A phenology-based approach to the analysis of conifers intra-annual xylem anatomy in water-limited environments

Xylem structure and cambial phenology (i.e. onset and cessation of cambial cell division) of conifers growing under severe water-limitations can change dramatically in relation to moisture availability. In hyperarid environments, analytical tools commonly used to investigate intra-annual variability of xylem anatomy (i.e. tracheidograms), may fail to capture the complexity of tree phenological responses to environmental conditions. This greatly limits our ability to accurately date the onset of intra-annual density variations, including the transition between earlywood and latewood. I present a new approach for developing phenological tracheidograms (“pheno-tracheidograms”) calibrated to account for the seasonal variations in cell division rates. Pheno-tracheidograms were developed for a population of Pinus ponderosa in the Mojave Desert (Nevada, USA) during the period 2015–2016 in order 1) to determine the onset date of latewood formation and 2) to investigate relationships between environmental conditions, lumen diameter, and cell wall thickness targeting specific climatic windows for each tracheid. Pheno-tracheidograms were standardized at the tree-level, showing more flexibility compared to tracheidograms standardized according to a pre-determined number of cells. By displaying cellular parameters with respect to the date of formation of the tracheid to which each measurement is associated, pheno-tracheidograms allowed to determine the beginning of latewood formation with daily resolution. Lumen diameter was significantly correlated with the onset date of cellular enlargement, while cell wall thickness showed a weaker relationship with the beginning of secondary wall deposition. Soil moisture positively affected the duration of cell enlargement and tracheid lumen diameter, particularly in the earlywood, while cell wall thickness was not significantly influenced by environmental conditions. Pheno-tracheidograms represent an empirical, yet effective way to date intra-annual xylem structures and to investigate high-resolution climate-anatomy relationships in conifer species from arid environments characterized by high phenological plasticity.     

Siberian spruce tree ring anatomy: imprint of development processes and their high-temporal environmental regulation

Wood anatomy was offered as spatiotemporal proxy record for tracheid differentiation kinetics due to its advantages in terms of much longer cover period and less demanding measurements. In this study, external and internal regulation of earlywood-to-latewood transition and properties of latewood of Picea obovata Ledeb were considered. The values and interrelations between cell number, tree ring width, maximal and mean radial cell diameter, maximal cell wall thickness and position of the transition to thick-walled tracheids were investigated within site and along the altitudinal gradient. Correlations with moving 21-day climatic series were used to estimate high-resolutional external influences. Relationships between tree ring traits are spatially stable and close within one stage of differentiation and between cells production and expansion. Relationships between sites differ in upper and lower parts of the gradient. Most of traits respond to the primary limiting factors near summer solstice; however, maximal cell wall thickness responds positively to the temperatures at the + 10 °C threshold. Altitudinal anatomical patterns revealed interaction of intrinsic and external factors in the regulation of tracheid differentiation. Timing of climatic response highlighted role of photoperiod as a trigger in the earlywood-to-latewood transition, and crucial role of the growth season ending for latewood development.     

Structural variation of tracheids in Norway spruce (Picea abies [L.] Karst.)

The orientation of cellulose microfibrils in the cell wall and the shape and the dimensions of the cells of earlywood of four Norway spruce (Picea abies [L.] Karst.) stems grown in Finland were studied by X-ray diffraction and optical microscopy. The average microfibril angle (MFA) decreased and the diameter of the cell increased rapidly up to rings 5-10 from the pith and remained at the same level after that. The average MFA close to the pith was over 20 degrees and decreased to about 8 degrees after ring 10 from the pith. The average diameter of the cells was 35 microm in the outer rings. The shape of the cross section of the lumen changed from circular to rectangular from the pith to the bark. The tracheid length increased also as a function of the distance from the pith. The thickness of the cell wall varied between 2.8 and 3.5 microm. Automatic cell lumen and cell wall recognition procedures were developed for the analysis of the images of the cross sections of the cells.     

Potential of Schinopsis lorentzii for dendrochronological studies in subtropical dry Chaco forests of South America

The lack of knowledge about species with well-delimited annual rings has hampered the development of dendrochronological records in the subtropical Chaco region of South America. In this contribution, we present the first tree-ring chronology of Schinopsis lorentzii (Anacardiaceae), a dominant species in the semi-arid Chaco. Cross sections were collected near Las Lajitas, Salta, Argentina, and processed following the methods commonly used in dendrochronology. Annual growth variations between radii from a single individual and between radii from different trees were highly correlated. To determine the climatic parameters that control radial growth, we compared annual tree-ring variations against regional temperature and precipitation records. Correlation functions indicate that tree growth is highly influenced by spring–summer rainfall variations, which represent more than 80% of the total annual precipitation. The chronology, which covers the interval from 1829 to 2004, provides a context for the unprecedented increase in precipitation since the mid-1970s in the region. The climatic-sensitivity of S. lorentzii provides a unique opportunity to reconstruct precipitation variations during past centuries in the extensive semiarid regions of subtropical South America.     

Intra-annual tracheid formation of Norway spruce provenances in southern Finland

We studied the intra-annual wood formation in a Norway spruce provenance experiment in southern Finland from 2004–2008. Two Finnish provenances, northern and southern, as well as German and Hungarian provenances were included. Timing of tracheid formation and differentiation, and tracheid dimensions were determined from periodically extracted microcores. The aim was to determine the differences between the years and provenances in the timing of the xylogenesis and in the xylem characteristics. Year-to-year variation was high both in timing of tracheid formation and xylem characteristics, while between-provenance differences were small. The onset of tracheid formation varied from early May to late June in different trees in different years. The onset of tracheid formation was not closely related to the annual variations of temperature sum. In all the years, daily temperatures exceeded the threshold +5°C for several weeks before the onset of tracheid formation. The highest tracheid formation rate occurred after the summer solstice in all years and generally coincided with the highest daily temperatures during the growing season. Tracheid production ceased early in 2006 due to a mid-summer drought. Cell differentiation continued late in autumn as non-mature tracheids were still observed around mid-September. No clear differences between the provenances in the timing of tracheid formation were observed, although the Finnish provenances tended to initiate tracheid formation slightly earlier than the other provenances. The tree-ring widths of the Finnish provenances were also wider, while tracheid diameter of the German provenance was slightly smaller. Our results indicate that between-tree variation in the timing of wood formation is high compared with the latitude effect of seed source.     

Tracheid anatomical responses to climate in a forest-steppe in Southern Siberia

Tree-rings are precious natural archives to assess ecosystem variability over time. Xylem anatomy in woody tissue is a promising source of information in tree-rings since it is closely linked to tree hydraulics and carbon fixation. However, despite the rising interest for cell anatomy in dendrochronology, still little is known about the interpretation of the variability of cell anatomical responses observed across different environments and species.Here we analyze cell anatomical responses to increasing summer drought on 18 trees from 3 conifer species (Picea obovata, Pinus sylvestris, and Larix sibirica) growing in the transition zone between forest and steppe in the Republic of Khakassia (Russia). Analyses include the comparison of tracheid size distributions along climatic gradients and contrasting micro-topography from 1986 to 2008.Results indicate an overall decrease of earlywood tracheid lumen and cell wall thickness to high temperature and drought regardless of species and site conditions. In particular an increase of one degree Celsius during the summer caused up to 5% reduction of earlywood cell lumen and wall thickness. These anatomical shifts suggest that a downscaling of hydraulic efficiency is not paralleled by increased hydraulic safety, presumably due to carbon limitation.Based on the results of this case study, we suggest that increasing drought stress might hamper the formation of a functional xylem structure, thus being a possible trigger for a miss-acclimation causing long-term decline and higher exposure to hydraulic failures. Despite the promising study approach, more studies including more data (trees, years) and broader climatic gradients would be needed to further improve our mechanistic understanding.     

COMPARISON OF DIMENSIONS AND FIBRIL ANGLES OF LOBLOLLY PINE TRACHEIDS FORMED IN WET OR DRY GROWING SEASONS

Diameter and wall thickness of tracheids and the fibrillar angle in their S₂ layers were investigated at five relative heights within two increment sheaths of one dominant loblolly pine (Pinus taeda L.). The sheaths investigated were formed during extremes of soil moisture availability. In both increment sheaths the radial and longitudinal trends of the respective anatomical features were similar; however, the sheaths differed in the degree and rate at which their size changed from the apex to the base of the tree. Soil moisture conditions directly affected the width of the annual rings, tracheid diameter, and wall thickness but not the fibril angle of tracheid walls.     

A Comparison of Root- and Shoot-wood Development in Conifer Seedlings

Tracheid diameter, wall thickness, and wall area per tracheidincreased towards the root tip in first-year seedlings of Piceasitchensis and Pinus sylvestris; this is shown to be associatedwith differences in duration of the expansion and wall thickeningphases of tracheid development. Transfer to short days producesa similar response throughout the plant, tracheid diameter andwall thickness decreasing shortly after transfer, due to a declinein rate of development. These data are discussed in relationto growth-regulator gradients likely to exist between root andshoot. It is pointed out that though effects of growth regulatorson tracheid dimensions are well documented, it has yet to beestablished whether this is due to their regulation of the rateor of the duration of development.     

Cedrela nebulosa: A novel species for dendroclimatological studies in the montane tropics of South America

Up to now, the development of dendrochronological records from tropical regions in South America has been limited to the lowlands with emphasis in the Amazon basin. In this contribution, we present the first chronology of Cedrela nebulosa, a species that develops in the tropical mountainous regions of South America. We collected samples from trees in Monobamba district in Peru, analysed the anatomical features that determine the growth rings, and processed following the methods commonly used in dendrochronology. The 133-years chronology covering the 1883–2015 period, showed large correlation between series. In order to determine the climatic variables that control tree growth, we performed correlation analyses between tree-growth and local and regional precipitation and temperature records. We found that precipitation triggers tree growth at the beginning of the spring season but temperature seems to be the main control in annual growth. Also, C. nebulosa chronology present coherent variations with Multivariate Enso Index (MEI) and Pacific Ocean sea surface temperatures during summer months. This climate-sensitive tree-ring record indicates good potential for dendroclimatic studies and provides an opportunity to reconstruct climatic variations in montane forests of the tropical Andes.     

Relationship between wood anatomy,tree-ring widths and wood density of Pinus sylvestris L. and climate at high latitudes in northern Sweden

In this study, wood anatomy, tree-ring width and wood density of Pinus sylvestris at the northern timberline in Fennoscandia were used to identify relationships among the parameters and to screen them for their climatic signals. Furthermore we investigated the influence of the juvenile wood section for all parameters developed. The measurements of wood anatomy were conducted with confocal laser scanning microscopy (CLSM) while the density profiles were produced using an Itrax MultiScanner. We developed chronologies of ring width, wood density and anatomy for a period between 1940 and 2010. Correlations between wood density and wood anatomy were strong in the latewood part. For some wood anatomy and density chronologies youth trends were found in the juvenile part. Wood density decreased from the pith up to the 9th ring and stabilized afterwards, while cell lumen diameter and lumen area increased simultaneously up to the 15th ring. All chronologies contained strong summer temperature signals. The wood anatomical variables provided additional information about seasonal precipitation which could not be found in wood density and tree-ring widths. Our study confirmed previous results stating that the parameter maximum density contains the strongest climate signal, that is, summer temperatures at the northern timberline. Nevertheless, the intra-annual data on tracheid dimensions showed good potential to supply seasonal climatic information and improve our understanding of climatic effects on tree growth and wood formation.     

Vertical and radial profiles in tracheid characteristics along the trunk of Douglas-fir trees with implications for water transport

The main stems of three young Douglas-fir (Pseudotsuga menziesii var. menziesii (Mirbel) Franco) trees were dissected to obtain samples of secondary xylem from internodes axially along the trunk and radially within each internode. From these samples, measurements were obtained of tracheid diameter, length, the number of inter-tracheid pits per tracheid, and the diameter of the pit membranes. In addition, samples were obtained along the trunks of three old growth trees and also a small sample of roots for measurement of tracheid diameter. A gradient was apparent in all measured anatomical characters vertically along a sequence among the outer growth rings. These gradients arose not because of a gradient vertically along the internodes, but because of the strong gradients present at each internode among growth rings out from the pith. Tracheid characteristics were correlated: wider and longer tracheids had more numerous pits and wider pits, such that total pit area was about 6% of tracheid wall area independent of tracheid size. A stem model combining growth rings in parallel and internodes in series allowed for estimates of whole trunk conductance as a function of tree age. Conductance of the stem (xylem area specific conductivity) declined during the early growth of the trees, but appeared to approach a stable value as the trees aged.     

Effects of Environmental Change on Wood Production and Wood Structure in Picea sitchensis Seedlings

Changes in environment that would be expected to reduce substrateavailability, decrease the rate of xylem increment, tracheiddiameter and wall thickness, in seedlings of Picea sitchensis.But after reaching a minimum about 10 days to 3 weeks afterenvironmental change, xylem increment, tracheid wall thickness,and in some instances tracheid diameter, increase again up toabout 4 to 6 weeks after transfer. This recovery parallels arecovery in net assimilation rate, and is associated with anincrease in photosynthetic efficiency. Although the light intensity and temperature treatments imposedwere more drastic than those that would normally be expectedin the field, they had remarkably little net effect on tracheiddimensions. On the other hand change in photoperiod producedgreater changes in tracheid dimensions, photoperiodic effectsbeing superimposed on effects of change in substrate availability.It is suggested that adaptation to reduced substrate will bufferthe plant against climatic fluctuations during the growing season,while the photoperiodic response will ensure preparation forwinter dormancy. It is concluded that the major seasonal changes in tracheiddimensions are unlikely to be caused by variation in substrateavailability. Changes in light intensity and temperature haveminor effects on wood production and structure through effectson substrate availability, but the major seasonal trends aremore likely to be associated with changes in growth regulationproduction.     

Adaptive anatomy of Pinus halepensis trees from different Mediterranean environments in Spain

A study was conducted on the variation in growth, biomass, juvenile wood anatomy, and needle morphology of Pinus halepensis Mill. from three Spanish regions of provenance characterized by environmental differences, without the influence of the site factor. Seeds collected from two progenies in each region were planted in a single plot, and the trees were felled at the age of 7 years. The results showed significant differences between provenances, as well as the genetic or environmental influence on the traits analyzed. Trees adapted to moderate summer drought conditions (Inland Catalonia region) are primarily characterized by higher average values for height, diameter, biomass, cell wall thickness, inter-tracheid wall strength, pit membrane diameter, torus diameter, bordered pit aperture diameter, and ray tracheid abundance in comparison with trees adapted to severe summer drought conditions (Southern region and Balearic Islands region). The greater structural requirements of trees from the Inland Catalonia region, subjected to higher weight and wind loads, resulted in thick cell walls. Moreover, the large pits and more abundant ray tracheids in trees from this provenance would allow more efficient water transport and greater water storage capacity, respectively. The differences found between provenances suggest the adaptive nature of the anatomy of this species, which demonstrates the importance of the region of provenance when choosing reproduction material for reforestation.     

Xylem plasticity allows rapid hydraulic adjustment to annual climatic variability

Thanks to acclimation, trees overcome environmental changes and endure for centuries. The anatomy of water conducting cells is an important factor determining plant success. Forming cells are coupled with the environment and their properties are naturally archived in the wood. Its variability across tree rings can thus provide a retrospective of plant’s hydraulic adjustments. In this work, we measured lumen and wall thickness of tracheids along tree-rings to explore how trees regulate their conducting system under variable plant-water conditions. Tracheids were measured along 51 dated rings of five mature Larix decidua and Picea abies trees from a low elevation site. Anatomical-based chronologies of annual growth performance, hydraulic conductance and safety, and construction costs were built. Similarities among chronologies and the relation to monthly climate data were analyzed. Most parameters displayed high annual plasticity which was partly coherent among trees and mostly associated with radial growth. In general, summer drought reduced growth and potential hydraulic conductivity of the forming ring, and increased hydraulic safety and construction costs. To evaluate the functional relevance of the annual acclimation, the conductivity of the forming ring relative to the entire sapwood needs to be assessed.     

Variations in the tree-ring structure of Norway spruce (Picea abies) under contrasting climates

Variations in tree-ring structure from pith to bark of mature Norway spruce (Picea abies Karst. (L)) grown under contrasting climate conditions (warm-dry vs. cool-humid) in south-western Germany were investigated. Sample trees were from even-aged stands where no intensive silvicultural treatments had taken place. The cell number (CN), diameter (CD), lumen diameter (CL) and wall thickness (CW) were measured from stem cross-sections taken at breast height. A raw data chronology of each cell parameter was established for the whole annual ring (AR), earlywood (EW), latewood (LW), and transition wood (TW). The long-term trends of the cell parameters were generally non-linear, parameter-specific in AR and EW and similar over sites. Those in LW were site-specific and similar over cell parameters. The variation of the same parameter, expressed by the coefficient of variance (CV), tended to increase from EW towards LW and was clearly higher for CN than for other cell parameters of all tree-ring zones. Trees from the warm-dry site had more LW cells and substantially thicker CW, whereas those from the cool-humid site had larger EW cells. These observed differences are likely due to the hydraulic adaptation mechanisms of trees to different site conditions.     

Different climate response of three tree ring proxies of Pinus sylvestris from the Eastern Carpathians,Romania

The aim of this study was to compare the climatic responses of three tree rings proxies: tree ring width (TRW), maximum latewood density (MXD), and blue intensity (BI). For this study, 20 cores of Pinus sylvestris covering the period 1886–2015 were extracted from living non-damaged trees from the Eastern Carpathian Mountains (Romania). Each chronology was compared to monthly and daily climate data. All tree ring proxies had a stronger correlation with the daily climate data compared to monthly data. The highest correlation coefficient was obtained between the MXD chronology and daily maximum temperature over the period beginning with the end of July and ending in the middle of September (r = 0.64). The optimal intervals for the temperature signature were 01 Aug – 24 Sept for the MXD chronology, 05 Aug – 25 Aug for the BI chronology, and both 16 Nov of the previous year – 16 March of the current year and 15 Apr – 05 May for the TRW chronology. The results from our study indicate that MXD can be used as a proxy indicator for summer maximum temperature, while TRW can be used as a proxy indicator for just March maximum temperature. The weak and unstable relationship between BI and maximum temperature indicates that BI is not a good proxy indicator for climate reconstructions over the analysed region.     

Stem wood properties of mature Norway spruce after 3 years of continuous exposure to elevated [CO2] and temperature

The objective of the study was to investigate the interactive effects of elevated atmospheric carbon dioxide concentration, [CO₂], and temperature on the wood properties of mature field-grown Norway spruce ( Picea abies (L.) Karst.) trees. Material for the study was obtained from an experiment in Flakaliden, northern Sweden, where trees were grown for 3 years in whole-tree chambers at ambient (365 μmol mol⁻¹) or elevated [CO₂] (700 μmol mol⁻¹) and ambient or elevated air temperature (ambient +5.6 °C in winter and ambient +2.8 °C in summer). Elevated temperature affected both wood chemical composition and structure, but had no effect on stem radial growth. Elevated temperature decreased the concentrations of acetone-soluble extractives and soluble sugars, while mean and earlywood (EW) cell wall thickness and wood density were increased. Elevated [CO₂] had no effect on stem wood chemistry or radial growth. In wood structure, elevated [CO₂] decreased EW cell wall thickness and increased tracheid radial diameter in latewood (LW). Some significant interactions between elevated [CO₂] and temperature were found in the anatomical and physical properties of stem wood (e.g. microfibril angle, and LW cell wall thickness and density). Our results show that the wood material properties of mature Norway spruce were altered under exposure to elevated [CO₂] and temperature, although stem radial growth was not affected by the treatments.     

Effects of Light Intensity on Tracheid Dimensions in Picea sitchensis

In seedlings of Picea sitchensis grown in constant conditions,or within older trees in the field, light intensity had no neteffect on the wall thickness of tracheids produced at the samepoint in time. This appears to be due to a balanced regulatorysystem, effects of light intensity on rate of accumulation ofwall volume per leaf being offset by differences in rate ofxylem increment, and differences in wall material per tracheidbeing nullified in their effects on wall thickness by effectson tracheid diameter. Mean tracheid wall thickness across the growth ring increasedwith light intensity, due to increase in proportion of late-woodassociated with the longer duration of cambial activity at higherlight intensity, duration of wall thickening increasing duringthe season. Duration of wall thickening did not vary with lightintensity. The rate of increase in wall volume was limited by light intensity(and hence possibly by substrate availability) at all lightintensities in the field, but in seedlings in controlled conditionsthe rate of wall production was no greater at 20 000 lx thanat 6700 lx.     

Xylem traits of peatland Scots pines reveal a complex climatic signal: A study in the Eastern Italian Alps

Long-term climate reconstructions are frequently based on tree-ring high-resolution proxies extracted from subfossil peatland trees. Peatlands are peculiar ecosystems characterized by high moisture in the upper soil part which creates a harsh living environment for trees. The climate mostly indirectly influences tree growth determining seasonal variations in the water table level. Within this framework, the aim of this study was to investigate climate responses of trees (Pinus sylvestris L.) growing inside and outside a Southern Alpine peat bog, by using tree-ring and wood anatomical traits (e.g. tracheid number and dimension, cell-wall thickness). Our results showed differences in the xylem structure and climate signal recorded by peatland and mineral soil trees. Peatland trees were characterized by narrow rings and tracheids with thinner cell wall. Summer temperature and precipitation were the major drivers of xylem formation in peatland trees. At intra-annual level wood anatomical traits revealed a complex within-ring signal during the growing season. The multi-parameters approach together with the high-resolution gained by using tree-ring sectors allowed us to obtain new detailed information on the xylem development of peatland trees and climate drivers that influenced it.     

Wie wachsen Tropenbäume? Jahrringe als Ausdruck von Klimabedingungen und Lebensform

Growth of tropical trees is largely depending on the seasonality of the local climate. In many trees growing in areas with a distinct dry season, cambial activity ceases resulting in the formation of annual rings. In very humid mountain rainforests, trees stop to grow already after short rainless periods. By a combination of increment measurements and wood anatomical analyses, the climatic control of wood formation can be assessed. Intra‐annual wood density variations and content of various stable isotopes enable the climatological interpretation of the “wood signals”.