Early-stage detection of root freezing injuries of Scots pine (Pinus sylvestris L.) seedlings by impedance loss factor and hydraulic conductance.

The condition of the root system affects the quality of seedlings in forestry and horticulture. Previously, the electrical impedance loss factor (δ) and the reverse-flow hydraulic conductance (Kr ) of the roots of Scots pine seedlings were found to increase when assessed a few days after frost damage. How these variables change with time after the root damage is unknown. We arranged an experiment with 1.5-year-old Scots pine seedlings exposed to -5°C or - 30°C, with the control seedlings kept at 3°C. Then, δ and Kr of roots were monitored for 5 weeks in favorable growing conditions. The properties of the roots were observed to be in a dynamic state after the damage. A significant difference in δ was found between the test temperatures -30°C versus -5°C and 3°C (p = 0.004 and p < 0.001, respectively). The clearest effect of freezing injuries on δ of roots was observed in the first measurement 1 week after the freezing test. The temperature significantly affected Kr, too, with a significant difference between the low-temperature treated plants -30°C versus -5°C and control (p < 0.001, respectively). The difference in Kr between -30°C and the other two temperatures increased with time and was the largest in the last samples, taken after 5 weeks. We conclude that the impedance loss factor may detect root damage if the measurements occur early enough after the damage, but a longer time difference (3-5 weeks) is needed according to the reverse-flow hydraulic conductance.

Ecotrons: Powerful and versatile ecosystem analysers for ecology, agronomy and environmental science.

Ecosystems integrity and services are threatened by anthropogenic global changes. Mitigating and adapting to these changes require knowledge of ecosystem functioning in the expected novel environments, informed in large part through experimentation and modelling. This paper describes 13 advanced controlled environment facilities for experimental ecosystem studies, herein termed ecotrons, open to the international community. Ecotrons enable simulation of a wide range of natural environmental conditions in replicated and independent experimental units while measuring various ecosystem processes. This capacity to realistically control ecosystem environments is used to emulate a variety of climatic scenarios and soil conditions, in natural sunlight or through broad-spectrum lighting. The use of large ecosystem samples, intact or reconstructed, minimizes border effects and increases biological and physical complexity. Measurements of concentrations of greenhouse trace gases as well as their net exchange between the ecosystem and the atmosphere are performed in most ecotrons, often quasi continuously. The flow of matter is often tracked with the use of stable isotope tracers of carbon and other elements. Equipment is available for measurements of soil water status as well as root and canopy growth. The experiments ran so far emphasize the diversity of the hosted research. Half of them concern global changes, often with a manipulation of more than one driver. About a quarter deal with the impact of biodiversity loss on ecosystem functioning and one quarter with ecosystem or plant physiology. We discuss how the methodology for environmental simulation and process measurements, especially in soil, can be improved and stress the need to establish stronger links with modelling in future projects. These developments will enable further improvements in mechanistic understanding and predictive capacity of ecotron research which will play, in complementarity with field experimentation and monitoring, a crucial role in exploring the ecosystem consequences of environmental changes.

Biotic homogenization can decrease landscape-scale forest multifunctionality.

Many experiments have shown that local biodiversity loss impairs the ability of ecosystems to maintain multiple ecosystem functions at high levels (multifunctionality). In contrast, the role of biodiversity in driving ecosystem multifunctionality at landscape scales remains unresolved. We used a comprehensive pan-European dataset, including 16 ecosystem functions measured in 209 forest plots across six European countries, and performed simulations to investigate how local plot-scale richness of tree species (α-diversity) and their turnover between plots (ß-diversity) are related to landscape-scale multifunctionality. After accounting for variation in environmental conditions, we found that relationships between α-diversity and landscape-scale multifunctionality varied from positive to negative depending on the multifunctionality metric used. In contrast, when significant, relationships between ß-diversity and landscape-scale multifunctionality were always positive, because a high spatial turnover in species composition was closely related to a high spatial turnover in functions that were supported at high levels. Our findings have major implications for forest management and indicate that biotic homogenization can have previously unrecognized and negative consequences for large-scale ecosystem multifunctionality.

Continental mapping of forest ecosystem functions reveals a high but unrealised potential for forest multifunctionality.

Humans require multiple services from ecosystems, but it is largely unknown whether trade-offs between ecosystem functions prevent the realisation of high ecosystem multifunctionality across spatial scales. Here, we combined a comprehensive dataset (28 ecosystem functions measured on 209 forest plots) with a forest inventory dataset (105,316 plots) to extrapolate and map relationships between various ecosystem multifunctionality measures across Europe. These multifunctionality measures reflected different management objectives, related to timber production, climate regulation and biodiversity conservation/recreation. We found that trade-offs among them were rare across Europe, at both local and continental scales. This suggests a high potential for 'win-win' forest management strategies, where overall multifunctionality is maximised. However, across sites, multifunctionality was on average 45.8-49.8% below maximum levels and not necessarily highest in protected areas. Therefore, using one of the most comprehensive assessments so far, our study suggests a high but largely unrealised potential for management to promote multifunctional forests.

Biodiversity and ecosystem functioning relations in European forests depend on environmental context.

The importance of biodiversity in supporting ecosystem functioning is generally well accepted. However, most evidence comes from small-scale studies, and scaling-up patterns of biodiversity-ecosystem functioning (B-EF) remains challenging, in part because the importance of environmental factors in shaping B-EF relations is poorly understood. Using a forest research platform in which 26 ecosystem functions were measured along gradients of tree species richness in six regions across Europe, we investigated the extent and the potential drivers of context dependency of B-EF relations. Despite considerable variation in species richness effects across the continent, we found a tendency for stronger B-EF relations in drier climates as well as in areas with longer growing seasons and more functionally diverse tree species. The importance of water availability in driving context dependency suggests that as water limitation increases under climate change, biodiversity may become even more important to support high levels of functioning in European forests.

Does species richness affect fine root biomass and production in young forest plantations?

Tree species diversity has been reported to increase forest ecosystem above-ground biomass and productivity, but little is known about below-ground biomass and production in diverse mixed forests compared to single-species forests. For testing whether species richness increases below-ground biomass and production and thus complementarity between forest tree species in young stands, we determined fine root biomass and production of trees and ground vegetation in two experimental plantations representing gradients in tree species richness. Additionally, we measured tree fine root length and determined species composition from fine root biomass samples with the near-infrared reflectance spectroscopy method. We did not observe higher biomass or production in mixed stands compared to monocultures. Neither did we observe any differences in tree root length or fine root turnover. One reason for this could be that these stands were still young, and canopy closure had not always taken place, i.e. a situation where above- or below-ground competition did not yet exist. Another reason could be that the rooting traits of the tree species did not differ sufficiently to support niche differentiation. Our results suggested that functional group identity (i.e. conifers vs. broadleaved species) can be more important for below-ground biomass and production than the species richness itself, as conifers seemed to be more competitive in colonising the soil volume, compared to broadleaved species.

Separating the effects of air and soil temperature on silver birch. Part I. Does soil temperature or resource competition determine the timing of root growth?

The aboveground parts of boreal forest trees mostly grow earlier, and the roots later, in the growing season. We aimed to experimentally test whether the extrinsic driver of soil temperature or the intrinsic driver (resource competition between plant parts) is a more important control for the root and shoot growth of silver birch (Betula pendula Roth) seedlings. Sixteen two-year-old seedlings were grown in controlled environment rooms for two simulated growing seasons (GS1, GS2). In GS1, all the seedlings were acclimatized under the same conditions, but in GS2, the soil temperature treatments were: (i) constant 10 °C (Cool); (ii) constant 18 °C (Warm); (iii) early growing season at 10 °C, switched to 18 °C later (Early Cool Late Warm, ECLW) and (iv) early growing season 18 °C, switched to 10 °C later (Early Warm Late Cool, EWLC). The treatments did not affect growth allocation between shoots and roots. Warm soil benefitted shoot elongation as it slowed down in EWLC and accelerated in ECLW after the soil temperature switch. However, whole-tree biomasses were similar to Cool and the seedlings grew largest in Warm. Phenology was not strongly affected by soil temperature, and root and shoot growth did not usually peak simultaneously. Short root mortality increased strongly in ECLW and decreased in EWLC after the soil temperature switch. Long root longevity was not significantly affected but long root growth ceased earliest in ECLW. Soil warming increased foliar nutrient contents. Growth dynamics were not solely driven by soil temperature, but resource competition also played a significant role. The study showed the importance of soil temperature for fine root dynamics not only through root growth but also via root mortality, as soil warming increased mortality even more than growth. Soil temperature has complex effects on tree and soil functioning, which further affects carbon dynamics in forest ecosystems that have a climate feedback.

Separating the effects of air and soil temperature on silver birch. Part II. The relation of physiology and leaf anatomy to growth dynamics.

The aboveground parts of boreal forest trees grow earlier in the growing season, the roots mostly later. The idea was to examine whether root growth followed soil temperature, or whether shoot growth also demanded most resources in the early growing season (soil temperature vs internal sink strengths for resources). The linkage between air and soil temperature was broken by switching the soil temperature. We aimed here to identify the direct effects of different soil temperature patterns on physiology, leaf anatomy and their interactions, and how they relate to the control of the growth dynamics of silver birch (Betula pendula Roth). Sixteen 2-year-old seedlings were grown in a controlled environment for two 14-week simulated growing seasons (GS1, GS2). An 8-week dormancy period interposed the GSs. In GS2, soil temperature treatments were applied: constant 10 °C (Cool), constant 18 °C (Warm), early growing season at 10 °C switched to 18 °C later (Early Cool Late Warm) and 18 °C followed by 10 °C (Early Warm Late Cool) were applied during GS2. The switch from cool to warm enhanced the water status, net photosynthesis, chlorophyll content index, effective yield of photosystem II (ΔF/Fm') and leaf expansion of the seedlings. Warm treatment increased the stomatal number per leaf. In contrast, soil cooling increased glandular trichomes. This investment in increasing the chemical defense potential may be associated with the decreased growth in cool soil. Non-structural carbohydrates were accumulated in leaves at a low soil temperature showing that growth was more hindered than net photosynthesis. Leaf anatomy differed between the first and second leaf flush of silver birch, which may promote tree fitness in the prevailing growing conditions. The interaction of birch structure and function changes with soil temperature, which can further reflect to ecosystem functioning.

Dynamics of above- and belowground responses of silver birch saplings and soil gases to soil freezing and waterlogging during dormancy.

Winter precipitation and soil freeze-thaw events have been predicted to increase in boreal regions with climate change. This may expose tree roots to waterlogging (WL) and soil freezing (Fr) more than in the current climate and therefore affect tree growth and survival. Using a whole-tree approach, we studied the responses of silver birch (Betula pendula Roth.) saplings, growing in mineral soil, to 6-week Fr and WL in factorial combinations during dormancy, with accompanying changes in soil gas concentrations. Physiological activation (dark-acclimated chlorophyll fluorescence and chlorophyll content index) and growth of leaves and shoot elongation and stem diameter growth started earlier in Fr than NoFr (soil not frozen). The starch content of leaves was temporarily higher in Fr than NoFr in the latter part of the growing season. Short and long root production and longevity decreased, and mortality increased by soil Fr, while there were no significant effects of WL. Increased fine root damage was followed by increased compensatory root growth. At the beginning of the growing season, stem sap flow increased fastest in Fr + WL, with some delay in both NoWL (without WL) treatments. At the end of the follow-up growing season, the hydraulic conductance and impedance loss factor of roots were higher in Fr than in NoFr, but there were no differences in above- and belowground biomasses. The concentration of soil carbon dioxide increased and methane decreased by soil Fr at the end of dormancy. At the beginning of the growing season, the concentration of nitrous oxide was higher in WL than in NoWL and higher in Fr than in NoFr. In general, soil Fr had more consistent effects on soil greenhouse gas concentrations than WL. To conclude, winter-time WL alone is not as harmful for roots as WL during the growing season.

Here comes the flood! Stress effects of continuous and interval waterlogging periods during the growing season on Scots pine saplings.

Future climate scenarios for the boreal zone project increasing temperatures and precipitation, as well as extreme weather events such as heavy rain during the growing season. This can result in more frequent short-term waterlogging (WL) leading to unfavorable conditions for tree roots. In addition, it is decisive whether short-term WL periods during the growing season occur continuously or periodically. We assessed the effects of short-termed WL on 4-year-old Scots pine (Pinus sylvestris L.) saplings after shoot elongation started. Waterlogging (WL) lasted either continuously for 2.5 weeks (ContWL) or noncontinuously for 5 weeks, consisting of three repeated 1-week-interval WL periods (IntWL). Both treatments resulted in the same duration of soil anoxia. We studied soil gases, root and shoot growth and physiology, and root survival probability and longevity during the experiment. In the final harvest, we determined shoot and root biomass and hydraulic conductance and electrical impedance spectra of the root systems. Soil CO2 and CH4 concentrations increased immediately after WL onset and O2 decreased until anoxia. Waterlogging decreased fine root survival probability, but there was no difference between WL treatments. Shoot growth suffered more from ContWL and root growth more from IntWL. Needle concentrations of pinitol increased in the WL saplings, indicating stress. No WL effects were observed in photosynthesis and chlorophyll fluorescence. Increased starch concentration in needles by WL may be due to damaged roots and thus a missing belowground sink. Electrical impedance indicated suffering of WL saplings, although root hydraulic conductance did not differ between the treatments. Oxidative stress of short-term and interval WL can have long-lasting effects on shoot and root growth and the physiology of Scots pine. We conclude that even short-term WL during the growing season is a stress factor, which will probably increase in the future and can affect carbon allocation and dynamics in boreal forests.

Let it snow! Winter conditions affect growth of birch seedlings during the following growing season.

Air temperatures and precipitation are predicted to increase in the future, especially at high latitudes and particularly so during winter. In contrast to air temperatures, changes in soil temperatures are more difficult to predict, as the fate of the insulating snow cover is crucial in this respect. Soil conditions can also be affected by rain-on-snow events and warm spells during winter, resulting in freeze-thaw cycles, compacted snow, ice encasement and local flooding. These adverse conditions during winter could counteract the otherwise positive effects of climate change on forest growth and productivity. For studying the effects of different winter and snow conditions on young Downy birch (Betula pubescens Ehrh.) seedlings, we carried out a laboratory experiment with birch seedlings subjected to four different winter scenarios: snow covering the seedlings (SNOW), compressed snow and ice encasement (ICE), flooded and frozen soil (FLOOD) and no snow at all (NO SNOW). After the winter treatments we simulated a spring and early summer period of 9.5 weeks, and monitored the growth by measuring shoot and root biomass of the seedlings, and starch and soluble sugar concentrations. We also assessed the stress experienced by the seedlings by measuring leaf chlorophyll fluorescence and gas exchange. Although no difference in mortality was observed between the treatments, the seedlings in the SNOW and ICE treatments had significantly higher shoot and root biomass compared with those in the FLOOD and NO SNOW treatments. We found higher starch concentrations in roots of the seedlings in the SNOW and ICE treatments, compared with those in the FLOOD and NO SNOW treatments, although photosynthesis did not differ. Our results suggest a malfunction of carbohydrate distribution in the seedlings of the FLOOD and NO SNOW treatments, probably resulting from decreased sinks. The results underline the importance of an insulating and protecting snow cover for small tree seedlings, and that future winters with changed snow pattern might affect the growth of tree seedlings and thus possibly species composition and forest productivity.

Waterlogging and soil freezing during dormancy affected root and shoot phenology and growth of Scots pine saplings.

Soil waterlogging is predicted to increase in the future climate in boreal regions due to increased precipitation. Snowmelt periods in winter may also become more common and further increase the amount of water in soil. It is not well known how waterlogging and soil freezing during winter affect the physiology, phenology and growth of trees. Our aim was to study the below- and aboveground responses of Scots pine (Pinus sylvestris L.) saplings to waterlogging (WL) in frozen (Fr) and unfrozen (NoFr) soils in a growth chamber experiment. The soil was either -2 °C or +2 °C and either waterlogged or not in a split-plot design for 6 weeks during dormancy, with similar air conditions in all treatments, which were Fr + WL, NoFr + WL, Fr + NoWL and NoFr + NoWL. Needles showed a shift towards a deeper dormancy in frozen than unfrozen soil in terms of chlorophyll fluorescence (Fv/Fm), water potential and apoplastic electrical resistance. In spring, initiation of shoot elongation started earlier if the soil was frozen during dormancy. In Fr + WL, initiation of root growth was delayed by 20 days compared with other treatments; after that, the root growth peaked at the same time as needle elongation. Needles remained smaller in Fr + WL than in the other treatments, indicating that roots formed a strong sink for carbon. Shoot and root biomass were not negatively affected by waterlogging if the soil remained unfrozen. In Fr + WL, survival and growth capacity of new terminal and whorl buds, the number of bud scales and the number of dwarf shoots were reduced. We conclude that soil freezing on sites prone to waterlogging should be considered in management of boreal forests, especially in the face of predicted climate change.

Winter survival of Scots pine seedlings under different snow conditions.

Future climate scenarios predict increased air temperatures and precipitation, particularly at high latitudes, and especially so during winter. Soil temperatures, however, are more difficult to predict, since they depend strongly on the fate of the insulating snow cover. 'Rain-on-snow' events and warm spells during winter can lead to thaw-freeze cycles, compacted snow and ice encasement, as well as local flooding. These adverse conditions could counteract the otherwise positive effects of climatic changes on forest seedling growth. In order to study the effects of different winter and snow conditions on young Scots pine (Pinus sylvestris L.) seedlings, we conducted a laboratory experiment in which 80 1-year-old Scots pine seedlings were distributed between four winter treatments in dasotrons: ambient snow cover (SNOW), compressed snow and ice encasement (ICE), flooded and frozen soil (FLOOD) and no snow (NO SNOW). During the winter treatment period and a 1.5-month simulated spring/early summer phase, we monitored the needle, stem and root biomass of the seedlings, and determined their starch and soluble sugar concentrations. In addition, we assessed the stress experienced by the seedlings by measuring chlorophyll fluorescence, electric impedance and photosynthesis of the previous-year needles. Compared with the SNOW treatment, carbohydrate concentrations were lower in the FLOOD and NO SNOW treatments where the seedlings had almost died before the end of the experiment, presumably due to frost desiccation of aboveground parts during the winter treatments. The seedlings of the ICE treatment showed dead needles and stems only above the snow and ice cover. The results emphasize the importance of an insulating and protecting snow cover for small forest tree seedlings, and that future winters with changed snow patterns might affect the survival of tree seedlings and thus forest productivity.

Jack-of-all-trades effects drive biodiversity-ecosystem multifunctionality relationships in European forests.

There is considerable evidence that biodiversity promotes multiple ecosystem functions (multifunctionality), thus ensuring the delivery of ecosystem services important for human well-being. However, the mechanisms underlying this relationship are poorly understood, especially in natural ecosystems. We develop a novel approach to partition biodiversity effects on multifunctionality into three mechanisms and apply this to European forest data. We show that throughout Europe, tree diversity is positively related with multifunctionality when moderate levels of functioning are required, but negatively when very high function levels are desired. For two well-known mechanisms, 'complementarity' and 'selection', we detect only minor effects on multifunctionality. Instead a third, so far overlooked mechanism, the 'jack-of-all-trades' effect, caused by the averaging of individual species effects on function, drives observed patterns. Simulations demonstrate that jack-of-all-trades effects occur whenever species effects on different functions are not perfectly correlated, meaning they may contribute to diversity-multifunctionality relationships in many of the world's ecosystems.

Effects of timing of soil frost thawing on Scots pine.

Effects of the timing of soil thawing in the spring on Scots pine (Pinus sylvestris L.) were studied under controlled laboratory conditions. Sixteen 6-year-old saplings were lifted from the field, replanted in containers and placed in four treatments in controlled environment (CE) chambers with four replicate saplings per chamber. The saplings were held in the CE chambers during one simulated winter and one simulated growing season. The soil was frozen to -2 degrees C during a second simulated winter in the CE chambers, and the soil thawing treatments began at the end of the second simulated winter. Soil thawing began at various times before (no delay in thawing) and after (delay in thawing) chamber air conditions were changed from simulated winter to simulated summer. Delayed soil thawing subjected saplings to stress, with the severity of stress depending on the length of the delay in thawing. If there was no delay or only a short delay in soil thawing, stress was minor and reversible. A 2-week delay in soil thawing led to death of the saplings. Stress was apparent as decreases in the variable to maximal chlorophyll fluorescence ratio (Fv/Fm), chlorophyll a/b ratio and needle water potential. In needles of stressed saplings, apoplastic electrical resistance first decreased and then increased and there were anomalies in the electrical impedance spectra of the stems. Stress from the soil thawing treatments affected both root and shoot growth.