models that attempt to account for changes in saturation use the electric circuit analogy to define capacitance as the change in saturation per change in pressure. Given that capacitance is constant, this relationship implies that subjecting a block of wood to a pressure of -2.5 MPa for 2 min results in the same change in saturation as subjecting the same block to the same pressure for 2 days. Given the definition of capacitance, it is unclear how the electric circuit analogy could be used to predict changes in saturation separately from changes in pressure. The inadequacies in the electric circuit analogy discussed in this paper necessitate a new theory of tree water flow that recognizes the sapwood as being a porous medium and explicitly deals with the full implications of the unsaturated flow occurring in the sapwood. The theory proposed in this paper combines the Cohesion theory with a mathematical theory of multiphase flow through porous media. Based on this theory, both saturated and unsaturated tree water flow models are presented. Previous partial differential equation models of tree water flow based on the electric circuit analogy are shown to be mathematically equivalent to the model of saturated porous flow. The unsaturated model of tree water flow explicitly models the pressure profile and the rates of change in saturation and specific interfacial area (a measure of how the water in the unsaturated sapwood is partitioned between mobile and immobile components). The unsaturated model highlights the differences between saturated and unsaturated flow and the need to measure the variables governing tree water flow at higher spatial and temporal resolutions.
... The standard approach is to determine the conducting capacity of the ensemble of vascular conduits within the measured segment and thus the ability of the measured segment to supply downstream regions of the plant with water (Sperry et al., 1988a). The hydraulic conductivity of an individual segment may change with time due to the cavitation of xylem conduits and any subsequent re®lling (Waring and Running, 1978;Milburn, 1979;Sperry, 1986;Sperry et al., 1988b;Pickard, 1989;Tyree and Yang, 1992;Edwards et al., 1994;Cochard et al., 1994;Magnani and Borghetti, 1995;Zwieniecki and Holbrook, 1998). Because cavitation and embolism repair take place at the level of individual vessels, understanding dynamic changes in conductivity requires methods that address the hydraulic properties of individual conduits. ...
Studies of the hydraulic properties of xylem vessels have been limited to measurements of whole plant or whole stem segments. This approach allows the longitudinal transport properties of the ensemble of vessels within a stem to be determined, but provides little information on radial transport. Here the xylem of Fraxinus americana L. has been examined using a new method that allows the transport properties of individual vessels to be examined. One goal of this study was to quantify transport parameters relevant to embolism repair. The longitudinal conductivity of vessel segments open at both ends (i.e. no end walls) agreed with values predicted by the Poiseuille equation. Radial specific conductance (conductance per unit area) was approximately six orders of magnitude lower than the longitudinal conductance of the vessel segment normalized by the cross‐sectional area of the vessel lumen. There was a step increase in the radial specific conductance of previously gas‐filled vessels when the delivery pressure exceeded 0.4 MPa. This is consistent with the idea that positive pressure, required for embolism repair, can be compartmentalized within a vessel if the bordered pit chambers are gas‐filled. The diffusion coefficient for the movement of gas from a pressurized air‐filled vessel was of the same order of magnitude as that for air diffusing through water (1.95 e ⁻⁹ m ² s ⁻¹ ). Estimates of the time needed to displace all of the gas from an air‐filled vessel were in the order of 20 min, suggesting that gas removal may not be a major limitation in embolism repair.
... In plants, xylem hydraulic conductance recovery has two possible mechanisms: xylem refilling, which typically refills embolised conduits within hours or days in angiosperms (Bucci et al. 2003;Salleo et al. 2004); xylem repair, as the growth of a new ring (Brodribb and Cochard 2009); both can be common mechanisms in P. halepensis (De Luis et al. 2011). Due to the torus-margo complex in conifers, whether tracheids can be refilled after widespread cavitation is still a controversial issue (Sobrado et al. 1992;Edwards et al. 1994). Recent studies have suggested that the tracheid embolism is non-reversible after drought (Brodribb and Cochard 2009), but needs to be explored for P. halepensis in particular. ...
... Angiosperms are generally considered to have lower hydraulic safety margins but also a greater capacity to recover from droughtinduced embolism than conifers (Meinzer et al. 2009, Choat et al. 2012, Johnson et al. 2012. Nevertheless, evidence of embolism repair has been observed in several conifers ( Borghetti et al. 1991, Edwards et al. 1994, McCulloh et al. 2011, including Sequoia (Litvak et al. 2011), indicating that traits influencing embolism avoidance and repair may not be strictly limited by phylogeny. ...
We compared the physiology and growth of seedlings originating from different Sequoia sempervirens (D. Don.) Endl. (coast redwood) and Sequoiadendron giganteum (Lindl.) Buchh. (giant sequoia) populations subjected to progressive drought followed by a recovery period in a controlled greenhouse experiment. Our objective was to examine how multiple plant traits interact to influence the response of seedlings of each species and seed population to a single drought and recovery cycle. We measured soil and plant water status, leaf gas exchange, stem embolism and growth of control (well-watered) and drought-stressed (water withheld) seedlings from each population at the beginning, middle and end of a 6-week drought period and again 2 weeks after re-watering. The drought had a significant effect on many aspects of seedling performance, but water-stressed seedlings regained most physiological functioning by the end of the recovery period. Sequoiadendron seedlings exhibited a greater degree of isohydry (water status regulation), lower levels of stem embolism, higher biomass allocation to roots and lower sensitivity of growth to drought compared with Sequoia. Only minor intra-specific differences were observed among populations. Our results show that seedlings of the two redwood species exhibit contrasting drought-response strategies that align with the environmental conditions these trees experience in their native habitats, and demonstrate trade-offs and coordination among traits affecting plant water use, carbon gain and growth under drought.
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... Can axial parenchyma account for the reversal of embolisms, or conceivably even the prevention of embolisms, in associated tracheary elements? These functions have repeatedly been claimed to have experimental support (Braun, 1970(Braun, , 1984Salleo & Lo Gullo, 1989, 1993Edwards et al., 1994;Salleo et al., 1996;Trifilo et al., 2004;Salleo, Trifilo & Lo Gullo, 2006;Holbrook & Zwieniecki, 1999;Holbrook, Zwieniecki & Melcher, 2002;Zwieniecki & Holbrook, 2009;Brodersen & McElrone, 2013). Phloem may also be involved (Trifilo et al., 2004;, as may bordered pit structures of tracheary elements (Zwieniecki & Holbrook, 2000). ...
The diversity of expression in axial parenchyma (or lack of it) in woods is reviewed and synthesized with recent work in wood physiology, and questions and hypotheses relative to axial parenchyma anatomy are offered. Cell shape, location, abundance, size, wall characteristics and contents are all characteristics for the assessment of the physiological functions of axial parenchyma, a tissue that has been neglected in the consideration of how wood histology has evolved. Axial parenchyma occurrence should be considered with respect to mechanisms for the prevention and reversal of embolisms in tracheary elements. This mechanism complements cohesion–tension-based water movement and root pressure as a way of maintaining flow in xylem. Septate fibres can substitute for axial parenchyma (‘axial parenchyma absent’) and account for water movement in xylem and for the supply of carbohydrate abundance underlying massive and sudden events of foliation, flowering and fruiting, as can fibre dimorphism and the co-occurrence of septate fibres and axial parenchyma. Rayless woods may or may not contain axial parenchyma and are informative when analysing parenchyma function. Interconnections between ray and axial parenchyma are common, and so axial and radial parenchyma must be considered as complementary parts of a network, with distinctive but interactive functions. Upright ray cells and more numerous rays per millimetre enhance interconnection and are more often found in woods that contain tracheids. Vesselless woods in both gymnosperms and angiosperms have axial parenchyma, the distribution of which suggests a function in osmotic water shifting. Water and photosynthate storage in axial parenchyma may be associated with seasonal changes and with succulent or subsucculent modes of construction. Apotracheal axial parenchyma distribution often demonstrates storage functions that can be read independently of osmotic water shifting capabilities. Axial parenchyma may serve to both enhance mechanical strength or, when parenchyma is thin-walled, as a tissue that adapts to volume change with a change in water content. Other functions of axial parenchyma (contributing resistance to pathogens; a site for the recovery of physical damage) are considered. The diagnostic features of axial parenchyma and septate fibres are reviewed in order to clarify distinctions and to aid in cell type identification. Systematic listings are given for particular axial parenchyma conditions (e.g. axial parenchyma ‘absent’ with septate fibres substituting). A knowledge of the axial parenchyma information presented here is desirable for a full understanding of xylem function. © 2015 The Linnean Society of London, Botanical Journal of the Linnean Society, 2015, 177, 291–321.
... Strains during stretching beyond the elastic limit are likely to weaken the chemical bonding of the membrane because it seems impossible that plants could repair their cellulose microfibrils within their dead tracheid cells. Even though conifers appear to go through embolism and refilling cycles under laboratory and field conditions (Edwards et al., 1994;Mayr et al., 2002;Domec et al., 2005), this elastic functioning of the membrane can explain the phenomenon of embolism fatigue (Hacke et al., 2001). Although bordered pit membranes deteriorated with age in one hardwood species (Sperry et al., 1991), our results suggest that between outer and inner sapwood at the base of the trunk of this coniferous species, pit membrane functioning was sustained for more than 35 years. ...
Every wood anatomist knows that the wood near the center of a tree (juvenile
wood) differs from the wood laid down at some distance from the pith (mature
wood), and that the wood produced during the spring (earlywood) differs from the
wood produced during the summer (latewood). There is a progressive increase in
the dimensions of the cells from inner to outer growth rings. These differences
affect the structure and function of the wood for water transport and mechanics.
However, why do trees produce different wood quality as a function of cambial
age? Is it as an adaptation to hydraulics or mechanical demands? No research has
been undertaken in this area, because of the historic lack of communication
between wood scientist and ecophysiologists, and because the hydraulic
architecture field had few insights to offer until its recent wave of increasing
sophistication. The chapters presented here are founded on these questions and
provide new concepts and understandings of the trade-off between hydraulic
properties and mechanical support in trees. We measured specific conductivity (ks)
and vulnerability to embolism (loss of k) to map tree hydraulic properties at
different vertical and radial locations in the trunk and branches. In addition, field
measurements, mechanical characteristics and anatomical features were
determined. To investigate a wide range of wood properties, this research was
conducted in two conifer species with contrasting amount of sapwood Douglas-fir
(Pseudotsuga menziesii Mirb.) and ponderosa pine (Pinusponderosa Dougi) and
within three different age-classes. In Douglas-fir, the differences in wood properties
from the pith to the bark, from the bottom to the top of a tree, and within earlywood
and latewood had more effect on hydraulic than on mechanical properties. In
ponderosa pine, change in wood properties did not affect the hydraulic
characteristics as much as in Douglas-fir. We showed that ponderosa pine sapwood
has so much potential storage of water that it can compensate and level off the
differences in water transport. Any change in wood density from pith to bark is
more reflective of the need to alter hydraulic efficiency than the need to increase
mechanical strength as trees grow.
... Predawn water potentials were still negative (about ±1 MPa) in the period when embolism was reversed in the xylem, and substantial refilling took place when no growth was apparent in apical twigs of previously-covered trees (Figs. 4, 8). Interpretation is difficult on how refilling may occur under these biophysical conditions (Borghetti et al. 1991; Edwards et al. 1994; Lewis et al. 1994). In hardwood species the reversal of xylem embolism is commonly associated with above or near atmospheric pressures in the xylem (Hacke and Sauter 1995) or the production of new xylem (Magnani and Borghetti 1995). ...
The present study was carried out to elucidate the response mechanisms of 50-year-old Pinus halepensis Mill. trees to a long-term and severe drought. The amount of water available to trees was artificially restricted for 12 months by covering the soil with a plastic roof. Over the short term a direct and rapid impact of drought was evident on the water relations and gas exchanges of trees: as the soil dried out in the Spring, there was a concurrent decrease of predawn water potential; transpiration was strongly reduced by stomatal closure. Seasonal changes in the water volume fractions of twig and stem xylem were observed and interpreted as the result of cavitation and refilling in the xylem. When droughted trees recovered to a more favourable water status, refilling of embolized xylem was observed; twig predawn water potentials were still negative in the period when the embolism was reversed in the twig xylem. A few months after the removal of the covering, no differences in whole plant hydraulic resistance were observed between droughted and control trees. Needle and shoot elongation and stem radial growth were considerably reduced in droughted trees; no strategy of trees to allocate carbon preferentially to the stem conducting tissues was apparent throughout the experiment. An after-effect of the drought on growth was observed.
... The observed differences of threshold between angiosperm and conifer trees may reflect the greater ability of vessel-bearing species to repair embolism, as reported in F. sylvatica (Holbrook and Zwieniecki 1999, Cochard et al. 2001, Bucci et al. 2003, Salleo et al. 2004), and, therefore, to cope with higher levels of embolism. In conifers, refilling of stem embolism has also been observed (Edwards et al. 1994, Sobrado et al. 1992, McCulloh et al. 2011) but embolism repair mostly occurred in distal organs (leaves and roots) for this taxa (Johnson et al. 2012). Moreover, the dynamics of gas exchange recovery in these species matches the rate of hydraulic repair due to xylem regrowth (Brodribb et al. 2010). ...
Hydraulic failure is one of the main causes of tree mortality in conditions of severe drought. Resistance to cavitation is known to be strongly related to drought tolerance and species survival in conifers, but the threshold of water-stress-induced embolism leading to catastrophic xylem dysfunction in angiosperms has been little studied. We investigated the link between drought tolerance, survival and xylem cavitation resistance in five angiosperm tree species known to have contrasting desiccation resistance thresholds. We exposed seedlings in a greenhouse to severe drought to generate extreme water stress. We monitored leaf water potential, total plant water loss rate, leaf transpiration, stomatal conductance and CO2 assimilation rate during drought exposure and after rewatering (recovery phase). The time required for the recovery of 50% of the maximum value of a given ecophysiological variable after rewatering was used to determine the critical water potential corresponding to the threshold beyond which the plant failed to recover. We also investigated the relationship between this potential and stem xylem cavitation resistance, as assessed from vulnerability curves. This minimum recoverable water potential was consistent between ecophysiological variables and varied considerably between species, from -3.4 to -6.0 MPa. This minimum recoverable water potential was strongly correlated with P50 and P88, the pressures inducing 50 and 88% losses of stem hydraulic conductance, respectively. Moreover, the embolism threshold leading to irreversible drought damage was found to be close to 88%, rather than the 50% previously reported for conifers. Hydraulic failure leading to irreversible drought-induced global dysfunction in angiosperm tree species occurred at a very high level of xylem embolism, possibly reflecting the physiological characteristics of their stem water-transport system.
... These species also showed the largest apparent hydraulic safety margins expressed as the difference between P 50 and the daily minimum stem water potential. While other studies have reported limits on xylem refilling following tension-induced embolism (Sobrado et al. 1992, Edwards et al. 1994, Tyree et al. 1999Hacke and Sperry 2003), the study of Ogasa et al. (2013) is among the first to have investigated multiple species in a systematic manner. The generality of the relationships reported by Ogasa et al. (2013) is not known. ...
... . 1, right-hand -2 T / r limit). Experiments on isolated stem segments under negative pressure in the laboratory have demonstrated refilling, but always within what we refer to here as the ' -2 T / r limit'. When conditions were altered so that refilling would not be expected, none was observed (Borghetti et al . 1991; Sobrado, Grace & Jarvis 1992; Edwards et al . 1994). In contrast, experiments on intact plants have suggested that embolism can be reversed when the ambient Y PX is more negative than the -2 T / r limit. The extreme of this novel refilling behaviour is no hysteresis in the vulnerability curve (Fig. 1 , dotted line, 'novel refilling'). The most extensive evidence is for L. nobilis (Salle ...
The ability of juvenile Laurus nobilis and Acer negundo plants to refill embolized xylem vessels was tested under conditions of soil drought when xylem sap pressure was substantially negative, thus violating the expected condition that pressure must rise to near atmospheric for refilling. Intact potted plants were dried to a stem water potential (ΣW) corresponding with approximately 80% loss of hydraulic conductivity (PLC) in shoots. Then plants were re-watered and kept at a less negative target ΨW for 1–48 h. The ΨW was measured continuously with stem psychrometers. Rewatered L. nobilis held at the target ΨW for 1 h showed no evidence for refilling unless ΨW was within a few tenths of a MPa of zero. In contrast, re-watered L. nobilis held for 24 and 48 h at water potentials well below zero showed a significant reduction in PLC. The recovery was highly variable, being complete in some stem segments, and scarcely evident in others. Embolism repair was accompanied by a significant but moderate decrease in the osmotic potential (Ψ) of the bulk xylem sap (Ψ = −67 kPa in recovering plants versus −31 kPa in controls). In contrast, embolized and re-watered A. negundo plants held for 24 h at target ΨW of −0·9 and −0·3 MPa showed no embolism reversal. The mechanism allowing L. nobilis plants to refill under negative pressure is unknown, but does not appear to operate in A. negundo, and is slower to act for drought-induced embolism than when embolism was artificially induced by air injection as previously shown for L. nobilis.
... For that species phloem transport appears to be essential to the refilling process, although the exact mechanism of refilling is unknown. Also unknown is the mechanism by which conifer tracheids can often reverse embolism even when the xylem appears to be under negative pressure (Borghetti et al. 1991; Grace 1993; Edwards et al. 1994). In contrast to embolism reversal studies, several seasonal studies of embolism in woody angiosperms suggest that in some species once embolism occurs in vessels, it will result in permanent blockage, with new wood production as the only mechanism to enhance conductivity (Sperry and Sullivan 1992; Cochard and Tyree 1994; Kolb and Davis 1994; Sperry et al. 1994). ...
Pre-dawn xylem pressures were measured with bubble manometers attached near the stem bases of 32 species of vines on Barro
Colorado Island, Panama, to determine if pressures were sufficient to allow for possible refilling of embolized vessels. Of
29 dicotyledonous species 26 exhibited only negative xylem pressures, even pre-dawn during the wet season. In contrast, three
members of the Dilleniaceae exhibited positive pre-dawn xylem pressures, with a maximum of 64 kPa in Doliocarpusmajor. A pressure of 64 kPa is sufficient to push water to a height of 6.4 m against gravity, but the specimens reached heights
of 18 m. Thus, in all 29 dicotyledons examined, the xylem pressures were not sufficient to refill embolized vessels in the
upper stems. In contrast, two of the smaller, non-dicotyledonous vines, the climbing fern Lygodiumvenustrum and the viny bamboo Rhipidocladumracemiflorum, had xylem pressures sufficient to push water to the apex of the plants. Therefore, a root pressure mechanism to reverse
embolisms in stem xylem could apply to some but not to most of the climbing plants that were studied.
... To our knowledge, refilling of vessels in intact branches has not been studied before, although there are numerous reports on recovery of hydraulic conductivity in isolated stem segments (Just and Sauter 1991;Edwards et al. 1994, and literature cited therein). A pressure of 20 kPa led to a sharp increase in k h. ...
Xylem embolism in winter and spring as well as the occurrence of positive xylem pressure were monitored in several diffuse-porous and one ring-porous tree species (Fraxinus excelsior). In Acer pseudoplatanus and Betula pendula embolism reversal was associated with positive (above-atmospheric) xylem pressures that frequently occurred during a 2-month period prior to leaf expansion. In Acer high stem pressures were occasionally triggered on sunny days after a night frost. The other species investigated showed no positive xylem pressure during the monitoring period in 1995. Populus balsamifera exhibited a complete embolism reversal in 1994, but, like Fagus sylvatica, recovery was slow and incomplete in 1995. Fraxinus did not refill embolized vessels, but relied entirely on the production of new earlywood conduits in May. Populus canadensis Moench robusta did not recover from embolism during the monitoring period. Under a simulated root pressure of 20 kPa however, excised branches of Populus canadensis restored maximum hydraulic conductance within 2 days, illustrating the great influence of even small positive pressures on cnductivity recovery in spring. In the absence of positive pressure there was no substantial refilling of embolized vessels within a rehydration period of 9 days.
... The mechanisms responsible for vessel refilling when P x is negative in surrounding vessels are unknown. Although previous work has shown that living cells are not likely to be involved in embolism refilling in conifers (Borghetti et al. 1991; Edwards et al. 1994), more recent studies suggest that living xylem parenchyma surrounding cavitated vessels might play a role in vessel refilling (Zwieniecki and Holbrook 1998; Holbrook and Zwieniecki 1999). The ability of R. mangle to refill embolized vessels could also result from the high molecular weight mucopolysaccharides that have been previously observed within intact xylem vessel lumens (Zimmermann et al. 1994). ...
Physiological traits related to water transport were studied in Rhizophora mangle (red mangrove) growing in coastal and estuarine sites in Hawaii. The magnitude of xylem pressure potential (P
x), the vulnerability of xylem to cavitation, the frequency of embolized vessels in situ, and the capacity of R. mangle to repair embolized vessels were evaluated with conventional and recently developed techniques. The osmotic potential of the interstitial soil water (πsw) surrounding the roots of R. mangle was c. –2.6±5.52×10–3 and –0.4±6.13×10–3 MPa in the coastal and estuarine sites, respectively. Midday covered (non-transpiring) leaf water potentials (ΨL) determined with a pressure chamber were 0.6–0.8 MPa more positive than those of exposed, freely-transpiring leaves, and osmotic potential of the xylem sap (πx) ranged from –0.1 to –0.3 MPa. Consequently, estimated midday values of P
x (calculated by subtracting πx from covered ΨL) were about 1 MPa more positive than ΨL determined on freely transpiring leaves. The differences in ΨL between covered and transpiring leaves were linearly related to the transpiration rates. The slope of this relationship was steeper for the coastal site, suggesting that the hydraulic resistance was larger in leaves of coastal R. mangle plants. This was confirmed by both hydraulic conductivity measurements on stem segments and high-pressure flowmeter studies made on excised leafy twigs. Based on two independent criteria, loss of hydraulic conductivity and proportions of gas- and liquid-filled vessels in cryo-scanning electron microscope (cryo-SEM) images, the xylem of R. mangle plants growing at the estuarine site was found to be more vulnerable to cavitation than that of plants growing at the coastal site. However, the cryo-SEM analyses suggested that cavitation occurred more readily in intact plants than in excised branches that were air-dried in the laboratory. Cryo-SEM analyses also revealed that, in both sites, the proportion of gas-filled vessels was 20–30% greater at midday than at dawn or during the late afternoon. Refilling of cavitated vessels thus occurred during the late afternoon when considerable tension was present in neighboring vessels. These results and results from pressure-volume relationships suggest that R. mangle adjusts hydraulic properties of the water-transport system, as well as the leaf osmotic potential, in concert with the environmental growing conditions.
... Recent studies have revealed that the rapid refilling of embolized conduits is common in both woody and herbaceous plants, even while tension is present in the xylem (Sobrado et al., 1992;Edwards et al., 1994).Salleo et al. (1996)demonstrated xylem refilling in Laurus nobilis L. stems within 20 min of induction of emboli using positive pressure. Refilling occurred while xylem pressure was below −1.0 MPa. ...
This review emphasizes recent developments and controversies related to the uptake, transport and loss of water by trees. Comparisons of the stable isotope composition of soil and xylem water have provided new and sometimes unexpected insights concerning spatial and temporal partitioning of soil water by roots. Passive, hydraulic redistribution of water from moister to drier portions of the soil profile via plant root systems may have a substantial impact on vertical profiles of soil water distribution, partitioning of water within and among species, and on ecosystem water balance. The recent development of a technique for direct measurement of pressure in individual xylem elements of intact, transpiring plants elicited a number of challenges to the century-old cohesion–tension theory. The ongoing debate over mechanisms of long-distance water transport has stimulated an intense interest in the phenomenon and mechanisms of embolism repair. Rather than embolism being essentially irreversible, it now appears that there is a dynamic balance between embolism formation and repair throughout the day and that daily release of water from the xylem via cavitation may serve to stabilize leaf water balance by minimizing the temporal imbalance between water supply and demand. Leaf physiology is closely linked to hydraulic architecture and hydraulic perturbations, but the precise nature of the signals to which stomata respond remains to be elucidated. When water transport in trees is studied at multiple scales from single leaves to the whole organism, considerable functional convergence in regulation of water use among phylogenetically diverse species is revealed.
... Predawn water potentials were still negative (about ±1 MPa) in the period when embolism was reversed in the xylem, and substantial refilling took place when no growth was apparent in apical twigs of previously-covered trees (Figs. 4, 8). Interpretation is difficult on how refilling may occur under these biophysical conditions (Borghetti et al. 1991;Edwards et al. 1994;Lewis et al. 1994). In hardwood species the reversal of xylem embolism is commonly associated with above or near atmospheric pressures in the xylem (Hacke and Sauter 1995) or the production of new xylem (Magnani and Borghetti 1995). ...
The present study was carried out to elucidate the response mechanisms of 50-year-old Pinus halepensis Mill. trees to a long-term and severe drought. The amount of water available to trees was artificially restricted for 12 months by covering the soil with a plastic roof. Over the short term a direct and rapid impact of drought was evident on the water relations and gas exchanges of trees: as the soil dried out in the spring, there was a concurrent decrease of predawn water potential; transpiration was strongly reduced by stomatal closure. Seasonal changes in the water volume fractions of twig and stem xylem were observed and interpreted as the result of cavitation and refilling in the xylem. When droughted trees recovered to a more favourable water status, refilling of embolized xylem was observed; twig predawn water potentials were still negative in the period when the embolism was reversed in the twig xylem. A few months after the removal of the covering, no differences in whole plant hydraulic resistance were observed between droughted and control trees. Needle and shoot elongation and stem radial growth were considerably reduced in droughted trees; no strategy of trees to allocate carbon preferentially to the stem conducting tissues was apparent throughout the experiment. An after-effect of the drought on growth was observed.
... Strains during stretching beyond the elastic limit are likely to weaken the chemical bonding of the membrane because it seems impossible that plants could repair their cellulose microfibrils within their dead tracheid cells. Even though conifers appear to go through embolism and refilling cycles under laboratory and field conditions (Edwards et al., 1994; Mayr et al., 2002; Domec et al., 2005), this elastic functioning of the membrane can explain the phenomenon of embolism fatigue (Hacke et al., 2001). Although bordered pit membranes deteriorated with age in one hardwood species (Sperry et al., 1991), our results suggest that between outer and inner sapwood at the base of the trunk of this coniferous species, pit membrane functioning was sustained for more than 35 years. ...
The air-seeding hypothesis predicts that xylem embolism resistance is linked directly to bordered pit functioning. We tested this prediction in trunks, roots, and branches at different vertical and radial locations in young and old trees of Pseudotsuga menziesii. Dimensions of bordered pits were measured from light and scanning electron micrographs, and physiological data were from published values. Consistent with observations, calculations showed that earlywood tracheids were more resistant to embolism than latewood tracheids, mainly from earlywood having stretchier pit membranes that can distend and cover the pit aperture. Air seeding that occurs in earlywood appears to happen through gaps between the torus edge and pit border, as shown by the similar calculated pressures required to stretch the membrane over the pit aperture and to cause embolism. Although bordered pit functioning was correlated with tracheid hydraulic diameter, pit pore size and above all pit aperture constrained conductivity the most. From roots to branches and from the trunk base to higher on the trunk, hydraulic resistance of the earlywood pit membrane increased significantly because of a decrease in the size of the pit aperture and size and number of margo pores. Moreover, overall wood conductivity decreased, in part due to lower pit conductivity and a decrease in size and frequency of pits. Structural and functional constraints leading to the trade-off of efficiency against safety of water transport were also demonstrated at the individual pit level, with a positive correlation between pit membrane resistance on an area basis and the pressure differential required to cause membrane stretching, a characteristic that is essential for pit aspiration.
... A number of studies have observed loss of hydraulic conductivity in species with narrow conduits ( < 44 µ m) exposed to repeated freeze – thaw cycles ( Sperry and Sullivan, 1992 ; Sperry et al., 1994 ; Mayr et al., 2003a Mayr et al., , b , 2006 ) or when the thaw was accompanied by severe water stress ( Langan et al., 1997 ; Pittermann and Sperry, 2006 ). Regardless of whether embolism is drought-induced or formed because of a freeze – thaw cycle, it is well established that plants can refi ll these nonfunctional conduits when the xylem pressure is negative but close to 0 MPa (e.g., Sobrado et al., 1992 ; Edwards et al., 1994 ). To shrink a bubble and refi ll a conduit, the pressure in the xylem ( P x ) surrounding the bubble must be > − 2 T / r b, as defi ned by La Place ' s law ( Yang and Tyree, 1992 ), where T is the surface tension of water (0.0728 Pa m) and r b is the radius of the air bubble , which in an embolized tracheid is approximately the radius of the tracheid ( Tyree and Zimmermann, 2002 ). ...
The Pacific Northwest of North America experiences relatively mild winters and dry summers. For the tall coniferous trees that grow in this region, we predicted that loss in the hydraulic conductivity of uppermost branches would be avoided because of difficulty reversing accumulated emboli in xylem that is always under negative pressure.
To test this hypothesis, we measured native percent loss in hydraulic conductivity (PLC; the decrease of in situ hydraulic conductivity relative to the maximum) monthly throughout 2009 in branches at the tops (∼50 m) of four species in an old growth forest in southern Washington.
Contrary to our prediction, freeze-thaw cycles resulted in considerable native PLC. Branches showed hydraulic recovery in the spring and after a moderate increase in native embolism that was observed after an unusually hot period in August. The September recovery occurred despite decreases in the leaf and stem water potentials compared to August values.
Recoveries in branches of these trees could not have occurred by raising the water potential enough to dissolve bubbles simply by transporting water from roots and must have occurred either through water absorption through needles and/or refilling under negative pressure. Excluding the August value, native embolism values correlated strongly with air temperature of the preceding 10 d. For three species, we found that branches with lower wood density had higher specific conductivity, but not greater native PLC than branches with higher wood density, which calls into question whether there is any hydraulic benefit to higher wood density in small branches in those species.
... Measured rates of basal area growth in C. rhomboidea after drought were capable of accounting for most of the observed recovery of hydraulic conductance and gas exchange, as demonstrated by a model of hydraulic recovery predicted by area growth (Fig. 7). This is an important result because controversy remains about whether tracheids are able to be refilled after cavitation (Sobrado et al., 1992; Edwards et al., 1994). Our results suggest that tracheid embolism in Callitris is nonreversible after drought, probably because of the irreversible aspiration of the torus–margo pit structure (Utsumi et al., 2003). ...
• Motivated by the urgent need to understand how water stress-induced embolism limits the survival and recovery of plants during drought, the linkage between water-stress tolerance and xylem cavitation resistance was examined in one of the world's most drought resistant conifer genera, Callitris. • Four species were subjected to drought treatments of -5, -8 and -10 MPa for a period of 3-4 wk, after which plants were rewatered. Transpiration, basal growth and leaf water potential were monitored during and after drought. • Lethal water potential was correlated with the tension producing a 50% loss of stem hydraulic conductivity. The most resilient species suffered minimal embolism and recovered gas exchange within days of rewatering from -10 MPa, while the most sensitive species suffered major embolism and recovered very slowly. The rate of repair of water transport in the latter case was equal to the rate of basal area growth, indicating xylem reiteration as the primary means of hydraulic repair. • The survival of, and recovery from, water stress in Callitris are accurately predicted by the physiology of the stem water-transport system. As the only apparent means of xylem repair after embolism, basal area growth is a critical part of this equation.
... Winter freezethaw cycles commonly cause annual xylem cavitation in some conifers, however the cavitated tracheids refill by spring (Sparks and Black 2000, Sperry et al. 1994). Refilling has been demonstrated in detached segments in several conifer species (Edwards et al. 1994, Zwieniecki and Holbrook 1998); however, the mechanism has not been fully described (Holbrook and Zwieniecki 1999), and no comprehensive studies have been done on intact segments (see summary in Clearwater and Gold- stein [2005] ). The mechanisms currently hypothesized involve close proximity to either water-filled tracheids to supply water to the cavitated tracheid or close proximity to living parenchyma cells that can provide the energy to drive the refilling process (Holbrook and Zwieniecki 1999). ...
Current operational methods for predicting tree mortality from fire injury are regression-based models that only indirectly consider underlying causes and, thus, have limited generality. A better understanding of the physiological consequences of tree heating and injury are needed to develop biophysical process models that can make predictions under changing or novel conditions. As an illustration of the benefits that may arise from including physiological processes in models of fire-caused tree mortality, we develop a testable, biophysical hypothesis for explaining pervasive patterns in conifer injury and functional impairment in response to fires. We use a plume model to estimate vapor pressure deficits (D) in tree canopies during surface fires and show that D are sufficiently high to cause embolism in canopy branches. The potential implications of plume conditions and tree response are discussed.
... Refilling under lower pressures has been reported not only for the frozen xylem studies in corn and sunflower (McCully, Huang, and Ling, 1998), but for conifers (Edwards et al., 1994) and dicot trees (Salleo et al., 1996). These interesting findings need more confirmation and study, but do not by themselves require a new theory of water transport. ...
Canny's compensating pressure theory for water transport (American Journal of Botany 85: 897-909) has evolved from the premise that cavitation pressures are only a few tenths of a megapascal negative (approximately -0.3 MPa). In contradiction, "vulnerability curves" indicate that xylem pressures can drop below -3 MPa in some species without causing a loss of hydraulic conductivity. Canny claims these curves do not measure the limits to negative pressure by cavitation, but rather the limits to the compensating tissue pressure that otherwise quickly refills cavitated conduits. Compensating pressure is derived from the turgor pressure of the living cells in the tissue. To test this claim, we compared vulnerability curves of Betula nigra stems given three treatments: (1) living control, (2) killed in a microwave oven, and (3) perfused with a -1.5 MPa (10% w/w) mannitol solution. According to Canny's theory, the microwaved and mannitol curves should show cavitation and loss of conductance beginning at approximately -0.3 MPa because in both cases, the turgor pressure would be eliminated or substantially reduced compared to controls. We also tested the refilling capability of nonstressed stems where compensating pressure would be in full operation and compared this with dead stems with no compensating pressure. According to Canny's interpretation of vulnerability curves, the living stems should refill within 5 min. Results failed to support the compensating tissue theory because (a) all vulnerability curves were identical, reaching a -1.5 MPa threshold before substantial loss of conductance occurred, and (b) killed or living stems had equally slow refilling rates showing no significant increase in conductivity after 30 min. In consequence, the cohesion theory remains the most parsimonious explanation of xylem sap ascent in plants.
... The standard approach is to determine the conducting capacity of the ensemble of vascular conduits within the measured segment and thus the ability of the measured segment to supply downstream regions of the plant with water (Sperry et al., 1988a). The hydraulic conductivity of an individual segment may change with time due to the cavitation of xylem conduits and any subsequent re®lling (Waring and Running, 1978; Milburn, 1979; Sperry, 1986; Sperry et al., 1988b; Pickard, 1989; Tyree and Yang, 1992; Edwards et al., 1994; Cochard et al., 1994; Magnani and Borghetti, 1995; Zwieniecki and Holbrook, 1998). Because cavitation and embolism repair take place at the level of individual vessels, understanding dynamic changes in conductivity requires methods that address the hydraulic properties of individual conduits. ...
Studies of the hydraulic properties of xylem vessels have been limited to measurements of whole plant or whole stem segments. This approach allows the longitudinal transport properties of the ensemble of vessels within a stem to be determined, but provides little information on radial transport. Here the xylem of Fraxinus americana L. has been examined using a new method that allows the transport properties of individual vessels to be examined. One goal of this study was to quantify transport parameters relevant to embolism repair. The longitudinal conductivity of vessel segments open at both ends (i.e. no end walls) agreed with values predicted by the Poiseuille equation. Radial specific conductance (conductance per unit area) was approximately six orders of magnitude lower than the longitudinal conductance of the vessel segment normalized by the cross-sectional area of the vessel lumen. There was a step increase in the radial specific conductance of previously gas-filled vessels when the delivery pressure exceeded 0.4 MPa. This is consistent with the idea that positive pressure, required for embolism repair, can be compartmentalized within a vessel if the bordered pit chambers are gas-filled. The diffusion coefficient for the movement of gas from a pressurized air-filled vessel was of the same order of magnitude as that for air diffusing through water (1.95 e(-9) m(2) s(-1)). Estimates of the time needed to displace all of the gas from an air-filled vessel were in the order of 20 min, suggesting that gas removal may not be a major limitation in embolism repair.
... During this time of the year, both shrub species experienced near zero water potentials. Further, no remarkable difference in conduit diameter exists between Sorbus and Sambucus (Vogt, 1999) that would explain differences in embolism removal (Yang and Tyree, 1992; Edwards et al., 1994). Species-speci®c differences in wood structure such as the interaction of xylem parenchyma, vessel wall chemistry and the geometry of intervessel pits as considered earlier (Holbrook and Zwieniecki, 1999), or a metabolic control of re®lling (Salleo et al., 1996) may explain species-speci®c differences in re®lling. ...
Differences in the seasonal variation in stem water potential between the two shrub species Sorbus aucuparia and Sambucus nigra were related with their vulnerability to xylem cavitation. It was also demonstrated indirectly that the two species differ
in the extent to which they reverse cavitation. Seasonal variation in stem water potential was investigated during three growing
seasons with in situ stem psychrometers. Sorbus experienced wide water potential variations and reached a minimum of −4.2 MPa during drought. Under the same microclimatic
conditions, Sambucus experienced consistent stem water potentials with a minimum of −1.7 MPa. The relationship between percentage loss in hydraulic
conductivity (PLC) and water potential (hydraulic vulnerability curve) of the two species differed in shape: a flat curve
with nearly total loss of conductivity at −6 MPa was found for Sorbus. Sambucus showed a steep vulnerability curve with 90% loss conductivity at −2.2 MPa. Thus, Sambucus is extremely vulnerable to cavitation, but Sorbus is an almost invulnerable species. This different cavitation resistance adjusted the ranges of field stem water potential
that the species experienced. Finally, seasonal courses of naturally occurring (native) embolism were compared with calculated
PLC courses. This comparison indicates that Sorbus did not refill embolized xylem vessels whereas Sambucus reversed embolism. It was concluded that species which are highly vulnerable to cavitation and drought‐induced embolism need
refilling of embolized vessels as well as isohydric water potential patterns as two strategies of survival.
... Water content has a considerable effect on the permeability of wood (e.g., Edwards et al. 1994). Nikinmaa et al. (1997) reported a considerable wood water content variation in Scots pine during summer and also demonstrated its effect on conductivity. ...
A dynamic model for simulating water flow in a Scots pine (Pinus sylvestris L.) tree was developed. The model is based on the cohesion theory and the assumption that fluctuating water tension driven by transpiration, together with the elasticity of wood tissue, causes variations in the diameter of a tree stem and branches. The change in xylem diameter can be linked to water tension in accordance with Hookeâ s law. The model was tested against field measurements of the diurnal xylem diameter change at different heights in a 37-year-old Scots pine at Hyytiälä, southern Finland (61 degrees 51' N, 24 degrees 17' E, 181 m a.s.l.). Shoot transpiration and soil water potential were input data for the model. The biomechanical and hydraulic properties of wood and fine root hydraulic conductance were estimated from simulated and measured stem diameter changes during the course of 1 day. The estimated parameters attained values similar to literature values. The ratios of estimated parameters to literature values ranged from 0.5 to 0.9. The model predictions (stem diameters at several heights) were in close agreement with the measurements for a period of 6 days. The time lag between changes in transpiration rate and in sap flow rate at the base of the tree was about half an hour. The analysis showed that 40% of the resistance between the soil and the top of the tree was located in the rhizosphere. Modeling the water tension gradient and consequent woody diameter changes offer a convenient means of studying the link between wood hydraulic conductivity and control of transpiration.
... The warm and rainy weather situation before the second sampling probably provided optimal conditions for such a process. Refilling of embolized conduits –– even under negative potentials –– was published, e.g. for Pinus sylvestris (Borghetti et al. 1991, Sobrado et al. 1992, Edwards et al. 1994), for Abies lasiocarpa, Larix laricina, and Picea glauca (Sperry et al. 1994) and Picea rubens (Zwiniecki and Holbrook 1998). Embolism of the observed extent is certainly costly, as trees have to reactivate water transport after the winter season to maintain vitality and growth. ...
At the timberline in the Central Alps, climatic conditions during winter frequently cause excessive drought stress (frost drought, 'Frosttrocknis'), which we hypothesized to induce cavitation in trees. We investigated the extent of winter-embolism in Norway spruce (Picea abies (L.) Karst.) growing near the timberline and analysed adaptations in vulnerability and anatomy. We found conductivity losses of up to 100% at the highest elevation (2020 m) correlated with low water potentials down to - 4.0 MPa. Vulnerability thresholds (50% loss in conductivity) decreased from - 3.39 MPa at 800 m to - 3.88 MPa at 1600 m corresponding to a decrease in tracheid cross-sectional area as well as pit and pit pore diameters. These thresholds were lower than potentials measured in embolized twigs near the timberline at the sampling dates probably due to lower potentials and/or a role of freeze-thaw events earlier in winter. Data indicated refilling processes, which may be of particular relevance for trees at the timberline, since adaptations in drought-induced vulnerability failed to prevent winter-embolism.
... There is much empirical evidence that the water content of the sapwood changes seasonally (Chalk & Bigg, 1956;Waring & Running, 1978;Borghetti & Vendramin, 1987) and that such changes are accompanied by changes in the hydraulic conductivity of the sapwood (Tyree & Yang, 1992;Sobrado et al., 1992;Salleo et al., 1996;Edwards et al., 1994). An embolism is an obstruction to the flow of sap. ...
The theory of tree water flow proposed in Aumann & Ford (submitted) is assessed by numerically solving the model developed from this theory under a variety of functional parameterizations. The unknown functions in this nonlinear partial differential equation model are determined using a tracheid-level model of water flow in a block of Douglas fir tracheids. The processes of flow, cavitation, pit aspiration/deaspiration, flow through the cell wall and ray exudation in a block of approximately 79 000 tracheids are modeled. Output from the tracheid model facilitates determination of the hydraulic conductivities in the sapwood as a function of saturation and interfacial area between liquid and gaseous phases of water, the function governing the rate of change in saturation, and the function governing the rate of change in interfacial area. The models show complementary things. The tracheid model shows that capacitance, or the change in saturation per change in pressure, is not constant. When all refilling is stopped, it takes over 180 days for the hydraulic conductivity in the vertical direction to reach 1/4 of its maximal value, showing the robustness of the transpiration stream for conducting water. The shape of the functions determined with the tracheid model change with different tracheid-level assumptions. When these functions are used in the differential equation model, it is shown that cell-wall conductivity plays an important part in the lag in flow observed in many conifers. The flow velocities and rates of change in saturation predicted by the differential equation model agree with those measured in Douglas fir. Both models support the theory of tree water flow presented in Aumann & Ford (submitted) and undermine the theory that water flow in trees is analogous to the flow of current in electric circuits.
... Recovery of embolized vessels has been observed in some tree species including sugar maple (Acer saccharum Marsh.) under slight positive pressure (Tyree and Yang 1992) and Scotch pine (Pinus sylvestris L.) (Borghetti et al. 1991, Sobrado et al. 1992, Edwards et al. 1994). Sapwood cross-sectional area is a simple biometric parameter widely used for scaling transpiration data between measurement points and trees and between trees and forest stands. ...
Variations in radial patterns of xylem water content and sap flow rate were measured in five laurel forest tree species (Laurus azorica (Seub.) Franco, Persea indica (L.) Spreng., Myrica faya Ait., Erica arborea L. and Ilex perado Ait. ssp. platyphylla (Webb & Berth.) Tutin) growing in an experimental plot at Agua García, Tenerife, Canary Islands. Measurements were performed around midday during warm and sunny days by the heat field deformation method. In all species, water content was almost constant (around 35% by volume) over the whole xylem cross-sectional area. There were no differences in wood color over the whole cross-sectional area of the stem in most species with the exception of E. arborea, whose wood became darker in the inner layers. Radial patterns of sap flow were highly variable and did not show clear relationships with tree diameter or species. Sap flow occurred over the whole xylem cross-sectional area in some species, whereas it was limited to the outer xylem layers in others. Sap flow rate was either similar along the xylem radius or exhibited a peak in the outer part of the xylem area. Low sap flow rates with little variation in radial pattern were typical for shaded suppressed trees, whereas dominant trees exhibited high sap flow rates with a peak in the radial pattern. Stem damage resulted in a significant decrease in sap flow rate in the outer xylem layers. The outer xylem is more important for whole tree water supply than the inner xylem because of its larger size. We conclude that measurement of radial flow pattern provides a reliable method of integrating sap flow from individual measuring points to the whole tree.
... The severe stress treatment probably caused massive embolism in the xylem, yet the embolism must have dissipated quickly on return to low stress conditions. Similarly, Edwards et al. (1994) have shown that detached branch segments can recover quickly from embolism even when PWP is negative, and L.J. Heidmann (unpublished data) observed that ponderosa pine stressed to −6.3 MPa recovered to −0.3 MPa Figure 2. Predawn plant water potential over 28 days of unstressed (A), moderately drought stressed (B), and severely stressed (C) interior Douglas-fir seedlings subjected to a root temperature treatment of 10 (solid line), 20 (dashed line), or 28 °C (dotted line). Vertical bars are standard errors. ...
Container-grown quiescent Douglas-fir (Pseudotsuga menziesii var. glauca (Beissn.) Franco) seedlings were air dried to plant water potentials of –0.2, –2.2 or –3.8 MPa (unstressed, moderate, and
severe stress treatments, respectively). Trees from each treatment were either placed in root mist chambers held at 10, 20,
or 28 °C for 28 days and root growth potential (RGP) and plant water potential (PWP) measured weekly, or potted in a 1/1 mix
of peat and vermiculite, watered only once, and height growth and survival recorded after 10 weeks in an unheated greenhouse.
Root growth potential of unstressed trees was greater than that of moderately stressed trees at all temperatures. Root growth
potential of severely stressed trees was zero. Predawn plant water potentials of unstressed and moderately stressed trees
were initially high, fell to –0.5 to –0.8 MPa, and then increased. Predawn plant water potential of severely stressed trees
declined continuously over the 28-day experiment. Survival and height growth of the severely stressed trees were reduced compared
to the unstressed and moderately stressed trees. Among the root growth potential measurements, RGP measured after 7 days at
10 °C was most sensitive to drought stress history and revealed differences in vigor that were not apparent from the survival
and height growth data.
... Indirect evidence for refilling in other trees comes from fluctuations in relative water content (Chalk and Bigg 1957, Waring and Running 1978). In the laboratory, recovery has been observed, but only at very low xylem tensions (Dixon et al. 1984, Sobrado et al. 1992, Edwards et al. 1994 ). Holbrook (1995) suggests that seasonal refilling may be a feature of conifers, but not of other trees. ...
The natural abundance of stable carbon isotopes in the annual rings of forest trees is used as a tracer of environmental changes such as climate and atmospheric pollution. Although tree-ring delta(13)C varies by about 2 per thousand from year to year, variability within the foliage can be as high as 6 per thousand. Recent studies have shown that branch length affects stomatal response, which influences the integrated foliar delta(13)C signal. To improve the ability of delta(13)C to predict climate differences, we examined the relationship between branch length and foliar delta(13)C in Pseudotsuga menziesii (Mirb.) Franco from four sites across a steep climate gradient in Oregon. The transect spanned the boundary between the ranges of the coastal variety, P. menziesii var. menziesii (three sites), and the Rocky Mountain variety, P. menziesii var. glauca (one site). At the most maritime site, branch length explained 76% of within-site variation of 5 per thousand, whereas at the harshest site, branch length accounted for only 15% of this variation. We considered the possibility that cavitation in the water-conducting xylem obscures the branch length effect in the harsher climates. Cavitation, as measured by dye perfusion, was most extensive at sites where the branch length effect in the coastal variety was weakest. Trees at the site with the most substantial cavitation displayed seasonal xylem refilling. Branch length standardization significantly improved the relationship between delta(13)C and climate. With standardization to constant length, delta(13)C values were significantly related to the degree that climatic variables, as modeled with a forest growth simulation model, constrain transpiration (R(2) = 0.69, P < 0.0001). Without standardization, the R(2) was 0.27. We conclude that sampling standard length branches or tree rings from trees of similar shape and size is desirable when seeking correlations between isotopic composition and climate.
After drought-induced embolism and repair, tree xylem may be weakened against future drought events (cavitation fatigue). Since there are few data on cavitation fatigue in conifers available, we quantified vulnerability curves (VCs) after embolism/repair cycles on eight European conifer species. We induced 50 and 100% loss of conductivity (LC) with a cavitron, and analysed VCs. Embolism repair was obtained by vacuum infiltration. All species demonstrated complete embolism repair and a lack of any cavitation fatigue after 50% LC. After 100% LC, European larch (Larix decidua), stone pine (Pinus cembra), Norway spruce (Picea abies) and silver fir (Abies alba) remained unaffected, while mountain pine (Pinus mugo), yew (Taxus baccata) and common juniper (Juniperus communis) exhibited 0.4 to 0.9 MPa higher vulnerability to embolism. A small cavitation fatigue observed in Scots pine (Pinus sylvestris) was probably biased by incomplete embolism repair, as indicated by a correlation of vulnerability shifts and conductivity restoration. Our data demonstrate that cavitation fatigue in conifers is species-specific and depends on the intensity of preceding LC. The lack of fatigue effects after moderate LC, and relevant effects in only three species after high LC, indicate that conifers are relatively resistant against cavitation fatigue. This is remarkable considering the complex and delicate conifer pit architecture and may be important considering climate change projections.
This chapter focuses on the ecological and physiological significance of stem water storage. The basic components necessary to examine the contribution of stem water storage are straightforward and include: determination of water uptake from the soil, water loss by the entire canopy, and changes in stem water content. The water storage capacity of plant tissues is defined as the amount of water that can be withdrawn for a given change in driving force (water potential) and the structural features that influence the same is discussed. Environments in which periods of high soil water availability are unpredictable, infrequent, and of short duration represent conditions well suited to within-plant water storage provided that net carbon gain can be sustained at very low total water loss rates. In most plants, stem water storage appears to be most important in enabling them to survive periods of drought. In addition, stem water storage may provide a strategic reserve during limited periods of adverse environmental conditions (e.g., giant rosette plants, dry-season flowering in tropical trees). Understanding the temporal dynamics of stem water utilization requires that it be examined in the context of stomatal behavior, roofing patterns, and stem hydraulic conductivity. Because of its close proximity to the transpiring surfaces, coordination between the hydraulics and patterns of water use are necessary to prevent the depletion of stem water stores prior to the onset of extreme conditions.
The productivity of plants depends on a continuous supply of water to the photosynthetic tissue. Without a water supply, the tissue could not access CO2 through open stomata without desiccation. Maintaining a water supply line requires, among other things, maintaining water as a liquid under pressures below vapour pressure. Water in this metastable condition is potentially vulnerable to the nucleation of the vapour phase, a process called ‘cavitation’. Once cavitation occurs, a vapour void expands to fill the xylem conduit and the conduit becomes ‘embolized’ as air diffuses in from surrounding tissue. The gas blockage is confined to a single conduit because the gas-water interface is trapped by meniscal forces in the mesh-like structure of the interconduit pit membranes. Extensive cavitation reduces the hydraulic conductance of the xylem and increases the water stress on the foliage under transpirational conditions.
Woody plants such as trees have a significant economic and climatic influence on global economies and ecologies. This completely revised classic book is an up-to-date synthesis of the intensive research devoted to woody plants published in the second edition, with additional important aspects from the authors' previous book, Growth Control in Woody Plants. Intended primarily as a reference for researchers, the interdisciplinary nature of the book makes it useful to a broad range of scientists and researchers from agroforesters, agronomists, and arborists to plant pathologists and soil scientists. This third edition provides crutial updates to many chapters, including: responses of plants to elevated CO2; the process and regulation of cambial growth; photoinhibition and photoprotection of photosynthesis; nitrogen metabolism and internal recycling, and more. Revised chapters focus on emerging discoveries of the patterns and processes of woody plant physiology. * The only book to provide recommendations for the use of specific management practices and experimental procedures and equipment * Interdisciplinary approach will appeal to a broad range of scientists, researchers, and growers * Thoroughly updated with the latest research devoted to woody plants.
Abstract
Key message
Pine mortality was related to water stress, which caused xylem cavitation. Hydraulic failure and carbon starvation are likely interrelated, and bark beetles attacks did not seem to be directly involved.
Abstract
Forests are extremely important for society given the many services they provide. Climate models reflect increases in temperature and less annual rainfall, which will generate hotter drier environments. Under these conditions, it is predicted that forest ecosystems will be severely affected, and recent studies have accumulated evidence for drought-induced tree mortality. Consequently, many studies have attempted to explain mechanisms of survival and mortality in forest species. However, the physiological mechanisms that underlie drought mortality are not completely understood. The aim of the present study was to analyse the effect of an extremely dry year on the cause of mortality of pines and on forest decline in pine forest populations in southeast Spain. Specifically, we studied the effect of drought stress that caused pine mortality, dynamics of carbohydrates reserves and bark beetle attack. The results suggest that pine mortality can be attributed to an intense drought stress level that caused xylem cavitation. The results also indicate that hydraulic failure and carbon starvation are likely interrelated, which makes separating both mechanisms very difficult. Finally, the recorded bark beetles attack did not seem to be directly involved in mortality, at least not in the forests with less intense drought conditions.
Keywords
Pine mortality Xylem cavitation Carbohydrates Bark beetle infestation Drought Temperature anomalies
This chapter reviews how hydraulic architectures of tropical trees and lianas (woody vines) influence the flow of water from roots to leaves. The hydraulic design potentially can limit plant water relations, gas exchange, successional distribution, and even the maximum height (or length, in the case of lianas) that a species can attain. Important parameters include vulnerability to drought-induced cavitation (since embolism reduces hydraulic conductance), root pressures (since these potentially could result in re-filling of conduits following cavitation events, thereby increasing conductance), leaf specific conductivity (which, together with transpiration rates, can predict pressure gradients throughout the plant), and water storage capacity (since this might determine the ability to survive water shortage). Some of the issues that are dealt with here are the impact of vessel diameter on drought- and freezing-induced embolism, the role of root pressures in the occasional removal of embolisms, and the ways in which the hydraulic architecture differs in different growth forms such as trees, shrubs, lianas, and hemiepiphytes. The ecological and physiological trade-offs of different architectures are discussed, and comparisons are made with temperate plants.
Tree distribution could be highly affected by climate change. Results of paleogeographic studies showed that tree distribution ranges have already shifted with past climate changes. These data are currently used to model the evolution of species distribution in response to global warming. However, the ecological context in which species have to cope with climate change is very different than the past one: the current increase of temperature occurs faster than the past global warming, the areas being likely colonized are covered by various ecosystems (forests, agricultural surfaces, urban areas). So will tree species be able to cope with the current global change? Will they be able to migrate to find more favourable conditions or to survive to drier environmental conditions? Firstly, the analysis of historical data (French National Forest Office and Spanish National Forest Inventories) allowed determining colonization and extirpation events, and quantifying migration rates of tree species populations situated at the edges or the core of their distribution range. We evidenced that Q. ilex has substantially colonized new areas at its northern margin during the last 130 years, confirming the model trends. However, the colonization rates of Q. ilex are much lower than the shift of its bioclimate predicted by bioclimatic models. Species located at their rear edge showed higher upward shifts than other species located at the core of their range. To conclude, our results showed that global change have already impacted tree distribution although a time-lag between forest species migration responses and their bioclimate shift. Water stress is the main factor explaining tree dieback when water is limited and so particularly at the warm limit of tree species distribution range. Therefore, we studied drought resistance and its mechanisms in angiosperm tree species. Our results showed that embolism threshold of 90% leads to irreversible damages and tree death by dehydration. This threshold is considerably higher than the observed in Conifers. The study of hydraulic functioning of co-occurring oaks showed that the survival of Q. robur could be threatened in the context of increasing drought in the Atlantic forests because of its functioning at high levels of embolism. On the contrary, Q. ilex presented negligible levels of embolism in the same study area. The migration rates form primordial empirical data that give us information about tree effective migration abilities. They could be integrated within vegetation distribution models as well as embolism thresholds leading to tree mortality.
Evidence is fast accumulating that some form of refilling mechanism does operate in the xylem of some species. If it is a common phenomenon, refilling under tension has important implications for our understanding of long distance transport in plants. The involvement of living cells suggests that some plants can exert a degree of active control over the hydraulic properties of their xylem. Instead of being an irreversible dysfunction, variation in conductance caused by cavitation may be part of important regulatory mechanisms. The hydraulic conductance of the xylem in species exhibiting refilling may be a dynamic balance between embolism formation and repair that varies throughout the day in response to changes in xylem tension and the vigor of the refilling mechanism. In many species stomatal conductance is closely coordinated with the hydraulic conductance of the soil to leaf pathway. Transpiration is usually regulated in a way that allows maximum xylem tension to approach the threshold at which significant cavitation occurs. This fine balance between normal xylem tension and the loss of conductivity suggests a functional role for cavitation as part of a feedback mechanism linking stomatal regulation to hydraulic conductance and plant water status. A sensitive signaling mechanism linked directly to the onset of hydraulic failure in the xylem would integrate aspects of both the supply and demand for water at the leaf surface, allowing the plant to maintain maximum rates of photosynthesis and respond quickly to short-term changes in evaporative demand.
Hydraulic architecture prescribes water flow in plants and is, therefore, fundamental to many areas of plant physiology. It is usually analysed destructively, or on excised material. A method is explored here based on displacement transducers for the continuous, nondestructive assessment of functional hydraulic connections within the intact plant. The graft union was chosen as a test system. The technique involves repeated application of water at some point in the system, while simultaneously observing patterns of swelling (increase in water status) at other points. Such patterns will reflect the hydraulic resistance of the intervening pathways.
It is demonstrated that the major hydraulic connections within the graft union of tomato become functional over a period of about 48 h from the fifth day after grafting. This is consistent with histological observations on the appearance of wound-xylem bridges at this time.
This approach could be useful for non-destructive monitoring of changes in hydraulic connections in various other intact systems, for example, during abscission, drought-induced embolism, or attack by vascular-wilt pathogens.
Comparison of the vascular anatomy of the earliest known vascular plants (Upper Silurian/ Lower Devonian) with the functional anatomy of extant vascular plants permits the following conclusions (excluding previous analyses of xylem conductivity and biomechanics). The absence of an endodermis from early vascular plants may have hindered the regulation of the supply of soil-derived nutrients to the shoot. The absence of intraxylary parenchyma in early vascular plants may have interfered with the differential distribution of soil-derived nutrients among aerial branches. The earliest vascular plants, like extant plants, lacked gas spaces in vascular tissues, so that the early plants could have shared with extant plants some protection from the impact of embolism of xylem and, less importantly, reduce O2 damage to ‘phloem’. Early vascular plants also lacked the lignified UV-B screen found around the phloem in some extant plants, although this was probably not a serious lack in their relatively short-lived, nucleate phloem cells. An early vascular plant with a main axis and laterals shares with extant plants a xylem constriction at the base of lateral branches, which favours survival of the main axis during water shortage.
Wood sections of eight species of angiosperm and gymnosperm were made and observed under microscope. When a dehydrated section was rewet, the air inside its conduits contracted under the force of surface tension for several seconds to form elongated or spherical bubbles. The elongated bubbles in smaller conduits shortened till vanished. In addition, we also discorved that bubbles in larger conduits extended at first, then collapsed and disappeared; the bubbles outside conduits appeared gradualy or popped up in the field of view one after another; for some samples, they originated mainly from the cross sections of the wood rays. The smaller ones also collapsed and the larger ones grew up gradually. We suspected that air might transfer from the bubbles with short radii to those with large radii, both inside and outside conduits. The calculation of the amount of gas in all bubbles in a field of view supported our hypothesis. There are two possible mechanisms to explain the phenomena. First, based on the capillay equation, air can move from a smaller bubble to a larger one. Another reason is that the dissolving air from smaller bubbles can enter into the adjacent bubbles with larger curvature radii. Gas movement should obey the same rules in living plants. Therefore, we suggest that after cavitation events, instead of air moving from xylem into ambient atmosphere, two mechanisms could induce air to transfer from smaller conduits into larger conduits or the regions with lower pressures, leading the embolized conduits in the smaller conduits to repair. Furthermore, the differnce of values of contact angles in conduits might promote the refilling of embolism at lower xylem pressure.
We investigated the potential links between stomatal control of transpiration and the risk of embolism in root and shoot xylem of seedlings of three Mediterranean conifers (Cupressus sempervirens, Pinus halepensis and P. nigra) grown in a greenhouse under semi-controlled conditions. We measured the intrinsic vulnerability to embolism in roots and current year shoots by the air injection method. Root and shoot segments were subjected to increasing pressures, and the induced loss of hydraulic conductivity recorded. The three species displayed very different vulnerabilities in shoots, with P. nigra being much more vulnerable than P. halepensis and C. sempervirens. Roots were distinctly more vulnerable than shoots in C. sempervirens and P. halepensis (50% loss of conductivity induced at 3.0 MPa and 1.7 MPa higher xylem water potential in roots vs shoots). In P. nigra, no significant difference of vulnerability between shoots and roots was found. Seedlings were subjected to soil drought, and stomatal conductance, twig hydraulic conductivity and needle water potential were measured. The water potential resulting in almost complete stomatal closure (90%) was very close to the threshold water potential inducing loss of conductivity (10%) in twigs in P nigra, resulting in a very narrow safety margin between stomatal closure and embolism induction. The safety margin was larger in P. halepensis and greatest in C. sempervirens. Unexpectedly, this water potential threshold produced a 30–50% loss of conductivity in 3–5 mm diameter roots, depending on the species. The implications of this finding are discussed.
Typescript (photocopy). Thesis (M.S.)--Oregon State University, 2000. Includes bibliographical references (leaves 83-88).
Embolism results in a dramatic loss of xylem hydraulic transport capacity that can lead to decreased plant productivity and even death. The ability to refill embolized conduits despite the presence of tension in the xylem seems to be widespread, but how this occurs is not known. To promote discussion and future research on this topic, we describe how we believe refilling under tension might take place. Our scenario includes: (i) an osmotic role for low-molecular weight sugars; (ii) an apoplastic sugar-sensing mechanism to activate refilling; (iii) the contribution of vapor transport in both the influx of water and removal of entrapped gases; and (iv) the need for a mechanism that can synchronize reconnection to the transpiration stream through multiple bordered pits.
Embolism and refilling of vessels was monitored directly by cryomicroscopy of field-grown corn (Zea mays L.) roots. To test the reliability of an earlier study showing embolism refilling in roots at negative leaf water potentials, embolisms were counted, and root water potentials (Psiroot) and osmotic potentials of exuded xylem sap from the same roots were measured by isopiestic psychrometry. All vessels were full at dawn (Psiroot -0.1 MPa). Embolisms were first seen in late metaxylem vessels at 8 AM. Embolized late metaxylem vessels peaked at 50% at 10 AM (Psiroot -0.1 MPa), fell to 44% by 12 PM (Psiroot -0.23 MPa), then dropped steadily to zero by early evening (Psiroot -0.28 MPa). Transpiration was highest (8.5 μg cm-2 s-1) between 12 and 2 PM when the percentage of vessels embolized was falling. Embolized vessels were refilled by liquid moving through their lateral walls. Xylem sap was very low in solutes. The mechanism of vessel refilling, when Psiroot is negative, requires further investigation. Daily embolism and refilling in roots of well-watered plants is a normal occurrence and may be a component of an important hydraulic signaling mechanism between roots and shoots.
Recovery of hydraulic conductivity after the induction of embolisms was studied in woody stems of laurel (Laurus nobilis). Previous experiments confirming the recovery of hydraulic conductivity when xylem pressure potential was less than -1 MPa were repeated, and new experiments were done to investigate the changes in solute composition in xylem vessels during refilling. Xylem sap collected by perfusion of excised stem segments showed elevated levels of several ions during refilling. Stem segments were frozen in liquid N2 to view refilling vessels using cryoscanning electron microscopy. Vessels could be found in all three states of presumed refilling: (a) mostly water with a little air, (b) mostly air with a little water, or (c) water droplets extruding from vessel pits adjacent to living cells. Radiographic probe microanalysis of refilling vessels revealed nondetectable levels of dissolved solutes. Results are discussed in terms of proposed mechanisms of refilling in vessels while surrounding vessels were at a xylem pressure potential of less than -1 MPa. We have concluded that none of the existing paradigms explains the results.
Freezing and thawing lead to xylem embolism when gas bubbles caused by ice formation expand during the thaw process. However, previous experimental studies indicated that conifers are resistant to freezing-induced embolism, unless xylem pressure becomes very negative during the freezing. In this study, we show that conifers experienced freezing-induced embolism when exposed to repeated freeze-thaw cycles and simultaneously to drought. Simulating conditions at the alpine timberline (128 days with freeze-thaw events and thawing rates of up to 9.5 K h(-1) in the xylem of exposed twigs during winter), young trees of Norway spruce [Picea abies (L.) Karst.] and stone pine (Pinus cembra L.) were exposed to 50 and 100 freeze-thaw cycles. This treatment caused a significant increase in embolism rates in drought-stressed samples. Upon 100 freeze-thaw cycles, vulnerability thresholds (50% loss of conductivity) were shifted 1.8 MPa (Norway spruce) and 0.8 MPa (stone pine) towards less negative water potentials. The results demonstrate that freeze-thaw cycles are a possible reason for winter-embolism in conifers observed in several field studies. Freezing-induced embolism may contribute to the altitudinal limits of conifers.
Xylem embolism, the reduction of water flow by air-filled vessels, was measured in a stand of 5- to 8-year-old sugar maple (Acer saccharum Marsh.) saplings growing in a nursery bed in northwestern Vermont. Embolism was quantified as percentage loss in hydraulic conductivity of trunk and branch segments relative to maximum values obtained by removing air from vessels by repeated high pressure (173 kPa) perfusions. Ten segments per tree were cut from 6 trees for each of 11 measurement periods spaced at roughly monthly intervals from May 1986 to June 1987. Journal Article
Xylem vessels in grapevines Vitis labrusca L. and Vitis riparia Michx. growing in New England contained air over winter and yet filled with xylem sap and recovered their maximum hydraulic conductance during the month before leaf expansion in late May. During this period root pressures between 10 and 100 kilopascals were measured. Although some air in vessels apparently dissolved in ascending xylem sap, results indicated that some is pushed out of vessels and then out of the vine. Air in the vessel network distal to advancing xylem sap was compressed at about 3 kilopascals; independent measurements indicated this was sufficient to push air across vessel ends, and from vessels to the exterior through dead vine tips, inflorescence scars, and points on the bark. Once wetted, vessel ends previously air-permeable at 3 kilopascals remained sealed against air at pressures up to 2 and 3 megapascals. Permeability at 3 kilopascals was restored by dehydrating vines below -2.4 megapascals. We suggest that the decrease in permeability with hydration is due to formation of water films across pores in intervascular pit membranes; this water seal can maintain a pressure difference of roughly 2 megapascals, and prevents cavitation by aspirated air at xylem pressures less negative than -2.4 megapascals.
We discuss the relationship between the dynamically changing tension gradients required to move water rapidly through the xylem conduits of plants and the proportion of conduits lost through embolism as a result of water tension. We consider the implications of this relationship to the water relations of trees. We have compiled quantitative data on the water relations, hydraulic architecture and vulnerability of embolism of four widely different species: Rhizophora mangle, Cassipourea elliptica, Acer saccharum, and Thuja occidentalis. Using these data, we modeled the dynamics of water flow and xylem blockage for these species. The model is specifically focused on the conditions required to generate ;runaway embolism,' whereby the blockage of xylem conduits through embolism leads to reduced hydraulic conductance causing increased tension in the remaining vessels and generating more tension in a vicious circle. The model predicted that all species operate near the point of catastrophic xylem failure due to dynamic water stress. The model supports Zimmermann's plant segmentation hypothesis. Zimmermann suggested that plants are designed hydraulically to sacrifice highly vulnerable minor branches and thus improve the water balance of remaining parts. The model results are discussed in terms of the morphology, hydraulic architecture, eco-physiology, and evolution of woody plants.
Xylem embolism, the reduction of water flow by air-filled vessels, was measured in a stand of 5- to 8-year-old sugar maple (Acer saccharum Marsh.) saplings growing in a nursery bed in northwestern Vermont. Embolism was quantified as percentage loss in hydraulic conductivity of trunk and branch segments relative to maximum values obtained by removing air from vessels by repeated high pressure (173 kPa) perfusions. Ten segments per tree were cut from 6 trees for each of 11 measurement periods spaced at roughly monthly intervals from May 1986 to June 1987. During the 1986 growing season, embolism increased significantly from 11 to 31% in the larger branches and trunk (segment diameter #8805;0.5 cm), but remained at about 10% in twigs (segment diameter <0.5 cm). This was unexpected because the greatest water stess and thus potential for embolism occurs in twigs. During the winter, embolism increased throughout the trees and the trend with diameter was reversed; by February, small twigs were 84% embolized vs. 69% for larger branches and trunk. Dye perfusions showed that winter embolism in trunks was localized on the south side; this may have resulted from water loss by sublimation or evaporation in the absence of water uptake. Beginning in late March, embolism decreased throughout the trees to approximately 20% in June. This decrease was associated with positive xylem pressure of at least 16 kPa which may have originated in the roots, because weather conditions at the time were unfavorable for the generation of stem pressures characteristic of Acer species in early spring.
An apparatus has been constructed for the detection of vibrations generated within plant tissue. This can detect vibrations due to water cavitation within fern sporangia. Using this detector 'clicks' have been obtained from Ricinus petioles and leaves in a condition when, from previous work, water cavitation might be expected.Evidence is provided to show: 1. That 'click' production is correlated with the water status of the plant tissue. 2. There are reasons for opposing the possibility that 'clicks' result from tissue fracture alone. 3. The 'clicks' may be detected in a wide range of plants. The implications of the apparent vulnerability of water conducting systems in plants are discussed.
1 Conducting Units: Tracheids and Vessels.- 2 The Vessel Network in the Stem.- 3 The Cohesion-Tension Theory of Sap Ascent.- 4 Xylem Dysfunction: When Cohesion Breaks Down.- 5 Hydraulic Architecture of Woody Shoots.- 6 Hydraulic Architecture of Whole Plants and Plant Performance.- 7 Other Functional Adaptations.- 8 Failure and "Senescence" of Xylem Function.- 9 Pathology of the Xylem.- References.
Water stored within the tree and released to the transpiration stream was considered as a possible explanation for a discrepancy
between two independent estimates of evaporation from a Pinus sylvestris L. plantation in Thetford Chase, East Anglia. A technique is described by which an estimate is made of the quantity of stored
water. Trees were allowed to transpire only stored water and estimates made of the quantity available. The results showed,
however, that the amount of water available from store is insignificant and could not account for the discrepancy between
evaporation estimates.
The influence of sapwood water content on the conductivity of sapwood to water was measured on stem sections of Pinus contorta. A reduction in relative water content from 100 to 90% caused permeability to fall to about 10% of the saturated value.Pressure–volume curves of branchwood and stem sapwood of Pinus contorta and Picea sitchensis have been analysed to definè the tissue capacitance and the time constant and resistance for water movement between stored water and the functional xylem as functions of tissue water potential. Three phases in water loss were discernible. In the initial phase at high water potentials (> –0.5 MPa), the capacitance was large, the time constant long and the resistance to flow large in comparison with intermediate water potentials (−0.5 to −1.5 MPa). At still lower water potentials (−1.5 to −3.0 MPa), the time constant and resistance declined still further but the capacitance had a tendency to increase again, especially in the stemwood of Sitka spruce. Typical values in the second phase were for the time constant 5 s, for the resistance 4 × 10−13 N s m−5 and for the capacitance (change in relative water content per unit change in potential) 1×10−11 m3 Pa−1. These parameters define the availability of stored water and are being used in a dynamic model of water transport in trees.
A theoretical model of bubble dissolution in xylem conduits of stems was designed using the finite differential method and iterative calculations via computer. The model was based on Fick's, Henry's and Charles' laws and the capillary equation. The model predicted the tempo of recovery from embolism in small diameter branches of woody plants with various xylem structures under different xylem water pressures. The model predicted the time required to recover conductivity in any position in the stem. Repeated iterative solution of the model for different situations yielded an empirical formula to calculate the time for complete recovery of conductivity in stems from a fully embolised initial state. The time, tp, is given by:
where α is a temperature coefficient; D is the coefficient of diffusion of air in wood at 25°C; rcs is the ratio of the area of total conduit cross section to the stem cross section; Ψxp is the stem xylem pressure potential (Pa, where 0 Pa equals atmospheric pressure); τ is solution surface tension (0.072 N m−1); and Dc and Ds are diameters of the conduits and the stem, respectively (m). The equation is valid only when Ψxp > –4τ/Dc. The model predicts no recovery of conductivity when Ψxp≤–4τ/Dc. The model agreed with experiments.
An apparatus has been constructed for the detection of vibrations generated within plant tissue. This can detect vibrations due to water cavitation within fern sporangia. Using this detector clicks have been obtained from Ricinus petioles and leaves in a condition when, from previous work, water cavitation might be expected.Evidence is provided to show:1.
That click production is correlated with the water status of the plant tissue.
2.
There are reasons for opposing the possibility that clicks result from tissue fracture alone.
3.
The clicks may be detected in a wide range of plants.
The implications of the apparent vulnerability of water conducting systems in plants are discussed.
In this paper, we have reviewed how the hydraulic design of trees influences the movement of water from roots to leaves. The hydraulic architecture of trees can limit their water relations, gas exchange throughout the crown of trees, the distribution of trees over different habitats and, perhaps, even tbe maximum height that a particular species can achieve. Parameters of particular importance include:
(1) tbe vulnerabihty of stems to drought induced cavitation events because cavitation reduces the hydraulic conductance of stems,
(2) the leaf specific conductivity of stems because it determines the pressure gradients and most negative water potentials needed to sustain evaporation from leaves,
(3) the water storage capacity of tissues because this might determine the ability of trees to survive long drought periods.
All of these parameters are determined by the structure and function of anatomical components of trees. Some of the ecological and physiological trade-offs of specific structures are discussed.
In this studys we test the hypothesis that, when water supply is under tension, reversal of cavitation can occur as long as water continuity is maintained in the vicinity of tracheids. The experiments were conducted on young branches, 7-8 mm diameter, of Pinus sylvestris L., freshly collected and allowed to lose water on the bench after being debarked. During dehydration, the volumetric fractions of water (Vw) and gas (Vg) changed steadily as relative water content (theta) declined. Meanwhile, ultrasonic emission (UAE) started after a threshold q = 90% was reached and were maximal at q = 75%. Before and after dehydration, branch segments were connected to water-filled tubing and placed from 0.2 to 3.6 m above a water source and water inflow and outflow were recorded. These distances provided a source of water at a potential of -2.0 to -36 kPa. We considered that the segment water potential would be a function of the surface tension across the water meniscii at the ends of the embolized trachaeids. Thus, water potentials calculated from trachaeid dimensions would be as low as -43 kPa. Water inflow to segments declined when the distacnce from the source was increased or the segments were very dehydrated. Increasing the distance above the water source would be expected to increase the water potential difference but to reduce water uptake. The most dehydrated segments absorbed water faster at the beginning of the refilling period ( simeq 2 h), but at the end of 16 h, q was lower and Vg larger than in less embolized tissue. Recovery of water flow followed a similar trend, and was lost when embolisms increased. For a narrow range of q, hydraulic conductance was reduced sharply, indicating that wide tracheids were still gas-filled. Thus, the number of trachaeids remaining embolized increased when the source water potential was low and there was severe embolism. We conclude that embolism can be reversed in P. sylvestris at a rate depending on the water potential of the source, severity of embolism and hydraulic conductivity.
With the neglect of the translational motion of the bubble, approximate solutions may be found for the rate of solution by diffusion of a gas bubble in an undersaturated liquid-gas solution; approximate solutions are also presented for the rate of growth of a bubble in an oversaturated liquid-gas solution. The effect of surface tension on the diffusion process is also considered.
Sapwood water storage: its conductivity recovery from embolism with comparison to exper-contribution to transpiration and effect upon water conductance imental data on Acer saccharum. Plant, Cell and Environment through the stems of old-growth Douglas-fir. Plant, Cell and 15
- Waring R H Running
Waring R.H. & Running S.W. (1978) Sapwood water storage: its conductivity recovery from embolism with comparison to exper-contribution to transpiration and effect upon water conductance imental data on Acer saccharum. Plant, Cell and Environment through the stems of old-growth Douglas-fir. Plant, Cell and 15,633-643.
Variation in longitudinal permeability of green radiata pine wood
- G H Aylward
- T J V Findlay
Aylward G. H. & Findlay T.J.V. (1971) 5/ Chemical Data, John Wiley & Sons Australasia Ltd, Sydney. Booker R.E. & Kininmonth J.A. (1978) Variation in longitudinal permeability of green radiata pine wood. New Zealand Journal of Forestry Science 8, 295-308.
Patterns in the seasonal water content of trees
- R D Gibbs
Gibbs R.D. (1958) Patterns in the seasonal water content of trees.