Planta
Planta (1990)182:420-426
9 Springer-Verlag1990
Water-storage capacity of Thuja, Tsuga and Acer stems measured by dehydration isotherms The contribution o f capillary water and cavitation Melvin T. Tyree 1 and Shudong Yang 2 1 Northeastern Forest Experiment Station, U.S. Forest Service, P.O. Box 698, Burlington, VT 05402, and 2 Department of Botany, University of Vermont, Burlington, VT 05405, USA Received 9 December 1989; accepted 14 May 1990
Abstract. Water-storage capacity was measured in Thuja occidentalis L., Tsuga canadensis (L.) Carr., and Acer saccharum Marsh. during the dehydration of stem seg-
ments 1.5-2.5 cm in diameter. Stem water potential was measured with a temperature-corrected stem hygrometer and cavitations were detected acoustically. Water loss was measured by weight change. Dehydration isotherms consistently displayed three phases. The first phase, from water potential (~) 0 to about - 0 . 2 MPa, had a high capacitance (C>0.4 kg water lost.(1 of tissue)-1. MPa-1) and we have attributed this high C to capillary water as defined by Zimmermann (1983, Xylem structure and the ascent of sap, Springer-Verlag). The second phase from 7 / = - 0 . 5 to about - 2 . 0 had the lowest C values ( < 0.02 kg. 1- 1. MPa - 1) and was accompanied by a few cavitation events. This phase may have been a transition zone between capillary storage and water released by cavitation events as well as water drawn from living cells of the bark. The third phase also had a high C (about 0.0%0.22 kg.1-1. MPa- 1) and was associated with many cavitation events while 7j declined below about - 2 . 5 MPa; we presume the high capacitance was the consequence of water released by cavitation events. We discuss the ecological adaptive advantage of these three phases of water-storage in trees. In moist environments, water withdrawn from capillary storage may be an important fraction of transpiration, but may be of little adaptive advantage. For most of the growth season trees draw mainly on elastic storage, but stem elastic storage is less than leaf elastic storage and therefore unlikely to be important. In very dry environments, water relased by cavitation events might be important to the short-term survival of trees.
Key words: Acer
Capillary water - Cavitation - Thuja
- Tsuga - Water storage capacity
Abbreviations and symbols: AE=acoustic emissions; C=capacitance; ~ = water potential
Introduction Storage of "available" water in plants can be loosely defined as the mass or volume of water that can be extracted from leaves, stems, and roots in a "physiological" range of water potentials (~), e.g. 0 to - 2 or - 3 MPa. Trees are potentially capable of storing more water than all other plants (with the possible exception of succulents); because trees have more biomass in stems per unit leaf area than most plants. Stand-level analyses of forests have shown that water-storage in the woody part of boles (that is, trunks excluding bark and cambium) account for 50-80% of the available water in Douglas-fir (Waring and Running 1978) and Scots pine (Waring et al. 1979). Water-storage in plants is important to understand because of the potential adaptive advantage that the retrieval of stored water may have to permit plants to survive transitory periods of drought. While the mechanism of water-storage in herbaceous plants is fairly well understood, the mechanism of storage in woody species (which comprise most of the vascular-plant biomass of the earth) is not so well defined. In this paper we propose that water-storage can occur in plants by three mechanisms and we perform experiments to demonstrate the differences in the mechanisms. The three mechanisms are: elastic storage, capillary storage, and "cavitation release" (that is storage water released by cavitation). Elastic storage is perhaps the most studied mechanism and occurs in plant cells surrounded by elastic cell walls. When hu changes, the cell walls either stretch or contract elastically to allow water to flow in or out of the cells. Most cells in herbaceous plants and in leaves of trees are very elastic. Based on 7/ isotherms (Tyree and Karamanos 1980), water-storage in elastic tissues is known to be in the range of %25% of the cell volume. The cell volume changes in elastic cells cause a corresponding change in tissue or organ volume. Because woody cells have thick, lignified, inelastic walls, elastic water-storage in wood is considered minimal. Most of the diameter change recorded in stems of trees is caused
M.T. Tyree and S. Yang: Water-storage capacity of woody stems by growth or by diurnal volume changes of bark and cambium (Klepper et al. 1971). Capillary storage has been discussed at length by Zimmermann (1983, pp. 47-54) and is thought to occur in embolized wood cells (wood fibers, tracheids, vessels) and in intercellular spaces. Capillary storage is most in small-diameter lumina with gradually tapering ends. Water can be held in the tapered ends by capillary forces generated across the menisci at the gas-water interface. Capillary forces will lower the pressure of the water in the tapered ends by an amount given by the capillary equation: Pc=-2T/r+Pg,
Eq. (1)
where Pc is the pressure of the capillary water which must be in equilibrium with the xylem pressure potential in water-filled xylem conduits, T is the surface tension of water, r is the radius of curvature of the gas-water interface; and Pg is the pressure of the gas bubble trapped in the lumen. (All pressures are relative to atmospheric pressure, i.e., if the bubble is at atmospheric pressure then Pg=0.) As stem water potentials change, Pc will tend to come into equilibrium with the xylem pressure potential. So as 7~ decreases water is withdrawn from capillary storage, moving the menisci towards the tapered ends which decreases r and brings Pc into equilibrium, and this process is reversed when ~b increases. If this hypothesis is correct, then most available capillary water ought to be released by the time 7j and Pc reach equilibrium at - 0 . 6 MPa, because r will be reduced to about 0.25 [am and the menisci will be near the tips of the tapered lumina. We know of no discussion of the dynamics of capillary water-storage, but we would expect it to be complicated because of the presence of the gas bubbles. When 7j decreases, the gas-bubble volume expands and the gas pressure must initially decrease. Since the solubility of gas in water is proportional to the gas pressure at the gas-water interface, gas will come out of solution from the adjacent water-filled cells. More gas will then diffuse through surrounding water-filled tissue and come out of solution raising P, back to atmospheric pressure, causing a rise in Pc followed by further meniscus movement and volume adjustment. The reverse happens when increases; meniscus movement towards the center of the lumina causes Pg to increase which in turn will make the gas dissolve in surrounding tissue and diffuse away. Since gas diffusion is quite slow in liquid, these volume adjustments should cause a diurnal hysteresis in the relationship between capillary water volume and ~. Cavitation release occurs when ~ gets negative enough to cause a cavitation event which is now thought to occur when an gas bubble is sucked into a water filled lumen (Tyree and Sperry 1989a). This process creates a new capillary storage cell and most of the water in the cell lumen is immediately sucked into surrounding tissue. Cavitated cells initially contain only water vapor and liquid water in the lumen, but eventually, gas comes out of solution from surrounding tissue to increase the gas pressure to atmospheric pressure producing a new
421 embolized cell. All cavitated cells contribute to capillary water-storage whether they are filled with gases or only water vapor. Since most woody plants do not start cavitating until g~ falls below - 1 MPa, water released by cavitation should be easily distinguished from capillary storage. Tyree and Sperry (1989a) have suggested that embolized cells do not refill in most trees until spring, if at all. Exceptions to this rule might be smaller woody plants that can develop root or stem pressure at night (Sperry et al. 1987, 1988). So cavitation release can be viewed as more or less irreversible during the growing season of large woody plants. Herbaceous plants may be capable of producing enough root pressure to disolve emboli every night (Milburn and McLaughlin 1974; Tyree et al. 1986). There is growing evidence that some woody plants may also be capable of nightly embolism reversal (Salleo and LoGullo 1989). At present we have no convincing evidence that gas bubbles can dissolve without the xylem pressure potential returning to near-atmospheric values. The physics surrounding surface-tension phenomena would seem to make this manditory (Eq. 1) as explained at length in the discussion. The purpose of this study was to measure the waterstorage capacity of stems of three species of trees and to see if there was evidence of a relatively quickly reversible water-storage component when stem ku was in the range of 0 to - 0 . 5 MPa, and a less reversible component when 7j was < - 1 or - 2 MPa. Measurements of waterstorage capacity are needed also to make more refined models of the dynamics of water movement within trees (Tyree 1988) and to understand the ecological adaptive advantages of water-storage.
Material and methods Plant material. Stem segments were collected from Thuja occidentalis L., Tsuga eanadensis (L.) Carr., and Aeer saceharum Marsh.
trees growing in or near Burlington, Vermont. Stem segments were collected from terminal shoots of 2-3 m Thuja trees. Stem segments of Tsuga were collected from lateral stems from 2-10 m trees. Acer segments were cut from the main stems of 3-5 m trees in a closely spaced nursery bed. Diameters of the cut segment ranged from 2.5 cm at the base to 1.5 cm at the apex. All stems were brought back to the laboratory, the leaves were removed and the stem bases were recut under water and left to rehydrate with the bases in water overnight. Since cut cells at the ends of stem segments will all contribute to capillary water, stem segments used for dehydration experiments were cut much longer than the longest vessels or tracheids. Tsuga and Thuja segments were cut to a length of 15-20 cm (tracheid lengths were typically 0.1 cm) and Acer stems were 80-100 cm long (vessel lengths were typically 10 cm or less and wood fibers 0.1~.2 cm). Water-potential measurements. Stem water potentials were measured by a temperature-corrected stem hygrometer as described in Dixon and Tyree (1984). A strip of bark about 4 cm long and 0.5 cm wide was removed near the center of the stem segment for mounting the hygrometer. Exposed sapwood outside the hygrometer chamber was covered with silicone grease. Cavitation measurements. Cavitations were measured with an ultrasonic acoustic emission (AE) counter (Model 4615 Drought Stress Monitor; Physical Acoustic Corp., Lawrenceville, M.J., USA; see
422
M.T. Tyree and S. Yang: Water-storage capacity of woody stems
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Planta (1990)182:420-426
9 Springer-Verlag1990
Water-storage capacity of Thuja, Tsuga and Acer stems measured by dehydration isotherms The contribution o f capillary water and cavitation Melvin T. Tyree 1 and Shudong Yang 2 1 Northeastern Forest Experiment Station, U.S. Forest Service, P.O. Box 698, Burlington, VT 05402, and 2 Department of Botany, University of Vermont, Burlington, VT 05405, USA Received 9 December 1989; accepted 14 May 1990
Abstract. Water-storage capacity was measured in Thuja occidentalis L., Tsuga canadensis (L.) Carr., and Acer saccharum Marsh. during the dehydration of stem seg-
ments 1.5-2.5 cm in diameter. Stem water potential was measured with a temperature-corrected stem hygrometer and cavitations were detected acoustically. Water loss was measured by weight change. Dehydration isotherms consistently displayed three phases. The first phase, from water potential (~) 0 to about - 0 . 2 MPa, had a high capacitance (C>0.4 kg water lost.(1 of tissue)-1. MPa-1) and we have attributed this high C to capillary water as defined by Zimmermann (1983, Xylem structure and the ascent of sap, Springer-Verlag). The second phase from 7 / = - 0 . 5 to about - 2 . 0 had the lowest C values ( < 0.02 kg. 1- 1. MPa - 1) and was accompanied by a few cavitation events. This phase may have been a transition zone between capillary storage and water released by cavitation events as well as water drawn from living cells of the bark. The third phase also had a high C (about 0.0%0.22 kg.1-1. MPa- 1) and was associated with many cavitation events while 7j declined below about - 2 . 5 MPa; we presume the high capacitance was the consequence of water released by cavitation events. We discuss the ecological adaptive advantage of these three phases of water-storage in trees. In moist environments, water withdrawn from capillary storage may be an important fraction of transpiration, but may be of little adaptive advantage. For most of the growth season trees draw mainly on elastic storage, but stem elastic storage is less than leaf elastic storage and therefore unlikely to be important. In very dry environments, water relased by cavitation events might be important to the short-term survival of trees.
Key words: Acer
Capillary water - Cavitation - Thuja
- Tsuga - Water storage capacity
Abbreviations and symbols: AE=acoustic emissions; C=capacitance; ~ = water potential
Introduction Storage of "available" water in plants can be loosely defined as the mass or volume of water that can be extracted from leaves, stems, and roots in a "physiological" range of water potentials (~), e.g. 0 to - 2 or - 3 MPa. Trees are potentially capable of storing more water than all other plants (with the possible exception of succulents); because trees have more biomass in stems per unit leaf area than most plants. Stand-level analyses of forests have shown that water-storage in the woody part of boles (that is, trunks excluding bark and cambium) account for 50-80% of the available water in Douglas-fir (Waring and Running 1978) and Scots pine (Waring et al. 1979). Water-storage in plants is important to understand because of the potential adaptive advantage that the retrieval of stored water may have to permit plants to survive transitory periods of drought. While the mechanism of water-storage in herbaceous plants is fairly well understood, the mechanism of storage in woody species (which comprise most of the vascular-plant biomass of the earth) is not so well defined. In this paper we propose that water-storage can occur in plants by three mechanisms and we perform experiments to demonstrate the differences in the mechanisms. The three mechanisms are: elastic storage, capillary storage, and "cavitation release" (that is storage water released by cavitation). Elastic storage is perhaps the most studied mechanism and occurs in plant cells surrounded by elastic cell walls. When hu changes, the cell walls either stretch or contract elastically to allow water to flow in or out of the cells. Most cells in herbaceous plants and in leaves of trees are very elastic. Based on 7/ isotherms (Tyree and Karamanos 1980), water-storage in elastic tissues is known to be in the range of %25% of the cell volume. The cell volume changes in elastic cells cause a corresponding change in tissue or organ volume. Because woody cells have thick, lignified, inelastic walls, elastic water-storage in wood is considered minimal. Most of the diameter change recorded in stems of trees is caused
M.T. Tyree and S. Yang: Water-storage capacity of woody stems by growth or by diurnal volume changes of bark and cambium (Klepper et al. 1971). Capillary storage has been discussed at length by Zimmermann (1983, pp. 47-54) and is thought to occur in embolized wood cells (wood fibers, tracheids, vessels) and in intercellular spaces. Capillary storage is most in small-diameter lumina with gradually tapering ends. Water can be held in the tapered ends by capillary forces generated across the menisci at the gas-water interface. Capillary forces will lower the pressure of the water in the tapered ends by an amount given by the capillary equation: Pc=-2T/r+Pg,
Eq. (1)
where Pc is the pressure of the capillary water which must be in equilibrium with the xylem pressure potential in water-filled xylem conduits, T is the surface tension of water, r is the radius of curvature of the gas-water interface; and Pg is the pressure of the gas bubble trapped in the lumen. (All pressures are relative to atmospheric pressure, i.e., if the bubble is at atmospheric pressure then Pg=0.) As stem water potentials change, Pc will tend to come into equilibrium with the xylem pressure potential. So as 7~ decreases water is withdrawn from capillary storage, moving the menisci towards the tapered ends which decreases r and brings Pc into equilibrium, and this process is reversed when ~b increases. If this hypothesis is correct, then most available capillary water ought to be released by the time 7j and Pc reach equilibrium at - 0 . 6 MPa, because r will be reduced to about 0.25 [am and the menisci will be near the tips of the tapered lumina. We know of no discussion of the dynamics of capillary water-storage, but we would expect it to be complicated because of the presence of the gas bubbles. When 7j decreases, the gas-bubble volume expands and the gas pressure must initially decrease. Since the solubility of gas in water is proportional to the gas pressure at the gas-water interface, gas will come out of solution from the adjacent water-filled cells. More gas will then diffuse through surrounding water-filled tissue and come out of solution raising P, back to atmospheric pressure, causing a rise in Pc followed by further meniscus movement and volume adjustment. The reverse happens when increases; meniscus movement towards the center of the lumina causes Pg to increase which in turn will make the gas dissolve in surrounding tissue and diffuse away. Since gas diffusion is quite slow in liquid, these volume adjustments should cause a diurnal hysteresis in the relationship between capillary water volume and ~. Cavitation release occurs when ~ gets negative enough to cause a cavitation event which is now thought to occur when an gas bubble is sucked into a water filled lumen (Tyree and Sperry 1989a). This process creates a new capillary storage cell and most of the water in the cell lumen is immediately sucked into surrounding tissue. Cavitated cells initially contain only water vapor and liquid water in the lumen, but eventually, gas comes out of solution from surrounding tissue to increase the gas pressure to atmospheric pressure producing a new
421 embolized cell. All cavitated cells contribute to capillary water-storage whether they are filled with gases or only water vapor. Since most woody plants do not start cavitating until g~ falls below - 1 MPa, water released by cavitation should be easily distinguished from capillary storage. Tyree and Sperry (1989a) have suggested that embolized cells do not refill in most trees until spring, if at all. Exceptions to this rule might be smaller woody plants that can develop root or stem pressure at night (Sperry et al. 1987, 1988). So cavitation release can be viewed as more or less irreversible during the growing season of large woody plants. Herbaceous plants may be capable of producing enough root pressure to disolve emboli every night (Milburn and McLaughlin 1974; Tyree et al. 1986). There is growing evidence that some woody plants may also be capable of nightly embolism reversal (Salleo and LoGullo 1989). At present we have no convincing evidence that gas bubbles can dissolve without the xylem pressure potential returning to near-atmospheric values. The physics surrounding surface-tension phenomena would seem to make this manditory (Eq. 1) as explained at length in the discussion. The purpose of this study was to measure the waterstorage capacity of stems of three species of trees and to see if there was evidence of a relatively quickly reversible water-storage component when stem ku was in the range of 0 to - 0 . 5 MPa, and a less reversible component when 7j was < - 1 or - 2 MPa. Measurements of waterstorage capacity are needed also to make more refined models of the dynamics of water movement within trees (Tyree 1988) and to understand the ecological adaptive advantages of water-storage.
Material and methods Plant material. Stem segments were collected from Thuja occidentalis L., Tsuga eanadensis (L.) Carr., and Aeer saceharum Marsh.
trees growing in or near Burlington, Vermont. Stem segments were collected from terminal shoots of 2-3 m Thuja trees. Stem segments of Tsuga were collected from lateral stems from 2-10 m trees. Acer segments were cut from the main stems of 3-5 m trees in a closely spaced nursery bed. Diameters of the cut segment ranged from 2.5 cm at the base to 1.5 cm at the apex. All stems were brought back to the laboratory, the leaves were removed and the stem bases were recut under water and left to rehydrate with the bases in water overnight. Since cut cells at the ends of stem segments will all contribute to capillary water, stem segments used for dehydration experiments were cut much longer than the longest vessels or tracheids. Tsuga and Thuja segments were cut to a length of 15-20 cm (tracheid lengths were typically 0.1 cm) and Acer stems were 80-100 cm long (vessel lengths were typically 10 cm or less and wood fibers 0.1~.2 cm). Water-potential measurements. Stem water potentials were measured by a temperature-corrected stem hygrometer as described in Dixon and Tyree (1984). A strip of bark about 4 cm long and 0.5 cm wide was removed near the center of the stem segment for mounting the hygrometer. Exposed sapwood outside the hygrometer chamber was covered with silicone grease. Cavitation measurements. Cavitations were measured with an ultrasonic acoustic emission (AE) counter (Model 4615 Drought Stress Monitor; Physical Acoustic Corp., Lawrenceville, M.J., USA; see
422
M.T. Tyree and S. Yang: Water-storage capacity of woody stems
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