Bell-shaped tree-ring responses to air temperature drive productivity trends in long-lived mountain Mediterranean pines.

We investigated the dendroclimatic response of a Pinus heldreichii metapopulation distributed over a wide elevation interval (from 882 to 2143 m a.s.l.), spanning from low mountain to upper subalpine vegetation belts in the southern Italian Apennines. The tested hypothesis is that wood growth along an elevational gradient is non-linearly related to air temperature. During three years of fieldwork (2012-2015) at 24 sites, we collected wood cores from a total of 214 pine trees with diameter at breast height from 19 to 180 cm (average 82.7 ± 32.9 cm). We used a combination of tree-ring and genetic methods to reveal factors involved in growth acclimation using a space-for-time approach. Scores from canonical correspondence analysis were used to combine individual tree-ring series into four composite chronologies related to air temperature along the elevation gradient. Overall, the June dendroclimatic response followed a bell-shaped thermal niche curve, increasing until a peak around 13-14 °C. A similarly bell-shaped response was found with previous autumn air temperature, and both dendroclimatic signals interacted with stem size and growth rates, generating a divergent growth response between the top and the bottom of the elevation gradient. Increased tree growth in the upper subalpine belt was consistent with the consequences of increasing air temperature under no drought stress. A positive link was uncovered between pine growth at all elevations and April mean temperature, with trees growing at the lowest elevations showing the strongest growth response. No elevational genetic differences were found, hence long-lived tree species with small geographical ranges may reverse their climatic response between the lower and upper bioclimatic zones of their environmental niche. Our study revealed a high resistance and acclimation capability of Mediterranean forest stands, and such low vulnerability to changing climatic conditions highlights the potential to store carbon in these ecosystems for the coming decades.

Maximum tree lifespans derived from public-domain dendrochronological data.

The public-domain International Tree-Ring Data Bank (ITRDB) is an under-utilized dataset to improve existing estimates of global tree longevity. We used the longest continuous ring-width series of existing ITRDB collections as an index of maximum tree age for that species and site. Using a total of 3,689 collections, we obtained longevity estimates for 237 unique tree species, 157 conifers and 80 angiosperms, distributed all over the world. More than half of the species (167) were represented by no more than 10 collections, and a similar number of species (144) reached longevity greater than 300 years. Maximum tree ages exceeded 1,000 years for several species (22), all of them conifers, whereas angiosperm longevity peaked around 500 years. Given the current emphasis on identifying human-induced impacts on global systems, detailed analyses of ITRDB holdings provide one of the most reliable sources of information for tree longevity as an ecological trait.

Historical ecology identifies long-term rewilding strategy for conserving Mediterranean mountain forests in south Italy.

In the context of global decline in old-growth forest, historical ecology is a valuable tool to derive insights into vegetation legacies and dynamics and develop new conservation and restoration strategies. In this cross-disciplinary study, we integrate palynology (Lago del Pesce record), history, dendrochronology, and historical and contemporary land cover maps to assess drivers of vegetation change over the last millennium in a Mediterranean mountain forest (Pollino National Park, southern Italy) and discuss implications in conservation ecology. The study site hosts a remnant beech-fir (Fagus sylvatica-Abies alba) mixed forest, a priority habitat for biodiversity conservation in Europe. In the 10th century, the pollen record showed an open environment that was quickly colonized by silver fir when sociopolitical instabilities reduced anthropogenic pressures in mountain forests. The highest forest cover and biomass was reached between the 14th and the 17th centuries following land abandonment due to recurring plague pandemics. This rewilding process is also reflected in the recruitment history of Bosnian pine (Pinus heldreichii) in the subalpine elevation belt. Our results show that human impacts have been one of the main drivers of silver fir population contraction in the last centuries in the Mediterranean, and that the removal of direct human pressure led to ecosystem renovation. Since 1910, the Rubbio State Forest has locally protected and restored the mixed beech-fir forest. The institutions in 1972 for the Rubbio Natural Reserve and in 1993 for Pollino National Park have guaranteed the survival of the silver fir population, demonstrating the effectiveness of targeted conservation and restoration policies despite a warming climate. Monitoring silver fir populations can measure the effectiveness of conservation measures. In the last decades, the abandonment of rural environments (rewilding) along the mountains of southern Italy has reduced the pressure on ecosystems, thus boosting forest expansion. However, after four decades of natural regeneration and increasing biomass, pollen influx and forest composition are still far from the natural attributes of the medieval forest ecosystem. We conclude that long-term forest planning encouraging limited direct human disturbance will lead toward rewilding and renovation of carbon-rich and highly biodiverse Mediterranean old-growth forests, which will be more resistant and resilient to future climate change.

Modelling Fagus sylvatica stem growth along a wide thermal gradient in Italy by incorporating dendroclimatic classification and land surface phenology metrics.

Calibrating land surface phenology (LSP) with tree rings is important to model spatio-temporal variations in forest productivity. We used MODIS (resolution: 250 m) NDVI, WDRVI and EVI series 2000-2014 to derive LSP metrics quantifying phenophase timing and canopy photosynthetic rates of 26 European beech forests covering a large thermal gradient (5-16 °C) in Italy. Average phenophase timing changed greatly with site temperature (e.g. growing season 70 days longer at low- than high-elevation); average VI values were affected by precipitation. An annual temperature about 12 °C (c. 1100 m asl) represented a bioclimatic threshold dividing warm from cold beech forests, distinguished by different phenology-BAI (basal area increment) relationships and LSP trends. Cold forests showed decreasing VI values (browning) and delayed phenophases and had negative BAI slopes. Warmer forests tended to increase VI (greening), and positive BAI slopes. NDVI peak, commonly used in global trend assessments, changed with elevation in agreement with changes in wood production. A cross-validation modelling approach demonstrated the ability of LSP to predict average BAI and its interannual variability. Merging sites into bioclimatic groups improved models by amplifying the signal in growth or LSP. NDVI had highest performances when informing on BAI trends; WDRVI and EVI were mostly selected for modelling mean and interannual BAI. WDRVI association with tree rings, tested in this study for the first time, showed that this VI is highly promising for studying forest dynamics. MODIS LSP can quantify forest functioning changes across landscapes and model interannual spatial variations and trends in productivity dynamics under climate change.

Ancient trees: irreplaceable conservation resource for ecosystem restoration.

Ancient trees contribute multifaceted ecosystem benefits to old-growth forests, rewilding, and human cultural landscapes. As such, we call for international efforts to preserve these hubs of diversity and resilience. A global coalition utilizing advanced technologies and community scientists to discover, protect, and propagate ancient trees is needed before they disappear.

Old and ancient trees are life history lottery winners and vital evolutionary resources for long-term adaptive capacity.

Trees can live for many centuries with sustained fecundity and death is largely stochastic. We use a neutral stochastic model to examine tree demographic patterns that emerge over time, across a range of population sizes and empirically observed mortality rates. A small proportion of trees (~1% at 1.5% mortality) are life-history 'lottery winners', achieving ages >10-20× the median age. Maximum age increases with bigger populations and lower mortality rates. One-quarter of trees (~24%) achieve ages that are three to four times greater than the median age. Three age classes (mature, old and ancient) contribute unique evolutionary diversity across complex environmental cycles. Ancient trees are an emergent property of forests that requires many centuries to generate. They radically change variance in generation time and population fitness, bridging centennial environmental cycles. These life-history 'lottery' winners are vital to long-term forest adaptive capacity and provide invaluable data about environmental history and individual longevity. Old and ancient trees cannot be replaced through restoration or regeneration for many centuries. They must be protected to preserve their invaluable diversity.

Mediterranean old-growth forests exhibit resistance to climate warming.

Old-growth mountain forests represent an ideal setting for studying long-term impacts of climate change. We studied the few remnants of old-growth forests located within the Pollino massif (southern Italy) to evaluate how the growth of conspecific young and old trees responded to climate change. We investigated two conifer species (Abies alba and Pinus leucodermis) and two hardwood species (Fagus sylvatica and Quercus cerris). We sampled one stand per species along an altitudinal gradient, ranging from a drought-limited low-elevation hardwood forest to a cold-limited subalpine pine forest. We used a dendrochronological approach to characterize the long-term growth dynamics of old (age > 120 years) versus young (age < 120 years) trees. Younger trees grew faster than their older conspecifics during their juvenile stage, regardless of species. Linear mixed effect models were used to quantify recent growth trends (1950-2015) and responses to climate for old and young trees. Climate sensitivity, expressed as radial growth responses to climate during the last three decades, partially differed between species because high spring temperatures enhanced conifer growth, whereas F. sylvatica growth was negatively affected by warmer spring conditions. Furthermore, tree growth was negatively impacted by summer drought in all species. Climate sensitivity differed between young and old trees, with younger trees tending to be more sensitive in P. leucodermis and A. alba, whereas older F. sylvatica trees were more sensitive. In low-elevation Q. cerris stands, limitation of growth due to drought was not related to tree age, suggesting symmetric water competition. We found evidence for a fast-growth trend in young individuals compared with that in their older conspecifics. Notably, old trees tended to have relatively stable growth rates, showing remarkable resistance to climate warming. These responses to climate change should be recognized when forecasting the future dynamics of old-growth forests for their sustainable management.

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.

On tree longevity.

Large, majestic trees are iconic symbols of great age among living organisms. Published evidence suggests that trees do not die because of genetically programmed senescence in their meristems, but rather are killed by an external agent or a disturbance event. Long tree lifespans are therefore allowed by specific combinations of life history traits within realized niches that support resistance to, or avoidance of, extrinsic mortality. Another requirement for trees to achieve their maximum longevity is either sustained growth over extended periods of time or at least the capacity to increase their growth rates when conditions allow it. The growth plasticity and modularity of trees can then be viewed as an evolutionary advantage that allows them to survive and reproduce for centuries and millennia. As more and more scientific information is systematically collected on tree ages under various ecological settings, it is becoming clear that tree longevity is a key trait for global syntheses of life history strategies, especially in connection with disturbance regimes and their possible future modifications. In addition, we challenge the long-held notion that shade-tolerant, late-successional species have longer lifespans than early-successional species by pointing out that tree species with extreme longevity do not fit this paradigm. Identifying extremely old trees is therefore the groundwork not only for protecting and/or restoring entire landscapes, but also to revisit and update classic ecological theories that shape our understanding of environmental change.

Climate-human interactions contributed to historical forest recruitment dynamics in Mediterranean subalpine ecosystems.

Long-term tree recruitment dynamics of subalpine forests mainly depend on temperature changes, but little is known about the feedbacks between historical land use and climate. Here, we analyze a southern European, millennium-long dataset of tree recruitment from three high-elevation pine forests located in Mediterranean mountains (Pyrenees, northeastern Spain; Pollino, southern Italy; and Mt. Smolikas, northern Greece). We identify synchronized recruitment peaks in the late 15th and early 16th centuries, following prolonged periods of societal and climate instability. Major European population crises in the 14th and 15th centuries associated with recurrent famines, the Black Death pandemic, and political turmoil are likely to have reduced the deforestation of subalpine environments and caused widespread rewilding. We suggest that a distinct cold phase in the Little Ice Age around 1450 ce could also have accelerated the cessation of grazing pressure, particularly in the Pyrenees, where the demographic crisis was less severe. Most pronounced in the Pyrenees, the enhanced pine recruitment from around 1500-1550 ce coincides with temporarily warmer temperatures associated with a positive phase of the North Atlantic Oscillation. We diagnose that a mixture of human and climate factors has influenced past forest recruitment dynamics in Mediterranean subalpine ecosystems. Our results highlight how complex human-climate interactions shaped forest dynamics during pre-industrial times and provide historical analogies to recent rewilding.

Need for a global map of forest naturalness for a sustainable future.

There is a growing need to assess and monitor forest cover and its conservation status over global scales to determine human impact on ecosystems and to develop sustainability plans. Recent approaches to measure regional and global forest status and dynamics are based on remotely sensed estimates of tree cover. We argue that tree cover should not be used to assess the area of forest ecosystems because tree cover is an undefined subset of forest cover. For example, tree cover can indicate a positive trend even in the presence of deforestation, as in the case of plantations. We believe a global map of forest naturalness that accounts for the bio-ecological integrity of forest ecosystems, for example, intact forests, old-growth forest patches, rewilding forests (exploited forest landscapes undergoing long-term natural succession), and managed forests is needed for global forest assessment.

La Necesidad de Tener un Mapa Global de la Naturalidad Forestal para un Futuro Sustentable Resumen Existe una creciente necesidad de evaluar y monitorear la cobertura forestal y su estado de conservación a escala global para determinar el impacto humano sobre los ecosistemas y así desarrollar planes de sustentabilidad. Las estrategias recientes para medir el estado regional y global de los bosques, así como sus dinámicas, están basadas en estimaciones de la cobertura de árboles detectados remotamente. Discutimos que la cobertura de árboles no debería usarse para evaluar el área de los ecosistemas boscosos porque ésta es un subconjunto indefinido de la cobertura forestal. Por ejemplo, la cobertura de árboles puede indicar una tendencia positiva incluso con la presencia de la deforestación, como sucede en el caso de las plantaciones. Creemos que se necesita un mapa global de la naturalidad de los bosques que considere la integridad bio-ecológica de los ecosistemas boscosos, por ejemplo, los bosques intactos, los fragmentos de bosques primarios, los bosques de resilvestración (paisajes de bosques explotados que están pasando por una sucesión natural a largo plazo) y los bosques manejados, para la evaluación mundial de los bosques.

Geographical adaptation prevails over species-specific determinism in trees' vulnerability to climate change at Mediterranean rear-edge forests.

Climate change may reduce forest growth and increase forest mortality, which is connected to high carbon costs through reductions in gross primary production and net ecosystem exchange. Yet, the spatiotemporal patterns of vulnerability to both short-term extreme events and gradual environmental changes are quite uncertain across the species' limits of tolerance to dryness. Such information is fundamental for defining ecologically relevant upper limits of species tolerance to drought and, hence, to predict the risk of increased forest mortality and shifts in species composition. We investigate here to what extent the impact of short- and long-term environmental changes determines vulnerability to climate change of three evergreen conifers (Scots pine, silver fir, Norway spruce) and two deciduous hardwoods (European beech, sessile oak) tree species at their southernmost limits of distribution in the Mediterranean Basin. Finally, we simulated future forest growth under RCP 2.6 and 8.5 emission scenarios using a multispecies generalized linear mixed model. Our analysis provides four key insights into the patterns of species' vulnerability to climate change. First, site climatic marginality was significantly linked to the growth trends: increasing growth was related to less climatically limited sites. Second, estimated species-specific vulnerability did not match their a priori rank in drought tolerance: Scots pine and beech seem to be the most vulnerable species among those studied despite their contrasting physiologies. Third, adaptation to site conditions prevails over species-specific determinism in forest response to climate change. And fourth, regional differences in forests vulnerability to climate change across the Mediterranean Basin are linked to the influence of summer atmospheric circulation patterns, which are not correctly represented in global climate models. Thus, projections of forest performance should reconsider the traditional classification of tree species in functional types and critically evaluate the fine-scale limitations of the climate data generated by global climate models.

Historical ecology reveals landscape transformation coincident with cultural development in central Italy since the Roman Period.

Knowledge of the direct role humans have had in changing the landscape requires the perspective of historical and archaeological sources, as well as climatic and ecologic processes, when interpreting paleoecological records. People directly impact land at the local scale and land use decisions are strongly influenced by local sociopolitical priorities that change through time. A complete picture of the potential drivers of past environmental change must include a detailed and integrated analysis of evolving sociopolitical priorities, climatic change and ecological processes. However, there are surprisingly few localities that possess high-quality historical, archeological and high-resolution paleoecologic datasets. We present a high resolution 2700-year pollen record from central Italy and interpret it in relation to archival documents and archaeological data to reconstruct the relationship between changing sociopolitical conditions, and their effect on the landscape. We found that: (1) abrupt environmental change was more closely linked to sociopolitical and demographic transformation than climate change; (2) landscape changes reflected the new sociopolitical priorities and persisted until the sociopolitical conditions shifted; (3) reorganization of new plant communities was very rapid, on the order of decades not centuries; and (4) legacies of forest management adopted by earlier societies continue to influence ecosystem services today.

Dating old hollow trees by applying a multistep tree-ring and radiocarbon procedure to trunk and exposed roots.

In the process of dating the oldest trees, which are often hollow, we developed a new method that combines tree-ring cross dating and wiggle matching radiocarbon techniques on wood samples extracted from the stem and from exposed roots. The method can be illustrated by the following steps: •crossdated tree-ring series from trunk cores reveal a multi-century tree age, and the hollow section is large enough to contain several more years (decades to centuries)•exposed roots can be cored for acquiring wood samples older than the stem cores and for construction of a floating root average tree-ring series•if synchronization between stem and exposed roots is unclear, proceed to date the root wood samples by radiocarbon wiggle matching; match root and stem tree-ring series within the radiocarbon-dated period to more accurately date the tree. This new multistep dating method allowed for refining the age estimation of the oldest Pinus heldreichii tree in Pollino National Park by 166 years, to 789 CE. This tree, which we named Italus, was 1229 years old in 2017, making it the oldest, scientifically dated, living tree in Europe. Any study that relies on tree age determination for paleo-reconstructions, for biological and genetic research on what controls longevity, or for understanding structural dynamics and succession in old-growth forests, would potentially benefit from the multistep dating method we tested.