Divergent structural leaf trait spectra in succulent versus non-succulent plant taxa.

BACKGROUND AND SCOPE: Plant functional traits are the result of natural selection to optimize carbon gain, leading to a broad spectrum of traits across environmental gradients. Among plant traits, leaf water storage capacity is paramount for plant drought resistance. We explored whether leaf-succulent taxa follow similar trait correlations as non-leaf-succulent taxa to evaluate whether both are similarly constrained by relationships between leaf water storage and climate. We tested the relationships among three leaf traits related to water storage capacity and resource use strategies in 132 species comprising three primary leaf types: succulent, sclerophyllous, and leaves with rapid returns on water investment - referred to as fast return. Correlation coefficients among specific leaf area (SLA), water mass per unit of area (WMA), and saturated water content (SWC) were tested, along with relationships between leaf trait spectra and aridity determined from species occurrence records. CONCLUSION: Both SWC and WMA at a given SLA were approximately 10-fold higher in succulent leaves than in non-succulent leaves. While SWC actually increased with SLA in non-succulent leaves, no relationship was detected between SWC and SLA in succulent leaves, although WMA decreased with SLA in all leaf types. A principal component analysis revealed that succulent-taxa occupied a widely different mean trait space than either fast-return (P < 0.0001) and sclerophyllous taxa (P < 0.0001) along the first PCA axis, that explained 63% of mean trait expression among species. However, aridity only explained 12% of the variation in PCA1 values. This study is among the first to establish a structural leaf trait spectrum in succulent leaf taxa and quantify contrasts in leaf water storage among leaf types relative to specific leaf area. Results show that trait coordination in succulent leaf taxa may not follow similar patterns as widely studied non-succulent taxa.

The oldest known clones of Salix herbacea growing in the Northern Apennines, Italy are at least 2000 years old.

PREMISE: Dominant in many ecosystems around the world, clonal plants can reach considerable ages and sizes. Due to their modular growth patterns, individual clonal plants (genets) can consist of many subunits (ramets). Since single ramets do not reflect the actual age of genets, the ratio between genet size (radius) and longitudinal annual growth rate (LAGR) of living ramets is often used to approximate the age of clonal plants. However, information on how the LAGR changes along ramets and how LAGR variability may affect age estimates of genets is still limited. METHODS: We assessed the variability of LAGR based on wood-section position along the ramets and on the duration of the growing season on three genetically distinct genets of Salix herbacea growing in the Northern Apennines (Italy). We compared genet ages estimated by dividing genet radius by the LAGRs of its ramets. RESULTS: LAGR increased significantly from the stem apex to the root collar; indicating that ramet growth rate decreased with time. Furthermore, a difference of ca. 2 weeks in the onset of the growing period did not impact LAGR. Considering the high LAGR variability, we estimated that the three genets started to grow between ~2100 and ~7000 years ago, which makes them the oldest known clones of S. herbacea even considering the most conservative age estimate. CONCLUSIONS: Our findings indicate that analyzing ramets at the root collar provides an integrative measurement of their overall LAGR, which is crucial for estimating the age of genets.

Plants in the UK flower a month earlier under recent warming.

Global temperatures are rising at an unprecedented rate, but environmental responses are often difficult to recognize and quantify. Long-term observations of plant phenology, the annually recurring sequence of plant developmental stages, can provide sensitive measures of climate change and important information for ecosystem services. Here, we present 419 354 recordings of the first flowering date from 406 plant species in the UK between 1753 and 2019 CE. Community-wide first flowering advanced by almost one month on average when comparing all observations before and after 1986 (p < 0.0001). The mean first flowering time is 6 days earlier in southern than northern sites, 5 days earlier under urban than rural settings, and 1 day earlier at lower than higher elevations. Compared to trees and shrubs, the largest lifeform-specific phenological shift of 32 days is found in herbs, which are generally characterized by fast turnover rates and potentially high levels of genetic adaptation. Correlated with January-April maximum temperatures at -0.81 from 1952-2019 (p < 0.0001), the observed trends (5.4 days per decade) and extremes (66 days between the earliest and latest annual mean) in the UK's first flowering dataset can affect the functioning and productivity of ecosystems and agriculture.

Comparative anatomy of leaf petioles in temperate trees and shrubs: the role of plant size, environment and phylogeny.

BACKGROUND AND AIMS: Petioles are important plant organs connecting stems with leaf blades and affecting light-harvesting ability of the leaf as well as transport of water, nutrients and biochemical signals. Despite the high diversity in petiole size, shape and anatomy, little information is available regarding their structural adaptations across evolutionary lineages and environmental conditions. To fill this knowledge gap, we investigated the variation of petiole morphology and anatomy of mainly European woody species to better understand the drivers of internal and external constraints in an evolutionary context. METHODS: We studied how petiole anatomical features differed according to whole-plant size, leaf traits, thermal and hydrological conditions, and taxonomic origin in 95 shrubs and trees using phylogenetic distance-based generalized least squares models. KEY RESULTS: Two major axes of variation were related to leaf area and plant size. Larger and softer leaves are found in taller trees of more productive habitats. Their petioles are longer, with a circular outline and are anatomically characterized by the predominance of sclerenchyma, larger vessels, interfascicular areas with fibres and indistinct phloem rays. In contrast, smaller and tougher leaves are found in shorter trees and shrubs of colder or drier habitats. Their petioles have a terete outline, phloem composed of small cells and radially arranged vessels, fibreless xylem and lamellar collenchyma. Individual anatomical traits were linked to different internal and external drivers. Petiole length and vessel diameter increase with increasing leaf blade area. Collenchyma becomes absent with increasing temperature, and petiole outline becomes polygonal with increasing precipitation. CONCLUSIONS: We conclude that species' temperature and precipitation optima, plant height, and leaf area and thickness exerted a significant control on petiole anatomical and morphological structures not confounded by phylogenetic inertia. Species with different evolutionary histories but similar thermal and hydrological requirements have converged to similar petiole anatomical structures.

Tree differences in primary and secondary growth drive convergent scaling in leaf area to sapwood area across Europe.

Trees scale leaf (AL ) and xylem (AX ) areas to couple leaf transpiration and carbon gain with xylem water transport. Some species are known to acclimate in AL  : AX balance in response to climate conditions, but whether trees of different species acclimate in AL  : AX in similar ways over their entire (continental) distributions is unknown. We analyzed the species and climate effects on the scaling of AL vs AX in branches of conifers (Pinus sylvestris, Picea abies) and broadleaved (Betula pendula, Populus tremula) sampled across a continental wide transect in Europe. Along the branch axis, AL and AX change in equal proportion (isometric scaling: b Ëœ 1) as for trees. Branches of similar length converged in the scaling of AL vs AX with an exponent of b = 0.58 across European climates irrespective of species. Branches of slow-growing trees from Northern and Southern regions preferentially allocated into new leaf rather than xylem area, with older xylem rings contributing to maintaining total xylem conductivity. In conclusion, trees in contrasting climates adjust their functional balance between water transport and leaf transpiration by maintaining biomass allocation to leaves, and adjusting their growth rate and xylem production to maintain xylem conductance.

Universal hydraulics of the flowering plants: vessel diameter scales with stem length across angiosperm lineages, habits and climates.

Angiosperm hydraulic performance is crucially affected by the diameters of vessels, the water conducting conduits in the wood. Hydraulic optimality models suggest that vessels should widen predictably from stem tip to base, buffering hydrodynamic resistance accruing as stems, and therefore conductive path, increase in length. Data from 257 species (609 samples) show that vessels widen as predicted with distance from the stem apex across angiosperm orders, habits and habitats. Standardising for stem length, vessels are only slightly wider in warm/moist climates and in lianas, showing that, rather than climate or habit, plant size is by far the main driver of global variation in mean vessel diameter. Terminal twig vessels become wider as plant height increases, while vessel density decreases slightly less than expected tip to base. These patterns lead to testable predictions regarding evolutionary strategies allowing plants to minimise carbon costs per unit leaf area even as height increases.

Priorities for Bark Anatomical Research: Study Venues and Open Questions.

The bark fulfils several essential functions in vascular plants and yields a wealth of raw materials, but the understanding of bark structure and function strongly lags behind our knowledge with respect to other plant tissues. The recent technological advances in sampling and preparation of barks for anatomical studies, along with the establishment of an agreed bark terminology, paved the way for more bark anatomical research. Whilst datasets reveal bark's taxonomic and functional diversity in various ecosystems, a better understanding of the bark can advance the understanding of plants' physiological and environmental challenges and solutions. We propose a set of priorities for understanding and further developing bark anatomical studies, including periderm structure in woody plants, phloem phenology, methods in bark anatomy research, bark functional ecology, relationships between bark macroscopic appearance, and its microscopic structure and discuss how to achieve these ambitious goals.

Biogeographic implication of temperature-induced plant cell wall lignification.

More than 200 years after von Humboldt's pioneering work on the treeline, our understanding of the cold distribution limit of upright plant growth is still incomplete. Here, we use wood anatomical techniques to estimate the degree of stem cell wall lignification in 1770 plant species from six continents. Contrary to the frequent belief that small plants are less lignified, we show that cell wall lignification in 'woody' herbs varies considerably. Although trees and shrubs always exhibit lignified cell walls in their upright stems, small plants above the treeline may contain less lignin. Our findings suggest that extremely cold growing season temperatures can reduce the ability of plants to lignify their secondary cell walls. Corroborating experimental and observational evidence, this study proposes to revisit existing theories about the thermal distribution limit of upright plant growth and to consider biochemical and biomechanical factors for explaining the global treeline position.

The Response of Beech (Fagus sylvatica L.) Populations to Climate in the Easternmost Sites of Its European Distribution.

In the context of forecasted climate change scenarios, the growth of forest tree species at their distribution margin is crucial to adapt current forest management strategies. Analyses of beech (Fagus sylvatica L.) growth have shown high plasticity, but easternmost beech populations have been rarely studied. To describe the response of the marginal beech population to the climate in the far east sites of its distribution, we first compiled new tree ring width chronologies. Then we analyzed climate-growth relationships for three marginal beech populations in the Republic of Moldova. We observed a relatively high growth rate in the marginal populations compared to core distribution sites. Our analyses further revealed a distinct and significant response of beech growth to all climatic variables, assessing for the first time the relationship between growth and vapor pressure deficit (VPD) which described how plant growth responds to drought. These results highlight that accumulated water deficit is an essential limiting factor of beech growth in this region. In conclusion, beech growth in the easternmost marginal population is drought-limited, and the sensitivity to VPD will need to be considered in future studies to update the forest management of other economic and ecologically important species.

Global wood anatomical perspective on the onset of the Late Antique Little Ice Age (LALIA) in the mid-6th century CE.

Linked to major volcanic eruptions around 536 and 540 CE, the onset of the Late Antique Little Ice Age has been described as the coldest period of the past two millennia. The exact timing and spatial extent of this exceptional cold phase are, however, still under debate because of the limited resolution and geographical distribution of the available proxy archives. Here, we use 106 wood anatomical thin sections from 23 forest sites and 20 tree species in both hemispheres to search for cell-level fingerprints of ephemeral summer cooling between 530 and 550 CE. After cross-dating and double-staining, we identified 89 Blue Rings (lack of cell wall lignification), nine Frost Rings (cell deformation and collapse), and 93 Light Rings (reduced cell wall thickening) in the Northern Hemisphere. Our network reveals evidence for the strongest temperature depression between mid-July and early-August 536 CE across North America and Eurasia, whereas more localised cold spells occurred in the summers of 532, 540-43, and 548 CE. The lack of anatomical signatures in the austral trees suggests limited incursion of stratospheric volcanic aerosol into the Southern Hemisphere extra-tropics, that any forcing was mitigated by atmosphere-ocean dynamical responses and/or concentrated outside the growing season, or a combination of factors. Our findings demonstrate the advantage of wood anatomical investigations over traditional dendrochronological measurements, provide a benchmark for Earth system models, support cross-disciplinary studies into the entanglements of climate and history, and question the relevance of global climate averages.

New Evidence of Thermally Constrained Plant Cell Wall Lignification.

Lignin enhances the mechanical strength of plants and enables their intrinsic water transport. Dendrochronological, wood anatomical, and plant physiological evidence now suggests that the degree of lignin deposition is constrained by low temperature. Placing these findings in an ecological context implies rethinking of the global treeline position.

Functional Relationships of Wood Anatomical Traits in Norway Spruce.

The quantitative assessment of wood anatomical traits offers important insights into those factors that shape tree growth. While it is known that conduit diameter, cell wall thickness, and wood density vary substantially between and within species, the interconnection between wood anatomical traits, tree-ring width, tree height and age, as well as environment effects on wood anatomy remain unclear. Here, we measure and derived 65 wood anatomical traits in cross-sections of the five outermost tree rings (2008-2012) of 30 Norway spruce [Picea abies (L.) H. Karst.] trees growing along an altitudinal gradient (1,400-1,750 m a.s.l.) in the northern Apennines (Italy). We assess the relationship among each anatomical trait and between anatomical trait groups according to their function for (i) tree-ring growth, (ii) cell growth, (iii) hydraulic traits, and (iv) mechanical traits. The results show that tree height significantly affects wood hydraulic traits, as well as number and tangential diameter of tracheids, and ultimately the total ring width. Moreover, the amount of earlywood and latewood percentage influence wood hydraulic safety and efficiency, as well as mechanical traits. Mechanically relevant wood anatomical traits are mainly influenced by tree age, not necessarily correlated with tree height. An additional level of complexity is also indicated by some anatomical traits, such as latewood lumen diameter and the cell wall reinforcement index, showing large inter-annual variation as a proxy of phenotypic plasticity. This study unravels the complex interconnection of tree-ring tracheid structure and identifies anatomical traits showing a large inter-individual variation and a strong interannual coherency. Knowing and quantifying anatomical variation in cells of plant stem is crucial in ecological and biological studies for an appropriate interpretation of abiotic drivers of wood formation often related to tree height and/or tree age.

Author Correction: Limited capacity of tree growth to mitigate the global greenhouse effect under predicted warming.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Limited capacity of tree growth to mitigate the global greenhouse effect under predicted warming.

It is generally accepted that animal heartbeat and lifespan are often inversely correlated, however, the relationship between productivity and longevity has not yet been described for trees growing under industrial and pre-industrial climates. Using 1768 annually resolved and absolutely dated ring width measurement series from living and dead conifers that grew in undisturbed, high-elevation sites in the Spanish Pyrenees and the Russian Altai over the past 2000 years, we test the hypothesis of grow fast-die young. We find maximum tree ages are significantly correlated with slow juvenile growth rates. We conclude, the interdependence between higher stem productivity, faster tree turnover, and shorter carbon residence time, reduces the capacity of forest ecosystems to store carbon under a climate warming-induced stimulation of tree growth at policy-relevant timescales.

Quantitative Wood Anatomy-Practical Guidelines.

Quantitative wood anatomy analyzes the variability of xylem anatomical features in trees, shrubs, and herbaceous species to address research questions related to plant functioning, growth, and environment. Among the more frequently considered anatomical features are lumen dimensions and wall thickness of conducting cells, fibers, and several ray properties. The structural properties of each xylem anatomical feature are mostly fixed once they are formed, and define to a large extent its functionality, including transport and storage of water, nutrients, sugars, and hormones, and providing mechanical support. The anatomical features can often be localized within an annual growth ring, which allows to establish intra-annual past and present structure-function relationships and its sensitivity to environmental variability. However, there are many methodological challenges to handle when aiming at producing (large) data sets of xylem anatomical data. Here we describe the different steps from wood sample collection to xylem anatomical data, provide guidance and identify pitfalls, and present different image-analysis tools for the quantification of anatomical features, in particular conducting cells. We show that each data production step from sample collection in the field, microslide preparation in the lab, image capturing through an optical microscope and image analysis with specific tools can readily introduce measurement errors between 5 and 30% and more, whereby the magnitude usually increases the smaller the anatomical features. Such measurement errors-if not avoided or corrected-may make it impossible to extract meaningful xylem anatomical data in light of the rather small range of variability in many anatomical features as observed, for example, within time series of individual plants. Following a rigid protocol and quality control as proposed in this paper is thus mandatory to use quantitative data of xylem anatomical features as a powerful source for many research topics.

Evaluation of drought response of two poplar clones (Populus x canadensis Monch 'I-214' and P. deltoides Marsh. 'Dvina') through high resolution analysis of stem growth.

Different irrigation effects on stem radius variation (DeltaR) and maximum daily shrinkage (MDS) in Populus deltoides 'Dvina' and Populusxcanadensis 'I-214' were studied to assess differences in drought tolerance between clones. One-year-old trees growing in concrete tanks were submitted to two irrigation regimes (natural rainfall and irrigation) from 24 June to 10 August, and DeltaR was monitored by automatic point dendrometers. Independently of the irrigation regime, 'Dvina' showed a higher stem radial increment than 'I-214'. In both clones, the first response to changed soil water content was a significant increase in MDS, whilst DeltaR decreased about 20 d later when pre-dawn leaf water potential (Psipd) dropped below -0.4 MPa. However, they displayed different strategies to overcome drought. 'Dvina' maintained a positive DeltaR for longer than 'I-214', which had lower leaf Psipd and greater leaf abscission at the end of the drought period. After irrigation resumed, 'Dvina' showed a higher capacity to restore stem growth. 'I-214' was probably unable to recover secondary growth because of higher leaf abscission during drought stress and the production of newly expanded leaves during recovery. It is concluded that the larger radial growth of 'Dvina' derived from a better water use (carbon uptake versus water loss) than 'I-214' under limited water availability.