Effects of lianas on forest biogeochemistry during their lives and afterlives.

Climate change and other anthropogenic disturbances are increasing liana abundance and biomass in many tropical and subtropical forests. While the effects of living lianas on species diversity, ecosystem carbon, and nutrient dynamics are receiving increasing attention, the role of dead lianas in forest ecosystems has been little studied and is poorly understood. Trees and lianas coexist as the major woody components of forests worldwide, but they have very different ecological strategies, with lianas relying on trees for mechanical support. Consequently, trees and lianas have evolved highly divergent stem, leaf, and root traits. Here we show that this trait divergence is likely to persist after death, into the afterlives of these organs, leading to divergent effects on forest biogeochemistry. We introduce a conceptual framework combining horizontal, vertical, and time dimensions for the effects of liana proliferation and liana tissue decomposition on ecosystem carbon and nutrient cycling. We propose a series of empirical studies comparing traits between lianas and trees to answer questions concerning the influence of trait afterlives on the decomposability of liana and tree organs. Such studies will increase our understanding of the contribution of lianas to terrestrial biogeochemical cycling, and help predict the effects of their increasing abundance.

Anatomical adjustment of mature leaves of sycamore maple (Acer pseudoplatanus L.) to increased irradiance.

Trees regenerating in the understory respond to increased availability of light caused by gap formation by undergoing a range of morphological and physiological adjustments. These adjustments include the production of thick, sun-type leaves containing thicker mesophyll and longer palisade cells than in shade-type leaves. We asked whether in the shade-regenerating tree Acer pseudoplatanus, the increase in leaf thickness and expansion of leaf tissues are possible also in leaves that had been fully formed prior to the increase in irradiance, a response reported so far only for a handful of species. We acclimated potted seedlings to eight levels (from 1 to 100%) of solar irradiance and, in late summer, transferred a subset of them to full sunlight. Within 30 days, the shaded leaves increased leaf mass per area and became thicker mostly due to elongation of palisade cells, except for the most shaded individuals which suffered irreversible photo-oxidative damage. This anatomical acclimation was accompanied by partial degradation of chlorophyll and a transient decline in photosynthetic efficiency of PSII (Fv/FM). These effects were related to the degree of pre-shading. The Fv/FM recovered substantially within the re-acclimation period. However, leaves of transferred plants were shed significantly earlier in the fall, indicating that the acclimation was not fully effective. These results show that A. pseudoplatanus is one of the few known species in which mature leaves may re-acclimate anatomically to increased irradiance. This may be a potentially important mechanism enhancing utilization of gaps created during the growing season.

Anatomical acclimation of mature leaves to increased irradiance in sycamore maple (Acer pseudoplatanus L.).

Trees regenerating in the understory respond to increased availability of light caused by gap formation by undergoing a range of morphological and physiological adjustments. These adjustments include the production of thick, sun-type leaves containing thicker mesophyll and longer palisade cells than in shade-type leaves. We asked whether in the shade-regenerating tree Acer pseudoplatanus, the increase in leaf thickness and expansion of leaf tissues are possible also in leaves that are already fully formed, a response reported so far only for a handful of species. We acclimated potted seedlings to eight levels (from 1 to 100%) of solar irradiance and, in late summer, transferred a subset of them to full sunlight. Within 30 days, the pre-shaded leaves increased leaf mass per area and became thicker mostly due to the elongation of palisade cells, except for the most shaded individuals which suffered irreversible photo-oxidative damage. This anatomical acclimation was accompanied by a transient decline in photosynthetic efficiency of PSII (Fv/FM), the magnitude of which was related to the degree of pre-shading. The Fv/FM recovered substantially within the re-acclimation period. However, leaves of transferred plants were shed earlier in the fall, indicating that the acclimation was not fully effective. These results show that A. pseudoplatanus is one of the few known species in which mature leaves may re-acclimate anatomically to increased irradiance. This may be an important mechanism enhancing utilization of gaps created during the growing season.

Mechanistic drivers of stem respiration: A modelling exercise across species and seasons.

Stem respiration (RS ) plays a crucial role in plant carbon budgets. However, its poor understanding limits our ability to model woody tissue and whole-tree respiration. A biophysical model of stem water and carbon fluxes (TReSpire) was calibrated on cedar, maple and oak trees during spring and late summer. For this, stem sap flow, water potential, diameter variation, temperature, CO2 efflux, allometry and biochemistry were monitored. Shoot photosynthesis (PN ) and nonstructural carbohydrates (NSC) were additionally measured to evaluate source-sink relations. The highest RS and stem growth was found in maple and oak during spring, both being seasonally decoupled from PN and [NSC]. Temperature largely affected maintenance respiration (RM ) in the short term, but temperature-normalized RM was highly variable on a seasonal timescale. Overall, most of the respired CO2 radially diffused to the atmosphere (>87%) while the remainder was transported upward with the transpiration stream. The modelling exercise highlights the sink-driven behaviour of RS and the significance of overall metabolic activity on nitrogen (N) allocation patterns and N-normalized respiratory costs to capture RS variability over the long term. These insights should be considered when modelling plant respiration, whose representation is currently biased towards a better understanding of leaf metabolism.

Stomatal density in Pinus sylvestris as an indicator of temperature rather than CO2 : Evidence from a pan-European transect.

The commonly observed negative relationship between stomatal density (SD) and atmospheric CO2 has led to SD being proposed as an indicator of atmospheric CO2 concentration. The use of SD as a proxy for CO2 , however, has been hampered by an insufficient understanding of the intraspecific variation of this trait. We hypothesized that SD in Pinus sylvestris, a widely distributed conifer, varies geographically and that this variation is determined by major climatic variables. By sampling needles from naturally growing trees along a latitudinal range of 32.25°, equivalent to 13.7°C gradient of mean annual temperature (MAT) across Europe, we found that SD decreased from the warmest southern sites to the coldest sites in the north at a rate of 4 stomata per mm2 for each 1°C, with MAT explaining 44% of the variation. Additionally, samples from a provenance trial exhibited a positive relationship between SD and the MAT of the original localities, suggesting that high SD is an adaptation to warm temperature. Our study revealed one of the strongest intraspecific relationships between SD and climate in any woody species, supporting the utility of SD as a temperature, rather than direct CO2 , proxy. In addition, our results predict the response of SD to climate warming.

Higher biomass partitioning to absorptive roots improves needle nutrition but does not alleviate stomatal limitation of northern Scots pine.

Harsh environmental conditions affect both leaf structure and root traits. However, shoot growth in high-latitude systems is predominately under photoperiod control while root growth may occur for as long as thermal conditions are favorable. The different sensitivities of these organs may alter functional relationships above- and belowground along environmental gradients. We examined the relationship between absorptive root and foliar traits of Scots pine trees growing in situ along a temperate-boreal transect and in trees grown in a long-term common garden at a temperate latitude. We related changes in foliar nitrogen, phosphorus, specific leaf area, needle mass and 13 C signatures to geographic trends in absorptive root biomass to better understand patterns of altered tree nutrition and water balance. Increased allocation to absorptive fine roots was associated with greater uptake of soil nutrients and subsequently higher needle nutrient contents in the northern provenances compared with more southern provenances when grown together in a common garden setting. In contrast, the leaf δ13 C in northern and southern provenances were similar within the common garden suggesting that higher absorptive root biomass fractions could not adequately increase water supply in warmer climates. These results highlight the importance of allocation within the fine-root system and its impacts on needle nutrition while also suggesting increasing stomatal limitation of photosynthesis in the context of anticipated climatic changes.

A fingerprint of climate change across pine forests of Sweden.

Climate change has likely altered high-latitude forests globally, but direct evidence remains rare. Here we show that throughout a ≈1000-km transect in Scots pine (Pinus sylvestris L.) forests in Sweden, mature trees in ≈2015 had longer needles with shorter lifetimes than did trees in ≈1915. These century-scale shifts in needle traits were detected by sampling needles at 74 sites from 2012 to 2017 along the same transect where needle traits had been assessed at 57 sites in 1914-1915. Climate warming of ≈1 °C all along the transect in the past century has driven this temporal shift in foliage traits known to be physiologically critical to growth and carbon cycling processes. These century-scale changes in Scandinavian Scots pine forests represent a fingerprint of climate change on a fundamental biological element, the leaf, with repercussions for productivity and sensitivity to future climate, which are likely to be mirrored by similar changes for evergreen conifers across the boreal biome.

Woody tissue photosynthesis delays drought stress in Populus tremula trees and maintains starch reserves in branch xylem tissues.

Photosynthesis in woody tissues (Pwt ) is less sensitive to water shortage than in leaves, hence, Pwt might be a crucial carbon source to alleviate drought stress. To evaluate the impact of Pwt on tree drought tolerance, woody tissues of 4-m-tall drought-stressed Populus tremula trees were subjected to a light-exclusion treatment across the entire plant to inhibit Pwt . Xylem water potential (Ψxylem ), sap flow ( FH2O ), leaf net photosynthesis (Pn,l ), stem diameter variations (ΔD), in vivo acoustic emissions in stems (AEs) and nonstructural carbohydrate concentrations ([NSC]) were monitored to comprehensively assess water and carbon relations at whole-tree level. Under well-watered conditions, Pwt kept Ψxylem at a higher level, lowered FH2O and had no effect on [NSC]. Under drought, Ψxylem , FH2O and Pn,l in light-excluded trees rapidly decreased in concert with reductions in branch xylem starch concentration. Moreover, sub-daily patterns of ΔD, FH2O and AEs were strongly related, suggesting that in vivo AEs may inform not only about embolism events, but also about capacitive release and replenishment of stem water pools. Results highlight the importance of Pwt in maintaining xylem hydraulic integrity under drought conditions and in sustaining NSC pools to potentially limit increases in xylem tension.

TReSpire - a biophysical TRee Stem respiration model.

Mechanistic models of plant respiration remain poorly developed, especially in stems and woody tissues where measurements of CO2 efflux do not necessarily reflect local respiratory activity. We built a process-based model of stem respiration that couples water and carbon fluxes at the organ level (TReSpire). To this end, sap flow, stem diameter variations, xylem and soil water potential, stem temperature, stem CO2 efflux and nonstructural carbohydrates were measured in a maple tree, while xylem CO2 concentration and additional stem and xylem diameter variations were monitored in an ancillary tree for model validation. TReSpire realistically described: (1) turgor pressure to differentiate growing from nongrowing metabolism; (2) maintenance expenditures in xylem and outer tissues based on Arrhenius kinetics and nitrogen content; and (3) radial CO2 diffusivity and CO2 solubility and transport in the sap solution. Collinearity issues with phloem unloading rates and sugar-starch interconversion rates suggest parallel submodelling to close the stem carbon balance. TReSpire brings a breakthrough in the modelling of stem water and carbon fluxes at a detailed (hourly) temporal resolution. TReSpire is calibrated from a sink-driven perspective, and has potential to advance our understanding on stem growth dynamics, CO2 fluxes and underlying respiratory physiology across different species and phenological stages.

Three keys to the radiation of angiosperms into freezing environments.

Early flowering plants are thought to have been woody species restricted to warm habitats. This lineage has since radiated into almost every climate, with manifold growth forms. As angiosperms spread and climate changed, they evolved mechanisms to cope with episodic freezing. To explore the evolution of traits underpinning the ability to persist in freezing conditions, we assembled a large species-level database of growth habit (woody or herbaceous; 49,064 species), as well as leaf phenology (evergreen or deciduous), diameter of hydraulic conduits (that is, xylem vessels and tracheids) and climate occupancies (exposure to freezing). To model the evolution of species' traits and climate occupancies, we combined these data with an unparalleled dated molecular phylogeny (32,223 species) for land plants. Here we show that woody clades successfully moved into freezing-prone environments by either possessing transport networks of small safe conduits and/or shutting down hydraulic function by dropping leaves during freezing. Herbaceous species largely avoided freezing periods by senescing cheaply constructed aboveground tissue. Growth habit has long been considered labile, but we find that growth habit was less labile than climate occupancy. Additionally, freezing environments were largely filled by lineages that had already become herbs or, when remaining woody, already had small conduits (that is, the trait evolved before the climate occupancy). By contrast, most deciduous woody lineages had an evolutionary shift to seasonally shedding their leaves only after exposure to freezing (that is, the climate occupancy evolved before the trait). For angiosperms to inhabit novel cold environments they had to gain new structural and functional trait solutions; our results suggest that many of these solutions were probably acquired before their foray into the cold.

Soil organic carbon stability in forests: Distinct effects of tree species identity and traits.

Rising atmospheric CO2 concentrations have increased interest in the potential for forest ecosystems and soils to act as carbon (C) sinks. While soil organic C contents often vary with tree species identity, little is known about if, and how, tree species influence the stability of C in soil. Using a 40 year old common garden experiment with replicated plots of eleven temperate tree species, we investigated relationships between soil organic matter (SOM) stability in mineral soils and 17 ecological factors (including tree tissue chemistry, magnitude of organic matter inputs to the soil and their turnover, microbial community descriptors, and soil physicochemical properties). We measured five SOM stability indices, including heterotrophic respiration, C in aggregate occluded particulate organic matter (POM) and mineral associated SOM, and bulk SOM δ15 N and ∆14 C. The stability of SOM varied substantially among tree species, and this variability was independent of the amount of organic C in soils. Thus, when considering forest soils as C sinks, the stability of C stocks must be considered in addition to their size. Further, our results suggest tree species regulate soil C stability via the composition of their tissues, especially roots. Stability of SOM appeared to be greater (as indicated by higher δ15 N and reduced respiration) beneath species with higher concentrations of nitrogen and lower amounts of acid insoluble compounds in their roots, while SOM stability appeared to be lower (as indicated by higher respiration and lower proportions of C in aggregate occluded POM) beneath species with higher tissue calcium contents. The proportion of C in mineral associated SOM and bulk soil ∆14 C, though, were negligibly dependent on tree species traits, likely reflecting an insensitivity of some SOM pools to decadal scale shifts in ecological factors. Strategies aiming to increase soil C stocks may thus focus on particulate C pools, which can more easily be manipulated and are most sensitive to climate change.

Biomass and nitrogen distribution ratios reveal a reduced root investment in temperate lianas vs. self-supporting plants.

BACKGROUND AND AIMS: The reliance on external support by lianas has been hypothesized to imply a reduction in the biomass cost of stem construction and root anchorage, and an increased investment in leaves, relative to self-supporting plants. These evolutionary trade-offs have not been adequately tested in an ontogenetic context and on the whole-plant scale. Moreover, the hypothesis may be extended to other potentially limiting resources, such as nitrogen (N.). METHODS: Plants belonging to five con-familiar pairs of temperate liana/shrub species were cultivated in 120 L barrels and sequentially harvested over up to three growing seasons. To account for the ontogenetic drift, organ biomass and nitrogen fractions were adjusted for plant biomass and N pool, respectively. KEY RESULTS: Lianas invested, on average, relatively less biomass in the root fraction in comparison with shrubs. This was offset by only insignificant increases in leaf or stem investment. Even though liana stems and roots showed higher N concentration in comparison with shrubs, plant N distribution was mostly driven by, and largely matched, the pattern of biomass distribution. Lianas also showed a greater relative growth rate than shrubs. The differences between the growth forms became apparent only when ontogenetic drift was controlled for. These results were confirmed regardless of whether reproductive biomass was included in the analysis. CONCLUSIONS: Our results suggest that temperate lianas, in spite of their diverse, species-specific resource distribution patterns, preferentially allocate resources to above-ground organs at the expense of roots. By identifying this trade-off and demonstrating the lack of a general trend for reduction in stem investment in lianas, we significantly modify the prevailing view of liana allocation strategies and evolutionary advantages. Such a resource distribution pattern, along with the cheap unit leaf area and stem unit length construction, situates lianas as a group close to the fast acquisition/rapid growth end of the life strategy spectrum.

Drought-induced shoot dieback starts with massive root xylem embolism and variable depletion of nonstructural carbohydrates in seedlings of two tree species.

Combining hydraulic- and carbon-related measurements helps to understand drought-induced plant mortality. Here, we investigated the role that plant respiration (R) plays in determining carbon budgets under drought. We measured the hydraulic conductivity of stems and roots, and gas exchange and nonstructural carbohydrate (NSC) concentrations of leaves, stems and roots of seedlings of two resprouting species exposed to drought or well-watered conditions: Ulmus minor (riparian tree) and Quercus ilex (dryland tree). With increasing water stress (occurring more rapidly in larger U. minor), declines in leaf, stem and root R were less pronounced than that in leaf net photosynthetic CO2 uptake (Pn ). Daytime whole-plant carbon gain was negative below -4 and -6 MPa midday xylem water potential in U. minor and Q. ilex, respectively. Relative to controls, seedlings exhibiting shoot dieback suffered c. 80% loss of hydraulic conductivity in both species, and reductions in NSC concentrations in U. minor. Higher drought-induced depletion of NSC reserves in U. minor was related to higher plant R, faster stomatal closure, and premature leaf-shedding. Differences in drought resistance relied on the ability to maintain hydraulic conductivity during drought, rather than tolerating conductivity loss. Root hydraulic failure elicited shoot dieback and precluded resprouting without root NSC reserves being apparently limiting for R.

Patterns of structural and defense investments in fine roots of Scots pine (Pinus sylvestris L.) across a strong temperature and latitudinal gradient in Europe.

Plant functional traits may be altered as plants adapt to various environmental constraints. Cold, low fertility growing conditions are often associated with root adjustments to increase acquisition of limiting nutrient resources, but they may also result in construction of roots with reduced uptake potential but higher tissue persistence. It is ultimately unclear whether plants produce fine roots of different structure in response to decreasing temperatures and whether these changes represent a trade-off between root function or potential root persistence. We assessed patterns of root construction based on various root morphological, biochemical and defense traits including root diameter, specific root length (SRL), root tissue density (RTD), C:N ratio, phenolic compounds, and number of phellem layers across up to 10 root orders in diverse populations of Scots pine along a 2000-km climatic gradient in Europe. Our results showed that different root traits are related to mean annual temperature (MAT) and expressed a pattern of higher root diameter and lower SRL and RTD in northern sites with lower MAT. Among absorptive roots, we observed a gradual decline in chemical defenses (phenolic compounds) with decreasing MAT. In contrast, decreasing MAT resulted in an increase of structural protection (number of phellem layers) in transport fine roots. This indicated that absorptive roots with high capacity for nutrient uptake, and transport roots with low uptake capacity, were characterized by distinct and contrasting trade-offs. Our observations suggest that diminishing structural and chemical investments into the more distal, absorptive roots in colder climates is consistent with building roots of higher absorptive capacity. At the same time, roots that play a more prominent role in transport of nutrients and water within the root system saw an increase in structural investment, which can increase persistence and reduce long-term costs associated with their frequent replacement.

Biogeographic variation in evergreen conifer needle longevity and impacts on boreal forest carbon cycle projections.

Leaf life span is an important plant trait associated with interspecific variation in leaf, organismal, and ecosystem processes. We hypothesized that intraspecific variation in gymnosperm needle traits with latitude reflects both selection and acclimation for traits adaptive to the associated temperature and moisture gradient. This hypothesis was supported, because across 127 sites along a 2,160-km gradient in North America individuals of Picea glauca, Picea mariana, Pinus banksiana, and Abies balsamea had longer needle life span and lower tissue nitrogen concentration with decreasing mean annual temperature. Similar patterns were noted for Pinus sylvestris across a north-south gradient in Europe. These differences highlight needle longevity as an adaptive feature important to ecological success of boreal conifers across broad climatic ranges. Additionally, differences in leaf life span directly affect annual foliage turnover rate, which along with needle physiology partially regulates carbon cycling through effects on gross primary production and net canopy carbon export. However, most, if not all, global land surface models parameterize needle longevity of boreal evergreen forests as if it were a constant. We incorporated temperature-dependent needle longevity and %nitrogen, and biomass allocation, into a land surface model, Community Atmosphere Biosphere Land Exchange, to assess their impacts on carbon cycling processes. Incorporating realistic parameterization of these variables improved predictions of canopy leaf area index and gross primary production compared with observations from flux sites. Finally, increasingly low foliage turnover and biomass fraction toward the cold far north indicate that a surprisingly small fraction of new biomass is allocated to foliage under such conditions.

Temperature drives global patterns in forest biomass distribution in leaves, stems, and roots.

Whether the fraction of total forest biomass distributed in roots, stems, or leaves varies systematically across geographic gradients remains unknown despite its importance for understanding forest ecology and modeling global carbon cycles. It has been hypothesized that plants should maintain proportionally more biomass in the organ that acquires the most limiting resource. Accordingly, we hypothesize greater biomass distribution in roots and less in stems and foliage in increasingly arid climates and in colder environments at high latitudes. Such a strategy would increase uptake of soil water in dry conditions and of soil nutrients in cold soils, where they are at low supply and are less mobile. We use a large global biomass dataset (>6,200 forests from 61 countries, across a 40 °C gradient in mean annual temperature) to address these questions. Climate metrics involving temperature were better predictors of biomass partitioning than those involving moisture availability, because, surprisingly, fractional distribution of biomass to roots or foliage was unrelated to aridity. In contrast, in increasingly cold climates, the proportion of total forest biomass in roots was greater and in foliage was smaller for both angiosperm and gymnosperm forests. These findings support hypotheses about adaptive strategies of forest trees to temperature and provide biogeographically explicit relationships to improve ecosystem and earth system models. They also will allow, for the first time to our knowledge, representations of root carbon pools that consider biogeographic differences, which are useful for quantifying whole-ecosystem carbon stocks and cycles and for assessing the impact of climate change on forest carbon dynamics.

Accumulation of particulate matter, heavy metals, and polycyclic aromatic hydrocarbons on the leaves of Tilia cordata Mill. in five Polish cities with different levels of air pollution.

Urbanized areas are struggling with the problem of air pollution and as the number of people living in cities is increasing, the situation is likely to deteriorate. One of the most harmful pollutants is particulate matter (PM). Increased levels of PM in the atmosphere are likely to have a negative impact on human health. Phytoremediation technology could be a solution. It involves plants acting as bio-filters by accumulating particles on, and in the leaves, thus removing the particles from the atmosphere. This study investigates the accumulation of PM including heavy metals (HMs) and polycyclic aromatic hydrocarbons (PAHs), on the foliage of small-leaved lime (Tilia cordata Mill.) in five Polish cities. There were significantly different PM amounts found in the trees between the cities which related to the different quantities of PM in the atmosphere at these cities. Significant differences were found between cities for the amounts of the different particulate size fractions, and the HMs and PAHs in leaves. Strong winds reduced the amount of PM on leaves, especially the smallest fractions, but no relationship with precipitation was found. The results suggest that T. cordata improves the air quality in cities and can be used as an effective bioindicator for PM air pollution.

Scots pine fine roots adjust along a 2000-km latitudinal climatic gradient.

Patterns of plant biomass allocation and functional adjustments along climatic gradients are poorly understood, particularly belowground. Generally, low temperatures suppress nutrient release and uptake, and forests under such conditions have a greater proportion of their biomass in roots. However, it is not clear whether 'more roots' means better capacity to acquire soil resources. Herein we quantified patterns of fine-root anatomy and their biomass distribution across Scots pine (Pinus sylvestris) populations both along a 2000-km latitudinal gradient and within a common garden experiment with a similar range of populations. We found that with decreasing mean temperature, a greater percentage of Scots pine root biomass was allocated to roots with higher potential absorptive capacity. Similar results were seen in the common experimental site, where cold-adapted populations produced roots with greater absorptive capacity than populations originating from warmer climates. These results demonstrate that plants growing in or originated from colder climates have more acquisitive roots, a trait that is likely adaptive in the face of the low resource availability typical of cold soils.