Filipe Campelo

Climatic significance of tree-ring width and intra-annual density fluctuations in Pinus pinea from a dry Mediterranean area in Portugal

In Mediterranean climates trees may go through two periods of dormancy, resulting in special anatomical features such as false rings and other intra-annual density fluctuations (IADFs). In this paper, ring growth and the presence of IADFs were studied in Pinus pinea L. growing in the coastal and inland regions of Alentejo (southern Portugal). In order to identify the triggering factors associated with the IADFs, a new classification was proposed for the IADFs in P. pinea: Type E (latewoodlike cells within earlywood); Type E+ (transition cells between earlywood and latewood); Type L (earlywoodlike cells within latewood) and Type L+ (earlywoodlike cells between latewood and earlywood of the next tree ring). Response function analyses showed that radial growth of P. pinea was strongly correlated with precipitation in southern Portugal. The climatic response of P. pinea was higher in the inland area where the summer drought is more severe, the winter temperatures are lower and the soils have low water-holding capacity, in comparison with the coastal area. IADFs were frequent in P. pinea and most of the IADFs were observed in latewood. The presence of IADFs was correlated with fluctuations in climate parameters during the growing season. The IADF type E+ was linked to precipitation events early in summer. The IADF type L and L+ were associated with above-average precipitation in early autumn.RésuméDans les climats méditerranéens, les arbres peuvent traverser deux périodes de dormance, ce qui a pour conséquence des caractéristiques anatomiques particulières telles que des faux cernes et des fluctuations intra annuelles de densité (IADFs). Dans cet article, la croissance des cernes et la présence de IADFs ont été étudiées chez Pinus pinea L. poussant dans les régions côtières et intérieures de l’Alentejo (sud-ouest du Portugal). Dans le but d’identifier les facteurs déclenchants associés à l’IADFs, une nouvelle classification a été proposée pour l’IADFs chez Pinus pinea : Type E (cellules ressemblant à du bois final dans le bois initial); Type E+ (cellules de transition entre bois initial et bois final); Type L (cellules ressemblant à du bois initial dans du bois final) et Type L+ (cellules ressemblant à du bois initial entre bois final et bois initial du prochain cerne). Les analyses des fonctions de réponse ont montré que la croissance radiale de Pinus pinea était fortement corrélée avec les précipitations dans le sud-ouest du Portugal. La réponse climatique de Pinus pinea a été plus forte dans la zone intérieure où la sécheresse d’été est plus sévère, les températures hivernales plus basses et où les sols ont une plus faible capacité de rétention de l’eau, comparativement aux zones côtières. IADFs a été fréquent chez Pinus pinea et la majorité d’IADFs a été observée dans le bois final. La présence d’IADFs a été corrélée avec des fluctuations des paramètres climatiques pendant la saison de croissance. L’IADFs type E+ était lié avec des événements pluvieux en début d’été. L’IADFs type L et l’IADFs type L+ étaient associés avec des précipitations supérieures à la moyenne en début d’automne.

Woody biomass production lags stem-girth increase by over one month in coniferous forests

Wood is the main terrestrial biotic reservoir for long-term carbon sequestration(1), and its formation in trees consumes around 15% of anthropogenic carbon dioxide emissions each year(2). However, the seasonal dynamics of woody biomass production cannot be quantified from eddy covariance or satellite observations. As such, our understanding of this key carbon cycle component, and its sensitivity to climate, remains limited. Here, we present high-resolution cellular based measurements of wood formation dynamics in three coniferous forest sites in northeastern France, performed over a period of 3 years. We show that stem woody biomass production lags behind stem-girth increase by over 1 month. We also analyse more general phenological observations of xylem tissue formation in Northern Hemisphere forests and find similar time lags in boreal, temperate, subalpine and Mediterranean forests. These time lags question the extension of the equivalence between stem size increase and woody biomass production to intra-annual time scales(3, 4, 5, 6). They also suggest that these two growth processes exhibit differential sensitivities to local environmental conditions. Indeed, in the well-watered French sites the seasonal dynamics of stem-girth increase matched the photoperiod cycle, whereas those of woody biomass production closely followed the seasonal course of temperature. We suggest that forecasted changes in the annual cycle of climatic factors(7) may shift the phase timing of stem size increase and woody biomass production in the future.

Which matters most for the formation of intra-annual density fluctuations in Pinus pinaster: age or size?

Key messageA new method is proposed to standardize chronologies of intra-annual density fluctuations to improve their intra-annual climatic signal.AbstractIn the Mediterranean area, intra-annual density fluctuations (IADFs) are triggered by short-term climatic variations during the growing season. It is known that the formation of these anatomical structures is dependent on age and size, which can represent a problem during the extraction of the environmental signal from IADF chronologies. We present a new method using a two-step approach to remove the effect of tree-ring width from IADF chronologies. The climatic signal of IADF chronologies obtained by the proposed method was compared with previous methods, using 160 Pinus pinaster tree cores from an even-aged stand on the west coast of Portugal. Our results show that the climatic signal of IADF chronologies was strongly affected by the standardization method used, and that it could be improved by removing the effect of the predisposing factors (cambial age and tree-ring width) on IADF formation. Moreover, additional climatic information (previous winter precipitation) was only revealed when the effect of tree-ring width was removed from IADF series. Finally, we propose that this new method should be tested for other species and across larger geographical areas to confirm its capacity to remove noise from IADF chronologies and to improve their intra-annual climatic signal.

Adjustment Capacity of Maritime Pine Cambial Activity in Drought-Prone Environments

Intra-annual density fluctuations (IADFs) are anatomical features formed in response to changes in the environmental conditions within the growing season. These anatomical features are commonly observed in Mediterranean pines, being more frequent in younger and wider tree rings. However, the process behind IADF formation is still unknown. Weekly monitoring of cambial activity and wood formation would fill this void. Although studies describing cambial activity and wood formation have become frequent, this knowledge is still fragmentary in the Mediterranean region. Here we present data from the monitoring of cambial activity and wood formation in two diameter classes of maritime pine (Pinus pinaster Ait.), over two years, in order to test: (i) whether the differences in stem diameter in an even-aged stand were due to timings and/or rates of xylogenesis; (ii) if IADFs were more common in large trees; and (iii) if their formation is triggered by cambial resumption after the summer drought. Larger trees showed higher rates of cell production and longer growing seasons, due to an earlier start and later end of xylogenesis. When a drier winter occurs, larger trees were more affected, probably limiting xylogenesis in the summer months. In both diameter classes a latewood IADF was formed in 2012 in response to late-September precipitation, confirming that the timing of the precipitation event after the summer drought is crucial in determining the resumption of cambial activity and whether or not an IADF is formed. It was the first time that the formation of a latewood IADF was monitored at a weekly time scale in maritime pine. The capacity of maritime pine to adjust cambial activity to the current environmental conditions represents a valuable strategy under the future climate change conditions.

Environmental control of vessel traits in Quercus ilex under Mediterranean climate: relating xylem anatomy to function

Time series of tree-ring anatomical features are important to understand the functional role of xylem plasticity over the life span of trees, and thus to reconstruct past ecological and climatic conditions. Holm oak (Quercus ilex L.) is a drought-tolerant tree widely distributed in the Mediterranean Basin. Chronologies of tree-ring width (TRW), vessel lumen area [maximum (MAX) and mean (MVA)] and vessel density (VD) were developed for the period 1942–2001. Each ring was divided into three sections to compare the intra-annual variation of vessel features with the climate conditions during the growing season. The common variability of tree-growth and vessel features was analyzed using a principal component analysis (PCA). Vessel lumen area (MAX and MVA) and TRW loaded positively on the first axis (PC1), whereas VD from the first and second part of the ring (VD1 and VD2) loaded negatively, suggesting that these variables share a common variance. On the other hand, VD in the last third of the ring (VD3) loaded positively on second axis (PC2). PC1 showed a strong positive correlation with precipitation during the hydrological year (prior October–September) and a negative correlation with temperature in spring (April–May), while PC2 showed a negative correlation with precipitation in June. Our results showed that TRW and vessel lumen area were mainly dependent on moisture conditions along the growing season, while vessel density probably plays an important role in the balance between hydraulic conductivity and safety to embolism to better adjust the hydraulic system to water availability.

Intra-annual density fluctuations in tree rings: how, when, where, and why?

Intra-annual density fluctuations (IADFs) in tree rings are generally considered structural anomalies caused by deviations from the “normal course” of xylogenesis during the growing season. This definition is based on the bias that, under “normal conditions”, cambial activity stops once a year. Each tree ring can thus be dated to one calendar year, which is one of the principles of dendrochronology. The formation of IADFs can be triggered directly by environmental changes, especially in precipitation and temperature, that affect cambial activity and cell differentiation. It can also be the result of limited photosynthesis, due to defoliation induced by biotic or abiotic constraints.Often indicated with alternative terms, IADFs were first described in the 1930s, and recently reported for many trees and shrubs from different ecosystems throughout the world, particularly for Mediterranean species. Different types of IADFs have been detected; their formation and structural properties depend on many factors including tree genotype, age, size, rooting depth, habitat, soil, climate, photosynthetic activity, and allocation strategies. Whether IADFs affect the adaptive capability of plants remains, however, unclear.We provide an overview of the main anatomical features of IADFs and their occurrence in tree rings from various environments and climatic regimes. We propose a simplified way of classifying them and discuss the hypotheses about their functional role and the factors triggering their formation. To understand the ecological role of IADFs better, we recommend a multidisciplinary approach, involving wood anatomy, dendroecology, and stable isotopes, which has already been applied for Mediterranean species. We conclude by considering that IADFs appear to be the “rule” rather than “anomalies” in some ecosystems where they help plants cope with fluctuating environmental conditions. Moreover, their anatomical structure represents a valuable proxy of past climatic conditions at a sub-seasonal resolution and may be relevant to adapt hydraulic functioning of living trees to changing climatic conditions.

Age effects and climate response in trees: a multi-proxy tree-ring test in old-growth life stages

Aging in trees implies a progressive reduction in the growth rate, related to a shortening of the growing period and changes in the photosynthetic capability and efficiency. These changes may continue during the old-growth life stages following the juvenile phase and are reflected in tree-ring properties such as growth increment, density or stable isotopes. We studied possible climate age effects in time series of several tree-ring parameters (ring width, wood density and stable carbon and oxygen isotopes) of mature individuals from two age groups of Pinus uncinata and P. nigra at two locations in Spain. The aim was to test whether age differences in trees in the old-growth life stages could lead to diverging climate responses. The results show some differences in response to climate between age groups at a monthly level, but most of these divergences are not significant for seasonal climate variables. Regardless of the age group, the main limiting climate factors constrained tree growth equally. Although our findings do not support the idea of an age-dependent response to climate that may lead to inaccurate climate reconstructions, further studies using tree-ring density and stable isotope series are urgently needed to verify the current results.

Structure and function of intra–annual density fluctuations: Mind the gaps

Tree rings are natural archives of climate and environmental information with a yearly resolution. Indeed, wood anatomical, chemical, and other properties of tree rings are a synthesis of several intrinsic and external factors, and their interaction during tree growth. In particular, Intra-Annual Density Fluctuations (IADFs) can be considered as tree-ring anomalies that can be used to better understand tree growth and to reconstruct past climate conditions with intra-annual resolution. However, the ecophysiological processes behind IADF formation, as well as their functional impact, remain unclear. Are IADFs resulting from a prompt adjustment to fluctuations in environmental conditions to avoid stressful conditions and/or to take advantage from favorable conditions? In this paper we discuss: (1) the influence of climatic factors on the formation of IADFs; (2) the occurrence of IADFs in different species and environments; (3) the potential of new approaches to study IADFs and identify their triggering factors. Our final aim is to underscore the advantages offered by network analyses of data and the importance of high-resolution measurements to gain insight into IADFs formation processes and their relations with climatic conditions, including extreme weather events.

Climatic Signals from Intra-annual Density Fluctuation Frequency in Mediterranean Pines at a Regional Scale

Tree rings provide information about the climatic conditions during the growing season by recording them in different anatomical features, such as intra-annual density fluctuations (IADFs). IADFs are intra-annual changes of wood density appearing as latewood-like cells within earlywood, or earlywood-like cells within latewood. The occurrence of IADFs is dependent on the age and size of the tree, and it is triggered by climatic drivers. The variations of IADF frequency of different species and their dependence on climate across a wide geographical range have still to be explored. The objective of this study is to investigate the effect of age, tree-ring width and climate on IADF formation and frequency at a regional scale across the Mediterranean Basin in Pinus halepensis Mill., Pinus pinaster Ait., and Pinus pinea L. The analyzed tree-ring network was composed of P. pinea trees growing at 10 sites (2 in Italy, 4 in Spain, and 4 in Portugal), P. pinaster from 19 sites (2 in Italy, 13 in Spain, and 4 in Portugal), and P. halepensis from 38 sites in Spain. The correlations between IADF frequency and monthly minimum, mean and maximum temperatures, as well as between IADF frequency and total precipitation, were analyzed. A significant negative relationship between IADF frequency and tree-ring age was found for the three Mediterranean pines. Moreover, IADFs were more frequent in wider rings than in narrower ones, although the widest rings showed a reduced IADF frequency. Wet conditions during late summer/early autumn triggered the formation of IADFs in the three species. Our results suggest the existence of a common climatic driver for the formation of IADFs in Mediterranean pines, highlighting the potential use of IADF frequency as a proxy for climate reconstructions with geographical resolution.

Plastic Response of Tracheids in Pinus pinaster in a Water-Limited Environment: Adjusting Lumen Size instead of Wall Thickness

The formation of wood results from cambial activity and its anatomical properties reflect the variability of environmental conditions during the growing season. Recently, it was found that wood density variations in conifers growing under cold-limited environment result from the adjustment of cell wall thickness (CWT) to temperature. Additionally, it is known that intra-annual density fluctuations (IADFs) are formed in response to precipitation after the summer drought. Although IADFs are frequent in Mediterranean conifers no study has yet been conducted to determine if these structures result from the adjustment of lumen diameter (LD) or CWT to soil water availability. Our main objective is to investigate the intra-ring variation of wood anatomical features (LD and CWT) in Pinus pinaster Ait. growing under a water-limited environment. We compared the tracheidograms of LD and CWT for the years 2010–2013 in P. pinaster growing in the west coast of Portugal. Our results suggest a close association between LD and soil moisture content along the growing season, reinforcing the role of water availability in determining tracheid size. Compared with CWT, LD showed a higher intra- and inter-annual variability suggesting its strong adjustment value to variations in water availability. The formation of a latewood IADF appears to be predisposed by higher rates of cell production in spring and triggered by early autumn precipitation. Our findings reinforce the crucial role of water availability on cambial activity and wood formation in Mediterranean conifers, and emphasize the high plasticity of wood anatomical features under Mediterranean climate.