Xylem Anatomical Traits Research Articles

Xylem anatomical and growth responses of the dwarf shrub Vaccinium myrtillus to experimental CO2 enrichment and soil warming at treeline

Plant growth responses to environmental changes may be linked to xylem anatomical adjustments. The study of such links is essential for improving our understanding of plant functioning under global change. We investigated the xylem anatomy and above-ground growth of the dwarf shrub Vaccinium myrtillus in the understorey of Larix decidua and Pinus uncinata at the Swiss treeline after 9 years of free-air CO2 enrichment (+200 ppm) and 6 years of soil warming (+4 °C). We aimed to determine the responses of xylem anatomical traits and growth to these treatments, and to analyse xylem anatomy–growth relationships. We quantified anatomical characteristics of vessels and ray parenchyma and measured xylem ring width (RW), above-ground biomass and shoot elongation as growth parameters. Our results showed strong positive correlations between theoretical hydraulic conductivity (Kh) and shoot increment length or total biomass across all treatments. However, while soil warming stimulated shoot elongation and RW, it reduced vessel size (Dh) by 14%. Elevated CO2 had smaller effects than soil warming: it increased Dh (5%) in the last experimental years and only influenced growth by increasing basal stem size. The abundance of ray parenchyma, representing storage capacity, did not change under any treatment. Our results demonstrate a link between growth and stem Kh in V. myrtillus, but its growth responses to warming were not explained by the observed xylem anatomical changes. Smaller Dh under warming may increase resistance to freezing events frequently occurring at treeline and suggests that hydraulic efficiency is not limiting for V. myrtillus growing on moist soils at treeline. Our findings suggest that future higher atmospheric CO2 concentrations will have smaller effects on V. myrtillus growth and functioning than rising temperatures at high elevations; further, growth stimulation of this species under future warmer conditions may not be synchronized with xylem adjustments favouring hydraulic efficiency.

Acclimation of branch and leaf hydraulics in adult Fagus sylvatica and Picea abies in a forest through-fall exclusion experiment.

Decreasing water availability due to climate change poses the question of whether and to what extent tree species are able to hydraulically acclimate and how hydraulic traits of stems and leaves are coordinated under drought. In a through-fall exclusion experiment, hydraulic acclimation was analyzed in a mixed forest stand of Fagus sylvatica L. and Picea abies (L.) Karst. In drought-stressed (TE, through-fall exclusion over 2 years) and control (CO) trees, hydraulic vulnerability was studied in branches as well as in leaves (F. sylvatica) and end-twigs (P. abies, entirely formed during the drought period) sampled at the same height in sun-exposed portions of the tree crown. In addition, relevant xylem anatomical traits and leaf pressure-volume relations were analyzed. The TE trees reached pre-dawn water potentials down to -1.6 MPa. In both species, water potentials at 50% loss of xylem hydraulic conductivity were ~0.4 MPa more negative in TE than in CO branches. Foliage hydraulic vulnerability (expressed as water potential at 50% loss of leaf/end-twig hydraulic conductance) and water potential at turgor loss point were also, respectively, 0.4 and 0.5 MPa lower in TE trees. Minor differences were observed in conduit mean hydraulic diameter and cell wall reinforcement. Our findings indicate significant and fast hydraulic acclimation under relatively mild drought in both tree species. Acclimation was well coordinated between branches and foliage, which might be essential for survival and productivity of mature trees under future drought periods.

Axial xylem architecture ofLarix deciduaexposed to CO2enrichment and soil warming at the tree line

AbstractTrees continuously adjust their axial xylem structure to meet changing needs imposed by ontogenetic and environmental changes. These axial structure–function responses need to be coordinated among competing biophysical constraints to avoid failure of the xylem system. Here, we investigated if ontogeny or experimental manipulation ofCO2and soil temperature influence these structure–function responses.We performed detailed xylem cell anatomical quantification along the axis of 40‐year‐oldLarix deciduatrees planted at the Swiss tree line and exposed to a combination of elevatedCO2(+200 ppm) and soil warming (+4°C) between 2001 and 2012. We assessed how mean hydraulic tracheid diameter (Dh), the cell wall reinforcement ((t/b)2), tracheid wall thickness (CWT) and the percent area of ray parenchyma (PERPAR)—proxies for hydraulic efficiency, hydraulic safety, biomechanical support and metabolic xylem functions, respectively—covary along the tree axis.Dh increased from the stem apex to base, strictly following a power function (R2=0.81), independent from ontogeny and experimental treatments. In contrast, axial trends of(t/b)2and CWT were either influenced by treatment and/or ontogeny, or showed no axial trend (PERPAR). Additionally, we found that a largerDh only at the stem apex promoted primary and secondary growth.Our approach of analysing xylem anatomical traits along the tree axis and across tree rings provides novel insights into xylem functional architecture and allows reconstructing xylem function over time. We conclude that the maintenance of hydraulic efficiency during ontogeny is very robust, that the tracheid diameter undergoes a strong apical control, and plays a fundamental role for assimilation and tree growth. Instead, the other functional traits more plastically vary with ontogeny and environmental changes.Aplain language summaryis available for this article.

Xylem Anatomical Trait Variability Provides Insight on the Climate-Growth Relationship of Betula nana in Western Greenland

ABSTRACTClimate change has been reported to affect shrub growth positively at several sites at high northern latitudes, including several arctic environments. The observed growth rates are, however, not uniform in space and time, and the mechanistic drivers of these patterns remain poorly understood. Here we investigated spatio-temporal interactions between climatic conditions, xylem anatomical traits, and annual growth of 21 Betula nana L. individuals from western Greenland for the period 2001–2011. Structural equation modeling showed that summer precipitation and winter temperature are affecting annual growth positively. Furthermore, vessel lumen area and vessel grouping, which are related to water conductivity and hydraulic connectivity of the xylem, respectively, positively influenced annual growth. To optimize growth B. nana was thus able to adjust its water transporting system. Annual variation in vessel lumen area seemed to be driven mostly by spring and summer temperatures, whereas annual variation in vessel grouping was driven by winter temperature. Linear models did not reveal a pattern in the spatial variation of xylem anatomical traits across the sampled climatic gradient. However, growth was positively correlated with local variation in insolation. Our results suggest that B. nana can adjust its hydraulic capacity to annual fluctuations in climatic conditions in order to optimize its total radial stem growth rate.

Vascular development in very young conifer seedlings: Theoretical hydraulic capacities and potential resistance to embolism.

Conifers have the highest rates of mortality during their first year, often attributed to water stress; yet, this tree life stage is the least studied in terms of hydraulic properties. Previous work has revealed correlations between xylem anatomy to both hydraulic transport capacity and resistance to hydraulic dysfunction. In this study, we compared xylem anatomical and plant functional traits of Pseudotsuga menziesii, Larix occidentalis, and Pinus ponderosa seedlings over the first 10 wk of growth to evaluate potential maximum hydraulic capabilities and resistance to drought-induced embolism. We hypothesized that, based on key functional traits of the xylem, predicted xylem embolism resistance of the species will reflect their previously determined drought tolerances with L. occidentalis, P. menziesii, and P. ponderosa in order of least to most embolism-resistant xylem. Xylem and pit anatomical characteristics and additional hydraulic-related functional traits were compared at five times during the first 10 wk of growth using confocal laser scanning microscopy (CLSM). Based on thickness to span ratio, torus to pit aperture overlap, and torus thickness, primary xylem appeared to be not only more hydraulically conductive but also less embolism-resistant than secondary xylem. By week 10, P. menziesii was predicted to have the most embolism-resistant xylem followed by P. ponderosa and L. occidentalis. Theoretical measurements suggest that hydraulic transport capacities and vulnerability to embolism varied for each species over the first 10 wk of growth; thus, the timing of germination and onset of limited soil moisture is critical for growth and survival of seedlings.

Sex determines xylem anatomy in a dioecious conifer: hydraulic consequences in a drier world.

Increased drought frequency and severity may reshape tree species distribution in arid environments. Dioecious tree species may be more sensitive to climate warming if sex-related vulnerability to drought occurs, since lower performance of one sex may drive differential stress tolerance, sex-related mortality rates and biased sex ratios. We explored the effect of sex and environment on branch hydraulic (hydraulic conductivity and vulnerability to embolism) and trunk anatomical traits in both sexes of the dioecious conifer Juniperus thurifera L. at two sites with contrasting water availability. Additionally, we tested for a trade-off between hydraulic safety (vulnerability to embolism) and efficiency (hydraulic conductivity). Vulnerability to embolism and hydraulic conductivity were unaffected by sex or site at branch level. In contrast, sex played a significant role in xylem anatomy. We found a trade-off between hydraulic safety and efficiency, with larger conductivities related to higher vulnerabilities to embolism. At the anatomical level, females' trunk showed xylem anatomical traits related to greater hydraulic efficiency (higher theoretical hydraulic conductivity) over safety (thinner tracheid walls, lower Mork's Index), whereas males' trunk anatomy followed a more conservative strategy, especially in the drier site. Reconciling the discrepancy between branch hydraulic function and trunk xylem anatomy would require a thorough and integrated understanding of the tree structure-function relationship at the whole-plant level. Nevertheless, lower construction costs and higher efficiency in females' xylem anatomy at trunk level might explain the previously observed higher growth rates in mesic habitats. However, prioritizing efficiency over safety in trunk construction might make females more sensitive to drought, endangering the species' persistence in a drier world.

Xylem anatomical traits reveal different strategies of two Mediterranean oaks to cope with drought and warming

Performance and survival of Mediterranean trees depend on their capacity to cope with water stress. In harsh environments, xylem growth strategies are critical to ensure efficient water transport, though these are largely unknown for many species, including most Mediterranean oaks. We investigated xylem anatomical traits in tree-ring series of deciduous Quercus ithaburensis and Q. boissieri in the South-Eastern Mediterranean Basin to assess xylem response to climate variability, with special attention to dry and warm years and to temperature increase over the last decades. Abundant precipitation and low temperature during the wet season (November–April) benefited xylem formation of both species. However, intra-ring analysis revealed different patterns, as the size of early-formed vessels in Q. boissieri was related to previous-year ring, while in Q. ithaburensis it was strongly affected by current wet season conditions. During dry years, vessel size and number in Q. ithaburensis were strongly reduced, but they fully recovered in the following year (high resilience). Conversely, Q. boissieri vessels were barely reduced during dry or warm years (high resistance). Different strategies allow both species to overcome dry and warm years, but their capacity to withstand long-term warming seems to differ. Q. ithaburensis xylem traits did not evidence any trend over the last few decades, while Q. boissieri was facing a decline in some traits. Our analysis suggests that the growth strategies of Q. ithaburensis would be effective under future drier conditions, while temperature increase could induce a hydraulic deterioration and a potential decline in the less fit Q. boissieri.

Fast-growing Acer rubrum differs from slow-growing Quercus alba in leaf, xylem and hydraulic trait coordination responses to simulated acid rain.

We investigated the effects of historic soil chemistry changes associated with acid rain, i.e., reduced soil pH and a shift from nitrogen (N)- to phosphorus (P)-limitation, on the coordination of leaf water demand and xylem hydraulic supply traits in two co-occurring temperate tree species differing in growth rate. Using a full-factorial design (N × P × pH), we measured leaf nutrient content, water relations, leaf-level and canopy-level gas exchange, total biomass and allocation, as well as stem xylem anatomy and hydraulic function for greenhouse-grown saplings of fast-growing Acer rubrum (L.) and slow-growing Quercus alba (L.). We used principle component analysis to characterize trait coordination. We found that N-limitation, but not P-limitation, had a significant impact on plant water relations and hydraulic coordination of both species. Fast-growing A. rubrum made hydraulic adjustments in response to N-limitation, but trait coordination was variable within treatments and did not fully compensate for changing allocation across N-availability. For slow-growing Q. alba, N-limitation engendered more strict coordination of leaf and xylem traits, resulting in similar leaf water content and hydraulic function across all treatments. Finally, low pH reduced the propensity of both species to adjust leaf water relations and xylem anatomical traits in response to nutrient manipulations. Our data suggest that a shift from N- to P-limitation has had a negative impact on the water relations and hydraulic function of A. rubrum to a greater extent than for Q. alba We suggest that current expansion of A. rubrum populations could be tempered by acidic N-deposition, which may restrict it to more mesic microsites. The disruption of hydraulic acclimation and coordination at low pH is emphasized as an interesting area of future study.

The Imprint of Extreme Climate Events in Century-Long Time Series of Wood Anatomical Traits in High-Elevation Conifers.

Extreme climate events are of key importance for forest ecosystems. However, both the inherent infrequency, stochasticity and multiplicity of extreme climate events, and the array of biological responses, challenges investigations. To cope with the long life cycle of trees and the paucity of the extreme events themselves, our inferences should be based on long-term observations. In this context, tree rings and the related xylem anatomical traits represent promising sources of information, due to the wide time perspective and quality of the information they can provide. Here we test, on two high-elevation conifers (Larix decidua and Picea abies sampled at 2100 m a.s.l. in the Eastern Alps), the associations among temperature extremes during the growing season and xylem anatomical traits, specifically the number of cells per ring (CN), cell wall thickness (CWT), and cell diameter (CD). To better track the effect of extreme events over the growing season, tree rings were partitioned in 10 sectors. Climate variability has been reconstructed, for 1800–2011 at monthly resolution and for 1926–2011 at daily resolution, by exploiting the excellent availability of very long and high quality instrumental records available for the surrounding area, and taking into account the relationship between meteorological variables and site topographical settings. Summer temperature influenced anatomical traits of both species, and tree-ring anatomical profiles resulted as being associated to temperature extremes. Most of the extreme values in anatomical traits occurred with warm (positive extremes) or cold (negative) conditions. However, 0–34% of occurrences did not match a temperature extreme event. Specifically, CWT and CN extremes were more clearly associated to climate than CD, which presented a bias to track cold extremes. Dendroanatomical analysis, coupled to high-quality daily-resolved climate records, seems a promising approach to study the effects of extreme events on trees, but further investigations are needed to improve our comprehension of the critical role of such elusive events in forest ecosystems.

Divergent climate response on hydraulic-related xylem anatomical traits of Picea abies along a 900-m altitudinal gradient.

Climate change can induce substantial modifications in xylem structure and water transport capacity of trees exposed to environmental constraints. To elucidate mechanisms of xylem plasticity in response to climate, we retrospectively analysed different cell anatomical parameters over tree-ring series in Norway spruce (Picea abies L. Karst.). We sampled 24 trees along an altitudinal gradient (1200, 1600 and 2100 m above sea level, a.s.l.) and processed 2335 ± 1809 cells per ring. Time series for median cell lumen area (MCA), cell number (CN), tree-ring width (RW) and tree-ring-specific hydraulic conductivity (Kr) were crossed with daily temperature and precipitation records (1926-2011) to identify climate influence on xylem anatomical traits. Higher Kr at the low elevation site was due to higher MCA and CN. These variables were related to different aspects of intra-seasonal climatic variability under different environmental conditions, with MCA being more sensitive to summer precipitation. Winter precipitation (snow) benefited most parameters in all the sites. Descending the gradient, sensitivity of xylem features to summer climate shifted mostly from temperature to precipitation. In the context of climate change, our results indicate that higher summer temperatures at high elevations will benefit cell production and xylem hydraulic efficiency, whereas reduced water availability at lower elevations could negatively affect tracheids enlargement and thus stem capacity to transport water.

Hydraulic architecture of lianas in a semiarid climate: efficiency or safety?

Xylem anatomical traits can provide insights regarding the mechanisms affecting the distribution of vascular plants across environmental gradients. In this study, we aimed to investigate the hypothesis that lianas occurring in semiarid environments have characteristics that maximize the xylem resistance to tension-induced cavitation along the root-stem-branch continuum. To gather information regarding the hydraulic architecture of the lianas, we analyzed several anatomical traits of wood: cross-sectional area occupied by the parenchyma (AP), fibers (AF), and vessels (AV); average vessel diameter (d); wood density (WD); pit diameter in the vessel wall (dpit); pit density (Npit), and potential hydraulic conductivity (Kp) in branches, stems, and roots of three congeneric species of lianas that occur in two vegetation types of the semiarid regions of Brazil. We found that lianas in these semiarid environments possess a number of the following xylem traits that may allow resistance to tension-induced cavitation:1) lower vessel diameter, lower Kp, and higher hydraulic safety in roots and branches; 2) Dimorphic vessels, ensuring both hydraulic efficiency and safety; and 3) small diameter of pits (potentially associated with a decrease in the membrane area of the vessel pits). This suite of traits may provide insight into mechanisms allowing lianas to occur in semiarid environments.

How drought and deciduousness shape xylem plasticity in three Costa Rican woody plant species

This paper explores the phenotypic plasticity of xylem in tropical trees in order to test the hypothesis that different leaf phenological patterns influence levels of xylem plasticity. Wood anatomy was studied in the wet-deciduous species Cordia alliodora (Ruiz & Pav.) Oken, the dry-deciduous species Tabebuia rosea (Bertol.) DC., and the evergreen species Ocotea veraguensis (Meisn.) Mez., collected from seasonally dry forest and tropical cloud forest in Costa Rica. Xylem plasticity and trait conservatism were examined by analysing the coefficient of variation (CV) and the relative distance plasticity index (RDPI) of xylem anatomical traits. The two deciduous species exhibited wider vessels, lower wood density, and higher Huber values than the evergreen species. Furthermore, intervessel connectivity was highest for the two deciduous species in seasonally dry forest compared to cloud forest, whereas the opposite was found for the evergreen species. Overall highest trait variability was found for all plants at the seasonally dry site. The evergreen species O. veraguensis had the highest plasticity values compared to the deciduous species. Highest plasticity was found for vessel composition index (vessel area/vessel number), whilestrongest trait conservatism was found for vessel diameter. In conclusion, our data indicate that evergreen O. veraguensis does not show less xylem plasticity than the two deciduous tree species studied.

Plasticity in xylem anatomical traits of two tropical species in response to intra-seasonal climate variability

Key message Analyses of tree-ring anatomical features showed to be more sensitive to specific intra-seasonal environmental factors than tree-ring width in Tectona grandis and Pinus caribaea growing in a subtropical region.

Hydraulic conductivity traits predict growth rates and adult stature of 40 Asian tropical tree species better than wood density

Summary1. Stem xylem characteristics have a great impact on growth and adult stature of trees because of their role in mechanical support, long‐distance water transport and whole‐plant carbon allocation. Yet, despite the potential causal link between xylem traits and plant growth/adult stature, most studies have tried to link wood density, an indirect but easy to measure proxy for wood properties, to tree growth and size.2. To determine whether xylem traits outperform wood density as predictors of tree growth and stature, we evaluated the covariation among wood density, xylem anatomical traits, tree diameter growth rate and adult stature in 40 Asian tropical tree species through principal component analyses and through bivariate correlation, both across species and across phylogenetically independent contrasts.3. Vessel diameter exhibited a tight negative relationship with vessel frequency. Wood density showed a significant correlation with vessel diameter and density, but not with vessel fraction. Most correlations between functional traits indicate adaptive coordination, demonstrated by significant correlations between phylogenetically independent contrasts.4. Across species, diameter growth rate and adult stature were positively correlated with vessel lumen diameter and potential hydraulic conductivity, but not with wood density. Thus, our results suggest that xylem anatomical traits that are linked to hydraulic conductivity are better predictors of tree growth rate and adult stature than wood density.5. Synthesis. We found that xylem anatomical traits have a more significant influence on whole‐plant performance due to their direct association with stem hydraulic conductivity, whereas wood density is decoupled from hydraulic function due to complex variations in xylem components.

Interspecific relationships among growth, mortality and xylem traits of woody species from New Zealand

Summary 1. Wood density is considered a key functional trait influencing the growth and survival of woody plants and has been shown to be related to a slow–fast rate‐of‐living continuum. Wood density is, however, an emergent trait arising from several vascular properties of wood, including the diameter and frequency of xylem conduits. 2. We aimed to test the hypotheses that there is a set of inter‐related trade‐offs linked to the different functions of wood, that these trade‐offs have direct consequences for tree growth and survival and that these trade‐offs underlie the observed correlations between wood density and demographic rates. We evaluated the covariation between xylem anatomical traits among woody species of New Zealand and whether that covariation had the potential to constrain variation in wood density and demographic rates. 3. Several xylem traits were strongly correlated with each other, but wood density was not correlated with any of them. We also found no significant relationships between wood density and growth or mortality rate. Instead, growth was strongly related to xylem traits associated with hydraulic capacity (conduit diameter and a conductivity index) and to maximum height, whereas mortality rate was strongly correlated only with maximum height. The diameter and frequency of conduits exhibited a significant negative relationship, suggesting a trade‐off, which restricted variation in wood density and growth rate, but not mortality rate. 4. Our results suggest, for woody species in New Zealand, that growth rate is more closely linked to xylem traits determining hydraulic conductance, rather than wood density. We also found no evidence that denser woods conferred higher survival, or that risk of cavitation caused by wide conduits increased mortality. 5. In summary, we found little support for the idea that wood density is a good proxy for position along a fast–slow rate‐of‐living continuum. Instead, the strong, negative relationship between vessel diameter and frequency may constrain the realized diversity of demographic niches of tree species in New Zealand. Trade‐offs in function therefore have the potential to shape functional diversity and ecology of forest communities by linking selection on structure and function to population‐level dynamics.

Stem responses to damage: the evolutionary ecology of Quercus species in contrasting fire regimes

* The ability of tree stems to recover from damage is critical for tree survival and may explain species distributions across disturbance regimes. Two primary responses to stem damage, decay compartmentalization and wound closure, act in concert to limit decay and pathogen spread. A previous study demonstrated a tradeoff between wound responses that varied with anatomical traits, but its wide taxonomic range made it hard to analyze responses in an evolutionary context. * Here, we tested the stem wound responses of 13 species of Quercus inhabiting three habitats across a gradient of fire intensity. We also quantified anatomical and structural traits and phylogenetic position, in order to assess the relative contributions of ecological adaptation and phylogenetic history in determining traits. * Xylem anatomical traits were phylogenetically constrained, while phloem traits and damage responses varied with habitat. Across habitats, hammock and sandhill species closed bark wounds effectively, whereas scrub species limited the spread of xylem decay. There was a tradeoff between wound closure and decay compartmentalization within the white+live oaks. * The fact that some wound response traits are phylogenetically constrained while others respond to ecological pressures suggests that damage responses integrate mechanisms operating at several levels within plants.

Xylem anatomical traits related to resinous heartwood formation in

Xylem anatomical traits related to resinous heartwood formation in