Tree growth response to drought partially explains regional-scale growth and mortality patterns in Iberian forests.

Tree-ring data has been widely used to inform about tree growth responses to drought at the individual scale, but less is known about how tree growth sensitivity to drought scales up driving changes in forest dynamics. Here, we related tree-ring growth chronologies and stand-level forest changes in basal area from two independent data sets to test if tree-ring responses to drought match stand forest dynamics (stand basal area growth, ingrowth, and mortality). We assessed if tree growth and changes in forest basal area covary as a function of spatial scale and tree taxa (gymnosperm or angiosperm). To this end, we compared a tree-ring network with stand data from the Spanish National Forest Inventory. We focused on the cumulative impact of drought on tree growth and demography in the period 1981-2005. Drought years were identified by the Standardized Precipitation Evapotranspiration Index, and their impacts on tree growth by quantifying tree-ring width reductions. We hypothesized that forests with greater drought impacts on tree growth will also show reduced stand basal area growth and ingrowth and enhanced mortality. This is expected to occur in forests dominated by gymnosperms on drought-prone regions. Cumulative growth reductions during dry years were higher in forests dominated by gymnosperms and presented a greater magnitude and spatial autocorrelation than for angiosperms. Cumulative drought-induced tree growth reductions and changes in forest basal area were related, but initial stand density and basal area were the main factors driving changes in basal area. In drought-prone gymnosperm forests, we observed that sites with greater growth reductions had lower stand basal area growth and greater mortality. Consequently, stand basal area, forest growth, and ingrowth in regions with large drought impacts was significantly lower than in regions less impacted by drought. Tree growth sensitivity to drought can be used as a predictor of gymnosperm demographic rates in terms of stand basal area growth and ingrowth at regional scales, but further studies may try to disentangle how initial stand density modulates such relationships. Drought-induced growth reductions and their cumulative impacts have strong potential to be used as early-warning indicators of regional forest vulnerability.

Warmer springs have increased the frequency and extension of late-frost defoliations in southern European beech forests.

Climate change is increasing the frequency of extreme climate events, causing profound impacts on forest function and composition. Late frost defoliation (LFD) events, the loss of photosynthetic tissues due to low temperatures at the start of the growing season, might become more recurrent under future climate scenarios. Therefore, the detection of changes in late-frost risk in response to global change emerges as a high-priority research topic. Here, we used a tree-ring network from southern European beech (Fagus sylvatica L.) forests comprising Spain, Italy and the Austrian Alps, to assess the incidence of LFD events in the last seven decades. We fitted linear-mixed models of basal area increment using different LFD indicators considering warm spring temperatures and late-spring frosts as fixed factors. We reconstructed major LFD events since 1950, matching extreme values of LFD climatic indicators with sharp tree-ring growth reductions. The last LFD events were validated using remote sensing. Lastly, reconstructed LFD events were climatically and spatially characterized. Warm temperatures before the late-spring frost, defined by high values of growing-degree days, influenced beech growth negatively, particularly in the southernmost populations. The number of LFD events increased towards beech southern distribution edge. Spanish and the southernmost Italian beech forests experienced higher frequency of LFD events since the 1990s. Until then, LFD events were circumscribed to local scales, but since that decade, LFD events became widespread, largely affecting the whole beech southwestern distribution area. Our study, based on in-situ evidence, sheds light on the climatic factors driving LFD occurrence and illustrates how increased occurrence and spatial extension of late-spring frosts might constrain future southern European beech forests' growth and functionality. Observed alterations in the climate-phenology interactions in response to climate change represent a potential threat for temperate deciduous forests persistence in their drier/southern distribution edge.

Xylem adjusts to maintain efficiency across a steep precipitation gradient in two coexisting generalist species.

Background and Aims: Trees adjust the configuration of their conductive system in response to changes in water availability, maximizing efficiency in wet environments and increasing safety in dry habitats. However, evidence of this general trend is not conclusive. Generalist species growing across broad climatic gradients provide an ideal framework to assess intra-specific xylem adjustments under contrasting environmental conditions. Our aims were to compare the response of xylem traits to variations in precipitation of two co-occurring generalist tree species, and to assess climate control on xylem trait variability and co-ordination. Methods: We evaluated xylem traits of Embothrium coccineum (Proteaceae, evergreen) and Nothofagus antarctica (Nothofagaceae, deciduous) in three areas across an abrupt precipitation gradient, from 500 to 2500 mm, in southern Chile. We measured wood density, vessel lumen area and density, percentage of conductive area and vessel grouping, and estimated the hydraulic function from anatomical measurements in 60 individuals per species. Key Results: Both species shared a common pattern of response along the precipitation gradient, with an increase in vessel density with dryness, but without changes in estimated hydraulic conductivity. Xylem traits in E. coccineum were more variable and more responsive to the climate gradient, decreasing vessel lumen area and increasing wood density, whereas vessel grouping showed contrasting patterns between species. Additionally, the analysis of trait co-ordination at the individual level revealed a tighter co-ordination among xylem traits in E. coccineum. Conclusions: Estimated xylem efficiency was maintained in combination with different levels of expected xylem safety within species. Reduction in vessel lumen area was compensated through large increases in vessel density, thus breaking the trade-off between xylem efficiency and safety. Otherwise, the existence of alternative internal adjustments in coexisting species to face similar climatic constraints might increase resilience of temperate forests against unpredictable changes in climatic conditions.

Forest resilience to drought varies across biomes.

Forecasted increase drought frequency and severity may drive worldwide declines in forest productivity. Species-level responses to a drier world are likely to be influenced by their functional traits. Here, we analyse forest resilience to drought using an extensive network of tree-ring width data and satellite imagery. We compiled proxies of forest growth and productivity (TRWi, absolutely dated ring-width indices; NDVI, Normalized Difference Vegetation Index) for 11 tree species and 502 forests in Spain corresponding to Mediterranean, temperate, and continental biomes. Four different components of forest resilience to drought were calculated based on TRWi and NDVI data before, during, and after four major droughts (1986, 1994-1995, 1999, and 2005), and pointed out that TRWi data were more sensitive metrics of forest resilience to drought than NDVI data. Resilience was related to both drought severity and forest composition. Evergreen gymnosperms dominating semi-arid Mediterranean forests showed the lowest resistance to drought, but higher recovery than deciduous angiosperms dominating humid temperate forests. Moreover, semi-arid gymnosperm forests presented a negative temporal trend in the resistance to drought, but this pattern was absent in continental and temperate forests. Although gymnosperms in dry Mediterranean forests showed a faster recovery after drought, their recovery potential could be constrained if droughts become more frequent. Conversely, angiosperms and gymnosperms inhabiting temperate and continental sites might have problems to recover after more intense droughts since they resist drought but are less able to recover afterwards.

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

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

Secondary Growth and Carbohydrate Storage Patterns Differ between Sexes in Juniperus thurifera.

Differences in reproductive costs between male and female plants have been shown to foster sex-related variability in growth and C-storage patterns. The extent to which differential secondary growth in dioecious trees is associated with changes in stem carbohydrate storage patterns, however, has not been fully assessed. We explored the long-term radial growth and the seasonal variation of non-structural carbohydrate (NSC) content in sapwood of 40 males and 40 females Juniperus thurifera trees at two sites. NSC content was analyzed bimonthly for 1 year, and tree-ring width was measured for the 1931-2010 period. Sex-related differences in secondary growth and carbohydrate storage were site-dependent. Under less restrictive environmental conditions females grew more and stored more non-soluble sugars than males. Our results reinforce that sex-related differences in growth and resource storage may be a consequence of local adaptation to environmental conditions. Seasonal variation in soluble sugars concentration was opposite to cambial activity, with minima seen during periods of maximal secondary growth, and did not differ between the sexes or sites. Trees with higher stem NSC levels at critical periods showed higher radial growth, suggesting a common mechanism irrespective of site or sex. Sex-related patterns of secondary growth were linked to differences in non-soluble sugars content indicating sex-specific strategies of long-term performance.

Disentangling Facilitation Along the Life Cycle: Impacts of Plant-Plant Interactions at Vegetative and Reproductive Stages in a Mediterranean Forb.

Facilitation enables plants to improve their fitness in stressful environments. The overall impact of plant-plant interactions on the population dynamics of protégées is the net result of both positive and negative effects that may act simultaneously along the plant life cycle, and depends on the environmental context. This study evaluates the impact of the nurse plant Juniperus sabina on different stages of the life cycle of the forb Helleborus foetidus. Growth, number of leaves, flowers, carpels, and seeds per flower were compared for 240 individuals collected under nurse canopies and in open areas at two sites with contrasting stress levels. Spatial associations with nurse plants and age structures were also checked. A structural equation model was built to test the effect of facilitation on fecundity, accounting for sequential steps from flowering to seed production. The net impact of nurse plants depended on a combination of positive and negative effects on vegetative and reproductive variables. Although nurse plants caused a decrease in flower production at the low-stress site, their net impact there was neutral. In contrast, at the high-stress site the net outcome of plant-plant interactions was positive due to an increase in effective recruitment, plant density, number of viable carpels per flower, and fruit set under nurse canopies. The naturally lower rates of secondary growth and flower production at the high-stress site were compensated by the net positive impact of nurse plants here. Our results emphasize the need to evaluate entire processes and not only final outcomes when studying plant-plant interactions.

Assessing Conifer Ray Parenchyma for Ecological Studies: Pitfalls and Guidelines.

Ray parenchyma is an essential tissue for tree functioning and survival. This living tissue plays a major role for storage and transport of water, nutrients, and non-structural carbohydrates (NSC), thus regulating xylem hydraulics and growth. However, despite the importance of rays for tree carbon and water relations, methodological challenges hamper knowledge about ray intra- and inter-tree variability and its ecological meaning. In this study we provide a methodological toolbox for soundly quantifying spatial and temporal variability of different ray features. Anatomical ray features were surveyed in different cutting planes (cross-sectional, tangential, and radial) using quantitative image analysis on stem-wood micro-sections sampled from 41 mature Scots pines (Pinus sylvestris). The percentage of ray surface (PERPAR), a proxy for ray volume, was compared among cutting planes and between early- and latewood to assess measurement-induced variability. Different tangential ray metrics were correlated to assess their similarities. The accuracy of cross-sectional and tangential measurements for PERPAR estimates as a function of number of samples and the measured wood surface was assessed using bootstrapping statistical technique. Tangential sections offered the best 3D insight of ray integration into the xylem and provided the most accurate estimates of PERPAR, with 10 samples of 4 mm(2) showing an estimate within ±6.0% of the true mean PERPAR (relative 95% confidence interval, CI95), and 20 samples of 4 mm(2) showing a CI95 of ±4.3%. Cross-sections were most efficient for establishment of time series, and facilitated comparisons with other widely used xylem anatomical features. Earlywood had significantly lower PERPAR (5.77 vs. 6.18%) and marginally fewer initiating rays than latewood. In comparison to tangential sections, PERPAR was systematically overestimated (6.50 vs. 4.92%) and required approximately twice the sample area for similar accuracy. Radial cuttings provided the least accurate PERPAR estimates. This evaluation of ray parenchyma in conifers and the presented guidelines regarding data accuracy as a function of measured wood surface and number of samples represent an important methodological reference for ray quantification, which will ultimately improve the understanding of the fundamental role of ray parenchyma tissue for the performance and survival of trees growing in stressed environments.

Increased evapotranspiration demand in a Mediterranean climate might cause a decline in fungal yields under global warming.

Wild fungi play a critical role in forest ecosystems, and its recollection is a relevant economic activity. Understanding fungal response to climate is necessary in order to predict future fungal production in Mediterranean forests under climate change scenarios. We used a 15-year data set to model the relationship between climate and epigeous fungal abundance and productivity, for mycorrhizal and saprotrophic guilds in a Mediterranean pine forest. The obtained models were used to predict fungal productivity for the 2021-2080 period by means of regional climate change models. Simple models based on early spring temperature and summer-autumn rainfall could provide accurate estimates for fungal abundance and productivity. Models including rainfall and climatic water balance showed similar results and explanatory power for the analyzed 15-year period. However, their predictions for the 2021-2080 period diverged. Rainfall-based models predicted a maintenance of fungal yield, whereas water balance-based models predicted a steady decrease of fungal productivity under a global warming scenario. Under Mediterranean conditions fungi responded to weather conditions in two distinct periods: early spring and late summer-autumn, suggesting a bimodal pattern of growth. Saprotrophic and mycorrhizal fungi showed differences in the climatic control. Increased atmospheric evaporative demand due to global warming might lead to a drop in fungal yields during the 21st century.

Facilitation promotes changes in leaf economics traits of a perennial forb.

Optimal allocation of resources is crucial to maximize plant success. Plants modify their economic strategies by adjusting functional traits in response to shifts in environmental conditions. Facilitation has been recognized as a major biotic filter of trait distribution in communities, although the effect of facilitation on intraspecific variability has been scarcely explored. We evaluated intraspecific shifts in leaf functional traits of a perennial forb (Helleborus foetidus) in relation to the presence of a nurse plant (Juniperus sabina) in two sites with contrasting abiotic stress levels. The effects of abiotic (site) and biotic (juniper presence, microsite) environments on specific leaf area (SLA), leaf area (LA), lamina/petiole length ratio (LPR), intrinsic water use efficiency (iWUE) and leaf nutrient content (N, P and N:P) per mass were evaluated. Alleviation of drought stress associated with nurse plant presence was reflected in SLA, LA, LPR and iWUE at the high-stress site. Individuals growing in open areas showed more resource-conservative traits, supporting the argument that this strategy is advantageous in environments that limit opportunities for rapid carbon gain. Leaf nutrients were unrelated to other traits. The large amount of intraspecific variation in leaf functional traits related to facilitative processes highlights the importance of facilitation as a major source of plant trait variation. Both positive and negative biotic interactions, as well as intraspecific trait variability, should be considered in mechanistic models of plant communities' functional responses to environmental changes.

Site effect is stronger than species identity in driving demographic responses of Helianthemum (Cistaceae) shrubs in gypsum environments.

PREMISE OF THE STUDY: Regional climatic patterns result in the synchrony of biological processes along large spatial areas. These patterns may be critical for effective plant recruitment in (semi)arid environments. Nevertheless, recruitment patterns of plant species within their range of distribution are still poorly known. Moreover, this response may be species-dependent, particularly between coexisting congenerics, which are thought to vary in demographic responses to climatic conditions as a coexistence-promoting mechanism. In this context, we investigated whether two congeneric plant species show synchronic age structures at varying spatial scales and whether they display demographic differences. METHODS: We sampled 600 Helianthemum squamatum and H. syriacum individuals at six localities in Spain. We used dendrochronological techniques to estimate age and radial growth. We compared the age structure among populations and between species and assessed the effect of site and species on different demographic parameters. Correlations between age structure and climatic factors were also determined. KEY RESULTS: We detected a very low intraspecific synchrony across sites but a high interspecific coupling in age structure within localities. Secondary growth, mean age, and flowering showed large intersite differences and small interspecific differences. Summer rainfall was a good predictor of age structure. CONCLUSIONS: Fine-scale climatic variability plays a major role in determining age structure of the studied species. Climatic variability is more relevant than interspecific differences. Our results illustrate the relevance of including spatial variation in summer rainfall patterns when modeling the impact of climate change on Mediterranean plant demography.

Distribution and evolutionary trends of photoprotective isoprenoids (xanthophylls and tocopherols) within the plant kingdom.

The earliest land photosynthesis would have increased the risk of photo-oxidations and the demand of anti-oxidative protection. In this work, we aimed to determine the evolutionary trends in photoprotection across a wide representation of the plant kingdom and to verify whether the non-ubiquitous lutein-epoxide (Lx) cycle is a polyphyletic or an ancient character. Carotenoids and alpha-tocopherol (alpha-toc) were analysed by HPLC in 266 species. Phylogenetic analyses of the presence of photoprotective compounds and zeaxanthin-epoxidase (ZE) sequences were performed. Violaxanthin-cycle pigments (VAZ) and alpha-toc were taxonomically ubiquitous. Ancient groups showed higher contents of VAZ than vascular plants, while alpha-toc showed the opposite pattern. Lutein-epoxide was present in 45% of the species. It showed a remarkable variation across groups but with a clear increasing trend from algae to basal angiosperms. Lutein-epoxide was also related to woody trait and leaf longevity. No correlation between the presence of Lx and recurrent mutations in ZE sequences, including the duplications, was found. Thus, there is an evolutionary trend to increase the content of alpha-toc and to decrease the total amount of VAZ pigments. Absence of Lx in algae discards an ancestral origin. Present results are also inconsistent with a polyphyletic origin of Lx in angiosperms.

The lutein epoxide cycle in vegetative buds of woody plants.

Recent works have shown that two xanthophyll cycles operate simultaneously in several plant species: the ubiquitous violaxanthin + anteraxanthin + zeaxanthin (VAZ) cycle and the lutein epoxide (Lx) cycle. In the present work we tested for the presence of the Lx cycle in vegetative buds of woody plants. After an extensive screening of 130 species, we have shown that Lx is present in buds of many different plant species and leaf primordia are enriched in Lx compared with leaves. As a result, the Lx pool was higher than the violaxanthin (V) pool in several species. Although Lx can be potentially de-epoxidised in buds, light attenuation by scales inhibited the daily operation of the Lx cycle. This finding would imply that the Lx cycle is not involved in short-term reversible photoprotection in buds. However, a light-induced decrease in Lx was observed through the winter. An extensive screening of 130 species in 49 families conducted to elucidate the taxonomic extension of this cycle showed a widespread presence of the Lx cycle. The presence of Lx has a high fidelity at the family level, but its presence in unrelated taxa suggests that this character has appeared independently in several different groups of plants.

The operation of the lutein epoxide cycle correlates with energy dissipation.

A new xanthophyll cycle involving de-epoxidation of lutein epoxide (Lx) into lutein in the light and epoxidation back in the dark has been recently described in parasitic plants and in trees from the genus Quercus. To explore the role of the Lx cycle in photoprotection, shade leaves of red oak (Q. rubra), with a relatively high Lx pool, were exposed to different light intensities. Both violaxanthin and Lx were de-epoxidised to the same extent, although the initial kinetics differed, with a rate proportional to the light intensity. De-epoxidation of violaxanthin and Lx was inhibited by dithiothreitol, suggesting that the same enzyme, violaxanthin de-epoxidase (VDE), catalyses both reactions. Dark recovery lagged in the case of Lx, and after 5 h in darkness, the Lx cycle was much more de-epoxidised than the violaxanthin cycle. The different rates of epoxidation of the violaxanthin and Lx cycles were used to study the role of the Lx cycle in photoprotection. Statistical approaches (partial correlation and multiple regression) indicate that in these leaves, maximal photochemical efficiency of PSII (Fv/Fm) and non-photochemical quenching are correlated with the level of Lx de-epoxidation. The potential implications of this finding for the understanding of the photosynthetic process in shaded and understorey leaves are discussed.

Relación entre la enfermedad de Hodgkin y factores socioeconómicos en pacientes menores de 18 años durante los años 1980-1988 en Bogotá

El siguiente trabajo fué inspirado por la revisión bibliográfica realizada, donde se evidencia la posible interacción de factores relacionados con la enfermedad de Hodgkin (E.H.), entre éstos los socioeconómicos, por lo cual iniciamos una revisión de los factores que pudieran estar relacionados. Realizamos la investigaciòn en 22 pacientes diagnosticados en el Hospital Lorencita Villegas de Santos con E.H. desde 1980-1988 a través del formulario-encuesta obtuvimos los datos a analizar y encontramos que la mayoría de pacientes llegaron tardiamente a ser estudiados, que tenían padres con poca escolaridad, regular ocupación y presentaron una gran incidencia del estado IV, y en general de un etado socioeconómico entre medio y bajo