Ecosystems DOI: 10.1007/s10021-010-9361-2 2010 Springer Science+Business Media, LLC

Responses of Vegetation and Ecosystem CO2 Exchange to 9 Years of Nutrient Addition at Mer Bleue

Sari Juutinen,1,3* Jill L. Bubier,1 and Tim R. Moore2

1Environmental Studies Program, Mount Holyoke College, 50 College Street, South Hadley, Massachusetts 01075, USA; 2Department of Geography, McGill University, 805 Sherbrooke St. W, Montreal, Quebec H3A 2K6, Canada; 3Department of Forest Sciences, University of Helsinki, P.O. Box 27, 00014 Helsinki, Finland

ABSTRACT

Anthropogenic nitrogen (N) loading has the poten- mum ecosystem photosynthesis (Pgmax) and net CO2 tial to affect plant community structure and func- exchange (NEEmax) were lowered (-19 and -46%, tion, and the carbon dioxide (CO2) sink of peatlands. respectively) in the highest NPK treatment. In the Our aim is to study how vegetation changes, induced following years, while shrub height increased, the by nutrient input, affect the CO2 exchange of a vascular foliar biomass did not fully compensate for nutrient-limited bog. We conducted 9- and 4-year the loss of moss biomass; yet, by year 8 there were no fertilization experiments at Mer Bleue bog, where significant differences in Pgmax and NEEmax between we applied N addition levels of 1.6, 3.2, and the nutrient and the control treatments. At the same 6.4 g N m-2 a-1, upon a background deposition of time, an increase (24–32%) in ecosystem respiration about 0.8 g N m-2 a-1, with or without phosphorus (ER) became evident. Trends in the N-only experi- and potassium (PK). Only the treatments 3.2 and ment resembled those in the older NPK experiment -2 -1 6.4 g N m a with PK significantly affected CO2 by the fourth year. The increasing ER with increas- fluxes. These treatments shifted the Sphagnum moss ing vascular plant and decreasing Sphagnum moss and dwarf shrub community to taller dwarf shrub biomass across the experimental plots suggest that thickets without moss, and the CO2 responses de- high N deposition may lessen the CO2 sink of a bog. pended on the phase of vegetation transition. Overall, compared to the large observed changes in Key words: atmospheric nitrogen deposition; the vegetation, the changes in CO2 fluxes were peatland; carbon; N; P; K; net ecosystem exchange; small. Following Sphagnum loss after 5 years, maxi- Sphagnum; Polytrichum strictum; shrubs.

INTRODUCTION to N release from combustion and agriculture. The excess of reactive N has the potential to enhance Atmospheric nitrogen (N) deposition has been plant productivity and alter vegetation composi- elevated in industrialized and populated areas due tion, because N is often the limiting plant nutrient. Therefore, it has been speculated that N deposition Received 23 December 2009; accepted 23 June 2010 could enhance CO2 uptake from the atmosphere Author contributions: SJ conducted the research and analyzed the into ecosystems (Gruber and Galloway 2008; data. JLB and TRM conceived the study and conducted the research, and all three wrote the paper. LeBauer and Treseder 2008). Peatlands have *Corresponding author; e-mail: [email protected] accumulated vast amounts of carbon (C) (Gorham S. Juutinen and others

1991), yet the annual C balance of a peatland is 2007) showed an initial trend of increasing eco- often a very small difference between plant pro- system CO2 uptake in high N [with phosphorus (P) duction and decomposition (for example Alm and and potassium (K)] treatments, which reversed others 1999; Roulet and others 2007). Ombro- after 5 years when the Sphagnum and sparse dwarf trophic are the most nutrient-limited types of shrub community was replaced by a dense shrub peatlands as they receive inputs only from the community having a lower photosynthetic capac- atmosphere (Rydin and Jeglum 2006). The key is- ity. By continuing the study, we wanted to inves- sues are how elevated atmospheric N deposition tigate (1) whether the lower photosynthetic affects the peatland plant communities and whe- capacity and lower net exchange of CO2 were only ther it will increase or decrease the CO2 sink transitional features, and (2) how the change in the function of peatlands. relative contribution of different plant functional Turunen and others (2004) have suggested that groups impacts ecosystem CO2 exchange. elevated N deposition ranging up to 0.8 g N m-2 In this article, we explore the temporal changes in -1 a could have increased C accumulation during vegetation composition and ecosystem CO2 fluxes the last 50 years in ombrotrophic bogs in eastern in a temperate bog, with plots fertilized for Canada. On the other hand, experimental and 8–9 years with N and NPK, and for 4 years with N gradient studies show that deposition higher than only. We investigated the statistical relationships -2 -1 1gNm a influences vegetation composition between vegetation characteristics and CO2 fluxes. in the most nutrient-poor sites, poor fens and bogs, Our hypotheses, following the previous study of and may reduce C accumulation. Typical responses Bubier and others (2007), were that increases in include a reduction in Sphagnum moss abundance dwarf shrub growth would continue in the and invasion or increased abundance of vascular communities affected by the highest fertilization plant species (Heijmans and others 2001; Vitt and treatments, but that increases in ecosystem photo- others 2003; Tomassen and others 2004; Bragazza synthesis would remain small, because a part of the and others 2004; Bubier and others 2007; Limpens new production would be allocated to woody, non- and others 2008). This change may reduce the C photosynthetic tissue. We also hypothesized an in- sequestration in peatlands as Sphagnum mosses are crease in ecosystem respiration because of increas- substantial builders through their slow ing shrub biomass and a change in the quality of decomposition, compared to vascular plant tissues substrates for decomposition, from dominantly (Clymo and Hayward 1982; Aerts and others 1999; Sphagnum moss to more easily decomposable shrub Malmer and others 2003; Turetsky 2003; Moore litter, in these altered communities. and others 2007). The coexistence of mosses and vascular plants in bogs is in balance when the moss surface traps the low atmospheric nutrient supply MATERIALS AND METHODS and conversely, shading and litterfall by vascular Study Site and Experimental Set-Up plants hamper moss growth. The balance can be shifted through a process in which saturation of the This study was conducted at Mer Bleue bog near moss layer with N allows more N uptake by vas- , , Canada (4540¢N, 7550¢W) with cular plants (Baxter and others 1992; Heijmans and a cool continental climate and a mean annual others 2001; Limpens and Berendse 2003; Malmer temperature of 6.0C, and mean annual precipita- and others 2003; Bragazza and others 2004; Bubier tion of 944 mm (Canadian Climate Normals 1971– and others 2007). 2000). The experimental site is located in the The general responses of bog vegetation to in- ombrotrophic part of the peatland, where vegeta- creased N deposition are quite well known on the tion is dominated by dwarf shrub species Cham- basis of experiments and long-term monitoring; but aedaphne calyculata Moench, Ledum groenlandicum few studies have assessed the effects of nutrient Oeder, Vaccinium myrtilloides Michx. and Kalmia addition on ecosystem CO2 exchange in nutrient- angustifolia L., and peat mosses Sphagnum magellan- poor peatlands (Saarnio and others 2003; Bubier icum Brid. and Sphagnum capillifolium (Ehrl.) Hedw. and others 2007; Gerdol and others 2008; Lund and Polytricum strictum Brid. is a common, but less others 2009). Most studies have spanned only a abundant, moss. Average aboveground biomass few years, but longer monitoring can show delayed including living moss is about 590 g m-2 (Bubier effects. Nutrient addition may trigger an ecosystem and others 2006). Onset of photosynthesis typically transition, where vegetation changes may not be- occurs soon after the disappearance of snow at the come evident for several years (Wiedermann and end of March to early April, and net CO2 exchange others 2009). Our earlier study (Bubier and others turns to ecosystem loss by November. The bog has Responses of Bog Vegetation and CO2 Fluxes to Fertilization been a long-term C sink of about 20 g C m-2 a-1, August during the summers of 2001, 2003, 2005, and the average contemporary net ecosystem and 2008. Each treatment plot had a pre-installed -2 -1 exchange of CO2 is about 40 g C m a (uptake), 0.6 m 9 0.6 m aluminum collar for the closed based on eddy covariance (EC) measurements made chamber measurements. A 0.5-m tall chamber was on a tower 150 m from the fertilization site (Lafleur used from 2001 to 2005, but was replaced in 2008 by and others 2003; Moore and others 2006; Roulet a 0.9-m tall chamber to accommodate increased and others 2007). At the EC tower, continuous shrub height. Net ecosystem exchange of CO2 (NEE) measurements of water table depth and thermal was measured using a clear plexan chamber equip- regime have been made since 1998. ped with fans and a cooling unit to ensure proper gas Background inorganic wet N deposition in this mixing and humidity and temperature control. region is about 0.8 g N m-2 a-1 (Turunen and Measurements were conducted only when photo- others 2004) and in this experiment the N fertil- synthetic photon flux density (PPFD) exceeded ization levels equal 5, 10, and 20 times the summer 1000 lmol photons m-2 s-1, the level of light satu- time wet N deposition and treatments are abbrevi- ration for photosynthesis. After each NEE mea- ated accordingly (Table 1). Fertilization experiment surement, the chamber was vented and covered I was started in the year 2000 with four treatments, with an opaque shroud to measure ecosystem res- and two more treatments were added in the year piration (ER). Light-saturated or maximum, eco- 2001 (Table 1). Treatments included control (Ci, system gross photosynthesis (Pgmax) was estimated distilled water), phosphorus and potassium (PK, as the sum of NEEmax and ER. Positive NEE repre- -2 -1 -2 -1 6.3 g P m a and 5.0 g K m a ), 5N sents ecosystem CO2 uptake, and both component (1.6 g N m-2 a-1), 5NPK, and 10NPK (3.2 g N m-2 fluxes, Pg and ER, are indicated with positive values. -1 -2 -1 a with PK) and 20NPK (6.4 g N m a with Fluxes of CO2 were determined on the basis of PK). Note that the amounts of P and K are the same concentration change over time in the chamber air in all the NPK treatments. Another set of treatments space and corrected for volume, temperature, and and control (Cii), experiment II, was established in air pressure. A LI-COR 6200 (Li-Cor Inc., Nebraska, the year 2005 to study the effects of 3.2 (10N) and USA) photosynthesis system was programmed to 6.4 g N m-2 a-1 (20N) without PK addition. Each record flux every 5 s and these readings were treatment had three replicate plots 3 9 3m2 in size. averaged every 30 s during the 2.5-min measure- Fertilization was given in soluble form, N as ment period. Fluxes were checked afterwards and NH4NO3 and PK as KH2PO4, dissolved in 2-mm the observation was rejected if flux rates were distilled water every third week from early May to changing over the measurement period due to late August. Earlier results and site description can leaking, increased humidity, variable irradiation, or be found in Basiliko and others (2006) and Bubier other chamber problems. PPFD (PPFD sensor, Li- and others (2007). 185B, Li-Cor Inc., Nebraska, USA), chamber tem- perature, and relative humidity were recorded Ecosystem CO2 Fluxes simultaneously with CO2 flux measurements. Soil temperature at depths of 5 and 10 cm and water We measured net ecosystem exchange of CO (NEE) 2 table depth were measured at the same time. weekly or bi-weekly from the end of May to mid-

Table 1. Experimental Set-Up

Treatment Start year N (g m-2 a-1) P (g m-2 a-1) K (g m-2 a-1)

Experiment I Ci 2000 0 0 0 PK 2000 0 6.3 5 5N 2000 1.6 0 0 5NPK 2000 1.6 6.3 5 10NPK 2001 3.2 6.3 5 20NPK 2001 6.4 6.3 5 Experiment II Cii 2005 0 0 0 10N 2005 3.2 0 0 20N 2005 6.4 0 0

N fertilization levels equal 5, 10, and 20 times the summer time wet N deposition and treatments are abbreviated accordingly. S. Juutinen and others

Vegetation Measurements table depth and peak season Sphagnum, Polytrichum, and total moss cover and vascular canopy height We monitored percentage cover of and Sphagnum were studied in experiment I. To examine the re- mosses, total moss cover, mean vascular Polytrichum sponses over the course of the 9-year experiment, a canopy height, species composition, and above- repeated measurements ANOVA was used. In ground foliar and woody biomass during the same addition, treatment effects were analyzed by one- years as CO flux measurements. Percent cover of 2 way ANOVA for each individual study year, and mosses in the collar area was determined visually differences between control and treatments were or with the point intercept method in July of each assessed using Dunnett’s two-way post hoc test. year, along with measurements of bryophyte and Data from experiment II for the year 2008 were vascular plant species composition, and mean analyzed separately. All data were transformed height of the shrub canopy. Point interception hits (Loge x + 1 or arc sine x) to meet the assumptions to a metal rod (radius 4 mm) were recorded in 61 of homogeneity of variance. Mean proportional grid points and hits to Sphagnum and Polytrichum treatment effects [((treatment - control)/con- mosses out of all ground hits were converted to trol) 9 100%] were used to illustrate the magni- percentage cover. Moss cover values exceeding tude of the impacts. 100% appear, because grows Polytrichum strictum We tested the treatment effects on a set of veg- through and on the top of the layer. Sphagnum etation features measured in 2008: moss biomass, These variables were used to examine the change aboveground vascular plant biomass, PAI, litter in vegetation from 2001 to 2008. accumulation rate from late May to October, and Point intercept hits recorded in July 2008 in each ratio of litter accumulation by mid August to CO2 flux measurement collar were used to estimate aboveground vascular biomass as an indication of aboveground vascular plant biomass. Number of leaf turnover rates. One-way ANOVAs were run hits to plant species and organs (leaf/woody stem/ separately for experiments I and II, and differences flower) were used as explanatory variables in between the treatments and the controls were as- regression equations. The regression relationships sessed using Dunnett’s test. All data were trans- between hit numbers and harvested biomass were formed (Log x + 1 or arc sine x) to meet the established using data collected from 30 plots out- e assumptions of homogeneity of variance. side the experimental area during the summer Statistical relationships among NEEmax, ER, 2007. We produced estimates of Sphagnum and Pg and plant community features in the 2008 biomass and total green biomass using max Polytrichum data were quantified using regression analyses the known moss cover in each plot and moss bio- pooling data from all 27 plots. The independent mass data collected from Mer Bleue bog earlier variables were: plant area index (PAI), mean shrub (Moore and others 2002; Bubier and others 2006). canopy height, Sphagnum, Polytrichum and total Mean biomass (130 g m-2) of the top 2 cm of moss biomass, total vascular aboveground biomass, Sphagnum capitulum at 100% cover, and mean -2 vascular leaf and wood biomass, ratio of woody to biomass (26 g m )ofPolytrichum strictum for 10% leaf vascular plant biomass, sum of vascular plant cover, were used in this estimation. The sum of leaf and moss biomass (green biomass), and ratio of vascular leaf biomass and moss biomass is called leaf and total green biomass. Mean water table green biomass. Other vegetation characteristics depth and soil temperature, as key abiotic envi- measured in summer 2008 were plant area index ronmental factors, were also included in the anal- (PAI) and aboveground vascular plant litter. PAI yses to assess their effect on the observed patterns. was measured using a LAI-2000 canopy analyzer The effect of each variable was tested indepen- (Li-Cor Inc., Nebraska, USA) under overcast con- dently. We also used mean July Pgmax as a depen- ditions in mid July. Aboveground vascular plant dent variable, because it represents the time period litter production rate from May to October was when vegetation parameters were measured. quantified with two litter traps, 7 9 10 cm, in each experimental plot. Litter was collected in mid Au- gust and late October, 2008, oven-dried at 60C RESULTS and weighed. Ecosystem CO2 Fluxes Data Analyses Differences in ecosystem CO2 fluxes among treat- ments were relatively small over the duration of Effects of treatments on seasonal averages of the experiment. CO2 fluxes in experiment I were NEEmax, ER, and Pgmax, soil temperature, water affected only by the two highest N addition levels, Responses of Bog Vegetation and CO2 Fluxes to Fertilization

3.2 and 6.4 g N m-2 a-1 in the treatments 10NPK eighth treatment year, 2008, ecosystem respiration and 20NPK (Figure 1). Study year, and rates were significantly increased in the treatments year 9 treatment interaction, had impacts on eco- 10NPK (+24%) and 20NPK (+32%) compared to system CO2 fluxes (Table 2; Figure 1). Responses to control treatment (Figure 1). This was the first time treatments were non-linear in time as the treat- that ER in a nutrient treatment differed from con- ments affected NEEmax,Pgmax, or ER during some trol since the beginning of the experiment in 2000, years but not in others (Table 2; Table 3). In the whereas the first significant CO2 response to treatment was increased NEEmax in the 10NPK treatment in the third year. Later on, in the fifth A Ci 5NPK treatment year, both Pgmax and NEEmax were sig- PK 10NPK ) 8 nificantly lower in the 20NPK treatment compared

-1 5N 20NPK s to control treatment (Figure 1). There was a trend -2 6 (P = 0.08) of increased Pgmax in the 10N treatment * (4 years with N only) relative to the control in experiment II (Table 3; Figure 1). (µmol m 4 Cii Year to year variation in NEEmax and Pgmax had max 10N similar patterns. The variation in Pgmax followed to 2 NEE 20N some degree the variation in water table depth * 2 (radj = 0.52, F = 86.570, P < 0.001, dfreg.,res. 1,79), 0 and the treatment means of Pgmax were the highest in 2008 when the mean water table of the mea- B surement period was closest to the peat surface 8 (Figures 1, 2). There was a weak negative rela-

) tionship between mean Pgmax and mean soil tem- -1 * s * peratures. The 20NPK treatment showed the largest

-2 6 variation in mean Pgmax among the study years. Ecosystem respiration varied less from year to year 4 than Pgmax, and it was only weakly related to var- 2

ER (µmol m iation in WT (radj = 0.05, F = 5.347, P = 0.023, 2 dfreg.,res. 1,79). From 2001 to 2007, there was no significant 0 difference in mean water table depth or surface peat temperature among the treatment and control C plots. Mean water table depths ranged from -55 to -41 in the control plots, which was in the range of

) 12

-1 measurements made near the EC tower (Figure 2). s

-2 Mean surface soil temperatures (during the gas flux 10 measurements) ranged from 22 to 27C in the control plots during this same period. In 2008,

(µmol m 8 mean water table depth was significantly closer to

max the peat surface in treatment 20NPK (-19 cm) * Pg 6 compared with controls (-33 cm), and surface temperature was significantly lower in treatments 10NPK (20.5C) and 20NPK (20C) than in control 4 2001 2002 2003 2004 2005 2006 2007 2008 plots (23C) (Table 3). Year

Figure 1. Seasonal means of A maximum net ecosystem Vegetation Characteristics exchange of CO2 (NEEmax), B ecosystem respiration Treatments affected vegetation more than the (ER), and C maximum ecosystem photosynthesis mean ecosystem CO2 fluxes. The largest significant (Pgmax). Experiment II was measured only during 2008 (data points on the right side of experiment I). Significant proportional treatment effects on CO2 exchange in differences between individual treatments and the con- experiment I were +77% (NEEmax), -19% (Pgmax), trols Ci and Cii (P < 0.05) are indicated by *. Means and +32% (ER), measured in the years 2001, 2005, represent the period from the end of May to mid-August. and 2008, respectively (Figure 1). In comparison, Standard deviations are not shown for clarity. Sphagnum cover was lost (-100%), and the signif- S. Juutinen and others

Table 2. Repeated Measurements ANOVA

NEEmax ER Pgmax Canopy H Sph Poly Moss Tsoil WT

Yr F 40.034 6.042 55.967 111.496 190.509 21.022 42.546 11.651 129.195 P <0.001 0.002 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 Yr 9 T F 1.634 3.365 2.750 5.665 5.866 5.583 9.230 0.943 3.916 P 0.113 0.001 0.006 <0.001 <0.001 <0.001 <0.001 0.529 <0.001 T F 0.796 2.415 1.941 3.762 11.659 2.278 10.505 1.633 1.746 P 0.573 0.098 0.161 0.028 <0.001 0.113 <0.001 0.225 0.199

Effects of year (Yr), year 9 treatment (Yr 9 T) and treatment (T) on the CO2 exchange (NEEmax, ER, Pgmax), shrub canopy height (H), Sphagnum, Polytrichum, and total moss cover (Sph, Poly, and Moss), soil temperature at 5 cm (Tsoil), and water table (WT). Years are 2001, 2003, 2005, and 2008. Dfyear,year9treatment,treatment = 3, 15, 5.

Table 3. ANOVA for the Treatment Effects on CO2 Exchange (NEEmax, ER, Pgmax), Shrub Canopy Height (H), Sphagnum, Polytrichum, and Total Moss Cover (Sph, Poly, and Moss), Soil Temperature at 5 cm (Tsoil), and Water Table (WT)

NEEmax ER Pgmax Canopy H Sph Poly Moss Tsoil WT

Exp I, 2001 F 1.151 3.771 2.549 3.048 0.800 1.000 1.000 1.241 2.289 P 0.387 0.028 0.086 0.053 0.571 0.458 0.458 0.349 0.111 Exp I, 2003 F 3.099 1.468 1.649 2.283 6.426 6.107 14.152 1.740 1.412 P 0.050 0.271 0.221 0.112 0.004 0.005 <0.001 0.200 0.288 Exp I, 2005 F 6.281 2.416 4.405 4.093 11.250 2.204 6.371 5.594 2.045 P 0.004 0.098 0.016 0.021 <0.001 0.122 0.004 0.007 0.144 Exp I, 2008 F 1.776 4.162 1.777 6.342 11.904 10.583 15.291 5.020 2.647 P 1.192 0.020 0.192 0.004 <0.001 <0.001 <0.001 0.010 0.078 Exp II, 2008 F 2.386 2.510 3.942 1.816 10.977 1.044 2.263 1.142 0.194 P 0.173 0.161 0.081 0.241 0.010 0.408 0.185 0.380 0.829

Differences between treatments and the control in each year were compared using Dunnett’s two-tailed test (P = 0.05) and are indicated in Figures 1, 2, and 3.Dfbetween,within 5,12 and 2,6 for experiments I and II, respectively. icant increases in canopy height and Polytrichum treatment. Change in vegetation over time resulted cover were up to +88 and +834%, respectively, in in significant year, year 9 treatment, and treat- different years of the experiment (Figure 3). Mean ment effects for Sphagnum and total moss cover Sphagnum cover decreased from 100% to less than (Table 2). Note that during the course of the 40% in 3 years and was almost absent by the fifth experiment, mean Sphagnum cover had a decreas- year in the treatments 20NPK and 10NPK; and all ing trend in the control plots from 100 to 80%, nutrient treatments had a significantly smaller which has been mirrored by the trend of increasing Sphagnum cover than the control in that year. After Polytrichum cover from 10 to 25% (Figure 3). that, Sphagnum cover recovered slightly in PK and Shrub canopy height increased significantly only 5N treatments and was no longer significantly dif- in the 10NPK and 20NPK treatments after 5 years, ferent from the control treatment. The strong initial and these canopies were 72 and 88% taller, increase of Polytrichum cover from about 10 to respectively, than the control by the eighth year 60–90%, significant in the treatments 5NPK, (2008) (Figure 3A). Along with taller canopies, 10NPK, and 20NPK, leveled off after 2003, except there were increases in leaf biomass (about +40%) that it diminished to almost 0% cover in the 20NPK and in woody biomass (+86%) in the 20NPK Responses of Bog Vegetation and CO2 Fluxes to Fertilization

Ci PK 5N Ci 5NPK *A Cii B 5NPK Cii EC tower, Jun PK 10NPK 10N 5N 20NPK * 20N 10NPK 10N EC tower, Jul 30 20NPK 20N EC tower, Aug * 0 A 20

Canopy Height (cm) Canopy 10 -20 *

) C D -2 *

m 1.0 -40 2 WT (cm) * 0.5 * -60 0.0 Moss area (m * *

100 E B F 26 80 60 40 24 * * * * 20 * * * 0 * * * Sphagnum Cover (%) Cover Sphagnum * * 22 100 T at 5 cm (°C) G H * * 80 * 20 * 60 * 40 1999 2001 2003 2005 2007 20 Year 0 * Polytrichum Cover (%) Cover Polytrichum Figure 2. Treatment means for A water table depth and 123456789 12345 B peat temperature at 5-cm depth measured together Year of Treatment Year of Treatment with CO2 exchange (June–August). Experiment II was measured only during 2008 (data points on the right side Figure 3. Treatment means of A–B shrub canopy of experiment I). Significant differences between treat- height, C–D total moss area, E–F Sphagnum cover, and ment and control (P < 0.05) are indicated for both G–H Polytrichum strictum cover in the different treat- experiments by *. Standard deviations are not shown for ments. Experiment I on the left and experiment II on the clarity. Monthly means for the mid summer WT for the right. Significant differences between treatment and years 1998–2008 are from the EC tower situated close by control (P < 0.05) are indicated for both experiments by the site. *. Standard deviations are not shown for clarity. treatment by 2008 (Figure 4). Mean Woody: leaf dramatic (Figures 3, 4). Only Sphagnum cover was biomass ratio was 1.1 in the control, and 1.5 in the decreased (-57%) significantly after 4 years in the 20NPK, but those were not significantly different. 20N treatment, and the decrease seemed to be The estimate of total green biomass, however, was smaller than that of the 20NPK and 10NPK treat- significantly smaller in the 20NPK treatment than ments in their third year (Figure 3). in the control due to the missing moss component (Figure 4E). All the N and the NPK treatments in- Relationships Between Vegetation and creased vascular aboveground litter production in CO Fluxes experiment I, and the ratio of litter accumulation 2 by mid August to the aboveground biomass was An examination of the relationship between veg- more than doubled in the 20NPK treatment com- etation and CO2 fluxes (year 2008) indicated that pared to the control (Figure 4F, G). both ER and Pgmax increased with increasing vas- Changes in vegetation in the N-only experiment cular plant contribution (Table 4; Figure 5). Plant II resembled those in experiment I, but were less area index of the tested variables was the best S. Juutinen and others

Figure 4. Treatment A F=5.323, p=0.008 E F=6.253, p=0.004 means, with standard ) ) -2 deviation as bar, of -2 400 400 A vascular leaf and * * * B wood biomass, C woody:leaf biomass 200 200 ratio, D vascular plant Leaf bm (g m

Green bm (g m area index (PAI), E total green biomass, F litter 0 0 accumulation from May to October 2008, and

F=3.969, p=0.023 ) F F=17.601, p<0.001

B -1 G litter:biomass ratio. X- )

-2 400 * * axis gap distinguishes 400 experiments I and II, * which were analyzed 6 months 6

-2 ** separately. ANOVA 200 200 showed significant differences only for Woody bm (g Woody m experiment I, and only Litterm (g 0 0 the treatments significantly different G than control are marked 2.0 C F=2.402, p=0.099 0.20 GF=3.425, p=0.037 * with *. 1.5 0.15

1.0 0.10 Wood:Leaf 0.5 Litter:Biomass 0.05

0.0 0.00 i ii C PK 5N PK PK PK C PK PK 5N 0N 0N 0N 0N D F=2.267, p=0.114 1 2 1 2 5 Treatment

4

3 PAI

2

1

0 i ii C PK 5N PK PK PK C PK PK N N N N N 5 10 20 10 20 Treatment

2 predictor for mean ER (r = 0.54) and Pgmax Table 4). Highest NEEmax values occurred in plots (r2 = 0.35) among the plots. ER was positively re- with only intermediate vascular leaf biomass, but lated with factors indicating more vascular plant with moss cover still remaining (Figure 5). In and less Sphagnum biomass (Table 4). Relationships general, however, the plant variables predicted ER were poor between mean Pgmax and each green better than either NEEmax or Pgmax (Figure 5; biomass component of the canopy, Sphagnum and Table 4) when seasonal means were inspected. Polytrichum mosses, vascular leaves, and the sum of these (Table 4; Figure 5). However, mean Pgmax of July was significantly related to vascular plant leaf DISCUSSION mass, even though the seasonal mean was not. Nutrient Effects on Vegetation and NEEmax had a weak positive relationship with total Ecosystem CO Fluxes green biomass of vascular plant and moss 2 (r2 = 0.11) and a weak negative relationship with Nitrogen addition at high rates of 3.2 and 6.4 g N -2 -1 wood to shrub foliar biomass ratio (r2 = 0.16, m a with PK and background deposition of Responses of Bog Vegetation and CO2 Fluxes to Fertilization

Table 4. Linear Regression Coefficients of Deter- exchange in 10NPK (P < 0.05) treatment in its mination Between Seasonal Mean Ecosystem CO2 third year and elevated ecosystem photosynthesis Fluxes and Vegetation and Environmental Variables in the N-only experiment (10N, P = 0.08), fertilized in 2008 (n = 27) for 4 years (Figure 1). Compared with control, we R2 FP observed lower ecosystem photosynthesis in the fifth year in 20NPK when the moss layer disap- ER peared. Possibly, the increase in vascular leaf mass +PAI 0.54 31.098 <0.001 was not enough to compensate for loss of moss +Canopy H 0.49 26.351 <0.001 photosynthesis (Bubier and others 2007). Sup- -Sphagnum bm 0.39 17.805 <0.001 porting our first hypothesis, shrub growth contin- -Leaf:green 0.33 13.544 0.001 ued after 5 years in the high NPK treatments; most +Wood bm 0.30 12.267 0.002 recently in 2008 these treatments had higher vas- +Tot bm 0.30 12.586 0.002 +WT 0.28 10.867 0.003 cular leaf biomass than the control, but the increase +Leaf bm 0.26 10.045 0.004 in woody biomass was even larger increasing the -Moss bm 0.26 9.991 0.004 woody:foliar biomass ratio. The increase in vascular +Wood:foliar 0.17 6.388 0.018 foliar biomass was about 40% compared with the -T5 0.14 5.059 0.034 control (Figure 4), but combined with the loss of Green bm ns moss, the total green biomass still remained smaller Polytrichum bm ns in the 20NPK treatment than in control plots after NEEmax 8 years (Figure 4). However, maximum ecosystem -Wood:foliar 0.16 5.864 0.023 photosynthesis rates recovered from 2005 to 2008 +Green bm 0.11 4.230 0.050 (Figure 1). Nonetheless, Pg was not significantly Pg (mean) max max different among treatments and controls in 2008. +PAI 0.35 15.183 0.001 +Canopy H 0.18 6.848 0.015 In undisturbed areas of Mer Bleue bog, Sphagnum capitulum and Polytrichum biomass is on average Pgmax (July) +PAI 0.39 16.111 0.001 half of the total foliar biomass (Bubier and others +Canopy H 0.34 13.202 0.001 2006) and it has been noted that the moss surface +Leaf bm 0.24 8.643 0.007 in an open mire canopy makes a substantial con- -T5 0.17 5.770 0.025 tribution to net ecosystem photosynthesis (for +Tot bm 0.13 4.630 0.042 example, Douma and others 2007; Riutta and others 2007a). Although higher photosynthetic The positive or negative relationships are indicated as + or -. The independent capacity of vascular leaves compared with mosses variables are: plant area index (PAI), mean shrub canopy height (canopy H), Sphagnum, Polytrichum, and total moss biomass (Sphagnum bm, Polytrichum can balance partly the decrease in moss biomass, bm, Moss bm), total vascular aboveground biomass (Tot bm), vascular leaf and self-shading in dense canopies, for example in wood biomass (leaf bm, wood bm), ratio of woody to leaf vascular biomass (wood:foliar), sum of vascular leaf and moss biomass (green bm), ratio of leaf, and those at Mer Bleue, restricts further increases in total green biomass (leaf:green), water table depth (WT), and soil temperature at ecosystem photosynthesis (Riutta and others 5-cm depth (T5). All variables tested with ER were tested also for Pgmax,Pgmax in July, and NEEmax, but only the significant relationships are shown. 2007b; Street and others 2007). There were no changes in maximum photosynthesis rates of shrub leaves among nutrient treatments during mid about 0.8 g N m-2 a-1 resulted in a major vege- growing season even though we expected N addi- tation transition from a mixed community of tion to increase photosynthetic capacity in this Sphagnum moss and dwarf shrubs to a community nutrient-limited bog ecosystem (Bubier and others, of tall shrubs without moss (Figure 3). Only these unpublished manuscript). treatments, 10NPK and 20NPK, significantly In support of our second hypothesis, ecosystem affected CO2 exchange (Figure 1) during the respiration increased after 8 years in the 10NPK experiment, and ecosystem CO2 fluxes responded and 20NPK plots (Figure 1) that had experienced a differently to nutrient treatments from year to loss of Sphagnum cover (Figure 3), an increase in year. The different phases of vegetation transition shrub biomass with a large woody component, and combined with climate variability are likely con- an increase in litter accumulation (Table 4; Fig- tributing to the variability in responses of the CO2 ure 5). Overall, it is difficult to quantify the relative fluxes. contributions of litter quantity and quality, auto- In the initial phase of nutrient addition, a mod- trophic respiration and stimulation of microbial erate increase in vascular plant biomass together activity on the observed change (for example, with only small changes in the moss mass or cover Hobbie and others 2002). But we postulated an can explain the trends of elevated net ecosystem increase in ER because the change in litter quality S. Juutinen and others

Cii 5NPK Cii PK 10NPK 10N 5N 20NPK 20N Figure 5. Relationships )

-1 between plot means of s ecosystem CO fluxes -2 8 2 (NEEmax, ER, and Pgmax) and plant area index (PAI) (left), vascular leaf (µmol m 6 biomass (middle), and max Sphagnum biomass (right)

NEE among all 27 plots in 8

) summer 2008. Regression -1

s lines for the significant

-2 relationships are included 6 (see Table 4 for the results).

ER (µmol m 4 ) -1 s

-2 14

12

(µmol m (µmol 10 max

Pg 8 12345 150 200 250 300 0 20 40 60 80 100 120 PAI Leaf bm (g m-2) Sphagnum bm (g m-2) and ground layer environment can have an impact 1.3 g N m-2 a-1 has decreased the recent C accu- on decomposition. It is known that stems and mulation rate at Storemoss bog, possibly by leaves of the dominant dwarf shrub, C. calyculata, enhancing decomposition. decompose much faster than Sphagnum tissues at Comparison with studies conducted in other the surface of Mer Bleue and that decomposition Sphagnum-dominated peatlands with N applications rates are higher in environments with less Sphag- of about 3 g N m-2 a-1 or more indicate that site num moss cover (Moore and others 2007). It is conditions affect how and when ecosystem CO2 unknown how the changes in temperature and exchange responds. For example, vegetation and moisture conditions due to altered vegetation have CO2 exchange were not affected by 2 years of fer- affected the soil processes. In the plots having no tilization in an oligotrophic low sedge, S. papillosum moss cover, the water table is closer to the peat pine fen in Finland (Saarnio and others 2003). surface (Figure 2); yet the top of the peat is drier, Conversely, 2 years with 4 g N + 0.05 g P m-2 a-1 the surface is cooler (Figure 2) and at 20-cm depth resulted in increases in both respiration and pho- it is slightly warmer than in control plots (Elyn tosynthesis in a bog in northern Sweden even Humphreys, personal communication 2009). though the vegetation was not significantly af- In addition to the change in litter type, an in- fected (Lund and others 2009). The same study crease in autotrophic respiration accompanies in- showed that in southern Sweden, where back- creased shrub biomass (for example, Johnson and ground N load is greater than northern Sweden, P others 2000; Lafleur and others 2003). Moreover, but not N addition increased ecosystem photosyn- an increase in rhizospheric activity and N input thesis (Lund and others 2009). No treatment re- stimulates the microbial community and minerali- sponses in ecosystem photosynthesis, but slight zation of soil organic matter (Jonasson and others increases in respiration, were observed after 5 years 2004; Mack and others 2004; Waldrop and Fire- of3gN+1gPm-2 a-1 in an Alpine bog in Italy; stone 2004; Bragazza and others 2006; Basiliko and but there the effect of treatments was hindered by others 2006; Shaver and others 2006). Recently, drought (Gerdol and others 2008). Fertilization Lund and others (2009) reported immediate short- experiments in tundra ecosystems provide addi- term increases in ER following fertilization events tional comparisons with peatland studies. For in boreal bogs. For example, Gunnarsson and oth- example, in arctic dwarf shrub tundra (Green- ers (2008) suggested that chronic N deposition of land), large increases in both photosynthesis and Responses of Bog Vegetation and CO2 Fluxes to Fertilization

ecosystem respiration, as well as net CO2 uptake, reduced, in contrast to our results (Chapin and were observed along with increased plant growth, others 2004). On the other hand, in the Nether- with 5 g N m-2 a-1 and PK after 2–3 years (Arens lands with high background N deposition and and others 2008). Eight years of additions of experimental N fertilization of 5 g N m-2 a-1, 10 g N m-2 a-1 with 5 g P m-2 a-1 increased sedge Heijmans and others (2001) observed no changes growth, net CO2 uptake, respiration, and photo- in Sphagnum cover during the third fertilization synthesis in wet sedge tundra in Toolik Lake, Alaska year, even though its height growth was signifi- (Johnson and others 2000). The plant assemblage of cantly reduced. the evergreen shrub-dominated Mer Bleue bog may The rapid responses seen at Mer Bleue may be due limit the responsiveness compared to the more in part to the background wet N deposition of about mineral rich sites dominated by graminoids 0.8 g N m-2 a-1 (Turunen and others 2004), which and deciduous species. Moreover, compensation is close to the proposed critical rate of 1 to 1.5 g N m-2 between mosses and shrubs likely kept the effects on a-1 (for example, Limpens and others 2008). In ecosystem CO2 exchange relatively few and small. addition, the experimental site at Mer Bleue bog has Our measurements allow us only to compare a relatively low average water table level, and peri- maximum summer time CO2 fluxes among treat- ods of even lower water tables occurred during the ments; however, the effects on net ecosystem CO2 early years of the experiment (Figure 2). In drier exchange on a seasonal or annual scale may be conditions, dwarf shrubs and Polytrichum strictum larger. If respiration also increased in autumn, moss have a competitive advantage over Sphagnum winter, and spring with lower CO2 uptake, the mosses and it has been indicated that N deposition threat of N deposition on peat C storage is more affects dry sites more strongly than wetter sites serious. In addition, shrub leaf turnover has accel- (Silvola and Aaltonen 1984; Aerts and others 2001; erated, particularly in the high N treatments, with Berendse and others 2001; Bubier and others 2003; an increase in the ratio of litter production to bio- Gerdol and others 2008; Wiedermann and others mass (Figure 4) (Bartsch 1994; Johnson and others 2009). During the 9-year experiment at Mer Bleue, 2000; Berendse and others 2001) enhancing vari- periods of lower than average water tables may ac- ation in the seasonal dynamics of ecosystem pho- count for Sphagnum and Polytrichum moss covers tosynthesis. In general, the pattern of year to year decreasing and increasing, respectively, in control dynamics and maximal CO2 flux rates in the con- plots. The recent increase in water table may explain trol plots are in accordance with eddy covariance the recovery of Sphagnum moss cover in PK, 5N, and measurements at Mer Bleue bog (Lafleur and oth- 5NPK plots in 2008 (Figure 3). Overall, the increase ers 2003; Roulet and others 2007; E. Humphreys, in shrubs and reduction in Sphagnum contribution personal communication 2008). due to nutrient addition may resemble the effects of water level draw down in bogs (Bubier and others 2003; Riutta and others 2007a). Vascular Plant and Moss Dynamics We observed small patches of Sphagnum and Responses of Sphagnum and Polytrichum moss cover Polytrichum occurring in openings in 10NPK and were large after only 3 years of fertilization at Mer 20NPK plots in the wet summer 2009, indicating Bleue bog. Responses have been slower and smaller that these mosses can tolerate fertilization to some in experiments using similar N addition (3 g m-2 degree if moisture and light conditions are favor- a-1) conducted in areas of lower (about 0.2 g m-2 able. Berendse and others (2001) attributed moss a-1) background N deposition. Wiedermann and decline to reduced light caused by vascular plant others (2007) detected the first signs of Sphagnum interception in several European mire sites. Lim- cover decrease after 4 years of fertilization, and pens and others (2003) found in their site that moss after 8 years it was reduced from 100 to 40%; height growth decreased after a light reduction of whereas at Mer Bleue, a similar reduction occurred about 50%. The ground layer in the 20NPK treat- after only 3 years of fertilization. The site of the ment in our study received less than 10% of the Wiederman and others (2007) study has a higher incoming irradiation, compared with 20–25% in water table and a larger sedge contribution than the control plots in 2008 (Humphreys, personal the Mer Bleue site. In a Minnesota bog, 3 years communication). Besides the light attenuation, with high N and P fertilization (6 g N and 2 g P m-2 tissue nutrient accumulation and imbalance could a-1) reduced Sphagnum cover moderately, from be deleterious to Sphagnum mosses (Heijmans and 84 to 68%, but high N with low P reduced it more, others 2001; Limpens and others 2003; van Wijk to 13%, and Polytrichum strictum cover was also and others 2003). S. Juutinen and others

The role of Sphagnum mosses in bog ecosystem There were no differences in maximum ecosystem biomass production is substantial and thus the ef- photosynthesis or net ecosystem CO2 exchange fect of N deposition is severe. Earlier, Chapin and between treatments and control after 8 years indi- others (2004) showed that N fertilization can in- cating that the increase in shrub foliar biomass can hibit whole bog community aboveground produc- compensate for the loss of moss. Given the large tion, because of moss responses. On the other observed changes in the vegetation, the responses hand, shrub growth can increase greatly; for in CO2 fluxes were rather small. However, losing example C. calyculata doubled in biomass when the Sphagnum component may risk the net CO2 fertilized for 2 years with 5 and 10 g N(+P) m-2 a-1 uptake capacity in a bog if it leads to faster in a Maine bog (Bartsch 1994). However, with decomposition and CO2 release. improved nutrient supply light competition among shrubs forces a large allocation to wood, and more ACKNOWLEDGEMENTS resources are invested to tissue renewal (Fig- ure 4).The appearance of a fern Thelypteris palustris We thank the National Science Foundation for the in the 20NPK plots after the fifth treatment year award DEB 0346625 to Jill Bubier, and the Natural and recently (2009) new patches of moss species Sciences and Engineering Research Council Dis- Pleurozium schreberi and Dicranum sp. in the 10NPK covery for grants to Tim Moore, and the National and 20NPK treatments are indicators of possible Capital Commission for access to the Mer Bleue. changes in plant assemblage. These species are We thank Peter Lafleur and Elyn Humphreys for found in drier and minerotrophic sites of Mer sharing data from the eddy covariance tower and Bleue. we thank Leszek Bledzki, Mike Dalva and Meaghan Vegetation trends were similar in NPK and Murphy for assistance in the field and laboratory. N-alone experiments after 4 years of fertilization, The valuable help of many Mount Holyoke College, though they were measured during different years. McGill University and Carleton University students N with PK seemed to induce slightly stronger re- in collecting the field data is acknowledged. The sponses in Sphagnum cover and smaller responses in comments of two anonymous reviewers and Gaius Polytrichum cover than N alone (Figure 3). Many Shaver greatly improved the manuscript. bogs and other nutrient poor wetlands are limited by P rather than N, and therefore, stronger re- REFERENCES sponses in growth have required balanced nutrition Aerts R, Verhoeven JTA, Whigham DF. 1999. Plant-mediated in many cases (Shaver and Chapin 1980; Bartsch controls on nutrient cycling in temperate fen and bogs. 1994; Nadelhoffer and others 2002; Arens and Ecology 80:2170–81. others 2008). We noted a decrease in Sphagnum Aerts R, Walle´n B, Malmer N, de Caluwe H. 2001. Nutritional cover (2005) compared to the control following PK constraints on Sphagnum-growth and potential decay in addition, which was high in our study. Using lower northern peatlands. J Ecol 89:292–9. P application levels in several European bog sites, Alm J, Sculman L, Walden J, Nyka¨nen H, Martikainen PJ, Sil- Limpens and others (2004) observed, in contrast, vola J. 1999. Carbon balance of a boreal mire during a year with an exceptionally dry summer. Ecology 80:161–74. that in some sites P addition improved Sphagnum Arens SJT, Sullivan PF, Welker JM. 2008. Nonlinear responses to growth or alleviated the negative impact of high N nitrogen and strong interactions with nitrogen and phospho- addition. rus additions drastically alter the structure and function of a high arctic ecosystem. J Geophys Res 11:G03S09. doi: 10.1029/2007JG000508. CONCLUSIONS Bartsch I. 1994. Effects of fertilization on growth and nutrient N addition at rates of 3.2 and 6.4 g N m-2 a-1 with use by Chamaedaphne calyculata in a raised bog. Can J Bot 72:323–9. PK upon a background deposition of about -2 -1 Basiliko N, Moore T, Jeannotte R, Bubier JL. 2006. Nutrient 0.8 g N m a significantly affected ecosystem input and carbon and microbial dynamics in an ombrotrophic CO2 exchange rates at Mer Bleue bog during the bog. Geomicrobiol J 23:531–43. 9 years of fertilization, but the responses were dif- Baxter R, Emes MJ, Lee JA. 1992. Effects of experimentally ferent from year to year depending on the phase of applied increase in ammonium on growth and amino-acid vegetation transition. These nutrient treatments metabolism of Sphagnum cuspidatum Ehrh. Ex. Hoffm. from shifted a bog community of Sphagnum moss and differently polluted areas. New Phytol 120:265–74. dwarf shrubs competing for nutrients to dwarf Berendse F, Breemen N, Rydin H, Buttler A, Heijmans M, Hoosbeek MR, Lee JA, Mitchell E, Saarinen T, Vasander H, shrub thickets competing for light, and led to an Wallen B. 2001. Raised atmospheric CO2 levels and increased increase in ecosystem respiration in the highest N deposition cause shifts in plant species composition and nutrient treatments after 8 years of fertilization. production in Sphagnum bogs. Glob Change Biol 7:591–8. Responses of Bog Vegetation and CO2 Fluxes to Fertilization

Bragazza L, Tahvanainen T, Kutnar L, Rydin H, Limpens J, Ha´jek dioxide exchange at an ombrotrophic bog. Global Biogeochem M, Grosvenier P, Ha´jek T, Hajkova P, Hansen I, Iacumin P, Cycles 17:1036. doi:10.1029/2002GB001983. Gerdol R. 2004. Nutritional constraints in ombrotrophic LeBauer DS, Treseder KK. 2008. Nitrogen limitation of net pri- Sphagnum plants under increasing atmospheric nitrogen mary productivity in terrestrial ecosystems is globally distrib- deposition in Europe. New Phytol 163:609–16. uted. Ecology 89:371–9. Bragazza L, Freeman C, Jones T, Rydin H, Limpens J, Fenner N, Limpens J, Berendse F. 2003. Growth reduction of Sphagnum Ellis T, Gerdol R, Ha´jek M, Ha´jek T, Iacumin P, Kutnar L, magellanicum subjected to high nitrogen deposition: the role of Tahvanainen T, Toberman H. 2006. Atmospheric nitrogen amino acid nitrogen concentration. Oecologia 135:339–45. deposition promotes carbon loss from peat bogs. Proc Natl Limpens J, Raymakers HTAG, Baar J, Berendse F, Zijlstra JD. Acad Sci 103:19386–9. 2003. The interaction between epiphytic algae, a parasitic Bubier JL, Bhatia G, Moore T, Roulet TR, Lafleur PM. 2003. fungus and Sphagnum as affected by N and P. Oikos 103:59–68. Spatial and temporal variability in growing season net eco- Limpens J, Berendse F, Klees H. 2004. How phosphorus avail- system carbon dioxide exchange at a large peatland in On- ability affects the impact of nitrogen deposition on Sphagnum tario, Canada. Ecosystems 6:353–67. and vascular plants in bogs. Ecosystems 7:793–804. Bubier JL, Moore TR, Crosby G. 2006. Fine-scale vegetation Limpens J, Berendse F, Blodau C, Canadell JG, Freeman C, distribution in a cool temperate peatland. Can J Bot Holden J, Roulet N, Rydin H, Schaepman-Strub G. 2008. 84:910–23. Peatland and the carbon cycle: from local processes to global Bubier JL, Moore TR, Bledzki LA. 2007. Effects of nutrient implications—a synthesis. Biogeosciences 5:1475–91. addition on vegetation and carbon cycling in an ombrotrophic Lund M, Christensen TR, Mastepanov M, Lindroth A, Stro¨ mL. bog. Glob Change Biol 13:1168–86. 2009. Effects of N and P fertilization on the greenhouse gas Canadian Climate Normals 1971–2000. Canada’s National Cli- exchange in two northern peatlands with contrasting N mate Archive. http://climate.weatheroffice.ec.gc.ca/climate_ deposition rates. Biogeosciences 6:2135–44. normals. Mack MC, Schuur EAG, Bret-Harte SM, Shaver GR, Chapin Chapin CT, Bridgham SD, Pastor J. 2004. pH and nutrient effects SFIII. 2004. Ecosystem carbon storage in arctic tundra reduced on above-ground net primary production in a Minnesota, by long-term fertilization. Nature 431:440–3. USA bog and fen. Wetlands 24:186–201. Malmer N, Albinsson C, Svensson BM, Walle´n B. 2003. Inter- Clymo RS, Hayward PM. 1982. The ecology of Sphagnum. In: ferences between Sphagnum and vascular plants: effects on Smith AJE, Ed. Bryophyte ecology. London: Chapman and plant community structure and peat formation. Oikos Hall. p 229–89. 100:469–82. Douma JC, van Wijk MT, Lang SI, Shaver GR. 2007. The con- Moore TR, Bubier JL, Frolking SE, Lafleur PM, Roulet NT. 2002. tribution of mosses to the carbon and water exchange of arctic Plant biomass and production and CO2 exchange in an om- ecosystems: quantification and relationships with system brotrophic bog. J Ecol 90:25–36. properties. Plant Cell Environ 30:1205–15. Moore TR, Lafleur PM, Poon DMI, Heumann BW, Seaquist JW, Gerdol R, Bragazza L, Brancaleoni L. 2008. Heatwave 2003: high Roulet NT. 2006. Spring photosynthesis in a cool temperate summer temperature, rather than experimental fertilization, bog. Glob Change Biol 12:2323–35. affects vegetation and CO2 exchange in an alpine bog. New Moore TR, Bubier JL, Bledzki L. 2007. Litter decomposition in Phytol 179:142–54. temperate peatland ecosystems: the effect of substrate and Gorham E. 1991. Northern peatlands: role in the carbon cycle and site. Ecosystems 10:949–63. probable responses to climatic warming. Ecol Appl 1:182–95. Nadelhoffer KJ, Johnson L, Laundre J, Giblin AE, Shaver GR. Gruber N, Galloway JN. 2008. An Earth-system perspective of 2002. Fine root production and nutrient content in wet moist the global nitrogen cycle. Nature 451:93–296. arctic tundra as influences by chronic fertilization. Plant Soil Gunnarsson U, Boresjo¨ Bronge LJ, Rydin H, Ohlson M. 2008. 242:107–13. Near-zero recent carbon accumulation in a bog with high Riutta T, Laine J, Tuittila E-S. 2007a. Sensitivity of CO2 ex- nitrogen deposition in SW Sweden. Glob Change Biol change of a fen ecosystem components to water level varia- 14:2152–65. tion. Ecosystems 10:718–33. Heijmans MPD, Berendse F, Arp WJ, Masselink ABK, Klees H, Riutta T, Laine J, Aurela M, Rinne J, Vesala T, Laurila T, Haa- de Visser W, van Breemen N. 2001. Effects of elevated carbon panala S, Pihlatie M, Tuittila ES. 2007b. Spatial variation in dioxide and increased nitrogen deposition on bog vegetation plant community functions regulates carbon gas dynamics in a in the Netherlands. J Ecol 89:268–79. boreal fen ecosystem. Tellus 59B:838–52. Hobbie S, Nadelhoffer KJ, Ho¨ gberg P. 2002. A synthesis: the role Roulet NT, Lafleur PM, Richard PJH, Moore TR, Humphreys ER, of nutrients as constraints on carbon balances in boreal and Bubier J. 2007. Contemporary carbon accumulation and late arctic regions. Plant Soil 242:163–70. Holocene carbon accumulation in a northern peatland. Glob Johnson LC, Shaver GR, Cades DH, Rastetter E, Nadelhoffer K, Change Biol 12:1–15. Giblin A, Laundre J, Stanley A. 2000. Plant carbon-nutrient Rydin H, Jeglum J. 2006. The biology of peatlands. Oxford: interactions control CO2 exchange in Alaskan wet sedge Oxford University Press. tundra ecosystems. Ecology 81:453–69. Saarnio S, Ja¨rvio¨ S, Saarinen T, Vasander H, Silvola J. 2003. Jonasson S, Castro J, Michelsen A. 2004. Litter, warming and Minor changes in vegetation and carbon gas balance in a plants affect respiration and allocation of soil microbial and boreal mire under a raised CO2 or NH4NO3 supply. Ecosystems plant C, N and P in arctic mesocosms. Soil Biol Biochem 6:46–60. 26:1129–39. Shaver GR, Giblin AE, Nadelhoffer KJ, Thieler KK, Downs MR, Lafleur PM, Roulet NT, Bubier JL, Frolking S, Moore TR. 2003. Laundre JA, Rastetter EB. 2006. Carbon turnover in Alaskan Interannual variability in the peatland-atmosphere carbon S. Juutinen and others

tundra soils: effects of organic matter quality, temperature, Van Wijk MT, Clemmensen KE, Shaver GR, Williams M, moisture and fertilizer. J Ecol 94:740–53. Callaghan TV, Chapin FSIII, Cornelissen JHC, Gought L, Shaver GR, Chapin FSIII. 1980. Response to fertilization by Hobbie SE, Jonasson S, Lee JA, Michelsen A, Press MC, various plant growth forms in an Alaskan tundra: nutrient Richardson SJ, Rueth H. 2003. Long-term ecosystem level accumulation and growth. Ecology 61:662–75. experiments at Toolik lake, Alaska, and at Abisko, northern Sweden: generalizations and differences in ecosystem and Silvola J, Aaltonen H. 1984. Water content and photosynthesis plant type responses to global change. Glob Change Biol in the peat mosses Sphagnum fuscum and S. angustifolium. Ann Bot Fenn 21:1–6. 10:105–23. Street LE, Shaver GR, Williams M, van Wijk MT. 2007. What is Vitt DH, Wieder K, Halsey LA, Turetsky M. 2003. Response the relationship between changes in canopy leaf area and of Sphagnum fuscum to nitrogen deposition: a case study of ombrogenous peatlands in Alberta, Canada. Bryologist 106: changes in photosynthetic CO2 flux in arctic ecosystems? J Ecol 95:139–50. 235–45. Tomassen HBM, Smolders AJP, Limpens J, Lamers LPM, Roefols Waldrop WP, Firestone MK. 2004. Altered utilization patterns of JGM. 2004. Expansion of invasive species on ombrotrophic young and old soil C by microorganisms caused by tempera- ture and shifts and N additions. Biogeochemistry 67:235–48. bogs: desiccation or high N deposition. J Appl Ecol 41:139–50. Turetsky MR. 2003. The role of bryophytes in carbon and Wiedermann MM, Nordin A, Gunnarsson U, Nilsson MB, Eric- nitrogen cycling. Bryologist 106:395–409. son L. 2007. Global change shifts vegetation and plant-para- site interactions in a boreal mire. Ecology 88:454–64. Turunen J, Roulet NT, Moore TR. 2004. Nitrogen deposition and increased carbon accumulation in ombrotrophic peatlands in Wiedermann MM, Gunnarsson U, Nilsson MB, Nordin A, Eric- son L. 2009. Can small-scale experiments predict ecosystem eastern Canada. Glob Biogeochem Cycles 18:GB2003. doi: 10.1029/2003GB002154. responses? An example from peatlands. Oikos 118:449–56.