Newtonian boreal forest ecology: The Scots pine ecosystem as an example.

Isaac Newton's approach to developing theories in his book Principia Mathematica proceeds in four steps. First, he defines various concepts, second, he formulates axioms utilising the concepts, third, he mathematically analyses the behaviour of the system defined by the concepts and axioms obtaining predictions and fourth, he tests the predictions with measurements. In this study, we formulated our theory of boreal forest ecosystems, called NewtonForest, following the four steps introduced by Newton. The forest ecosystem is a complicated entity and hence we needed altogether 27 concepts to describe the material and energy flows in the metabolism of trees, ground vegetation and microbes in the soil, and to describe the regularities in tree structure. Thirtyfour axioms described the most important features in the behaviour of the forest ecosystem. We utilised numerical simulations in the analysis of the behaviour of the system resulting in clear predictions that could be tested with field data. We collected retrospective time series of diameters and heights for test material from 6 stands in southern Finland and five stands in Estonia. The numerical simulations succeeded to predict the measured diameters and heights, providing clear corroboration with our theory.

Reliability of temperature signal in various climate indicators from northern Europe.

We collected relevant observational and measured annual-resolution time series dealing with climate in northern Europe, focusing in Finland. We analysed these series for the reliability of their temperature signal at annual and seasonal resolutions. Importantly, we analysed all of the indicators within the same statistical framework, which allows for their meaningful comparison. In this framework, we employed a cross-validation procedure designed to reduce the adverse effects of estimation bias that may inflate the reliability of various temperature indicators, especially when several indicators are used in a multiple regression model. In our data sets, timing of phenological observations and ice break-up were connected with spring, tree ring characteristics (width, density, carbon isotopic composition) with summer and ice formation with autumn temperatures. Baltic Sea ice extent and the duration of ice cover in different watercourses were good indicators of winter temperatures. Using combinations of various temperature indicator series resulted in reliable temperature signals for each of the four seasons, as well as a reliable annual temperature signal. The results hence demonstrated that we can obtain reliable temperature information over different seasons, using a careful selection of indicators, combining the results with regression analysis, and by determining the reliability of the obtained indicator.

Effect of Leaf Water Potential on Internal Humidity and CO2 Dissolution: Reverse Transpiration and Improved Water Use Efficiency under Negative Pressure.

The pull of water from the soil to the leaves causes water in the transpiration stream to be under negative pressure decreasing the water potential below zero. The osmotic concentration also contributes to the decrease in leaf water potential but with much lesser extent. Thus, the surface tension force is approximately balanced by a force induced by negative water potential resulting in concavely curved water-air interfaces in leaves. The lowered water potential causes a reduction in the equilibrium water vapor pressure in internal (sub-stomatal/intercellular) cavities in relation to that over water with the potential of zero, i.e., over the flat surface. The curved surface causes a reduction also in the equilibrium vapor pressure of dissolved CO2, thus enhancing its physical solubility to water. Although the water vapor reduction is acknowledged by plant physiologists its consequences for water vapor exchange at low water potential values have received very little attention. Consequences of the enhanced CO2 solubility to a leaf water-carbon budget have not been considered at all before this study. We use theoretical calculations and modeling to show how the reduction in the vapor pressures affects transpiration and carbon assimilation rates. Our results indicate that the reduction in vapor pressures of water and CO2 could enhance plant water use efficiency up to about 10% at a leaf water potential of -2 MPa, and much more when water potential decreases further. The low water potential allows for a direct stomatal water vapor uptake from the ambient air even at sub-100% relative humidity values. This alone could explain the observed rates of foliar water uptake by e.g., the coastal redwood in the fog belt region of coastal California provided the stomata are sufficiently open. The omission of the reduction in the water vapor pressure causes a bias in the estimates of the stomatal conductance and leaf internal CO2 concentration based on leaf gas exchange measurements. Manufactures of leaf gas exchange measurement systems should incorporate leaf water potentials in measurement set-ups.

(137)Cs distributions in soil and trees in forest ecosystems after the radioactive fallout - Comparison study between southern Finland and Fukushima, Japan.

The nuclear accidents at Chernobyl and Fukushima released large amounts of (137)Cs radionuclides into the atmosphere which spread over large forest areas. We compared the (137)Cs concentration distribution in different parts of two coniferous forest ecosystems (needle litter, stems and at different depths in the soil) over short and long term periods in Finland and Japan. We also estimated the change in (137)Cs activity concentrations in needle and soil between 1995 and 2013 in Southern Finland based on the back-calculated (137)Cs activity concentrations. We hypothesized that if the (137)Cs activity concentrations measured in 1995 and 2013 showed a similar decline in concentration, the (137)Cs activity concentration in the ecosystem was already stable in 1995. But if not, the (137)Cs activity concentrations were still changing in 2013. Our results showed that the vertical distribution of the (137)Cs fallout in the soil was similar in Hyytiälä and Fukushima. The highest (137)Cs concentrations were observed in the uppermost surface layers of the soil, and they decreased exponentially deeper in the soil. We also observed that (137)Cs activity concentrations estimated from the samples in 1995 and 2013 in Finland showed different behavior in the surface soil layers compared to the deep soil layer. These results suggested that the (137)Cs nuclei were still mobile in the surface soil layers 27 years after the accident. Our results further indicated that, in the aboveground parts of the trees, the (137)Cs concentrations were much closer to steady-state when compared to those of the surface soil layers based on the estimated declining rates of (137)Cs concentration activity in needles which were similar in 1995 and 2013. Despite its mobility and active role in the metabolism of trees, the (137)Cs remains in the structure of the trees for decades, and there is not much exchange of (137)Cs between the heartwood and surface layers of the stem.

Evidences on the Ability of Mycorrhizal Genus Piloderma to Use Organic Nitrogen and Deliver It to Scots Pine.

Ectomycorrhizal (ECM) symbiosis has been proposed to link plant photosynthesis and soil organic matter (SOM) decomposition through the production of fungal enzymes which promote SOM degradation and nitrogen (N) uptake. However, laboratory and field evidence for the existence of these processes are rare. Piloderma sp., a common ECM genus in boreal forest soil, was chosen as model mycorrhiza for this study. The abundance of Piloderma sp. was studied in root tips and soil over one growing season and in winter. Protease production was measured from ectomycorrhiza and soil solution in the field and pure fungal cultures. We also tested the effect of Piloderma olivaceum on host plant organic N nutrition in the laboratory. The results showed that Piloderma sp. was highly abundant in the field and produced extracellular proteases, which correlated positively with the gross primary production, temperature and soil respiration. In the laboratory, Piloderma olivaceum could improve the ability of Pinus sylvestris L. to utilize N from extragenous proteins. We suggest that ECM fungi, although potentially retaining N in their hyphae, are important in forest C and N cycling due to their ability to access proteinaeous N. As Piloderma sp. abundance appeared to be seasonally highly variable, recycling of fungal-bound N after hyphal death may therefore be of primary importance for the N cycling in boreal ecosystems.

Assimilate transport in phloem sets conditions for leaf gas exchange.

Carbon uptake and transpiration in plant leaves occurs through stomata that open and close. Stomatal action is usually considered a response to environmental driving factors. Here we show that leaf gas exchange is more strongly related to whole tree level transport of assimilates than previously thought, and that transport of assimilates is a restriction of stomatal opening comparable with hydraulic limitation. Assimilate transport in the phloem requires that osmotic pressure at phloem loading sites in leaves exceeds the drop in hydrostatic pressure that is due to transpiration. Assimilate transport thus competes with transpiration for water. Excess sugar loading, however, may block the assimilate transport because of viscosity build-up in phloem sap. Therefore, for given conditions, there is a stomatal opening that maximizes phloem transport if we assume that sugar loading is proportional to photosynthetic rate. Here we show that such opening produces the observed behaviour of leaf gas exchange. Our approach connects stomatal regulation directly with sink activity, plant structure and soil water availability as they all influence assimilate transport. It produces similar behaviour as the optimal stomatal control approach, but does not require determination of marginal cost of water parameter.

Seasonal acclimation of photosystem II in Pinus sylvestris. I. Estimating the rate constants of sustained thermal energy dissipation and photochemistry.

Acclimation of the partitioning of absorbed light energy in Photosystem II (PSII) between photochemical and non-photochemical processes includes short-term adjustments that are rapidly reversed in the dark and seasonal acclimation processes that are unaffected by dark acclimation. Thus, by using dark-acclimated leaves to study the seasonal acclimation of PSII, the confounding effect of short-term adjustments is eliminated. The maximum quantum yield of photochemistry, estimated by chlorophyll fluorescence analysis as F(v)/F(m), where F(v) = (F(m) - F(o)), and F(m) and F(o) are maximum and minimum chlorophyll fluorescence, respectively, has been widely used to follow the seasonal acclimation of PSII, because it is measured in dark-acclimated leaves. Seasonal changes in F(v)/F(m) can be caused by adjustments in either the photochemical capacity in PSII, or the capacity of thermal dissipation in PSII, or both. However, there is a lack of chlorophyll fluorescence parameters that can distinguish between these processes. In this study, we introduce two new parameters: the rate constants of sustained thermal energy dissipation (k(NPQ)) and of photochemistry (k(P)). We estimated k(NPQ) and k(P) from dark-acclimated F(o) and F(m) measured during spring recovery of photosynthesis in Scots pine (Pinus sylvestris L.) trees. We suggest that k(NPQ) and k(P) be used to study the mechanisms underlying the observed seasonal acclimation in PSII, because these parameters provide quantitative data that complement and extend F(v)/F(m) measurements.

Seasonal acclimation of photosystem II in Pinus sylvestris. II. Using the rate constants of sustained thermal energy dissipation and photochemistry to study the effect of the light environment.

Photosynthesis in evergreen conifers is characterized by down-regulation in autumn and rapid up-regulation in spring. This seasonal pattern is largely driven by temperature, but the light environment also plays a role. In overwintering Scots pine (Pinus sylvestris L.) trees, PSII is less down-regulated and recovers faster from winter stress in shaded needles than in needles exposed to full sunlight. Because the effect of light on the seasonal acclimation of PSII has not been quantitatively studied under field conditions, we used the rate constants for sustained thermal energy dissipation and photochemistry to investigate the dynamics and kinetics of the seasonal acclimation of PSII in needles exposed to different light environments. We monitored chlorophyll fluorescence and needle pigment concentration during the winter and spring in Scots pine seedlings growing in the field in different shading treatments, and within the crowns of mature trees. The results indicated that differences in acclimation of PSII in overwintering Scots pine among needles exposed to different light environments can be chiefly attributed to sustained thermal dissipation. We also present field evidence that zeaxanthin-facilitated thermal dissipation and aggregation of thylakoid membrane proteins are key mechanisms in the regulation of sustained thermal dissipation in Scots pine trees in the field.

A comparison of phenological models of leaf bud burst and flowering of boreal trees using independent observations.

We compared and tested Thermal Time, Sequential, Parallel and Flexible phenological models of leaf bud burst in birch (Betula pendula Roth. and B. pubescens Ehrh.) and flowering in bird cherry (Prunus padus L.) and rowan (Sorbus aucuparia L.). We used phenological records from Oulainen-Ohineva (64 degrees 13' N, 24 degrees 53' E) in central Finland from 1953 to 2002 to estimate model parameters. We tested the models with data collected in all but six years between 1896 and 2002 in southern and central Finland; we divided this dataset into two 50-year datasets. The use of three datasets enabled us to test the models with data that were independent of the parameter fitting data, facilitating robust evaluation of model performance. Several models that fitted the parameterization data well showed poorer performance when tested with the independent data. This may be because the models were over-parameterized and able to adapt to noise in the data in addition to the phenological phenomenon itself. Simple Thermal Time models performed best with independent data, and Sequential and Parallel models were similar in prediction accuracy. Although Thermal Time models simulated boreal phenological events under current climatic conditions, some precautions are needed with simulations of climatic warming. For example, changed conditions may increase the relative importance of chilling in the timing of bud burst under elevated temperature conditions, which could alter the performance of phenological models.

The human footprint in the carbon cycle of temperate and boreal forests.

Temperate and boreal forests in the Northern Hemisphere cover an area of about 2 x 10(7) square kilometres and act as a substantial carbon sink (0.6-0.7 petagrams of carbon per year). Although forest expansion following agricultural abandonment is certainly responsible for an important fraction of this carbon sink activity, the additional effects on the carbon balance of established forests of increased atmospheric carbon dioxide, increasing temperatures, changes in management practices and nitrogen deposition are difficult to disentangle, despite an extensive network of measurement stations. The relevance of this measurement effort has also been questioned, because spot measurements fail to take into account the role of disturbances, either natural (fire, pests, windstorms) or anthropogenic (forest harvesting). Here we show that the temporal dynamics following stand-replacing disturbances do indeed account for a very large fraction of the overall variability in forest carbon sequestration. After the confounding effects of disturbance have been factored out, however, forest net carbon sequestration is found to be overwhelmingly driven by nitrogen deposition, largely the result of anthropogenic activities. The effect is always positive over the range of nitrogen deposition covered by currently available data sets, casting doubts on the risk of widespread ecosystem nitrogen saturation under natural conditions. The results demonstrate that mankind is ultimately controlling the carbon balance of temperate and boreal forests, either directly (through forest management) or indirectly (through nitrogen deposition).

Wintertime photosynthesis and water uptake in a boreal forest.

Warm air in combination with frozen soil is a major cause of wintertime drought damage in evergreen plants in subalpine and boreal environments. We analyzed diurnal tree stem diameter variation (SDV), which reflects soil water uptake, canopy-level water vapor flux (Fw), stand photosynthesis (Ps), photosynthetically active radiation (PAR), soil and air temperatures (Ts and T air, respectively) and soil liquid water content (theta) to determine under what conditions photosynthesis is possible in wintertime and how crucial water uptake from soil is for photosynthesis. Measurements were made under field conditions in a Scots pine forest in southern Finland during winter 2002-2003. We found four wintertime periods when there was measurable Ps and SDV, the latter always starting 2-7 days after photosynthesis and both usually ending on the same day. Stand photosynthesis began when T air reached 3-4 degrees C and ended when T air dropped below -7 degrees C. The trees appeared to rely on stored stem water first and started taking up water from the soil a few days later, when the transpirational demand became strong enough. The more difficult it was to access soil water because of low Ts or low theta, the longer the trees used water stored in their stems. Even partial stem freezing did not prevent photosynthesis or soil water uptake.

Dynamics of the energy flow through photosystem II under changing light conditions: a model approach.

Several biochemical models of photosynthesis exist that consider the effects of the dynamic adjustment of enzymatic and stomatal processes on carbon assimilation under fluctuating light. However, the rate of electron transport through the light reactions is commonly modelled by means of an empirical equation, parameterised with data obtained at the steady state. A steady-state approach cannot capture the dynamic nature of the adjustment of the light reactions under fluctuating light. Here we present a dynamic model approach for photosystem II that considers the adjustments in the regulative non-photochemical processes. The model is initially derived to account for changes occurring at the seconds-to-minutes time-scale under field conditions, and is parameterised and tested with chlorophyll fluorescence data. Results derived from this model show good agreement with experimentally obtained photochemical and non-photochemical quantum yields, providing evidence for the effect that the dark reactions exert in the adjustment of the energy flows at the light reactions. Finally, we compare the traditional steady-state approach with our dynamic approach and find that the steady-state approach produces an underestimation of the modelled electron transport rate (ETR) under rapidly fluctuating light (1 s or less), whereas it produces overestimations under slower fluctuations of light (5 s or more).

Temperature dependence of leaf-level CO2 fixation: revising biochemical coefficients through analysis of leaf three-dimensional structure.

CO2 fixation in a leaf is determined by biochemical and physical processes within the boundaries set by leaf structure. Traditionally determined temperature dependencies of biochemical processes include physical processes related to CO2 exchange that result in inaccurate estimates of parameter values. A realistic three-dimensional model of a birch (Betula pendula) leaf was used to distinguish between the physical and biochemical processes affecting the temperature dependence of CO2 exchange, to determine new chloroplastic temperature dependencies for V c(max) and Jmax based on experiments, and to analyse mesophyll diffusion in detail. The constraint created by dissolution of CO2 at cell surfaces substantially decreased the CO2 flux and its concentration inside chloroplasts, especially at high temperatures. Consequently, newly determined chloroplastic V c(max) and Jmax were more temperature dependent than originally. The role of carbonic anhydrase in mesophyll diffusion appeared to be minor under representative mid-day nonwater-limited conditions. Leaf structure and physical processes significantly affect the apparent temperature dependence of CO2 exchange, especially at optimal high temperatures when the photosynthetic sink is strong. The influence of three-dimensional leaf structure on the light environment inside a leaf is marked and affects the local choice between Jmax and V c(max)-limited assimilation rates.

Acclimation of photosynthetic capacity in Scots pine to the annual cycle of temperature.

Coniferous trees growing in the boreal and temperate zones have a clear annual cycle of photosynthetic activity. A recent study demonstrated that the seasonal variation in photosynthetic capacity of Scots pine (Pinus sylvestris L.) could be attributed mainly to the light response curve of photosynthesis. The magnitude of the light response curve varied over the season while its shape remained constant, indicating that the two physiological parameters quantifying the curve-the quantum yield per unit internal carbon dioxide concentration and the corresponding light-saturated rate-remained proportional to each other. We now show, through modeling studies, that the quantum yield (and hence the light-saturated rate) is related to the annual cycle of temperature through a delayed dynamic response. The proposed model was tested by comparing model results with intensive measurements of photosynthesis and driving variables made from April to October in three shoots of Scots pine growing near the northern timberline. Photosynthetic capacity showed considerable acclimation during the growing season. A single model describing photosynthetic capacity as a reversible, first-order delay process driven by temperature explained most of the variation in photosynthetic capacity during the year. The proposed model is simpler but no less accurate than previous models of the annual cycle of photosynthetic capacity.

Use of modeled photosynthesis and decomposition to describe tree growth at the northern tree line.

Growth of subarctic Scots pine (Pinus sylvestris L.) trees was investigated by a combination of process-based models and dendroecological approaches. Tree ring width indices were strongly autocorrelated and correlated with simulated photosynthetic production of the previous year and with organic matter N mineralization of the current year. An autoregressive model, with photosynthesis and N mineralization as external inputs, explained growth of the trees well. However, relationships for the period 1950-1992 differed significantly from relationships for the period 1876-1949; the slope of the regression of tree ring width index and photosynthesis was lower for the 1950-1992 period. Also, the autocorrelation structure of the data changed. First-order autocorrelation decreased and second-order autocorrelation increased from the earlier to the later period. This means that growth is becoming less sensitive to variations in photosynthetic production, whereas the relationships between growth and N mineralization are remaining fairly constant. We postulate that, although photosynthesis has increased in response to increasing CO2 concentrations, tree growth rate cannot parallel the increase in photosynthesis because potential growth rate is limited directly by temperature.

Annual pattern of photosynthesis in Scots pine in the boreal zone.

To detect seasonal changes in photosynthetic rate in the field, a set of 18,000 photosynthetic measurements made between April and October on three shoots of Scots pine growing near the northern timberline was studied. The measurements were analyzed in the framework of an optimal stomatal control model of photosynthesis, in which irradiance (photosynthetically active radiation, I), air humidity and ambient temperature are driving variables. All driving variables were monitored concomitantly with gas exchange measurements throughout the growing season. The model has nine parameters, of which six were assumed to be constant over the growing season and were fixed based on previous information. The three variable parameters were the initial slope (alpha) and saturation value (gamma) of the light-response curve of carboxylation efficiency in the intercellular cavity, and the cost of transpiration (lambda), in carbon units, regulating the degree of stomatal opening. These parameters could not be estimated independently, nor could their values be satisfactorily found by standard nonlinear regression techniques. A Monte Carlo based simulation procedure was devised to analyze the best-fit parameters and their mutual correlations near the minimum of the residual sum of squares. This was accomplished by replacing the saturation value of the light-response curve with a linearity parameter that determined the shape of the curve. In the best fit solutions, only alpha and lambda varied from day to day, whereas the shape of the curve was constant (i.e., gamma was proportional to alpha). Both alpha and lambda showed consistent patterns from spring to autumn, but the seasonal variation was considerably greater for alpha than for lambda. The optimal stomatal control model with the seven fixed and two daily parameter values gave a good overall fit for photosynthetic rate over the season (PEV > 95%).

Predicting spring phenology and frost damage risk of Betula spp. under climatic warming: a comparison of two models.

Timing of bud burst and frost damage risk for leaves of Betula spp. in response to climatic warming in Finland was examined with two models. In the first model, ontogenetic development in spring was triggered by an accumulation of chilling temperatures. The second model assumed an additional signal from the light climate. The two models gave radically different estimates of frost damage risk in response to climate warming. The chilling-triggered model forecast a significant and increasing risk with increased warming, whereas the light-climate-triggered model predicted little or no risk. The chilling-triggered model is widely applied in phenological research; however, there is increasing experimental evidence that light conditions play a role in the timing of spring phenology. Although it is not clear if the light response mechanisms are appropriately represented in our model, the results imply that reliance on a light signal for spring development would afford a degree of protection against possible frost damage under climate warming that would not be present if chilling were the sole determinant. Further experimental tests are required to ascertain the light-related mechanisms controlling phenological timing, so that credible model extrapolations can be undertaken.

Analysis of gas exchange of Merkus pine populations by the optimality approach.

We hypothesized that northern and northeastern Thai populations of Merkus pine (Pinus merkusii Jungh. et de Vriese), which differ in the duration of their grass stage and which originate from slightly different climates in terms of water availability, differ in their gas exchange characteristics. We compared CO(2) exchange response to irradiance, diurnal regulation of leaf conductance within a 10-day period and structural properties among the populations. We used a model, which is based on the concept of optimal stomatal regulation, to analyze CO(2) exchange and transpiration rates. The two geographical groups did not differ in CO(2) exchange response to irradiance, diurnal transpiration, or water use. Mean stomatal length was significantly greater in the northeastern population than in the northern populations, but stomatal frequency did not differ among populations. First-year shoot growth and dry matter production, allocation of nitrogen to needles and root:shoot ratios were similar in the two geographical groups. Genotypic variation in the duration of the grass stage was not reflected in variation in gas exchange, indicating that the grass stage is an adaptation to more site-specific conditions. The modeled response of CO(2) exchange rates to irradiance fitted well the rates measured under laboratory conditions. The transpiration model, which utilized maximum leaf conductance and other parameters derived from the CO(2) exchange measurements, also fitted well the transpiration rates measured in a greenhouse under changing environmental conditions.