Wood anatomical correlates with theoretical conductivity and wood density across China: evolutionary evidence of the functional differentiation of axial and radial parenchyma

Background and Aims

In recent years considerable effort has focused on linking wood anatomy and key ecological traits. Studies analysing large databases have described how these ecological traits vary as a function of wood anatomical traits related to conduction and support, but have not considered how these functions interact with cells involved in storage of water and carbohydrates (i.e. parenchyma cells).

Methods

We analyzed, in a phylogenetic context, the functional relationship between cell types performing each of the three xylem functions (conduction, support and storage) and wood density and theoretical conductivity using a sample of approx. 800 tree species from China.

Key Results

Axial parenchyma and rays had distinct evolutionary correlation patterns. An evolutionary link was found between high conduction capacity and larger amounts of axial parenchyma that is probably related to water storage capacity and embolism repair, while larger amounts of ray tissue have evolved with increased mechanical support and reduced hydraulic capacity. In a phylogenetic principal component analysis this association of axial parenchyma with increased conduction capacity and rays with wood density represented orthogonal axes of variation. In multivariate space, however, the proportion of rays might be positively associated with conductance and negatively with wood density, indicating flexibility in these axes in species with wide rays.

Conclusions

The findings suggest that parenchyma types may differ in function. The functional axes represented by different cell types were conserved across lineages, suggesting a significant role in the ecological strategies of the angiosperms.     

Wood anatomy and wood density in shrubs: Responses to varying aridity along transcontinental transects

Wood density plays a key role in ecological strategies and life history variation in woody plants, but little is known about its anatomical basis in shrubs. We quantified the relationships between wood density, anatomy, and climate in 61 shrub species from eight field sites along latitudinal belts between 31° and 35° in North and South America. Measurements included cell dimensions, transverse areas of each xylem cell type and percentage contact between different cell types and vessels. Wood density was more significantly correlated with precipitation and aridity than with temperature. High wood density was achieved through reductions in cell size and increases in the proportion of wall relative to lumen. Wood density was independent of vessel traits, suggesting that this trait does not impose conduction limitations in shrubs. The proportion of fibers in direct contact with vessels decreased with and was independent of wood density, indicating that the number of fiber-vessel contacts does not explain the previously observed correlation between wood density and implosion resistance. Axial and radial parenchyma each had a significant but opposite association with wood density. Fiber size and wall thickness link wood density, life history, and ecological strategies by controlling the proportion of carbon invested per unit stem volume.     

Exploring wood anatomy,density and chemistry profiles to understand the tree-ring formation in Amazonian tree species

Long-term analysis of tree growth using annual tree rings is increasingly in demand for tropical tree species. The basis of these studies has traditionally been the anatomical identification of the annual ring boundary. However, the structure of these annual rings has been sparsely explored for complementary physical and chemical wood traits. Here, we explore the relationships among wood density features and chemical elements (S, K, Ca, Mn) involved in the annual tree ring formation of 12 tropical tree species from non-flooded forest in the southern Amazon basin. Transverse wood sections were used for each species to determine: 1) macroscopic distinction (radial growth and wood density), 2) microscopic analyse of vessels, axial and ray parenchyma (anatomy) and 3) X-ray densitometry (physical) and X-ray fluorescence (chemical). For some species, the profiles of wood density, and Ca and Mn content showed intra- and inter-annual patterns that allowed to define and characterize the growth boundary of tree rings. Ca, K and S were mainly distributed in axial parenchyma cells, and around vessels, whereas, Mn was mainly distributed in fibres. Our results showed significant species-specific correlations between tree-ring width, density and concentrations of Ca, K and Mn. The anatomical characterization and the complementary information provided by the density and chemical profiles in some Amazonian species can represent a valuable proxy to improve the definition of annual ring-boundaries and improve the understanding of long-term growth and physiological patterns.     

Revealing Polylepis microphylla as a suitable tree species for dendrochronology and quantitative wood anatomy in the Andean montane forests

In the tropical Andes climate change is expected to increase temperatures and change precipitation patterns. To overcome the lack of systematic weather records that limits the performance of climate models in this region, the use of the environmental information contained in tree rings from tropical Andean species have been found useful to reconstruct spatio-temporal climate variability. Because classical dendrochronology based on ring-width patterns is often challenging in the tropics, alternative approaches such as Quantitative Wood Anatomy (QWA) based on the measurement and quantification of anatomical traits within tree rings can be a significant advance in the field. Here we assess the dendrochronological potential of Polylepis microphylla and its climate sensitivity by using i) classic dendrochronological methods to generate the first Tree-ring Width (TRW) chronology for this tree species spanning from 1965 to 2018; ii) radiocarbon (¹⁴C) analyses as an independent validation method to assess the annual periodicity of the tree growth layers; and iii) QWA to generate tree-ring annual records of the number (VN) and size (VS) of vessels to investigate the climate sensitivity of these anatomical traits. The annual periodicity in P. microphylla radial growth was confirmed by both dendrochronological and ¹⁴C analyses. We found that VN and VS are promising new proxies to reconstruct climate variability in this region and that they provide different information than TRW. While TRW provides information at inter-annual resolution (i.e., year-to-year variability), VN and VS generated with sectorial QWA provide intra-annual resolution for each stage of the growing process. The TRW and the anatomical traits (i.e., VN and VS) showed strong positive correlation with maximum temperature for different periods of the growing season: while VS is higher with warmer conditions prior to the growing season onset, tree-rings are wider and present higher number of vessels when warmer conditions occur during the current growing season. Our findings pointed out the suitability of P. microphylla for dendrochronological studies and may suggest a good performance of this species under the significant warming expected according to future projections for the tropical Andes.     

Growth-ring boundaries of tropical tree species: Aiding delimitation by long histological sections and wood density profiles

Recent methodological advances have opened new perspectives for tropical dendrochonological studies by facilitating the visualization, delimitation, and analyses of tree-rings. One of those improvements was brought by X-ray densitometry, which allows building radial wood density profiles at microscopic scale. Furthermore, recent methods allow for cutting long histological sections to study anatomical variations along the entire radius of trees. These techniques have mainly been applied to low wood-density species from temperate and Mediterranean regions, with only limited applications in the tropics. Here we provide an improved protocol that allows for obtaining long histological sections of tropical woods, apply it to six species with varying wood densities 0.45−0.85 g cm⁻³ (Eucalyptus grandis, Tectona grandis, Acacia mangium, Cedrela fissilis, Hymenaea courbaril, and Copaifera duckei), and explore potential applications for tree-ring analyses. We provide instructions on core-microtome knife adjustments, procedures for softening and sectioning long histological samples of high wood-density species. We also present a multi-proxy approach that combines X-ray density profiles with the histological sections that improve the characterization and distinction of the various and complex tropical growth rings anatomical markers (fibre zone, marginal parenchyma, and ring porosity). This multi-proxy approach also opens the door for obtaining quantitative anatomy and physical parameters of tropical species with (intra-annual resolution. Our proposed approach is thus not only an additional tool to improve ring-boundary delimitation of tropical species, but it also paves the way to more innovative, borderline approaches in tropical dendrochronology.     

Wood anatomy of Krameriaceae with comparisons with Zygophyllaceae: phylesis, ecology and systematics

Wood of nine species of Krameria (including all clades proposed within the genus) reveals a few characters related to infrageneric systematics; most relate primarily to ecology and habit. Wood of Krameria closely fits quantitative data reported for desert shrubs. Lack of vessel grouping correlates with the presence of densely pitted tracheids. Wood xeromorphy in Krameria may relate in part to hemiparasitism. Tracheid presence may also account for relatively low vessel density. Wood anatomy of six species of Zygophyllaceae (including both genera of Morkillioideae) is compared with that of Krameriaceae because recent phylogenies propose that these two families comprise the order Zygophyllales. Several wood characters appear to represent synapomorphies reflecting this relationship. Differences in wood anatomy between Krameriaceae and Zygophyllaceae are believed to represent autapomorphies. Notable among these include Paedomorphic Type II rays (Krameriaceae), storying (Zygophyllaceae), presence of vestured pits (Zygophyllaceae), and differentiation into vasicentric tracheids and fibre-tracheids (Zygophyllaceae). The latter feature is referable to the concept of fibre-tracheid dimorphism. Recognition of Krameriaceae as separate from Zygophyllaceae is supported by wood characters. Wood of Zygophyllales does not conflict with the idea that the order belongs to rosids, with Malpighiaceae as the outgroup of Zygophyllales.  © 2005 The Linnean Society of London, Botanical Journal of the Linnean Society , 2005, 149 , 257–270.     

Living cells in wood. 1. Absence,scarcity and histology of axial parenchyma as keys to function

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.     

Vessel diameter is related to amount and spatial arrangement of axial parenchyma in woody angiosperms

Parenchyma represents a critically important living tissue in the sapwood of the secondary xylem of woody angiosperms. Considering various interactions between parenchyma and water transporting vessels, we hypothesize a structure–function relationship between both cell types. Through a generalized additive mixed model approach based on 2,332 woody angiosperm species derived from the literature, we explored the relationship between the proportion and spatial distribution of ray and axial parenchyma and vessel size, while controlling for maximum plant height and a range of climatic factors. When factoring in maximum plant height, we found that with increasing mean annual temperatures, mean vessel diameter showed a positive correlation with axial parenchyma proportion and arrangement, but not for ray parenchyma. Species with a high axial parenchyma tissue fraction tend to have wide vessels, with most of the parenchyma packed around vessels, whereas species with small diameter vessels show a reduced amount of axial parenchyma that is not directly connected to vessels. This finding provides evidence for independent functions of axial parenchyma and ray parenchyma in large vesselled species and further supports a strong role for axial parenchyma in long‐distance xylem water transport.     

Wood anatomy of Gentianaceae, tribe Helieae, in relation to ecology, habit, systematics, and sample diameter

Twenty collections representing one species each ofSymbolanthus andTachia, and 17 species ofMacrocarpaea were studied by means of light microscopy and scanning electron microscopy (SEM). Wood details show that the three genera form a coherent group;Tachia differs from the others in only a few minor characters. Because the species studied form a natural group, wood variations within Helieae offer the basis for correlations and interpretations with respect to habit and ecology. Diameter of stems studied proves to be an important variable that must be taken into account. Correlations with stem diameter include wider vessels in outer wood of wider samples. This would correspond to deeper penetration of reliable water tables by roots of helioid trees or large shrubs. Ray height decreases with increase in stem diameter, an indication of paedomorphosis. Rays of all species are paedomorphic in histology by virtue of relative paucity or even absence of procumbent cells in multiseriate rays. Pseusoscalariform lateral wall pitting of vessels is also a feature characteristic of paedomorphosis. The assemblage of paedomorphic features correlates well with the conclusion, reached by authors who used cladistic methods, that Gentianaceae other than Gentianeae are derived from suffrutescent prennials. The Mesomorphy Ratio, which incorporates three vessel features, correlates with leaf length and with stem diameter. All Helieae are mesophytic, but to various degrees. Septate fiber-tracheids, where present, are typically near vessels and form a substitute for or an addendum to vasicentric axial parenchyma as a mechanism for photosynthate storage. Vestured pits occur on lateral wall pits of vessels of all Helieae, but not on the fibertracheids. Vestured pits show diversity withinMacrocarpaea, a feature of possible systematic significance.     

Carbon isotope fractionation in tree ring early and late wood in relation to intra-growing season water balance

We determined the stable carbon isotope composition (δ^1.3C) of cellulose extracted from early and late wood in Douglas fir [Pseudotsuga menziexii (Mirb.) Franco] tree rings. Data were obtained for the period 1962 to 1981, at the start of which the trees were 20 years old. A water balance model was used to calculate daily stand transpiration and water deficit. The model incorporates site factors (soil water availability, slope and aspect) and environmental variables (solar radiation, air temperature and rainfall). There was far greater variability in late wood than in early wood δ^1.3C. In wet years, late wood δ^1.3C was significantly lighter (by as much as 2δ) than early wood δ^1.3C but in dry years this difference was reversed. Differences between spring and summer cumulative transpiration accounted for almost 60δ of the variability in differences between early and late wood δ^1.3C. We found excellent correspondence between summer cumulative transpiration and late wood δ^1.3C, with estimates of transpiration accounting for up to 93% of the variability in δ^1.3C. Correlations between early wood δ^1.3C and spring transpiration were generally poor (r2<0.4), but we were able to identify those exceptional years in which there had been a very dry spring. Our results indicate that, while tree ring δ^1.3C correlates reasonably well with basal area increment, it is a far better indicator of inter- and intra-annual variability in water availability than radial growth.     

Variation in wood density,wood water content,stem growth and mortality among twenty‐seven tree species in a tropical rainforest on Borneo Island

Abstract Interspecific variation among wood density (WD), wood water content (WWC), tree mortality and diameter at breast height (d.b.h.) increment was examined for 27 tree species (from 13 families), based on a 9‐year interval data obtained from a permanent 1‐ha forest plot setup for long‐term studies of tree dynamics in Kuala Belong rainforest, Brunei, on Borneo Island. The species were also categorized into three adult stature groups of understorey (maximum height ≤15–20 m tall, n = 14), midcanopy (maximum height, 20–30 m tall, n = 8) and canopy/emergent (>maximum height, >30 m tall, n = 5) tree species. All measured traits varied appreciably among species. Tree WD varied between 0.3 and 0.8 g cm⁻³, and exhibited the least coefficient of variation (14.7%). D.b.h. increment was low, averaging 1.05 (95% confidence limits: 0.57–2.13) mm year⁻¹ and was attributed to predominance of understorey species in the sampled plot. Overall, annual mortality was also low, averaging 2.73% per year. The three adult stature groups differed significantly in d.b.h. increment and WWC but not in tree mortality and WD. Across species and especially more so when phylogenetic effect is minimized, WD was negatively related to tree mortality and d.b.h. increment, while a positive trend was observed between d.b.h. increment and tree mortality. A negative trend was also detected between maximum plant height and WWC, which was interpreted as a consequence of increased evaporative demand and use of xylem stored water by taller trees in order to compensate for hydraulic limitations to water transport induced by frictional resistance. No doubt, the traits chosen may vary spatially, but the consistent interspecific patterns observed in this study among coexisting species of differing adult stature reflect ‘vertical’ niche differentiation and may help to explain population regulation in a multispecies ecosystem like tropical rainforest.     

Environmental correlates of tree biomass, basal area, wood specific gravity and stem density gradients in Borneo's tropical forests

Aim Tropical forests have been recognized as important global carbon sinks and sources. However, many uncertainties about the spatial distribution of live tree above‐ground biomass (AGB) remain, mostly due to limited availability of AGB field data. Recent studies in the Amazon have already shown the importance of large sample size for accurate AGB gradient analysis. Here we use a large stem density, basal area, community wood density and AGB dataset to study and explain their spatial patterns in an Asian tropical forest. Location Borneo, Southeast Asia. Methods We combined stem density, basal area, community wood density and AGB data from 83 locations in Borneo with an environmental database containing elevation, climate and soil variables. The Akaike information criterion was used to select models and environmental variables that best explained the observed values of stem density, basal area, community wood density and AGB. These models were used to extrapolate these parameters across Borneo. Results We found that wood density, stem density, basal area and AGB respond significantly, but differentially, to the environment. AGB was only correlated with basal area, but not with stem density and community wood specific gravity. Main conclusions Unlike results from Amazonian forests, soil fertility was an important positive correlate for AGB in Borneo while community wood density, which is a main driver of AGB in the Neotropics, did not correlate with AGB in Borneo. Also, Borneo's average AGB of 457.1 Mg ha^?1 was c. 60% higher than the Amazonian average of 288.6 Mg ha^?1. We find evidence that this difference might be partly explained by the high density of large wind‐dispersed Dipterocarpaceae in Borneo, which need to be tall and emergent to disperse their seeds. Our results emphasize the importance of Bornean forests as carbon sinks and sources due to their high carbon storage capacity.     

Wood density predicts plant damage and vegetative recovery rates caused by cyclone disturbance in tropical rainforest tree species of North Queensland,Australia

Abstract The ability to withstand disturbance (resistance) and the ability to recover biomass following disturbance (resilience) were investigated in Australian wet tropical rainforest tree species. These two attributes are expected to be negatively correlated, because investment of biomass in structural support (conferring resistance) results in trees exhibiting high wood densities and slow growth rates, and vice versa. We examined species’ responses to disturbance caused by a severe tropical cyclone to test this hypothesized trade‐off. We assessed cyclone damage in six species in three Mabi rainforest fragments on the Atherton Tablelands. Species differed in the proportion of individuals within four damage categories (minor damage, severe branch damage, snapped, uprooted). Resistance was positively related to wood density. We found a positive correlation between the proportion of trees experiencing minor damage only and wood density, supporting the hypothesized association between resistance and mechanical strength. Among the subset of trees in which stems snapped, rates of resprouting differed between species and were highest in low wood density species and lowest in species with highest wood density. Resilience, characterized as the ability to recover biomass following disturbance and estimated as growth rate standardized for stem diameter at breast height (g day^?1 · mm^?1), was negatively related to wood density. Thus, species with low wood densities were more likely to suffer stem and branch damage owing to cyclonic winds, but also demonstrated highest resprouting and fastest responses in terms of redeveloping biomass in the 8 months following disturbance. This suggests that a species’ position along the resistance–resilience spectrum can be predicted by mean wood density, which may allow managers to predict species’ responses to future cyclones. Our findings also provide mechanistic evidence for the ‘direct regeneration’ model of post‐cyclone succession, where response is characterized by resprouting and species composition is unchanged.     

Relationships between water,nutrients and productivity in Australian forests: Application to wood production and quality

The application of knowledge of water and nutrient relationships to improve forest management is discussed from an Australian perspective. The objectives of tree planting and forest management have become diverse, and there are outstanding examples of successful application of research results to forestry.Experiments seeking to explain the way water and nutrients influence growth tend to use treatments designed to ensure large differences in growth to increase the opportunities for identifying the mechanisms involved. The application of results from such research to many forestry situations, however, is harder than from research in which there is a closer match between treatments and management practices. The expectations of process-based models as management tools for economic decision-making is yet to be fulfilled. More progress is required in our ability to predict accurately the effects of soil and stand management practices on the production of marketable wood.The extent to which results of research on silvicultural practices are applied in practice is ultimately dependent upon economic return from investment. Water and nutrient relations have a significant influence on production, harvest index and log and wood quality. Recognition and understanding of this influence and the availability of management-oriented growth models incorporating process-based information, will permit better assessment of potential returns from management options.