Spring photosynthetic recovery of boreal Norway spruce under conditions of elevated [CO 2 ] and air temperature

Tree Physiology 33, 1177–1191 doi:10.1093/treephys/tpt066 Research paper: Part of a special section on the Flakaliden experiments Spring photosynthe...
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Tree Physiology 33, 1177–1191 doi:10.1093/treephys/tpt066

Research paper: Part of a special section on the Flakaliden experiments

Spring photosynthetic recovery of boreal Norway spruce under conditions of elevated [CO2] and air temperature Göran Wallin1,5, Marianne Hall1,2, Michelle Slaney3, Mats Räntfors1, Jane Medhurst4 and Sune Linder3 1Department

of Biological and Environmental Sciences, University of Gothenburg, PO Box 461, SE-405 30 Göteborg, Sweden; 2Centre for Environmental and Climate Research, Lund University, Sölvegatan 37, SE-223 62 Lund, Sweden; 3Southern Swedish Forest Research Centre, Swedish University of Agricultural Sciences, PO Box 49, SE-230 53 Alnarp, Sweden; 4University of Tasmania, CRC Forestry, Private Bag 12, Hobart, Tasmania 7001, Australia; 5Corresponding author ([email protected]) Received April 3, 2013; accepted July 30, 2013; published online October 28, 2013; handling Editor Michael G. Ryan

Accumulated carbon uptake, apparent quantum yield (AQY) and light-saturated net CO2 assimilation (A sat) were used to assess the responses of photosynthesis to environmental conditions during spring for three consecutive years. Whole-tree chambers were used to expose 40-year-old field-grown Norway spruce trees in northern Sweden to an elevated atmospheric CO2 concentration, [CO2], of 700 µmol CO2 mol−1 (CE) and an air temperature (T) between 2.8 and 5.6 °C above ambient T (TE), during summer and winter. Net shoot CO2 exchange (Anet) was measured continuously on 1-year-old shoots and was used to calculate the accumulated carbon uptake and daily A sat and AQY. The accumulated carbon uptake, from 1 March to 30 June, was stimulated by 33, 44 and 61% when trees were exposed to CE, TE, and CE and TE combined, respectively. Air temperature strongly influenced the timing and extent of photosynthetic recovery expressed as AQY and A sat during the spring. Under elevated T (TE), the recovery of AQY and A sat commenced ~10 days earlier and the activity of these parameters was significantly higher throughout the recovery period. In the absence of frost events, the photosynthetic recovery period was less than a week. However, frost events during spring slowed recovery so that full recovery could take up to 60 days to complete. Elevated [CO2] stimulated AQY and A sat on average by ~10 and ~50%, respectively, throughout the recovery period, but had minimal or no effect on the onset and length of the photosynthetic recovery period during the spring. However, AQY, A sat and Anet all recovered at significantly higher T (average +2.2 °C) in TE than in TA, possibly caused by acclimation or by shorter days and lower light levels during the early part of the recovery in TE compared with TA. The results suggest that predicted future climate changes will cause prominent stimulation of photosynthetic CO2 uptake in boreal Norway spruce forest during spring, mainly caused by elevated T, but also elevated [CO2]. However, the effects of elevated T may not be linearly extrapolated to future warmer climates. Keywords: apparent quantum yield, boreal forest, carbon dioxide, climate change, light-saturated photosynthesis, Picea abies, whole-tree chambers.

Introduction Rising atmospheric CO2 concentration, [CO2], is expected to cause significant increases in surface air temperatures with the greatest increases predicted to occur at high northern latitudes during the winter and spring months (IPCC 2007). This has important implications for boreal forests as the timing and

extent of photosynthetic recovery during spring is strongly related to air temperature (e.g., Pelkonen and Hari 1980, Linder and Lohammar 1981, Troeng and Linder 1982, Suni et al. 2003, Hall et al. 2009, 2013, Gea-Izquierdo et al. 2010) and the extent and speed of recovery will highly influence the degree to which carbon can be sequestered. During winter, at high latitudes, the maximum photosynthetic capacity is reduced to

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1178  Wallin et al. 5–10% of its late summer maximum, a reduction which starts with the first severe autumn frost (Troeng and Linder 1982, Bergh et al. 1998, Mäkelä et al. 2004). The reduction in capacity is the result of winter acclimation and damage of the photosynthetic apparatus caused by low temperatures and high photon flux densities while the needles are still frozen (e.g., Lundmark et al. 1988, Havranek and Tranquillini 1995). In addition to effects of air temperature, recovery is also strongly coupled to soil thawing and water availability (e.g., Troeng and Linder 1982, Goulden et al. 1998, Bergh and Linder 1999, Jarvis and Linder 2000, Sevanto et al. 2006, Ensminger et al. 2007). Wu et al. (2012) found in a modelling study (Pinus sylvestris L.) that although air temperature was the main regulatory factor during early spring, autumn and winter, soil temperature appeared to be a large limiting factor during spring. Because of the strong link between temperature (air and soil) and the onset and rate of spring events, bud burst (Slaney et al. 2007), reactivation of cambium activity (Kalliokoski et al. 2013) and spring recovery of photosynthesis are likely to occur earlier in the future if climate change results in elevated temperatures (e.g., Bergh et al. 1998, Hyvönen et al. 2007, Hall et al. 2013). As photosynthesis has CO2 as a substrate, it is, together with stomatal conductance, one of the main plant processes directly affected by atmospheric [CO2] (Mott 1990, Leakey et al. 2012). On a short-term basis, an almost invariable increase has been found in the photosynthetic response to elevated [CO2] (cf. reviews by Ceulemans and Mousseau 1994, Curtis 1996, Saxe et al. 1998, Urban 2003, Ainsworth and Long 2005, Hyvönen et al. 2007), but the long-term response is less clear (Stitt 1991, Long et al. 1993, Körner 2006, Hyvönen et al. 2007). Leakey et al. (2012) reported, in a literature overview, that results from [CO2] elevation experiments in enclosures generally indicate a down-regulation of the initial photosynthetic response, while results from open air free-air CO2 enrichment (FACE) experiments do not confirm these earlier results. Although the range of stimulation varies with position in crown and month of measurement, there is no indication in the FACE literature that the response weakens with time, and the down-regulation seen in enclosures have partly been attributed to chamber and pot artefacts (Leakey et al. 2012). Both theoretical assumptions and some measurements suggest that the positive effect of elevated [CO2] on the photosynthetic rate is further enhanced by increasing temperature (e.g., Long 1991, Medlyn et al. 2002, Uddling and Wallin 2012). Mechanistically, this is based on the temperature effect on the specificity of ribulose bisphosphate carboxylase/oxygenase (Rubisco) for CO2, as well as by different temperature dependencies of the solubility of CO2 and O2 in water (e.g., Jordan and Ogren 1984, Long 1991, Leakey et al. 2012). However, no interactive effect with elevated temperature is usually reported for photosynthesis during the main growing season (Tjoelker et al. 1998, Leverenz et al. 1999, Lewis et  al. 2001, Tingey et al.

Tree Physiology Volume 33, 2013

2007, Hall et al. 2009, 2013). This may be due to the experimentally elevated temperature range being relatively low compared with the physiologically active temperature range. In addition, the growing season temperature is close to the optimal for photosynthesis. In spring, however, elevated temperature will be relatively more important and less is known about how a combination of elevated temperature and [CO2] will affect the photosynthetic performance during spring. A decrease in the quantum yield of photosystem II in response to elevated [CO2] has been reported for Norway spruce [Picea abies (L.) Karst.] (Marek et al. 1997). An acclimation of the photosynthetic response to prolonged exposure to elevated [CO2] has been accompanied by a decrease in the variable chlorophyll fluorescence (Kalina et al. 2000), a reduction of photosynthetic capacity of leaves (DeLucia 1987) and an enhanced susceptibility to photoinhibition (Spunda et al. 1997). As photoinhibition is one of the causes of photosynthetic apparatus damage during spring (e.g., Strand and Öquist 1985, Öquist and Huner 2003), elevated [CO2] may influence photosynthetic spring recovery, leading to a secondary interactive effect of [CO2] and temperature elevation if spring recovery of photosynthesis occurs earlier in the season, e.g., under different prevailing light conditions. The aim of this study was to test the hypotheses that: (i) both elevated [CO2] and T stimulate photosynthesis during spring, but only elevated T will affect the timing and rate of recovery; (ii) the response of photosynthesis will be proportional to temperature independently of [CO2]; (iii) because of the effect of T on the specificity of Rubisco for CO2 and O2, and on the water solubility of CO2 and O2, elevated T will increase the effect of CO2 on photosynthesis during the spring, resulting in a positive interaction of T and [CO2]. The study used net photosynthesis measurements from the Flakaliden whole-tree chamber (WTC) experiment (Medhurst et al. 2006), where WTCs had been installed in a 40-year-old boreal Norway spruce stand in northern Sweden. The WTCs were used to expose individual trees to approximately a doubling of [CO2] and accompanying temperature elevation as projected for the region towards the end of the 21st century (cf. Christensen et al. 2001, Räisänen et al. 2001).

Materials and methods The study was conducted in a long-term nutrient optimization experiment at Flakaliden (64°07′N, 19°27′E, 310 m above sea level) in northern Sweden using 12 WTCs, with temperature and [CO2] control (cf. Medhurst et al. 2006). The WTCs were used to examine the long-term physiological responses of field-grown Norway spruce to ambient and elevated temperature and [CO2], separately and in combination.

Site description The nutrient optimization experiment was established in 1986 in a Norway spruce (P. abies) stand that had been planted in

Spring photosynthesis under climate change  1179 1963 with 4-year-old seedlings of local provenance (Linder 1995, Bergh et al. 1999). The nutrient treatments, which began in 1987, included untreated control plots, irrigation and two nutrient optimization treatments. The treatments were replicated four times in a randomized block design. Each replicate consisted of 50 × 50 m plots. Only untreated control plots were used in the present study. For further details of experimental design and treatments, see Linder (1995) and Bergh et al. (1999). The site belongs to the middle boreal sub-zone (Sjörs 1999) and has a harsh boreal climate with long cool days in the summer and short cold days in the winter. The mean annual air temperature is 2.5 °C and the mean monthly temperature varies from −7.5 °C in February to 14.6 °C in July (mean for 1990–2009). The mean annual rainfall is ~600 mm with approximately one-third falling as snow, which usually covers the frozen ground from mid-October to early May. The length of the growing season (the period with a daily mean air temperature +5 °C or more) averages ~150 days, but with large between-year variations. For detailed information on the weather conditions for the study period 2001–2004, see Sigurdsson et al. (2013). Soil at the site is a thin podzolic, sandy, post-glacial till with a mean depth of ~120 cm, with a 2- to 6-cm-thick humus layer, and with soil water content normally not limiting for tree growth (Bergh et al. 1999). Nitrogen (N) deposition averages 3 kg ha−1 year −1 (cf. Berggren et al. 2004, Karlsson et al. 2011, Phil Karlsson et al. 2012) and net N mineralization is 4 kg N ha−1 year −1 on the control plots (Andersson et al. 2002).

Whole-tree chamber system and treatments During summer 2001, 12 WTCs were each installed around individual trees. A combination of two temperature (TA, ambient and TE, elevated) and two [CO2] treatments (CA, ambient ~365 µmol mol−1 and CE, elevated ~700 µmol mol−1) was used as variables in the WTCs. Three reference trees (R) without WTCs were also selected and a randomized design was used where a total of 15 trees were assigned to five treatments (TACA, TECA, TACE, TECE, R). The enclosed trees represented the average tree size, and had an average height of 5.6 m when the treatments commenced in mid-August 2001. The experiment ended in late September 2004, when the trees were harvested (cf. Sigurdsson et al. 2013). The temperatures in the TE treatments were altered on a monthly time-step based on projections made within the Swedish Regional Climate Modelling Programme, SWECLIM, using the latitude of Flakaliden and an elevated [CO2] of 700 µmol mol−1 (cf. Christensen et al. 2001, Räisänen et al. 2001). The temperature elevation ranged between +2.8 and +5.6 °C above ambient temperature, during summer and winter, respectively, and resulted in an increase of the annual mean temperature by 3.9 °C.

Two micro-sprinklers were installed under the chamber floor and the trees received irrigation equivalent to precipitation measured with rain gauges outside the WTCs. The equivalent of winter precipitation was applied in the form of irrigation water in late April to mid-May after which the irrigation system was started. For more details on the WTC system, see Medhurst et al. (2006) and Slaney et al. (2007).

Shoot CO2 exchange Net shoot CO2 gas exchange was measured on a single 1-yearold shoot on the fifth or sixth whorl from the top of each tree. In 2002, however, in the R treatment the averages of two shoots from each tree were used. The chosen shoots were on the south-facing side of the trees (±90°). Measurements of each shoot were made for 30 s every 30 min, throughout the entire period of the experiment (2001–2004) on all 15 trees included in the study. Gas exchange was measured by means of shoot cuvettes (SCs), where a 55-mm portion of the shoots was enclosed in a temperature-controlled, 0.15-l cuvette fitted with a transparent Perspex (Plexiglas) top. Temperature in the SCs tracked ambient temperature by means of a Peltier heat exchanger. To prevent water condensation in the cuvette, the set temperature in the SCs was +0.2 °C above the WTC air temperature. In addition, the ambient air used to supply the SCs was passed through a condenser, maintained at a temperature 3 °C below ambient by means of a second Peltier heat exchanger. The SCs and a parallel reference cuvette were connected to a gas exchange system (running in open mode) with 36 parallels channels by using insulated and heated tubings (~+ 5 °C). The CO2 and H2O in the air from the SCs and reference cuvette was analysed by means of an infrared gas analyser (CIRAS-1, PP Systems, Hitchen, Herts, UK). Airflow rates were regulated and measured with mass flow controllers (F-201C, Bronkhorst High Tech, Ruurlo, The Netherlands). For more details on the SCs and gas exchange system see Wallin et al. (2001) and Hall et al. (2009). The measured shoots were changed, on average, twice a year. Within a given treatment, shoots on individual trees were changed on different dates to allow an overlap of ~1 month between previously and subsequently measured shoots. The rate of CO2 exchange was expressed on a projected needle area basis at the time of shoot harvest.

Shoot properties Following completion of gas exchange measurements, each shoot was harvested to determine needle area, mass, and N concentration. The projected needle area was calculated from scanned (Epson 1600+ scanner equipped with a transparency unit for dual scanning) images of the needles, using the WinSEEDLE software (WinSEEDLE Pro 5.1a, Regent Instruments, Inc., Quebec City, Quebec, Canada). Needle dry

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1180  Wallin et al. mass was determined after drying to constant weight at 70 °C. Nitrogen concentrations were measured using a CHNS-O analyser (model EA 1108, Fison Instruments, Rodano, Italy). In order to avoid large influence by starch accumulation on needle properties, shoots harvested from late September to March were used to quantify effects of temperature, [CO2] and WTC on needle properties (cf. Linder 1995). Specific needle area (SNA), needle N concentration on mass basis (Nmass), and needle N content on area basis (Narea) were determined.

Meteorological measurements Photosynthetic photon flux density (PPFD) was measured with a levelled cosine-corrected quantum sensor (PAR-1 (M), PP Systems) attached to each SC (within 5 cm from the shoot). The air temperature in each SC was measured by means of a Pt-100 sensor. The air temperatures inside and outside of the WTCs were measured using shielded and ventilated thermistors at a height of ~5 m. Soil temperature and soil volumetric water content were measured with Pt100 thermistors and Theta probes (Thetaprobe ML1, Delta-T Devices Ltd, Cambridge, UK) at 10and 15-cm depths, respectively, in the mineral soil under the base section of the WTCs and at three nearby positions outside the WTCs. During winter and until late April snow cover was simulated by placing insulation material on the floor of the chamber sections.

Data analysis and statistics Photosynthesis was calculated from the CO2 gas exchange measurements as net assimilation rate of CO2 (Anet, µmol CO2 m−2 s−1). The accumulated carbon (C, g m−2) uptake during March to June was calculated by integrating more than 5800 photosynthesis readings in each replicate. Because of different incident PPFD at the cuvettes (PPFDcuv), the accumulated C uptake was corrected by multiplying the light use efficiency (LUE) for each shoot with the average incident PPFD of all cuvettes in the WTCs. Light-use efficiency was calculated as



LUE =

Anet PPFD cuv 

(1)

using monthly means of Anet and PPFDcuv. Light-saturated photosynthesis (Asat, µmol CO2 m−2 s−1) was determined as the Anet at light intensities above a threshold of 200 and 400 µmol photons m−2 s−1 in March and April to June, respectively. The selected thresholds were chosen to be the light intensity that decreased the CO2 exchange values by

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