ALBERT

Description: Long-term fluctuations in forest recruitment, at time scales well beyond the life-span of individual trees, can be related to climate changes. The underlying climatic drivers are, however, often understudied. Here, we present the recruitment history of a high-elevation mountain pine (Pinus uncinata Ram.) forest in the Spanish central Pyrenees throughout the last millennium. A total of 1108 ring-width series translated into a continuous chronology from 924 to 2014 CE, which allowed estimated germination dates of 470 trees to be compared against decadal-scale temperature variability. High recruitment intensity mainly coincided with relatively warm periods in the early 14th, 15th, 19th, and 20th centuries, whereas cold phases during the mid-17th, early 18th, and mid-19th centuries overlapped with generally low recruitment rates. In revealing the importance of prolonged warm conditions for high-elevation pine recruitment in the Pyrenees, this study suggests increased densification and even possible upward migration of tree-line ecotones under predicted global warming.

Description: Juniperus thurifera L. is an endemic conifer of the western Mediterranean Basin where it is subjected to a severe climatic stress characterized by low winter temperatures and summer drought. Given the trend of increased warming-induced drought stress in this area and the climatic sensitivity of this species, we expect a negative impact of climate change on growth and ecophysiological performance of J. thurifera in the harsh environments where it dominates. To evaluate this, we measured long- and short-term radial growth using dendrochronology, photosynthesis and water-use efficiency in males, females and juveniles in three sites in Central Spain. Climate was monitored and completed with historical records. Mean annual temperature has increased +0.2 °C per decade in the study area, and the main warming trends corresponded to spring (+0.2 °C per decade) and summer (+0.3 °C per decade). Radial growth and maximum photosynthesis peaked in spring and autumn. Positive photosynthetic rates were maintained all year long, albeit at reduced rates in winter and summer. Radial growth was enhanced by wet conditions in the previous autumn and by warm springs and high precipitation in summer of the year of tree-ring formation. Cloud cover during the summer increased growth, while cloudy winters led to impaired carbon gain and reduced growth in the long term. We argue that maintenance of carbon gain under harsh conditions (low winter temperatures and dry summer months) and plastic xylogenesis underlie J. thurifera 's ability to profit from changing climatic conditions such as earlier spring onset and erratic summer rainfall. Our results highlight that not only the magnitude but also the sign of the impact of climate change on growth and persistence of Mediterranean trees is species specific.

Description: Tocochromanols are the most abundant lipid-soluble antioxidants in plants. Among them, α-tocopherol (α-Toc) shows a particularly high sensitivity to environmental stressors and its content is used as a stress biomarker even in non-photosynthetic tissues. Nevertheless, the presence of tocochromanols has not been described yet in the xylem of woody plants, even when their functions regarding cell membrane protection and the transport of photoassimilates may be crucial in this tissue and despite its potential utility in dendrometabolomics. Considering all these, we aimed to determine the presence and distribution of tocochromanols in the xylem of woody plants, to examine their responsiveness to high temperature and to evaluate their potential as environmental bioindicators. The analysis of 29 phyllogenetically diverse species showed that α-Toc is the most abundant and frequent tocochromanol in the xylem and is ubiquitously present in all the studied species, with a concentration ranging from 0.5 to 39.3 μg g –1 of dry weight. α-Tocopherol appeared to be mainly located in the parenchyma rays and was found in both the sapwood and the heartwood, suggesting that it is present even in dead parenchyma cells. The levels of α-Toc in the xylem did not change in response to locally induced xylem heating, but responded positively to the 3-year moving average of annual precipitation. The present findings suggest that α-Toc may be linked to changes in climatic stress. This should enhance further research on the environmental controls of α-Toc variation in the xylem as a first step towards a deeper understanding of dendrometabolomics.

Description: Forecasted warmer and drier conditions will probably lead to reduced growth rates and decreased carbon fixation in long-term woody pools in drought-prone areas. We therefore need a better understanding of how climate stressors such as drought constrain wood formation and drive changes in wood anatomy. Drying trends could lead to reduced growth if they are more intense in spring, when radial growth rates of conifers in continental Mediterranean climates peak. Since tree species from the aforementioned areas have to endure dry summers and also cold winters, we chose two coexisting species: Aleppo pine ( Pinus halepensis Mill., Pinaceae) and Spanish juniper ( Juniperus thurifera L., Cupressaceae) (10 randomly selected trees per species), to analyze how growth (tree-ring width) and wood-anatomical traits (lumen transversal area, cell-wall thickness, presence of intra-annual density fluctuations—IADFs—in the latewood) responded to climatic variables (minimum and maximum temperatures, precipitation, soil moisture deficit) calculated for different time intervals. Tree-ring width and mean lumen area showed similar year-to-year variability, which indicates that they encoded similar climatic signals. Wet and cool late-winter to early-spring conditions increased lumen area expansion, particularly in pine. In juniper, cell-wall thickness increased when early summer conditions became drier and the frequency of latewood IADFs increased in parallel with late-summer to early-autumn wet conditions. Thus, latewood IADFs of the juniper capture increased water availability during the late growing season, which is reflected in larger tracheid lumens. Soil water availability was one of the main drivers of wood formation and radial growth for the two species. These analyses allow long-term (several decades) growth and wood-anatomical responses to climate to be inferred at intra-annual scales, which agree with the growing patterns already described by xylogenesis approaches for the same species. A plastic bimodal growth behavior, driven by dry summer conditions, is coherent with the presented wood-anatomical data. The different wood-anatomical responses to drought stress are observed as IADFs with contrasting characteristics and responses to climate. These different responses suggest distinct capacities to access soil water between the two conifer species.

Description: Forest decline has been attributed to the interaction of several stressors including biotic factors such as mistletoes and climate-induced drought stress. However, few data exist on how mistletoes are spatially arranged within trees and how this spatial pattern is related to changes in radial growth, responses to drought stress and carbon use. We used dendrochronology to quantify how mistletoe ( Viscum album L.) infestation and drought stress affected long-term growth patterns in Pinus sylvestris L. at different heights. Basal area increment (BAI) trends and comparisons between trees of three different infestation degrees (without mistletoe, ID1; moderately infested trees, ID2; and severely infested trees, ID3) were performed using linear mixed-effects models. To identify the main climatic drivers of tree growth tree-ring widths were converted into indexed chronologies and related to climate data using correlation functions. We performed spatial analyses of the 3D distribution of mistletoe individuals and their ages within the crowns of three severely infested pines to describe their patterns. Lastly, we quantified carbohydrate and nitrogen concentrations in needles and sapwood of branches from severely infested trees and from trees without mistletoe. Mistletoe individuals formed strongly clustered groups of similar age within tree crowns and their age increased towards the crown apex. Mistletoe infestation negatively impacted growth but this effect was stronger near the tree apex than in the rest of sampled heights, causing an average loss of 64% in BAI (loss of BAI was ~51% at 1.3 m or near the tree base). We found that BAI of severely infested trees and moderately or non-infested trees diverged since 2001 and such divergence was magnified by drought. Infested trees had lower concentrations of soluble sugars in their needles than non-infested ones. We conclude that mistletoe infestation causes growth decline and increases the sensitivity of trees to drought stress.

Description: Changes in climate can alter the distribution and population dynamics of tree species by altering their recruitment patterns, especially at range edges. However, geographical patterns of genetic diversity could buffer the negative consequences of changing climate at rear range edges where populations might also harbour individuals with drought-adapted genotypes. Silver fir ( Abies alba Mill.) reaches its south-western distribution limit in the Spanish Pyrenees, where recent climatic dieback events have disproportionately affected westernmost populations. We hypothesized that silver fir populations from the eastern Pyrenees are less vulnerable to the expected changing climate due to the inclusion of drought-resistant genotypes. We performed an experiment under strictly controlled conditions simulating projected warming and drought compared with current conditions and analysed physiology, growth and survival of silver fir seedlings collected from eastern and western Pyrenean populations. Genetic analyses separated eastern and western provenances in two different lineages. Climate treatments affected seedling morphology and survival of both lineages in an overall similar way: elevated drought diminished survival and induced a higher biomass allocation to roots. Increased temperature and drought provoked more negative stem water potentials and increased 13 C ratios in leaves. Warming reduced nitrogen concentration and increased soluble sugar content in leaves, whereas drought increased nitrogen concentration. Lineage affected these physiological parameters, with western seedlings being more sensitive to warming and drought increase in terms of 13 C, nitrogen and content of soluble sugars. Our results demonstrate that, in A. alba , differences in the physiological response of this species to drought are also associated with differences in biogeographical history.

Description: Young and mature trees are usually characterized by asynchronous growth resumption of xylem. Here, we test the hypothesis that the later onset of xylem growth in older trees is related to the longer distance of the stem from the developing buds, which represents the main source of hormones triggering vascular tissue differentiation. We compared the onset of xylogenesis at different heights along the stems of young and mature Smith fir (Abies georgei var. smithii (Viguie & Gaussen) W. C. Cheng & L. K. Fu)) trees in the Sygera Mountains, southeastern Tibetan Plateau. Xylem formation was monitored weekly in 2012 on anatomical sections of wood microcores. The onset of xylogenesis differed between young and mature trees, with most phases occurring 2 weeks later in mature trees. No effect of the sampling height was observed on the growth resumption. Our results suggest that the later resumption of xylogenesis in older conifer trees is not related to their longer distance from the crown.

Description: In trees, wood anatomy is a more precise and informative measure of hydraulic responses to drought than radial growth. Tree populations located near the equatorial-range edge of their distribution (rear edge) are used to monitor responses to changes in hydroclimate; however, few studies have assessed the wood anatomy of these populations. We measured tracheid lumen diameter (LD) and cell wall thickness (CWT) in a rear-edge Douglas-fir (Pseudotsuga menziesii (Mirb.) Franco) population. We also evaluated the formation of intra-annual density fluctuations (IADFs), characterized by earlywood (EW) tracheids with narrow lumens. We expected that EW LD would be particularly sensitive to hydroclimate variability. We found that EW LD was directly related to precipitation during the previous year’s late winter and the current year’s spring. Wet conditions were associated with wider EW tracheids and improved growth. These correlations peaked when considering cumulative precipitation from January to May. EW IADFs were formed in response to dry conditions during March and April, suggesting that dry spring conditions limit tracheid expansion. The described associations in a rear-edge Douglas-fir population confirm that wood anatomy is highly responsive to drought. We conclude that EW LD is a valuable proxy for hydroclimate reconstruction in Douglas-fir.

Description: Insect outbreaks of increasing frequency and severity in forests are predicted due to climate change. Insect herbivory is known to promote physiological changes in forest trees. However, little is known about whether these plant phenotypic adjustments have cascading effects on tree microbial symbionts such as fungi in roots and foliage. We studied the impact of defoliation by the pine processionary moth in two infested Pinus nigra forests through a multilevel sampling of defoliated and non-defoliated trees. We measured tree growth, nutritional status and carbon allocation to chemical defenses. Simultaneously, we analysed the putative impact of defoliation on the needle endophytes and on the soil fungal communities. Higher concentrations of chemical defenses were found in defoliated trees, likely as a response to defoliation; however, no differences in non-structural carbohydrate reserves were found. In parallel to the reductions in tree growth and changes in chemical defenses, we observed shifts in the composition of needle endophytic and soil fungal communities in defoliated trees. Defoliated trees consistently corresponded with a lower biomass of ectomycorrhizal fungi in both sites, and a higher alpha diversity and greater relative abundance of belowground saprotrophs and pathogens. However, ectomycorrhizal alpha diversity was similar between non-defoliated and defoliated trees. Specific needle endophytes in old needles were strongly associated with non-defoliated trees. The potential role of these endophytic fungi in pine resistance should be further investigated. Our study suggests that lower biomass of ectomycorrhizal fungi in defoliated trees might slow down tree recovery since fungal shifts might affect tree-mycorrhizal feedbacks and can potentially influence carbon and nitrogen cycling in forest soils.

Description: Drought limits the long-distance transport of water in the xylem due to the reduced leaf-to-soil water potential difference and possible embolism-related losses of conductance and of sugars in the phloem due to the higher viscosity of the dehydrated sugary solution. This condition can have cascading effects in water and carbon (C) fluxes that may ultimately cause tree death. We hypothesize that the maintenance of xylem and phloem conductances is fundamental for survival also under reduced resource availability, when trees may produce effective and low C cost anatomical adjustments in the xylem and phloem close to the treetop where most of the hydraulic resistance is concentrated. We analyzed the treetop xylem and phloem anatomical characteristics in coexisting Scots pine trees, symptomatic and non-symptomatic of drought-induced dieback. We selected the topmost 55 cm of the main stem and selected several sampling positions at different distances from the stem apex to test for differences in the axial patterns between the two groups of trees. We measured the annual ring area, the tracheid hydraulic diameter (Dh) and cell wall thickness (CWT), the conductive phloem area and the average lumen diameter of the 20 largest phloem sieve cells (Dph). Declining trees grew less than the non-declining ones, and despite the similar axial scaling of anatomical traits, had larger Dh and lower CWT. Moreover, declining trees had wider Dph. Our results demonstrate that even under drought stress, maintenance of xylem and phloem efficiencies is of primary importance for survival, even if producing fewer larger tracheids may lead to a xylem more vulnerable to embolism formation.