Performance of High Arctic Tundra Plants Improved During but Deteriorated After Exposure to a Simulated Extreme Temperature Event

Global Change Biology (2005) 11, 2078–2089, doi: 10.1111/j.1365-2486.2005.01046.x

Performance of High Arctic tundra plants improved during but deteriorated after exposure to a simulated extreme temperature event

FLEUR L. MARCHAND*, SOFIE MERTENS*, FRED KOCKELBERGH*, LOUIS BEYENSw and IVAN NIJS* *Research Group Plant and Vegetation Ecology, Department of Biology, University of Antwerp (UA), Campus Drie Eiken, Universiteitsplein 1, B-2610 Wilrijk, Belgium, wResearch Group Polar Ecology, Limnology and Paleobiology, Department of Biology, University of Antwerp (UA), Campus Middelheim, Groenenborgerlaan 171, B-2020 Antwerpen, Belgium

Abstract Arctic ecosystems are known to be extremely vulnerable to climate change. As the Intergovernmental Panel on Climate Change scenarios project extreme climate events to increase in frequency and severity, we exposed High Arctic tundra plots during 8 days in summer to a temperature rise of approximately 9 1C, induced by infrared irradiation, followed by a recovery period. Increased plant growth rates during the heat wave, increased green cover at the end of the heat wave and higher chlorophyll concentrations of all four predominating species (Salix arctica Pall., Arctagrostis latifolia Griseb., Carex bigelowii Torr. ex Schwein and Polygonum viviparum L.) after the recovery period, indicated stimulation of vegetative growth. Improved plant performance during the heat

wave was conﬁrmed at plant level by higher leaf photochemical efﬁciency (Fv/Fm) and at ecosystem level by increased gross canopy photosynthesis. However, in the aftermath of the temperature extreme, the heated plants were more stressed than the unheated plants, probably because they acclimated to warmer conditions and experienced the return to (low) ambient as stressful. We also calculated the impact of the heat wave on the carbon balance of this tundra ecosystem. Below- and aboveground respiration were stimulated by the instantaneous warmer soil and canopy, respectively, outweighing the increased gross photosynthesis. As a result, during the heat wave, the heated plots were a smaller sink compared with their unheated counterparts, whereas afterwards the balance was not affected. If other High Arctic tundra ecosystems react similarly, more frequent extreme temperature events in a future climate may shift this biome towards a source. It is uncertain, however, whether these short-term effects will hold when C exchange rates acclimate to higher average temperatures. Keywords: arctic tundra, carbon balance, extreme temperature events, plant performance, stress

Received 20 December 2004; revised version received 31 August 2004 and accepted 17 July 2005

cially because their adaptive capacity is small. Plant Introduction communities in Arctic regions are, therefore, expected In the Arctic, extensive land areas show an observed to be extremely vulnerable to climate change. Responses 20th-century-warming trend in mean annual air tem- can be either direct, or indirect through warming effects perature of as much as 5 1C. Substantial further warming on soil processes (Phoenix & Lee, 2004), and can be is projected over the 21st century by almost all climate expressed in phenology, physiological activity, growth models: increases of 4–5 1C by 2080 are predicted (Call- and species composition (Maxwell, 1992). Plants react to aghan et al., 2004). Physiology and distribution of tundra environmental changes not only by fast short-term plants are highly restricted by the environmentally acclimation, mediated by, among others, diurnal stressful conditions (Bliss & Matveyeva, 1992), espe- changes in metabolic and cell division activities and growth pattern, but also by long-term acclimation in, Correspondence: Fleur L. Marchand, tel. 1 32 3 820 22 82, for example, leaf size and thickness, stomatal density fax 1 32 3 820 22 71, e-mail: ﬂ[email protected] and structure and function of chloroplasts. The latter

2078 r 2005 Blackwell Publishing Ltd PERFORMANCE OF HIGH ARCTIC TUNDRA PLANTS 2079 changes take place within days or weeks and act to at the level of the individual plant (growth rate, chlor- reduce stress constraints (Lichtenthaler, 1996). ophyll ﬂuorescence and chlorophyll content) are re- Most preceding warming experiments have investi- ﬂected at the community scale in green cover and gated effects of higher daily mean temperatures, by species relative abundance. The second objective was imposing limited increments for prolonged periods to assess whether such changes proliferate to alter also

(e.g. the International Tundra Experiment (ITEX), ecosystem carbon exchange (i.e. (i) uptake of CO2 by Henry & Molau, 1997). However, climate projections photosynthesis, (ii) loss of CO2 in belowground respira- suggest also extreme temperature events (e.g. hot days tion and (iii) loss of CO2 in canopy respiration). As and heat waves) to increase in frequency during the tundra ecosystems constitute large stocks of carbon next century (Easterling et al., 2000; Houghton et al., (Schlesinger, 1984; Wookey, 2002), they can attend either 2001), as relatively small changes in mean temperature a positive or negative feedback to climate change. If can result in relatively large changes in event probabil- increasing temperatures induce carbon release, climate ities (Mearns et al., 1984; Wigley, 1985; Karl & Nicholls, warming can be stimulated or vice versa (Oechel et al., 1997). Furthermore, increased temperature variance in a 1998). Factors at ecosystem scale that potentially govern warmer climate, shown by earlier studies (Gregory & the components of the C-balance (soil moisture, thaw- Mitchell, 1995; Zwiers & Kharin, 1998), adds to the ing depth, green cover and senescence) were monitored probability of extreme high-temperature events over during and after the heat wave. and above what could be expected from increases of the mean alone (Katz & Brown, 1992; Meehl et al., 2000). Materials and methods An upward trend in the frequency of extreme heat stress events has been reported in observations in Set-up and environmental measurements various parts of the world (e.g. in the eastern United States (Gaffen & Ross, 1998) and in Russia (Gruza et al., The study site was located in the vicinity of the Zack- 1999)). These changes in probability need to be taken enberg research station on the Northeast coast of Green- into consideration in order to obtain realistic estimates land (741280N, 201340W, 25 m elevation). It is chara- of the impact of climate change (Mearns et al., 1984). cterized by wet tundra with a high species richness Numerous biochemical and biophysical studies have of vascular plants (150) on a well-developed Podzol soil focused on the effects of heat on molecular mechanisms, with continuous permafrost (Meltofte & Thing, 1997). using plant parts or intact plants in chambers or iso- The growing season at Zackenberg lasts approximately lated chloroplasts in vitro (Berry & Bjo¨rkman, 1980). 2 months; mean annual air temperature is 10.4 1C and Such studies have, for example, demonstrated the annual precipitation 215 mm (means for 1961–1990 at synthesis of specific proteins upon heat-shock exposure the nearly station of Daneborg, Danish Meteorological (Howarth, 1991) or have tried to link foliar resistance, Institute). In early July 2001, six tundra plots estimated as membrane electrolyte leakage, to main (40 50 cm2) of similar species composition were se- resource-use characteristics such as leaf specific area, lected on a lower grassland plateau. Living plant cover toughness, N concentration or thickness (Gurvich et al., in the plots was estimated with the pin-frame method, 2002). Research on ecosystem level, has revealed that recording the species with a vertical needle at each extreme events, in spite of their ephemeral nature, can point of a 500-point matrix (40 50 cm2). The dominat- cause shifts in the structure of grasslands (White et al., ing species were Salix arctica Pall., Arctagrostis latifolia 2000, 2001; Van Peer et al., 2001) and other herbaceous Griseb., Carex bigelowii Torr. ex Schwein and Polygonum communities (MacGillivray et al., 1995). However, to viviparum L.; Juncus castaneus Sm. and Dryas spp. were our knowledge no ecological field studies have been subdominant. The six plots were allocated to two treat- carried out on the effects of extreme temperatures on ment groups (three plots each) to have approximately plants in Arctic tundra, the potentially most sensitive similar cover and species composition in both at the biome. In the current study, we exposed plots of High start of the experiment (MANOVA of cover by species,

Arctic tundra vegetation to an experimental heat wave P40.05, F1,5 between 0.001 and 4.000). From 14 to 22 (an 8-day warming with a 9 1C temperature increment) July 2001 (day of the year (DOY) 195–203), three plots at the Zackenberg Station in North-East Greenland. To (one group) were continuously heated with infrared avoid chamber effects from enclosing the plots, the heat irradiation (0.8–3 mm) from three individual FATI units wave was generated using the Free Air Temperature (two 1500 W irradiation sources in a waterproof housing Increase technique (FATI), which was designed to on a tripod) placed on the north side of each plot. homogeneously heat limited areas of short vegetation We aimed at an increment of vegetation temperature by controlled infrared irradiation (Nijs et al., 2000). One (Tvegetation)of91C, the maximum reach of the equip- aim of the study was to investigate whether responses ment (constant flux), to simulate a heat wave. As all r 2005 Blackwell Publishing Ltd, Global Change Biology, 11, 2078–2089 2080 F. L. MARCHAND et al. vegetation was short (o10 cm), the uniformity of leaf cence (Fm). Minimum fluorescence (F0)wasdetermined temperature increase along the vertical profile was from the initial fluorescence upon illumination. From this, guaranteed (Nijs et al., 1996): upper leaves, which PSII photochemical efficiency was calculated as (Fv/ receive higher infrared radiation, are also exposed to Fm 5 (FmF0)/Fm)(Schreiberet al., 1994). Fluorescence larger convective losses from higher windspeeds. The parameters were determined three times a day (at 09:00, control plots had ‘dummy’ units without lamps. In each 14:00 and 19:00 LDT) on each of 9 measurement days (1 plot, noncontact semiconductor sensors (‘infracouple’, before, 4 during and 4 after the heating period) on five type OS39-MVC-6, Omega Engineering, Stamford, CT, leaves per species (S. arctica, A. latifolia and C. bigelowii)

US) measured Tvegetation, while soil temperature (Tsoil)at per plot. 2.5, 7.5, 15 and 30 cm depth and air temperature (Tair)at 5 cm height were measured with NTC-thermistors CO exchange (EC95, Thermometrics, Edison, NJ, US). A gallium- 2 arsenide sensor (JYP-1000, SDEC, Reignac Sur Indre, We used a closed infrared gas analyzing system France) fixed in an open space near the site measured (CIRAS, PPSystems, Hitchin, Hertfordshire, UK) with photosynthetically active radiation (PAR). These data either a 40 50 cm2 (the size of the plots) rectangular were recorded with loggers (16 kb, 12 bit, eight-channel; acrylate chamber to measure net ecosystem CO2 ex- DL2E, Delta T, Cambridge, UK) once every 30 min from change rate (CERecosystem), or an 8 cm tall, 0.17 L cylind- 12 July 20:00 hours until 1 August 12:00 hours local rical polyvinyl chloride chamber to measure daylight time (LDT), so both during and after the heat belowground respiration (Rsoil). The latter chamber wave. Soil volumetric water content and thawing depth was placed on 5 cm-diameter, 7 cm-high collars. Two were measured simultaneously, nine times between 13 collars were placed per plot, on bare spots free of July (DOY 194) and 2 August (DOY 214) (one reading vascular plants, although some of them contained some per quadrant per plot), with time domain reflectometry moss. As flux data were not collected continually, the (Trime-FM, Eijkelkamp Agrisearch Equipment, Gies- carbon balance was reconstructed by interpolating the beek, The Netherlands; accuracy 3%) over the upper three components (gross photosynthesis (Pgross), Rsoil 11 cm soil horizon and a fiberglass rod of 5 mm dia- and canopy respiration (Rcanopy)) individually. To this meter, respectively. end, net ecosystem CO2 exchange was measured con- secutively in ambient PAR (CERecosystem) and in the dark (CER ) in each plot, on 9 days between 13 Plant measurements ecosystem, dark July and 2 August 2001, generally from 09:00 until 20:00 Cover readings of living plants (by species), litter, moss hours LDT to have a range in PAR conditions. With and bare soil were taken with the aforementioned pin- CERecosystem, dark 5 Rsoil 1 Rcanopy, Rcanopy could be de- frame method three times during the experiment: at the termined by subtracting Rsoil from CERecosystem, dark.As start, directly after the heat wave and 2 weeks later. CERecosystem 5 Pgross 1 CERecosystem, dark, Pgross could be Parallel, leaf length was measured in A. latifolia and determined by subtracting CERecosystem, dark from C. bigelowii to determine average plant growth rate in CERecosystem. The gross photosynthesis values recorded the heating and the recovery period. S. arctica and P. on a given day were fitted as a function of PAR: viviparum were not monitored as these species had aPgross;maxPAR Pgross ¼ ; ð1Þ stopped growing before the onset of the experiment. aPAR þ Pgross;max The measurements were carried out on five plants per a species per plot that had newly appearing leaves, and with stand-level quantum yield and Pgross, max asymp- a subsequent leaf initiation was taken into account to totic Pgross at infinite PAR. The resulting and Pgross, max calculate absolute plant growth rate (length increase of values for each measurement day were fitted as a all leaves combined). Leaf chlorophyll a and b concentra- function of time (polynomial) to reconstruct the time tions of the four dominating species (analyzed with the course of instantaneous Pgross from instantaneous PAR dimethylformamide method (Porra et al., 1989) on freeze- over the whole period. The Rsoil and Rcanopy readings, dried material) were determined at six samples per on the other hand, were each pooled across all measure- species per plot at the end of the experiment on DOY ment times and fitted as a function of Tsoil at 2.5 cm 215, as this method is destructive. To quantify the level of depth or Tair at 5 cm height, respectively: Tair10=10 stress induced by the heat wave, chlorophyll fluorescence Rsoil ¼ R10Q10 ; ð2Þ was measured with the Plant Efficiency Analyzer (Han- R ¼ R QTair10=10 ð3Þ satech Ltd., Cambridge, UK) in leaves pre-darkened for canopy 10 10

30 min. Leaves were exposed to a saturating pulse with R10 respiration rate at 10 1C and Q10 temperature- 2 1 (43000 mmol m s ) for 1 s, yielding maximum ﬂuores- sensitivity of respiration. Time courses of Rsoil and

r 2005 Blackwell Publishing Ltd, Global Change Biology, 11, 2078–2089 PERFORMANCE OF HIGH ARCTIC TUNDRA PLANTS 2081

Rcanopy were then reconstructed from instantaneous Tsoil beginning to 52.1 SE 0.8 and 57.7 SE 0.5 cm at the and Tair, respectively, over the whole period. end of the heating period in control and heated plots, respectively, reaching 55.6 SE 0.6 and 60.7 SE 0.7 cm by the end of the recovery period (RM-ANOVA, Statistical analysis Po0.05, F1,22 5 25.951). This corresponds with an aver- All analyses were conducted with SPSS 10.0. Kolmogor- age increase in active layer thickness during the heating ov–Smirnov and Shapiro–Wilkinson tests were used to period in the heated plots of 9.0 mm day1, which was test for normality. Effects of and interactions between much smaller in the control plots and during recovery factors were tested with univariate or multivariate in all plots (between 2.5 and 3.9 mm day1). Hence, analyses of variance (ANOVA, MANOVA,orANCOVA with stimulation of thawing was mainly limited to the heat a covariate). Data gathered on the same plots on differ- wave itself. Mean soil moisture content in the heated ent days, were analyzed with repeated-measures ANOVA plots (38.4%), on the other hand, did not differ signifi- (RM-ANOVA) with DOY as within-subject factor and treat- cantly from its unheated counterparts (35.9%, RM-ANOVA, ment as between-subject factor. We tested sphericity P40.05, F1,22 5 2.494). with Mauchly’s test; if violated we used the conservative Greenhouse–Geisser correction if the latter led to Plant measurements the same decision as the Huyhn–Feldt correction (Field, 2000). Otherwise, the correction with the same decision The heat wave induced a significant expansion of total as the average of the two significance values was used plant cover (plant cover was equal at the onset, MANOVA,

(Field, 2000). For post hoc multiple comparisons between P40.05, F1,4 5 0.175), while no expansion occurred in observed means, the conservative Bonferonni or Tukey the control plots (Fig. 1b, RM-ANOVA, Bonferroni test highly significant digit (HSD) tests were used. Multiple between DOY 191 and 202, Po0.05 and P40.05 for measurements from different plots were considered heated and unheated plots, respectively). After the replicates, as plot effects were absent. Various types of recovery period, again no difference in cover was ob- nonlinear regression were applied to fit dependent served between treatments (MANOVA, P40.05, variables to time. F1,4 5 0.006). In other words, the difference realized by the end of the heat wave (MANOVA, Po0.05, F1,4 5 8.304) was dissolved during the recovery period by a smaller Results growth rate and/or a higher mortality in heated plots (RM-ANOVA, Bonferroni test between DOY 191 and DOY Environmental measurements 215, Po0.05 and P40.05 for unheated and heated plots, Average July air temperatures recorded by the monitor- respectively). Interaction between species and treat- ing program of Zackenberg (Climatebasis) between its ment was not significant (RM-ANOVA, P40.05, start in 1996 and 2002 ranged from 3.7 to 6.2 1C. The July F7,32 5 0.560), so the species did not respond differently temperature of 2001, 4.9 1C, falls in this range, so the to the extreme event (Fig. 1c). In line with these cover background thermal conditions during the experiment changes, average plant growth rate during the heating were close to average. During the warming, the FATI period was significantly greater in the warmed plots in system increased Tvegetation on average 9.2 SD 3.3 1C both species measured (Fig. 2a; MANOVA, Po0.05, above the mean of 7.7 SD 3.8 1C in the unheated plots. F1,27 5 36.321 and 4.931 for A. latifolia and C. bigelowii, This delta-T raised the peak temperatures in the heated respectively), as a consequence of increased leaf size. plots (Fig. 1a) to values that were close to the maximum However, this growth response reversed during the temperatures recorded in summer at Zackenberg be- recovery period, although only significantly in A. lati- tween 1996 and 2002 (between 18.8 and 24.5 1C, Clima- folia (MANOVA, Po0.05, F1,27 5 4.303). Leaves from plots tebasis program). We used past extremes as a reference exposed to the heat wave had significant higher chlor- to set the intensity of the extreme event in the current ophyll a and b concentrations at the end of the recovery study. However, the vegetation was exposed to pro- (all species, Fig. 2b, MANOVA, F1,136 5 25.507 and 23.793, longed heating (8 days) relative to the warm periods for chlorophyll a and b, respectively). observed during 1996–2002, in order to simulate in- Before the heating (DOY 193), mean Fv/Fm varied creased severity of extremes in a future climate. with species (ANOVA, Po0.05,F2,252 5 8.030) and time Soil temperatures were raised 7.6 SD 1.5, 6.4 SD of the day (Po0.05, F2,252 5 3.857), but not between 1.4, 4.8 SD 1.3 and 2.5 SD 0.9 1C at 2.5, 7.5, 15 and treatment groups (P40.05, F1,252 5 1.005). Values were 30 cm depth, respectively. Mean thawing depth aug- lower in the evening and in C. bigelowii relative to the mented significantly faster under the simulated warm- other two species (Tukey HSD). To assess stress levels ing from 49.0 SE 0.8 and 50.6 SE 0.9 cm at the during the experiment, we calculated separate ANOVAs r 2005 Blackwell Publishing Ltd, Global Change Biology, 11, 2078–2089 2082 F. L. MARCHAND et al.

Heat wave 30 (a) (b) 75

C) 25 ° 60 ( 20 45

vegetation 15 T 30 10 Average Total plant cover (%) 15 5

0 0 194 196 198 200 202 204 190 195 200 205 210 215 DOY DOY (c) 35

15 Cover (%)

0 berberberberberberber Salix Arctagrostis Carex Polygonum Mosses Bare soil Litter arctica latifolia bigelowii viviparum

Fig. 1 (a) Average vegetation temperature (Tvegetation) during the simulated heat wave from day of the year (DOY) 195 to DOY 203 in three heated ( ) and three unheated plots ( ). (b) Time course of total living plant cover (all species combined) during the experiment determined from pin-frame measurements. Means 1 SE and ﬁtted polynomial curve (second order) for the unheated () and heated ( ) treatment. (c) Percentage cover of living vascular plants (by species), mosses, bare soil and litter before (b, DOY 190) and at the end of the heat wave (e, DOY 202), and at the end of the recovery period (r, DOY 215). Average 1 SE of three heated ( & ) and three unheated (&) plots.

of Fv/Fm for the heating and recovery periods with ANOVA, P40.05, F1,15 5 1.145), increased signiﬁcantly factors treatment, DOY, species and time of day (Table during the heat wave, to become equal to the controls

1). The heat wave significantly increased Fv/Fm during again in the recovery period (Fig. 4a and b, Table 2). We, exposure in all species almost immediately (Tukey HSD therefore, fitted Pgross to PAR on every measurement between DOY 194 and DOY 196, Po0.05 and P40.05 day (Eqn (1)) separately for the control and heated for heated and unheated plots, respectively), similar to plots. The Pgross, max and a values derived from these the growth measurements, this reversed during the curves, were in turn fitted as a function of DOY (not recovery period (Fig. 3, Table 1), where the previously shown, third-order polynomials) to reconstruct Pgross heated plants became more stressed. Treatment effects from PAR over the entire period (heat wave and recov- during the heat wave compensated for a declining Fv/ ery). For a, a single time course was used for both Fm in the controls (significant treatment DOY interac- treatments combined, as quantum yield did not differ tion, Table 1, Fig. 3). between the heated and the unheated plots (ANOVA,

P40.05,F1,15 5 1.283). Pgross, max, on the other hand, was ﬁtted separately to DOY by treatment, as it was CO exchange 2 signiﬁcantly greater in the warmed plots during the

Gross photosynthetic capacity, which did not differ heating period (ANOVA, Po0.05,F1,5 5 6.949). The recon- between treatments prior to the experiment (DOY 194, structed Pgross yielded cumulative values of 4.28 and

r 2005 Blackwell Publishing Ltd, Global Change Biology, 11, 2078–2089 PERFORMANCE OF HIGH ARCTIC TUNDRA PLANTS 2083

(a) 4.0 (b) 1600 )

1 3.5 −

3.0 1200

2.5

2.0 800 fresh matter) 1

1.5 − g

1.0 µ ( 400 Chlorophyll concentration

Plant growth rate (mm day 0.5

0.0 0 Heat wave Recovery Heat wave Recovery abababab Arctagrostis Carex Salix Arctagrostis Carex Polygonum latifolia bigelowii arctica latifolia bigelowii viviparum

Fig. 2 (a) Average plant growth rate (length increase of all leaves combined) in Arctagrostis latifolia and Carex bigelowii during the heating and recovery period. Means 1 SE of 15 plants per species (ﬁve per plot) in the heated ( & ) and unheated (&) treatment. Average leaf length at the start of the experiment was 12.1 0.9 SE and 11.2 1.6 SE for A. latifolia and 13.4 2.8 SE and 11.1 2.3 SE for C. bigelowii in unheated plots in heated plots, respectively. (b) Leaf chlorophyll a and b concentration of four dominating species at the end of the recovery period (day of the year 215). Means 1 SE of 18 samples per species (six per plot) in both the heated ( & ) and the unheated (&) treatment.

Table 1 F-values of ANOVAs (heating or recovery period) of PSII photochemical efﬁciency (Fv/Fm)inSalix arctica, Arctagrostis latifolia and Carex bigelowii, with heat wave treatment, day of the year (DOY), species and time of day as between-subject factors

Heating period Recovery period

Treatment 14.43* F1,1008 5 16.657*** DOY 5.518** F3,1008 5 15.816*** Species 72.417*** F2,1008 5 6.699*** Time of day 0.485 F2,1008 5 16.118*** Treatment DOY 0.631 F3,1008 5 7.384*** Treatment species 0.096 F2,1008 5 2.720 Treatment time of day 0.994 F2,1008 5 1.892 Treatment species DOY 0.265 F6,1008 5 0.698 Treatment time of day DOY 1.112 F6,1008 5 4.594*** Treatment species time of day 0.344 F4,1008 5 0.629 Treatment species time of day DOY 0.449 F12,1008 5 0.694 DOY species 0.468 F6,1008 5 1.184 DOY time of day 0.229 F6,1008 5 5.449*** DOY species time of day 0.518 F12,1008 5 0.612 Species time of day 0.339 F4,1008 5 0.315

*Po0.05; **Po0.01; ***Po0.001. r 2005 Blackwell Publishing Ltd, Global Change Biology, 11, 2078–2089 2084 F. L. MARCHAND et al.

Salix arctica curve (Eqn (2)) for both heated and control plots over Heat wave 0.85 the entire experimental period. We next veriﬁed 0.80 whether the Rsoil variation not explained by the model could be ascribed to other factors, such as soil moisture, 0.75 thawing depth, effects of DOY or green cover. None m

/F 0.70 of these factors explained a signiﬁcant fraction v

F of the variation of the calculated residuals (Rsoil,observed 0.65 Rsoil,ﬁtted). Belowground respiration was, therefore, 0.60 reconstructed from Tsoil only; this revealed a doubling of cumulative CO2 emission during the 8-day-long 0.55 2 192 196 200 204 208 212 216 heating period (1.82 mol CO2 m relative 0.92 mol 2 DOY CO2 m ), but little difference during the 12-day-long 2 recovery period (1.34 relative to 1.39 mol CO2 m ). Arctagrostis latifolia Canopy respiration, which was governed by Tair, was 0.85 Heat wave not altered by the warming treatment either when 0.80 compared at the same temperature, nor did DOY and treatment interact (Table 2, Fig. 4d). For these reasons, 0.75 we created one Rcanopy–Tair relationship (Eqn (3)) for the m

/F 0.70 control and the heated plots combined, as a basis for v

F reconstructing canopy CO2 efﬂux. Also in this case the 0.65 residuals did not depend on DOY, green cover, soil

0.60 moisture or thawing depth. The reconstructed Rcanopy 2 yielded total carbon losses of 1.45 and 1.68 mol CO2 m 0.55 during the 8-day-long heating period, and 2.35 and 192 196 200 204 208 212 216 2 DOY 2.32 mol CO2 m during the 12-day-long recovery period, for control and heated plots, respectively. Carex bigelowii Figure 5a reconstructs the time course of daily aver- 0.85 Heat wave age CERecosystem. Our tundra ecosystem was a sink for 0.80 carbon under both treatments, but a smaller one (44.0%) during the heat wave in the heated plots, where the 0.75 increase of below- and aboveground respiration out- m weighed the stimulation of photosynthesis (Fig. 5b). By /F 0.70 v

F regressing the observed instantaneous CERecosystem on 0.65 the modeled instantaneous CERecosystem (derived from 0.60 separately modeled Pgross, Rsoil and Rcanopy), we tested the accuracy of the reconstruction. As the regression 0.55 was linear, the slope close to 1, the offset negligible 192 196 200 204 208 212 216 5 DOY (y 0.99x0.025) and the coefficient of determination high (r2 5 0.88), deviations between observed and mod- Fig. 3 Time course of PSII photochemical efficiency (Fv/Fm)in eled fluxes were limited. three dominating species. Averages 1 SE of 15 readings (five per plot) for morning (09:00 hours), noon (14:00 hours) and evening (19:00 hours) in the heated () and the unheated () Discussion treatment. DOY, day of the year. The negative connotation associated with climatic extremes raises the expectation they will compromise 2 4.61 mol CO2 m during the 8-day-long heat wave per- ecosystem functioning. However, in our experiment 2 iod, and 6.34 and 6.47 mol CO2 m during the 12-day- the increased plant growth rates during the heat wave, long recovery period, for control and heated plots, the increased green cover at the end, and the higher respectively. chlorophyll concentrations after the recovery period,

A relationship between Rsoil and Tsoil could be clearly clearly indicate that limitations of vegetative growth distinguished during the heat wave, but not during the were alleviated. As Fv/Fm prior to the extreme event was recovery because of a too narrow Tsoil range (Table 2, below the value of 0.83 (maximum Fv/Fm, Bjorkman & Fig. 4c). As the warming treatment did not alter this Demmig, 1987), the plants were stressed from the start, relationship (Table 2), we constructed a single Rsoil–Tsoil especially at the end of the day. The marked rise in

r 2005 Blackwell Publishing Ltd, Global Change Biology, 11, 2078–2089 PERFORMANCE OF HIGH ARCTIC TUNDRA PLANTS 2085

(a) 16 (b) 16

14 14 2 ) ) 1 1 − − s

s 3

12 12 2 2 1 − − m m

10 10 2 2

8 8 mol CO mol CO µ µ 6 6 ( (

4 4 gross gross P P 2 2

0 0 0 200 400 600 800 1000 1200 0 200 400 600 800 1000 1200 PAR (µmol photons m−2 s−1) PAR (µmol photons m−2 s−1)

5 ) 5 1 ) − 1 s −

s 2

− 2

− 4 4 m

m 2

2 3 3 mol CO µ mol CO (

µ (

2 2 soil R canopy

1 P 1

− y = 2.33±SE 0.06×2.60±SE 0.15 (( x-10 ) /10) y = 2.71±SE 0.07×1.64±SE 0.13 (( x 10 ) /10) 0 0 0 5 10 15 20 0 5 10 15 20 ° ° Tsoil ( C) Tair ( C)

Fig. 4 (a) Measured gross canopy photosynthesis (Pgross) of tundra vegetation ﬁtted (Eqn (1)) to incident photosynthetically active radiation (PA R ) in ambient conditions ( , ) or during a simulated heat wave ( , ) on day of the year (DOY) 200. (b) Curves

ﬁtted (Eqn (1)) to Pgross, from unheated ( ) and heated plots ( ) on 3 characteristic days during the experiment; 1: DOY 194 (before the start of the heat wave), 2: DOY 200 (near the end of the heat wave), 3: DOY 205 (during the recovery period). (c) Belowground respiration (Rsoil) as a function of soil temperature (Tsoil) at a depth of 2.5 cm. (d) Aboveground respiration (Rcanopy) as a function of air temperature (Tair) at 5 cm height. (c) and (d): pooled measurements for control () and heated () plots over all measurement days (heat wave and recovery) and ﬁtted curve (Eqns (2) and (3), respectively).

Fv/Fm in response to the heat wave indicates that cold acclimation (Koroleva, 1996). The weather during warming diminished these stress levels. This improved our experiment (July 2001) being close to average condition at plant level and the increased photosynth- excludes the possibility that the simulated heat wave esis at ecosystem level in the heated plots may seem merely compensated for exceptionally adverse local remarkable as arctic plants are generally well adapted conditions. In other words, high arctic tundra seems to growth at low temperatures (Chapin, 1983, 1987). For to function well below the optimum in average years. example, they have a lower optimum temperature for Subsequently, the question arises whether, in arctic photosynthesis than temperate species and are rela- plants, heat extremes generally enhance temperatures tively insensitive to a wide range around it (Semikha- above the optimum, where activity declines rapidly tova et al., 1992). However, optimum temperatures in in temperate species (Taiz & Zeiger, 1991; Seddon & arctic plants are usually still higher than the mean Cheshire, 2001). In the current study, critical tempera- summer temperatures in Arctic regions (Tieszen et al., tures were in any case not exceeded, as no damage 1981). For example, the arctic–alpine Oxyria digyna even symptoms were observed during exposure. This may be photosynthesizes maximally around 28 1C, regardless of attributed in part to the observed lack of soil drought. r 2005 Blackwell Publishing Ltd, Global Change Biology, 11, 2078–2089 2086 F. L. MARCHAND et al.

Table 2 F-values of univariate ANCOVAs (heating or recovery Fv/Fm in the heated plants declined below that in the period) of gross canopy photosynthesis (Pgross), belowground plants not exposed to the heat wave, suggesting that respiration (Rsoil) or canopy respiration (Rcanopy), with day of protective mechanisms against the cold, which also the year (DOY) and heat wave treatment as factors and operate during the relatively warm summer, had di- photosynthetically active radiation (PAR), soil temperature minished. In the study of Koroleva (1996), cold acclima- (T ) and air temperature (T ) as covariate, respectively soil air tion in the arctic species O. digyna was expressed as Heating period Recovery period greater leaf thickness and a reduced leaf size, which affords the plant the opportunity to avoid the cooling Pgross and desiccation associated with cold winds (Nilsen & PAR F 1,71 5176.365*** F1,71 5 252.229*** Orcutt, 1996). In our study, the unheated plants (A. Treatment F1,71 5 8.269** F1,71 5 0.422 latifolia and C. bigelowii) had indeed smaller leaves DOY F3,71 5 2.422 F3,71 5 3.182* and associated reduced plant growth rates. Cold-accli- Treatment DOY F3,71 5 0.734 F3,71 5 0.177 mated plants may also exhibit biochemical protective R soil mechanisms. For example, a higher concentration of Tsoil F1,49 5 7.268* F1,39 5 1.428 zeaxanthin, through inhibition of its epoxidation, is Treatment F 5 0.960 F 5 1.805 1,49 1,39 thought to reduce sensitivity to photoinhibition (Dem- DOY F 5 2.209 F 5 5.555** 4,49 3,39 mig-Adams & Adams, 1992). At low temperatures, the Treatment DOY F4,49 5 0.896 F3,39 5 0.094 latter can already be induced by moderate light inten- Rcanopy sities (Somersalo & Krause, 1989). In spinach, increased Tair F1,69 5 72.668*** F1,65 5 23.779*** activities of superoxide dismutase, ascorbate peroxi- Treatment F1,69 5 0.537 F1,65 5 0.003 dase and monodehydro-ascorbate reductase have been DOY F3,69 5 3.431* F3,65 5 2.437 Treatment DOY F3,69 5 0.720 F3,65 5 0.054 observed during cold acclimation (Schoner & Krause, 1990); these enzymes deactivate the activated oxygen *Po0.05; **Po0.01; ***Po0.001. forms that accumulate during photoinhibition. Also, changes in the activity of Calvin cycle enzymes have been reported during low-temperature acclimation in Seddon & Cheshire (2001) found that higher tempera- this species (Holaday et al., 1992). We surmise that such tures alone had minimal influence on chlorophyll fluor- acclimations may have been lost during the heat wave escence in Amphibolis antarctica and Posidonia australis; in the current experiment, inducing the stress during the heat applied in this experiment only induced photo- the recovery. The fact that the cover difference created synthetic inhibition and photodamage if combined with by the heat wave had completely disappeared 2 weeks desiccation. More research is needed to establish the later (Fig. 1b), indicates that the increased stress levels thresholds of heat stress tolerance or heat stress resis- during the recovery period were more important than tance in arctic plants and the extent to which desiccation Fig. 3 suggests, and probably even led to enhanced lowers these thresholds. In spite of the fact that the mortality. critical temperature range was not reached in our plots, In controlled environments, tundra species almost the observed response pattern nevertheless suggests invariably grow faster in a warmer microclimate (Shaver that temperatures were raised above the optimum. In & Kummerow, 1992). In field experiments, on the other fact, the improved performance of the plants during the hand, responses vary (Chapin & Shaver, 1985). Field heat wave (both plant and community scale) is compa- responses reflect the combined effect of direct influ- tible with ‘eu-stress’, a mild form of stress that activates ences of warming and factors correlated with warming cell metabolism and increases physiological activity. such as enhanced mineralization or reduced soil moist- This type of stress does not cause any damage even ure, which are difficult to distinguish (Chapin, 1983, upon prolonged exposure and often results in acclima- 1987). In addition, novel indirect effects might arise tion or adaptation (Lichtenthaler, 1996). The fact that from interspecific competition in a warmer climate, damage (reduced growth) was observed during the which was previously considered as being overruled recovery is in agreement with this, as plants that have by the extreme arctic environment (Dormann et al., acclimated to significantly warmer conditions such as 2004). In our study, the short-term growth stimulation the heat wave imposed here, may experience the return in A. latifolia and C. bigelowii during the heat wave, and to (low) ambient as stressful. Had temperatures been its disappearance when warming was stopped, indicate raised only up to the optimum, clearly no such stress that the effects were direct. Similar patterns observed at response would have occurred. The Fv/Fm readings lend ecosystem scale in gross photosynthesis and below- and further support to this hypothesis. When high tempera- aboveground respiration, support this assumption. tures fell to ambient again during the recovery period, Temperature extremes are probably too short to cause

r 2005 Blackwell Publishing Ltd, Global Change Biology, 11, 2078–2089 PERFORMANCE OF HIGH ARCTIC TUNDRA PLANTS 2087

Heat wave (a) (b) 1 4 HRHRHRHR 0.5 3 DOY 2 0 ) ) 1 1 1

190 195 200 205 210 215 − − − s

s 0.5 2 2 0 − − m

m −

1 −1 2 2 −1.5 −2 −3

− mol CO mol CO 2 µ µ − ( 4 −2.5 −5 CER ( CER − 3 −6 −3.5 −7

−4 −8 Pgross Rsoil Rcanopy Total

Fig. 5 (a) Reconstructed time course of daily average net CO2 exchange rate (CERecosystem) during the experiment. DOY, day of the year.

(b) Average net CO2 exchange rate (CER), separated into its three components: gross canopy photosynthesis (Pgross), belowground respiration (Rsoil) and canopy respiration (Rcanopy), during the heat wave (H) and recovery (R) period. Values in (a) and (b) are averages & for the three control plots (, &) and the three heated plots (, ). Positive values are CO2 release.

indirect effects, which is consistent with the hypothesis global greenhouse effect (Raich & Schlesinger, 1992). of Shaver & Kummerow (1992), that direct responses of However, the increased mean temperatures, associated plants to a change in air temperature will be prior and with a future climate, will probably result in acclima- rapid, while later indirect responses may be limited by tion of respiratory C exchange rates, as has been seen in the rate of change in other variables. The warming was other ecosystems (Larigauderie & Ko¨rner, 1995; Enquist apparently also too ephemeral to affect the Q10 of et al., 2003). The observed short-term effects of the heat belowground respiration, which tends to be tempera- wave on the carbon balance (increased soil respiration ture and/or soil moisture dependent according to re- which outweighed increased photosynthesis) might, cent evidence (Tjoelker et al., 2001; Janssens & Pilegaard, therefore, not hold when plants are continuously ex- 2003). posed to elevated temperatures. Further research is Previous soil warming studies, mostly from tempe- needed to ascertain whether actual feedback to climate rate sites and during an entire growing season, have change is induced. demonstrated that soil respiratory losses and plant productivity increase at about the same rate (Rustad et al., 2001). Accordingly, in an earlier experiment at our Acknowledgements current tundra site, where vegetation temperature was We thank the Danish Polar Centre for providing access to and increased 2.5 1C during the snow-free season, the turn- logistics at the research station at Zackenberg under the frame- over of the carbon balance components was increased work program ZERO. This study was supported by the Fund for although the balance was not altered (Marchand et al., Scientific Research-Flanders (F.W.O., Belgium) under contract G.0086.98. 2004). The heat wave simulation in the present study reveals that, contrary to mild but continuous warming, short peak-temperature periods can shift the carbon References balance toward a smaller sink (Fig. 5). The respiratory fluxes were responsible for this, as together they were Berry J, Bjo¨rkman O (1980) Photosynthetic response and adapta- stimulated to a greater extent than photosynthesis, the tion to temperature in higher plants. Annual Review of Plant Physiology, 31, 491–543. largest component of the carbon balance. The shift Bjorkman O, Demmig B (1987) Photon yield of O evolution and could primarily be ascribed to belowground respira- 2 chlorophyll fluorescence characteristics at 77 K among vascu- 5 tion, which increased more (Q10 2.60) than canopy lar plants of diverse origins. Planta, 170, 489–504. respiration (Q10 5 1.64). If other High Arctic tundra Bliss LC, Matveyeva NV (1992) Circumpolar arctic vegetation. ecosystems react similarly, more frequent heat waves In: Arctic Ecosystems in a Changing Climate – an Ecophysiological in a future climate may, therefore, shift this biome Perspective (eds Chapin FS, Jefferies RL, Reynolds JF, Shaver toward a source and induce positive feedback in the GR, Svoboda J), pp. 59–89. Academic Press, California. r 2005 Blackwell Publishing Ltd, Global Change Biology, 11, 2078–2089 2088 F. L. MARCHAND et al.

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