Poplar vulnerability to xylem cavitation acclimates to drier soil conditions

Xylem vulnerability to cavitation differs between tree species according to their drought resistance, more xerophilous species being more resistant to xylem cavitation. Variability in xylem vulnerability to cavitation is also found within species, especially between in situ populations. The origin of this variability has not been clearly identified. Here we analyzed the response of xylem hydraulic traits of Populus tremula×Populus alba trees to three different soil water regimes. Stem xylem vulnerability was scored as the xylem water potential causing 12, 50 and 88% loss of conductivity (P₁₂, P₅₀ and P₈₈). Vulnerability to cavitation was found to acclimate to growing conditions under different levels of soil water content, with P₅₀ values of ?1.82, ?2.03 and ?2.45 MPa in well‐watered, moderately water‐stressed and severely water‐stressed poplars, respectively. The value of P₁₂, the xylem tension at which cavitation begins, was correlated with the lowest value of midday leaf water potential (ψm) experienced by each plant, the difference between the two parameters being approximately 0.5 MPa, consistent with the absence of any difference in embolism level between the different water treatments. These results support the hypothesis that vulnerability to cavitation is a critical trait for resistance to drought. The decrease in vulnerability to cavitation under growing conditions of soil drought was correlated with decreased vessel diameter, increased vessel wall thickness and a stronger bordered pit field (t/b)². The links between these parameters are discussed.     

Rare pits, large vessels and extreme vulnerability to cavitation in a ring-porous tree species

? The rare pit hypothesis predicts that the extensive inter-vessel pitting in large early-wood vessels of ring-porous trees should render many of these vessels extremely vulnerable to cavitation by air-seeding. This prediction was tested in Quercus gambelii. ? Cavitation was assessed from native hydraulic conductivity at field sap tension and in dehydrated branches. Single-vessel air injections gave air-seeding pressures through vessel files; these data were used to estimate air-seeding pressures for inter-vessel walls and pits. ? Extensive cavitation occurred at xylem sap tensions below 1 MPa. Refilling occurred below 0.5 MPa and was inhibited by phloem girdling. Remaining vessels cavitated over a wide range to above 4 MPa. Similarly, 40% of injected vessel files air-seeded below 1.0 MPa, whereas the remainder seeded over a wide range exceeding 5 MPa. Inter-vessel walls averaged 1.02 MPa air-seeding pressure, similar and opposite to the mean cavitation tension of 1.22 MPa. Consistent with the rare pit hypothesis, only 7% of inter-vessel pits were estimated to air-seed by 1.22 MPa. ? The results confirm the rare pit prediction that a significant fraction of large vessels in Q. gambelii experience high probability of failure by air-seeding.     

Soil salinity and drought alter wood density and vulnerability to xylem cavitation of baldcypress (Taxodium distichum (L.) Rich.) seedlings

We investigated the role of hydraulic conductivity, wood density, and xylem cavitation in the response of baldcypress (Taxodium distichum) seedlings to increased soil salinity and drought. One-year-old, greenhouse-grown seedlings were irrigated daily with a 100 mM (≈6‰) salt solution or once per week with fresh water (drought). Controls were irrigated daily with fresh water. Gas exchange rates of stressed plants were reduced by approximately 50% (salt) and 70% (drought), resulting in a 50–60% reduction in diameter growth for both treatments. Stem-specific hydraulic conductivity (K_{S native}) of stressed plants was 33% (salt) and 66% (drought) lower than controls and we observed a strong positive correlation between K_{S native} and gas exchange. In addition, we found a strong relationship between CO₂ assimilation rate (A) and the soil-to-leaf hydraulic conductance (k_L). The relationship was identical for all treatments, suggesting that our moderate salt stress (as well as drought) did not affect the photosynthetic biochemistry of leaves, but rather reduced A via stomatal closure. Lower K_{S native} of stressed plants was associated with increased wood density and greater resistance to xylem cavitation. Xylem pressures causing 50% loss of hydraulic conductivity (P₅₀) were ?2.88 ± 0.07 MPa (drought), ?2.50 ± 0.08 MPa (salt) and ?2.01 ± 0.04 MPa (controls). P₅₀s were strongly correlated with wood density (r = ?0.71, P < 0.01) and K_{S native} (r = 0.74, P < 0.01). These findings support the hypothesis that there is a significant trade-off between a plant's cavitation resistance and its hydraulic efficiency. The results of the present study indicate that stressed plants partitioned their biomass in a way that strengthened their xylem and reduced vulnerability to xylem cavitation. Hence, these seedlings could be better suited to be planted in environments with elevated soil salinity. For most parameters (especially P₅₀), drought had an even more pronounced effect than salinity. This is important as nurseries could produce “stress-acclimated” seedlings simply by reducing irrigation amounts and would not have to contaminate the soils in their nursery beds with salt applications.     

Evaluation of centrifugal methods for measuring xylem cavitation in conifers, diffuse- and ring-porous angiosperms

A centrifugal method is used to measure 'vulnerability curves' which show the loss of hydraulic conductivity in xylem by cavitation. Until recently, conductivity was measured between bouts of centrifugation using a gravity-induced head. Now, conductivity can be measured during centrifugation. This 'spin' method is faster than the 'gravity' technique, but correspondence between the two has not been evaluated. The two methods were compared on the same stem segments for two conifer, four diffuse-porous, and four ring-porous species. Only 17 of 60 conductivity measurements differed, with differences in the order of 10%. When different, the spin method gave higher conductivities at the beginning of the curve and lower at the end. Pressure at 50% loss of conductivity, and mean cavitation pressure, were the same in 14 of 20 comparisons. When different, the spin method averaged 0.32 MPa less negative. Ring-porous species showed a precipitous initial drop in conductivity by both techniques. This striking pattern was confirmed by the air-injection method and native embolism measurements. Close correspondence inspires confidence in both methods, each of which has unique advantages. The observation that ring-porous species operate at only a fraction of their potential conductivity at midday demands further study.     

Genotypic variability in vulnerability of leaf xylem to cavitation in water-stressed and well-irrigated sugarcane

Genotypic variability in vulnerability of leaf xylem to water-stress-induced cavitation was determined in four sugarcane (Saccharum sp.) clones using detached leaf segments in a hydraulic conductivity apparatus. Vulnerability curves were constructed by plotting the percentage of maximum conductivity versus leaf water potential (ψ_I) and fitting curves using a Weibull function. The ψ_I at which each clone lost 10, 50, and 80% of maximum conductivity was determined. Maximum conductivity per unit of leaf width was positively associated with metaxylem vessel diameter. The commercial clone H65-7052 exhibited the highest and the nondomesticated S. spontaneum exhibited the lowest conductivity. All four clones lost substantial conductivity at values of ψ_I less negative than −1.4 MPa, but H65-7052 was able to maintain 50% conductivity to lower ψ_I than the other clones. S. spontaneum sustained the most negative ψ_I (−1.99 MPa) before reaching the 80% conductivity loss point. Clone H69-8235 was consistently the most vulnerable to initial loss of conductivity. These vulnerability functions were used in conjunction with field measurements of ψ_I to estimate diurnal losses in leaf hydraulic conductivity under irrigated and droughted conditions. H69-8235 lost up to 50% of its conductivity during the day, even when well irrigated, and more than 80% when subjected to drought. The other clones exhibited lower conductivity losses. These losses are apparently reversed overnight by root pressure. Despite their close genetic relationships, these clones exhibited large differences in conductivity, in the vulnerability of their xylem to cavitation, and in gas exchange behavior. The potential for altering water relations by selecting for particular hydraulic characteristics is discussed.     

Radial patterns of xylem sap flow in non-, diffuse- and ring-porous tree species

We investigated radial patterns of sap flux density and wood properties in the sapwood of young loblolly pine (Finns taeda L.), mature white oak (Quercus alba L.) and sweetgum (Liquidambar styraciflua L.), which represent three major classes of wood anatomy: non-porous (coniferous), ring-porous and diffuse-porous. Radial measurements of xylem sap flux density were made in sections of xylem extending to 20 mm and 20–40 mm from the cambium. These measurements were compared with measurements of the relative water content (R_s) and sapwood specific gravity (ρ_r) of corresponding radial sections. In both hardwood species, sap flow differences were rarely significant between the two depth intervals. In pine, a 59% reduction in daily sap flux density from outer to inner sapwood was found. This could not be accounted for by a 3% drop in R_s; rather, an accompanying 9% reduction in ρ_r indicated a transition between the depth intervals from mature to juvenile sapwood, and is the probable cause of the lower flux rate in the inner xylem of pine.     

Relationship between the timing of vessel formation and leaf phenology in ten ring-porous and diffuse-porous deciduous tree species

The goal of this study is to clarify how different aspects of plant function are coordinated developmentally for species of ring-porous versus diffuse-porous deciduous trees, comparing the timing of leaf phenology and vessel formation in twigs and stems from an ecophysiological viewpoint. Cylindrical stem cores and twigs were collected at intervals from early spring through summer from five ring-porous and five diffuse-porous species in a cool temperate forest, and leaf and vessel formation were observed simultaneously. We found that the first-formed vessels of the year were lignified in twigs around the time of leaf appearance and at or before full leaf expansion of each tree in both groups of species with flush-leaves. Vessels in stems were lignified 2 weeks before to 4 weeks after leaf appearance and before or around full leaf expansion of the tree in ring-porous species. This was significantly earlier than in diffuse-porous species, in which stem vessel lignification was 2–8 weeks after leaf appearance and at or after full leaf expansion of the tree. The timing of vessel formation in twigs compared to stems was significantly earlier in ring-porous species than in diffuse-porous species. Lignification of vessels in stems occurred within 2 weeks of lignification in the twigs of ring-porous species and 2–8 weeks after lignification in twigs of diffuse-porous species. These results indicate the order and time-lag of leaf and vessel formation. Ring-porous species showed intensive leaf/vessel production, whereas diffuse-porous species showed less intensive leaf/vessel production.     

Xylem embolism in response to freeze-thaw cycles and water stress in ring-porous, diffuse-porous, and conifer species

Vulnerability to xylem embolism by freeze-thaw cycles and water stress was quantified in ring-porous (Quercus gambelii Nutt.), diffuse-porous (Populus tremuloides Michx., Betula occidentalis Hook.), and conifer species (Abies lasiocarpa Nutt., Juniperus scopulorum Sarg.). Embolism was measured by its reduction of xylem hydraulic conductivity; it was induced by xylem tension (water-stress response) and by a tension plus a freeze-thaw cycle (freeze response). Conifers showed little (Juniperus) or no (Abies) freeze response even to repeated cycles. In contrast, Quercus embolized more than 90% by freezing at tensions below 0.2 MPa, whereas similar embolism without freezing required tensions above 4.5 MPa. Diffuse-porous trees (Betula, Populus) showed an intermediate freeze response. The magnitude of the freeze response was correlated with conduit volume but occurred at higher tensions than predicted from theory. Large early-wood vessels (2.8 × 10⁻⁹ m³) in oak were most vulnerable to embolism by freezing, small vessels in Populus and Betula were intermediate (approximately 7 × 10⁻¹¹ m³), and tracheids in conifers (about 3 × 10⁻¹³ m³) were most resistant. The same trend was found within a stem: embolism by freeze-thawing occurred preferentially in wider conduits. The water-stress response was not correlated with conduit volume; previous work indicates it is a function of interconduit pit membrane structure. Native embolism levels during winter corroborated laboratory results on freezing: Quercus embolized 95% with the first fall freeze, Populus and Betula showed gradual increases to more than 90% embolism by winter's end, and Abies remained below 30%.     

Hydraulic failure and tree dieback are associated with high wood density in a temperate forest under extreme drought

Catastrophic hydraulic failure will likely be an important mechanism contributing to large‐scale tree dieback caused by increased frequency and intensity of droughts under global climate change. To compare the susceptibility of 22 temperate deciduous tree and shrub species to hydraulic failure during a record drought in the southeastern USA, we quantified leaf desiccation, native embolism, wood density, stomatal conductance and predawn and midday leaf water potential at four sites with varying drought intensities. At the two driest sites, there was widespread leaf wilting and desiccation, and most species exhibited predawn leaf water potentials of ≤3 MPa and >60% loss of xylem conductivity in branches. Although species with high wood density were more resistant to cavitation, they had higher levels of native embolism and greater canopy dieback than species with low wood density. This unexpected result can be explained by the failure of species with dense wood to avert a decline in water potential to dangerous levels during the drought. Leaf water potential was negatively correlated with wood density, and the relationship was strongest under conditions of severe water deficit. Species with low wood density avoided catastrophic embolism by relying on an avoidance strategy that involves partial drought deciduousness, higher sensitivity of stomata to leaf water potential and perhaps greater rooting depth. These species therefore maintained water potential at levels that ensured a greater margin of safety against embolism. These differences among species may mediate rapid shifts in species composition of temperate forests if droughts intensify due to climate change.     

The vulnerability to freezing-induced xylem cavitation of Larrea tridentata (Zygophyllaceae) in the Chihuahuan desert

The temperature dependence of freezing-induced xylem cavitation was studied in a Chihuahuan desert population of Larrea tridentata (Zygophyllaceae). Field measurements of wood temperature and xylem embolism were combined with anatomical studies and laboratory measurements of embolism in stem and root samples frozen under controlled conditions. Our laboratory experiments corroborated the previously observed relationship between minimum freezing temperature and embolism. The area of the low-temperature exotherms produced during the freezing treatments was correlated with the resulting embolism, suggesting that the freezing of water inside parenchyma cells is associated with the occurrence of xylem embolism. In the laboratory experiments, embolism in stems increased only at temperatures below -14°C. Although this meant that the studied population was more resistant to freezing-induced xylem embolism than a previously studied population from the Sonoran desert, the impact of freezing was nevertheless greater because of much lower environmental temperatures. This result suggests that dieback associated with periodic extreme freezes may contribute to limiting the present distribution of L. tridentata in central New Mexico. Although laboratory experiments showed that root xylem embolism increased after freezing to less negative minimum temperatures than stems (significant effects at T = -7°C), root embolism in the field was lower than shoot embolism in accordance with measured soil temperatures throughout the study.     

Sap flux of five co-occurring tree species in a temperate broad-leaved forest during seasonal soil drought

In an old-growth forest in Central Germany, sap flux was studied in five broad-leaved tree species that were assumed to differ in drought sensitivity. Under moist soil conditions, average daily sap flux density (J _s) in the outermost xylem varied by a factor of 2.3 among the species (67–152 g cm⁻² per day, n=5 trees per species), and declined in the sequence Fagus sylvatica > Acer pseudoplatanus > Tilia cordata > Carpinus betulus > Fraxinus excelsior. Decreasing soil moisture content (Θ) resulted in linearly reduced J _s in four of the species. During a dry period, J _s was reduced by 44% in T. cordata, 39% in F. sylvatica, 37% in A. pseudoplatanus and 31% in C. betulus compared to sap flux at equal vapour pressure deficit (D) in the wet period. F. excelsior, the only ring-porous species studied, lacked a significant response in J _s to D and Θ. The relative reduction in water use during the dry period was not related to the assumed drought sensitivity of the species as inferred from their abundance in natural woodlands. J _s was positively correlated with tree diameter at breast height (DBH) in three species but decreased with DBH in two species. Dyeing experiments revealed that DBH accounted for 94% of the variation in sapwood area found in a bulk sample of all diffuse-porous trees. This suggests that DBH is a reliable estimator of sapwood area of temperate diffuse-porous species irrespective of species identity. In contrast, sap flux density was found to be greatly dependent on tree species. The estimated whole-plant water use for diffuse-porous trees of a given diameter (49 cm) ranged between 74 and 168 kg per day per species under moist soil conditions. Thus, in temperate mixed forests, species-specific differences in water use can result in a considerable spatial heterogeneity of canopy transpiration.     

Water and ion regulation in cicadas in relation to xylem feeding

Cicadas feed on xylem fluid. This is hypotonic to the haemolymph and contains high concentrations of potassium, sodium, calcium, magnesium, chloride, and phosphate ions. The urine contains the same ions in the same proportions but in slightly lower concentrations. Amino acids and sucrose are present in xylem fluid and traces of amino acids are also found in urine.Water is rapidly shunted from foregut to hindgut via the filter chamber. Injection of xylem fluid into the oesophagus results in an immediate tenfold increase in flow rate in the ileum. The osmotic pressure of xylem fluid in the filter chamber rapidly rises whilst the osmotic pressure in the anterior part of the ileum rapidly falls.Absorption of nutrients and ions into the haemolymph probably occurs in the conical segment and anterior tubular midgut. Storage excretion of divalent ions occurs in the mid-midgut and ions may be transported from the haemolymph into the posterior tubular midgut.The Malpighian tubules secrete a fluid slightly hypertonic to blood containing K⁺ (42 mM/l.] and Na⁺ (14 mM/l.).The osmotic pressures within the internal Malpighian tubules and internal midgut in the filter chamber are considerably higher than the osmotic pressure of the xylem fluid when it first enters the filter chamber proper. Passive osmosis will occur and water will be shunted into the ileum.Reabsorption of K⁺ and Na⁺ occurs in the ileum.     

Physiological and morphological correlates of whole-plant light compensation point in temperate deciduous tree seedlings

A range of traits, including metabolic costs, biomass allocation and seed reserves, may contribute to interspecific variation in the shade tolerance of tree seedlings. In addition, shade tolerance may be affected by differential responses of species to soil resource availability at low light. We used a custom-built whole-plant gas-exchange chamber to quantify instantaneous whole-plant light compensation point (WPLCP) and to parameterize whole-plant daily C gain models for seedlings of eight temperate deciduous tree species. We examined the relationship of WPLCP to growth, biomass allocation and gas-exchange under high and low light and nutrient availabilities and compared it to WPCLP of naturally recruited saplings. For species showing a response, both increased light and nutrient availability resulted in increased WPLCP. However, species’ responses to resource availability did not correspond closely with shade tolerance as has generally been predicted. Variation in WPLCP within species was best predicted by whole-plant dark respiration rates, leaf-level light compensation point and leaf mass per area. Among species, seed size was a strong negative correlate of WPLCP, explaining 66% of the variation. Species with the lowest WPLCP maintained lower growth rates across treatments but greater biomass in the low-light treatment compared with more light-demanding species. These data suggest that a number of traits, in particular metabolic costs and seed size, contribute to WPLCP. However, gas-exchange-based WPLCP was 1.5–3.5 times lower than corresponding growth-based field estimates of WPLCP, suggesting that other factors such as biotic interactions or ontogenetic shifts in whole-plant light requirements may substantially increase species’ WPLCP under natural conditions.     

Carbon allocation to defense, storage, and growth in seedlings of two temperate broad-leaved tree species

Optimal carbon allocation to growth, defense, or storage is a critical trait in determining the shade tolerance of tree species. Thus, examining interspecific differences in carbon allocation patterns is useful when evaluating niche partitioning in forest communities. We hypothesized that shade-tolerant species allocate more carbon to defense and storage and less to growth compared to shade-intolerant species. In gaps and forest understory, we measured relative growth rates (RGR), carbon-based defensive compounds (condensed tannin, total phenolics), and storage compounds (total non-structural carbohydrate; TNC) in seedlings of two tree species differing in shade tolerance. RGR was greater in the shade-intolerant species, Castanea crenata, than in the shade-tolerant species, Quercus mongolica var. grosseserrata, in gaps, but did not differ between the species in the forest understory. In contrast, concentrations of condensed tannin and total phenolics were greater in Quercus than in Castanea at both sites. TNC pool sizes did not differ between the species. Condensed tannin concentrations increased with increasing growth rate of structural biomass (GRstr) in Quercus but not in Castanea. TNC pool sizes increased with increasing GRstr in both species, but the rate of increase did not differ between the species. Accordingly, the amount of condensed tannin against TNC pool sizes was usually higher in Quercus than in Castanea. Hence, Quercus preferentially invested more carbon in defense than in storage. Such a large allocation of carbon to defense would be advantageous for a shade-tolerant species, allowing Quercus to persist in the forest understory where damage from herbivores and pathogens is costly. In contrast, the shade-intolerant Castanea preferentially invested more carbon in growth rather than defense (and similar amounts in storage as Quercus), ensuring establishment success in gaps, where severe competition occurs for light among neighboring plants. These contrasting carbon allocation patterns are closely associated with strategies for persistence in these species’ respective habitats.     

Responses of temperate woody seedlings to shade and drought: do trade-offs limit potential niche differentiation?

Diversity in seedling responses to combined shade and drought can drive species niche differences, and thus natural forest and scrub establishment dynamics and diversity. However, inherent trade-offs between shade tolerance and drought tolerance, as hypothesized in the literature, would constrain potential niche differentiation. For thirteen species of European trees and shrubs the impacts were determined of moderate and extreme drought on the growth and survival of first-year seedlings in a given soil volume, in irradiances in the range typical for temperate forest and scrub understories (3% daylight) and large gaps (30% daylight). Pots were watered differentially each second day to equalize soil water content across species and irradiances. Comparisons within and across species supported independent tolerances of shade and drought rather than trade-offs. For all species, drought reduced relative growth rate in dry mass by the same proportion in 3% daylight and in 30% daylight. Consequently, drought generally reduced final dry mass significantly more strongly in 30% daylight than in 3% daylight. Extreme drought led to earlier mortality in 30% daylight than in 3% daylight for nine of the eleven species tested, to earlier mortality in 3% daylight for one species, and to equal mortality rate in both irradiances for one species. For each species, growth-based shade tolerance was quantified as the ratio of absolute growth in low irradiance to that in high irradiance, and growth-based drought tolerance as the ratio of absolute growth in low water supply to that in high water supply. Across species, growth-based shade tolerance varied ≈9-fold, and growth-based drought tolerance ≈2-fold; species’ tolerances correlated respectively with indices of field establishment in shade and drought. Growth-based drought tolerance correlated with survival time in extreme drought. Experimentally quantified shade and drought tolerances varied independently for the 13 species tested, indicating the potential for extensive species niche differentiation in combinations of irradiance and water supply.     

Relations between vulnerability to xylem embolism and xylem conduit dimensions in young trees of Quercus corris

Measurements of xylem conduit length and width and the distribution of xylem conduit ends were made in inter-nodes (I), nodes (N) and twig junctions (J) of 1-, 2- and 3-year-old twigs of plants of Quercus cerris L. Parallel measurements were also made of the loss of hydraulic conductivity of twigs subjected to pressure differentials across conduit pit membranes, equalling the leaf water potential at the turgor loss point. The loss of theoretical hydraulic conductivity was calculated as the ratio of i esivr⁴ (where r is the conduit radius) of the non-conducting conduits to that of all the conduits in the outermost wood ring of I, N and J. Stem zones such as 1-year-old nodes and junctions were localized with narrower and shorter xylem conduits and with higher percentages of conduit ends than internodes. Such ‘constricted zonesrsquo; were less vulnerable to embolism than internodes. Latewood conduits were consistently narrower, shorter and less vulnerable to embolism than earlywood ones. A positive relation therefore existed between conduit diameter and length and vulnerability to embolism. The overall vulnerability to embolism of Q. cerris plants is discussed in terms of xylem conduit width and length and of the distribution of conduit ends.