Wintertime photosynthesis and water uptake in a boreal forest
Jukka Pumpanen2006, Tree Physiology
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Abstract
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This research investigates wintertime photosynthesis and water uptake in a boreal Scots pine forest, challenging earlier assumptions about plant activity in cold conditions. The findings indicate that photosynthesis occurs in winter months, triggered by rising air temperatures and sufficient water availability, with trees relying on both soil and stem reservoirs. Importantly, while increased wintertime photosynthesis is linked to climate warming, the simultaneous increase in ecosystem respiration complicates the net impact on carbon dioxide uptake.
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The temperature dependence of photosynthetic parameters has been a focus of interest during recent years owing to its profound implications in the new climate scenario. Many studies have addressed the short-term responses of photosynthetic parameters to temperature change. Less attention has been given to the intraspecific variability in the biochemical parameters of photosynthesis in response to differences in growth temperature. This study explores the effects of winter harshness on the leaf traits of two evergreen tree species (Quercus ilex and Q. suber). Leaf mass per unit area (LMA) and the concentrations of fiber, nitrogen (N), soluble protein, chlorophyll and ribulose 1,5-bisphosphate carboxylase/oxygenase (Rubisco) were determined in both species throughout a temperature gradient. Several photosynthetic parameters [maximum carboxylation rate (V cmax), maximum light-driven electron flux (J max), day respiration rate (R d) and relative stomatal limitation to photosynthesis] were assessed by measuring leaf response curves of net CO 2 assimilation versus intercellular CO 2 partial pressure. LMA and structural carbohydrate concentrations increased with the decrease in winter temperatures, whereas N concentrations did not show definite patterns. Chlorophyll, soluble proteins, Rubisco, V cmax and J max declined with the decrease in winter temperatures, whereas R d at a set common temperature (25°C) was higher at colder sites. Our results suggest that an increase in LMA and in the concentration of structural carbohydrates in cold environments is associated with a reduced N allocation to the photosynthetic machinery, which leads to reduced photosynthetic capacity.
Intermittent low temperatures constrain spring recovery of photosynthesis in boreal Scots pine forests
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During winter and early spring, evergreen boreal conifers are severely stressed because light energy cannot be used when photosynthesis is pre-empted by low ambient temperatures. To study photosynthetic performance dynamics in a severe boreal climate, seasonal changes in photosynthetic pigments, chloroplast proteins and photochemical efficiency were studied in a Scots pine forest near Zotino, Central Siberia. In winter, downregulation of photosynthesis involved loss of chlorophylls, a twofold increase in xanthophyll cycle pigments and sustained high levels of the light stress-induced zeaxanthin pigment. The highest levels of xanthophylls and zeaxanthin did not occur during the coldest winter period, but rather in April when light was increasing, indicating an increased capacity for thermal dissipation of excitation energy at that time. Concomitantly, in early spring the D1 protein of the photosystem II (PSII) reaction centre and the light-harvesting complex of PSII dropped to their lowest annual levels. In April and May, recovery of PSII activity, chloroplast protein synthesis and rearrangements of pigments were observed as air temperatures increased above 0°C. Nevertheless, severe intermittent low-temperature episodes during this period not only halted but actually reversed the physiological recovery. During these spring low-temperature episodes, protective processes involved a complementary function of the PsbS and early light-induced protein thylakoid proteins. Full recovery of photosynthesis did not occur until the end of May. Our results show that even after winter cold hardening, photosynthetic activity in evergreens responds opportunistically to environmental change throughout the cold season. Therefore, climate change effects potentially improve the sink capacity of boreal forests for atmospheric carbon. However, earlier photosynthesis in spring in response to warmer temperatures is strongly constrained by environmental variation, counteracting the positive effects of an early recovery process.
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Temperature and daylength act as environmental signals that determine the length of the growing season in boreal evergreen conifers. Climate change might affect the seasonal development of these trees, as they will experience naturally decreasing daylength during autumn, while at the same time warmer air temperature will maintain photosynthesis and respiration. We characterized the down-regulation of photosynthetic gas exchange and the mechanisms involved in the dissipation of energy in Jack pine (Pinus banksiana) in controlled environments during a simulated summer-autumn transition under natural conditions and conditions with altered air temperature and photoperiod. Using a factorial design, we dissected the effects of daylength and temperature. Control plants were grown at either warm summer conditions with 16-h photoperiod and 22°C or conditions representing a cool autumn with 8 h/7°C. To assess the impact of photoperiod and temperature on photosynthesis and energy dissipation, plants were also grown under either cold summer (16-h photoperiod/7°C) or warm autumn conditions (8-h photoperiod/22°C). Photosynthetic gas exchange was affected by both daylength and temperature. Assimilation and respiration rates under warm autumn conditions were only about one-half of the summer values but were similar to values obtained for cold summer and natural autumn treatments. In contrast, photosynthetic efficiency was largely determined by temperature but not by daylength. Plants of different treatments followed different strategies for dissipating excess energy. Whereas in the warm summer treatment safe dissipation of excess energy was facilitated via zeaxanthin, in all other treatments dissipation of excess energy was facilitated predominantly via increased aggregation of the light-harvesting complex of photosystem II. These differences were accompanied by a lower deepoxidation state and larger amounts of b-carotene in the warm autumn treatment as well as by changes in the abundance of thylakoid membrane proteins compared to the summer condition. We conclude that photoperiod control of dormancy in Jack pine appears to negate any potential for an increased carbon gain associated with higher temperatures during the autumn season.
Climate warming effects on photosynthesis in boreal tree species depend on soil moisture 1 2 3 4
2018
Affiliations 8 9 1 Department of Forest Resources, University of Minnesota, St. Paul, MN 55108 USA. 10 2 Hawkesbury Institute for the Environment, Western Sydney University, Penrith NSW 2753, 11 Australia. 12 3 Department of Biology, Georgia Southern University, Statesboro, GA 30460, USA. 13 4 Smithsonian Environmental Research Center, Edgewater, MD, 21037, USA. 14 5 Department of Ecology, Evolution, and Behavior, University of Minnesota, St. Paul, MN 55108 15 USA. 16
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Climate change has caused shifts in species' ranges and extinctions of high-latitude and altitude species. Most cold-tolerant evergreen broadleaved woody plants (shortened to cold-evergreens below) are rare species occurring in a few sites in the alpine and subalpine zones in the Korean Peninsula. The aim of this research is to 1) identify climate factors controlling the range of cold-evergreens in the Korean Peninsula; and 2) predict the climate change effects on the range of cold-evergreens. We used multimodel inference based on combinations of climate variables to develop distribution models of cold-evergreens at a physiognomic-level. Presence/absence data of 12 species at 204 sites and 6 climatic factors, selected from among 23 candidate variables, were used for modeling. Model uncertainty was estimated by mapping a total variance calculated by adding the weighted average of within-model variation to the between-model variation. The range of cold-evergreens and model performance were validated by true skill statistics, the receiver operating characteristic curve and the kappa statistic. Climate change effects on the cold-evergreens were predicted according to the RCP 4.5 and RCP 8.5 scenarios. Multimodel inference approach excellently projected the spatial distribution of cold-evergreens (AUC = 0.95, kappa = 0.62 and TSS = 0.77). Temperature was a dominant factor in model-average estimates, while precipitation was minor. The climatic suitability increased from the southwest, lowland areas, to the northeast, high mountains. The range of cold-evergreens declined under climate change. Mountain-tops in the south and most of the area in the north remained suitable in 2050 and 2070 under the RCP 4.5 projection and 2050 under the RCP 8.5 projection. Only high-elevations in the northeastern Peninsula remained suitable under the RCP 8.5 projection. A northward and upper-elevational range shift indicates change in species composition at the alpine and subalpine ecosystems in the Korean Peninsula.
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Decreasing photosynthesis at different spatial scales during the late growing season on a boreal cutover
Tree physiology, 2005
The relationship between photosynthesis and accumulated cold degree days (CDD) over the late growing season was examined at the shoot, ecosystem and landscape scales in a boreal cutover in eastern Canada predominated by black spruce (Picea mariana Mill. BSP), lowbush blueberry (Vaccinium angustifolium Ait.) and sheep laurel (Kalmia angustifolia L.). We calculated CDD as the sum of minimum daily temperatures below a 5 degrees C threshold. Light-saturated photosynthesis at the shoot level (A(max)) of black spruce and V. angustifolium decreased steadily with increasing CDD once temperatures below the CDD threshold value became frequent in mid-September, whereas K. angustifolia showed a more irregular pattern. Tissue acclimation played an important role in the decrease in A(max) as the season progressed, but only V. angustifolium showed decreasing foliar nitrogen concentrations. Based on eddy covariance flux tower data, maximum daily gross primary productivity (GPP(max)-tower) at the ec...
Winter photosynthesis by saplings of evergreen broad-leaved trees in a deciduous temperate forest
New Phytologist, 2004
• Here we investigated photosynthetic traits of evergreen species under a deciduous canopy in a temperate forest and revealed the importance of CO2 assimilation during winter for annual CO2 assimilation.• Saplings were shaded by the canopy trees from spring through to autumn, but were less shaded during the winter months. Photosynthetic rates at light saturation (Aarea) were lower during winter than during the growing season. Aarea was higher in Camellia, Ilex and Photinia than in Castanopsis, Cleyera and Quercus during the winter, but differed little during summer and autumn.• Estimated daily CO2 assimilation (Aday) was higher during the winter than during the growing season in Camellia, Ilex and Photinia but was higher than that during the growing season only at the beginning and end of winter in Castanopsis, Cleyera and Quercus. Aday was higher in Camellia, Ilex and Photinia than in Castanopsis, Cleyera and Quercus but differed little among them during the growing season.• These results reveal the importance of winter CO2 assimilation for the growth of Camellia, Ilex and Photinia. Furthermore, differences in annual CO2 assimilation among species are strongly modified by species-specific photosynthetic traits during the winter under deciduous canopy trees.Here we investigated photosynthetic traits of evergreen species under a deciduous canopy in a temperate forest and revealed the importance of CO2 assimilation during winter for annual CO2 assimilation.Saplings were shaded by the canopy trees from spring through to autumn, but were less shaded during the winter months. Photosynthetic rates at light saturation (Aarea) were lower during winter than during the growing season. Aarea was higher in Camellia, Ilex and Photinia than in Castanopsis, Cleyera and Quercus during the winter, but differed little during summer and autumn.Estimated daily CO2 assimilation (Aday) was higher during the winter than during the growing season in Camellia, Ilex and Photinia but was higher than that during the growing season only at the beginning and end of winter in Castanopsis, Cleyera and Quercus. Aday was higher in Camellia, Ilex and Photinia than in Castanopsis, Cleyera and Quercus but differed little among them during the growing season.These results reveal the importance of winter CO2 assimilation for the growth of Camellia, Ilex and Photinia. Furthermore, differences in annual CO2 assimilation among species are strongly modified by species-specific photosynthetic traits during the winter under deciduous canopy trees.
Cold Tolerance and Photosystem Function in a Montane Red Spruce Population
Journal of Sustainable Forestry, 1999
Impacts of seasonal air and soil temperatures on photosynthesis in Scots pine trees
Tree Physiology, 2002
Seasonal courses of light-saturated rate of net photosynthesis (A 360 ) and stomatal conductance (g s ) were examined in detached 1-year-old needles of Scots pine (Pinus sylvestris L.) from early April to mid-November. To evaluate the effects of soil frost and low soil temperatures on gas exchange, the extent and duration of soil frost, as well as the onset of soil warming, were manipulated in the field. During spring, early summer and autumn, the patterns of A 360 and g s in needles from the control and warm-soil plots were generally strongly related to daily mean air temperatures and the frequency of severe frosts. The warm-soil treatment had little effect on gas exchange, although mean soil temperature in the warm-soil plot was 3.8°C higher than in the control plot during spring and summer, indicating that A 360 and g s in needles from control trees were not limited by low soil temperature alone. In contrast, prolonged exposure to soil temperatures slightly above 0°C severely restricted recovery of A 360 and especially g s in needles from the cold-soil treatment during spring and early summer; however, full recovery of both A 360 and g s occurred in late summer. We conclude that inhibition of A 360 by low soil temperatures is related to both stomatal closure and effects on the biochemistry of photosynthesis, the relative importance of which appeared to vary during spring and early summer. During the autumn, soil temperatures as low as 8°C did not affect either A 360 or g s .
Increased photosynthesis compensates for shorter growing season in subarctic tundra—8 years of snow accumulation manipulations
Climatic Change, 2014
This study was initiated to analyze the effect of increased snow cover on plant photosynthesis in subarctic mires underlain by permafrost. Snow fences were used to increase the accumulation of snow on a subarctic permafrost mire in northern Sweden. By measuring reflected photosynthetic active radiation (PAR) the effect of snow thickness and associated delay of the start of the growing season was assessed in terms of absorbed PAR and estimated gross primary production (GPP). Six plots experienced increased snow accumulation and six plots were untreated. Incoming and reflected PAR was logged hourly from August 2010 to October 2013. In 2010 PAR measurements were coupled with flux chamber measurements to assess GPP and light use efficiency of the plots. The increased snow thickness prolonged the duration of the snow cover in spring. The delay of the growing season start in the treated plots was 18 days in 2011, 3 days in 2012 and 22 days in 2013. Results show higher PAR absorption, together with almost 35 % higher light use efficiency, in treated plots compared to untreated plots. Estimations of GPP suggest that the loss in early season photosynthesis, due to the shortening of the growing season in the treatment plots, is well compensated for by the increased absorption of PAR and higher light use efficiency throughout the whole growing seasons. This compensation is likely to be explained by increased soil moisture and nutrients together with a shift in vegetation composition associated with the accelerated permafrost thaw in the treatment plots.
Effects of climate warming on photosynthesis in boreal tree species depend on soil moisture
Nature, 2018
Climate warming will influence photosynthesis via thermal effects and by altering soil moisture 1-11. Both effects may be important for the vast areas of global forests that fluctuate between periods when cool temperatures limit photosynthesis and periods when soil moisture may be limiting to carbon gain 4-6,9-11. Here we show that the effects of climate warming flip from positive to negative as southern boreal forests transition from rainy to modestly dry periods during the growing season. In a three-year open-air warming experiment with juveniles of 11 temperate and boreal tree species, an increase of 3.4 °C in temperature increased lightsaturated net photosynthesis and leaf diffusive conductance on average on the one-third of days with the wettest soils. In all 11 species, leaf diffusive conductance and, as a result, light-saturated net photosynthesis decreased during dry spells, and did so more sharply in warmed plants than in plants at ambient temperatures. Consequently, across the 11 species, warming reduced lightsaturated net photosynthesis on the two-thirds of days with driest soils. Thus, low soil moisture may reduce, or even reverse, the potential benefits of climate warming on photosynthesis in mesic, seasonally cold environments, both during drought and in regularly occurring, modestly dry periods during the growing season. A changing climate will influence plants by altering temperature, precipitation and soil moisture, as well as their variability and seasonality 1-11. In temperate and boreal climates, temperatures switch seasonally from cold (and limiting to biological processes) to warm and periodically dry, during which time moisture can be limiting 2-6,9-11. Both the 'law of the minimum' and multiple limitation theory 12-14 provide a conceptual basis for predicting climate warming interactions with soil moisture. Although higher temperatures may alleviate enzymatic limits on the biochemistry of photosynthesis, realized rates of CO 2 assimilation may decrease if and when low soil water causes stomatal closure and limitation of the CO 2 substrate for photosynthesis. As growing season conditions in temperate and boreal forests are likely to become effectively drier than in the past 3,8,9 , because climate warming will increase evapotranspiration more than precipitation 3,9 and increase variability in the amount of precipitation per event 1,9 , the importance of water availability to forest responses to rising temperature may increase in the future 3-6,9-11,15-18. Mid-and high-latitude plants will therefore probably experience both positive and negative effects of climate warming on photosynthesis within and across years-we propose that these will be positive when soil moisture is ample but negative when soils are drier 4-6,9-11,15-17. Whether such effects are in aggregate positive or negative is likely to depend on the balance of time that warming alleviates low temperature limitations to plant function as opposed to causing limitations to function through decreased soil moisture. However, direct tests of the effects of climate warming across a range of soil moisture conditions, caused by seasonal or interannual variation or by manipulations of temperature or moisture, are rare, and it remains unclear how plant responses to climate warming will be influenced by these indirect effects of soil moisture 4-6,9-11,16-18 .
Temperature and Snow-Mediated Moisture Controls of Summer Photosynthetic Activity in Northern Terrestrial Ecosystems between 1982 and 2011
Remote Sensing, 2014
Recent warming has stimulated the productivity of boreal and Arctic vegetation by reducing temperature limitations. However, several studies have hypothesized that warming may have also increased moisture limitations because of intensified summer drought severity. Establishing the connections between warming and drought stress has been difficult because soil moisture observations are scarce. Here we use recently developed gridded datasets of moisture variability to investigate the links between warming and changes in available soil moisture and summer vegetation photosynthetic activity at northern latitudes (>45 • N) based on the Normalized Difference Vegetation Index (NDVI) since 1982. Moisture and temperature exert a significant influence on the interannual variability of
Seasonally different response of photosynthetic activity to daytime and night-time warming in the Northern Hemisphere
Global Change Biology, 2014
Over the last century the Northern Hemisphere has experienced rapid climate warming, but this warming has not been evenly distributed seasonally, as well as diurnally. The implications of such seasonal and diurnal heterogeneous warming on regional and global vegetation photosynthetic activity, however, are still poorly understood. Here, we investigated for different seasons how photosynthetic activity of vegetation correlates with changes in seasonal daytime and night-time temperature across the Northern Hemisphere (>30°N), using Normalized Difference Vegetation Index (NDVI) data from 1982 to 2011 obtained from the Advanced Very High Resolution Radiometer (AVHRR). Our analysis revealed some striking seasonal differences in the response of NDVI to changes in day-
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