Lasse Tarvainen

Why does leaf nitrogen decline within tree canopies less rapidly than light? An explanation from optimization subject to a lower bound on leaf mass per area

A long-established theoretical result states that, for a given total canopy nitrogen (N) content, canopy photosynthesis is maximized when the within-canopy gradient in leaf N per unit area (N(a)) is equal to the light gradient. However, it is widely observed that N(a) declines less rapidly than light in real plant canopies. Here we show that this general observation can be explained by optimal leaf acclimation to light subject to a lower-bound constraint on the leaf mass per area (m(a)). Using a simple model of the carbon-nitrogen (C-N) balance of trees with a steady-state canopy, we implement this constraint within the framework of the MAXX optimization hypothesis that maximizes net canopy C export. Virtually all canopy traits predicted by MAXX (leaf N gradient, leaf N concentration, leaf photosynthetic capacity, canopy N content, leaf-area index) are in close agreement with the values observed in a mature stand of Norway spruce trees (Picea abies L. Karst.). An alternative upper-bound constraint on leaf photosynthetic capacity (A(sat)) does not reproduce the canopy traits of this stand. MAXX subject to a lower bound on m(a) is also qualitatively consistent with co-variations in leaf N gradient, m(a) and A(sat) observed across a range of temperate and tropical tree species. Our study highlights the key role of constraints in optimization models of plant function.

Vertical gradients and seasonal variation in stem CO2 efflux within a Norway spruce stand

Stem CO2 efflux is known to vary seasonally and vertically along tree stems. However, annual tree- and stand-scale efflux estimates are commonly based on measurements made only a few times a year, during daytime and at breast height. In this study, the effect of these simplifying assumptions on annual efflux estimates and their influence on the estimates of the importance of stems in stand-scale carbon cycling are evaluated. In order to assess the strength of seasonal, diurnal and along-stem variability in CO2 efflux, half-hourly measurements were carried out at three heights on three mature Norway spruce (Picea abies (L.) Karst.) trees over a period of 3 years. Making the common assumption of breast height efflux rates being representative of the entire stem was found to result in underestimations of 10-17% in the annual tree-scale CO2 efflux. Upscaling using only daytime measurements from breast height increased the underestimation to 15-20%. Furthermore, the results show that the strength of the vertical gradient varies seasonally, being strongest in the early summer and non-existent during the cool months. The observed seasonality in the vertical CO2 efflux gradient could not be explained by variation in stem temperature, temperature response of the CO2 efflux (Q10), outer-bark permeability, CO2 transport in the xylem or CO2 release from the phloem. However, the estimated CO2 concentration immediately beneath the bark was considerably higher in the upper stem during the main period of diameter growth, coinciding with the strongest vertical efflux gradient. These results suggest that higher growth rates in the upper stem are the main cause for the observed vertical variation in the stem CO2 effluxes. Furthermore, the results indicate that accounting for the vertical efflux variation is essential for assessments of the importance of stems in stand-scale carbon cycling.

Increased Needle Nitrogen Contents Did Not Improve Shoot Photosynthetic Performance of Mature Nitrogen-Poor Scots Pine Trees.

Numerous studies have shown that temperate and boreal forests are limited by nitrogen (N) availability. However, few studies have provided a detailed account of how carbon (C) acquisition of such forests reacts to increasing N supply. We combined measurements of needle-scale biochemical photosynthetic capacities and continuous observations of shoot-scale photosynthetic performance from several canopy positions with simple mechanistic modeling to evaluate the photosynthetic responses of mature N-poor boreal Pinus sylvestris to N fertilization. The measurements were carried out in August 2013 on 90-year-old pine trees growing at Rosinedalsheden research site in northern Sweden. In spite of a nearly doubling of needle N content in response to the fertilization, no effect on the long-term shoot-scale C uptake was recorded. This lack of N-effect was due to strong light limitation of photosynthesis in all investigated canopy positions. The effect of greater N availability on needle photosynthetic capacities was also constrained by development of foliar phosphorus (P) deficiency following N addition. Thus, P deficiency and accumulation of N in arginine appeared to contribute toward lower shoot-scale nitrogen-use efficiency in the fertilized trees, thereby additionally constraining tree-scale responses to increasing N availability. On the whole our study suggests that the C uptake response of the studied N-poor boreal P. sylvestris stand to enhanced N availability is constrained by the efficiency with which the additional N is utilized. This efficiency, in turn, depends on the ability of the trees to use the greater N availability for additional light capture. For stands that have not reached canopy closure, increase in leaf area following N fertilization would be the most effective way for improving light capture and C uptake while for mature stands an increased leaf area may have a rather limited effect on light capture owing to increased self-shading. This raises the question if N limitation in boreal forests acts primarily by constraining growth of young stands while the commonly recorded increase in stem growth of mature stands following N addition is primarily the result of altered allocation and only to a limited extent the result of increased stand C-capture.

Seasonal and within-canopy variation in shoot-scale resource-use efficiency trade-offs in a Norway spruce stand

Previous leaf-scale studies of carbon assimilation describe short-term resource-use efficiency (RUE) trade-offs where high use efficiency of one resource requires low RUE of another. However, varying resource availabilities may cause long-term RUE trade-offs to differ from the short-term patterns. This may have important implications for understanding canopy-scale resource use and allocation. We used continuous gas exchange measurements collected at five levels within a Norway spruce, Picea abies (L.) karst., canopy over 3 years to assess seasonal differences in the interactions between shoot-scale resource availability (light, water and nitrogen), net photosynthesis (An ) and the use efficiencies of light (LUE), water (WUE) and nitrogen (NUE) for carbon assimilation. The continuous data set was used to develop and evaluate multiple regression models for predicting monthly shoot-scale An . These models showed that shoot-scale An was strongly dependent on light availability and was generally well described with simple one- or two-parameter models. WUE peaked in spring, NUE in summer and LUE in autumn. However, the relative importance of LUE for carbon assimilation increased with canopy depth at all times. Our results suggest that accounting for seasonal and within-canopy trade-offs may be important for RUE-based modelling of canopy carbon uptake.

Stem compression reversibly reduces phloem transport in Pinus sylvestris trees

Manipulating tree belowground carbon (C) transport enables investigation of the ecological and physiological roles of tree roots and their associated mycorrhizal fungi, as well as a range of other soil organisms and processes. Girdling remains the most reliable method for manipulating this flux and it has been used in numerous studies. However, girdling is destructive and irreversible. Belowground C transport is mediated by phloem tissue, pressurized through the high osmotic potential resulting from its high content of soluble sugars. We speculated that phloem transport may be reversibly blocked through the application of an external pressure on tree stems. Thus, we here introduce a technique based on compression of the phloem, which interrupts belowground flow of assimilates, but allows trees to recover when the external pressure is removed. Metal clamps were wrapped around the stems and tightened to achieve a pressure theoretically sufficient to collapse the phloem tissue, thereby aiming to block transport. The compressions performance was tested in two field experiments: a (13)C canopy labelling study conducted on small Scots pine (Pinus sylvestris L.) trees [2-3 m tall, 3-7 cm diameter at breast height (DBH)] and a larger study involving mature pines (∼15 m tall, 15-25 cm DBH) where stem respiration, phloem and root carbohydrate contents, and soil CO2 efflux were measured. The compressions effectiveness was demonstrated by the successful blockage of (13)C transport. Stem compression doubled stem respiration above treatment, reduced soil CO2 efflux by 34% and reduced phloem sucrose content by 50% compared with control trees. Stem respiration and soil CO2 efflux returned to normal within 3 weeks after pressure release, and (13)C labelling revealed recovery of phloem function the following year. Thus, we show that belowground phloem C transport can be reduced by compression, and we also demonstrate that trees recover after treatment, resuming C transport in the phloem.

Photosynthetic refixation varies along the stem and reduces CO2 efflux in mature boreal Pinus sylvestris trees

Trees are able to reduce their carbon (C) losses by refixing some of the CO2 diffusing out of their stems through corticular photosynthesis. Previous studies have shown that under ideal conditions the outflowing CO2 can be completely assimilated in metabolically active, young stem and branch tissues. Fewer studies have, however, been carried out on the older stem sections of large trees and, accordingly, the importance of refixation is still unclear under natural environmental conditions. We investigated the spatial and temporal variation in refixation in ~90-year-old boreal Scots pine (Pinus sylvestris L.) trees by utilizing month-long continuous measurements of stem CO2 efflux (Ec) made at four heights along the bole. Refixation rates were found to vary considerably along the bole, leading to a 28% reduction in long-term Ec in the upper stem compared with a negligible reduction at breast height. This vertical pattern correlated with variation in light availability, bark chlorophyll content and bark type. Analysis of the vertical and diurnal patterns in Ec further suggested that the influence of sap flow on the observed daytime reduction in Ec was small. The areal rates of corticular photosynthesis were much lower than previous estimates of photosynthetic rates per unit leaf area from the same trees, implying that the impact of refixation on tree-scale C uptake was small. However, upscaling of refixation indicated that 23-27% of the potential Ec was refixed by the bole and the branches, thereby significantly reducing the woody tissue C losses. Thus, our results suggest that refixation needs to be considered when evaluating the aboveground C cycling of mature P. sylvestris stands and that breast-height estimates should not be extrapolated to the whole tree.

Temperature responses of photosynthetic capacity parameters were not affected by foliar nitrogen content in mature Pinus sylvestris

A key weakness in current Earth System Models is the representation of thermal acclimation of photosynthesis in response to changes in growth temperatures. Previous studies in boreal and temperate ecosystems have shown leaf-scale photosynthetic capacity parameters, the maximum rates of carboxylation (Vcmax ) and electron transport (Jmax ), to be positively correlated with foliar nitrogen (N) content at a given reference temperature. It is also known that Vcmax and Jmax exhibit temperature optima that are affected by various environmental factors and, further, that N partitioning among the foliar photosynthetic pools is affected by N availability. However, despite the strong recent anthropogenic influence on atmospheric temperatures and N deposition to forests, little is known about the role of foliar N contents in controlling the photosynthetic temperature responses. In this study, we investigated the temperature dependencies of Vcmax and Jmax in 1-year-old needles of mature boreal Pinus sylvestris (Scots pine) trees growing under low and high N availabilities in northern Sweden. We found that needle N status did not significantly affect the temperature responses of Vcmax or Jmax when the responses were fitted to a peaked function. If such N insensitivity is a common tree trait it will simplify the interpretation of the results from gradient and multi-species studies, which commonly use sites with differing N availabilities, on temperature acclimation of photosynthetic capacity. Moreover, it will simplify modeling efforts aimed at understanding future carbon uptake by precluding the need to adjust the shape of the temperature response curves to variation in N availability.