HABITAT TYPE DETERMINES HERBIVORY CONTROLS OVER CO 2 FLUXES IN A WARMER ARCTIC

Ecology, 89(8), 2008, pp. 2103–2116� 2008 by the Ecological Society of America

HABITAT TYPE DETERMINES HERBIVORY CONTROLSOVER CO2 FLUXES IN A WARMER ARCTIC

SOFIE SJOGERSTEN,1,5 RENE VAN DER WAL,2,3 AND SARAH J. WOODIN4

1School of Biosciences, University of Nottingham, University Park, Nottingham NG72RD United Kingdom2Centre of Ecology and Hydrology, Hill of Brathens, Banchory, Aberdeenshire AB31 4BW United Kingdom

3Aberdeen Centre for Environmental Sustainability (ACES), School of Biological Sciences, University of Aberdeen,Cruickshank Building, St. Machar Drive, Aberdeen AB24 3UU United Kingdom

4School of Biological Sciences, University of Aberdeen, Cruickshank Building, St. Machar Drive,Aberdeen AB24 3UU United Kingdom

Abstract. High-latitude ecosystems store large amounts of carbon (C); however, the Cstorage of these ecosystems is under threat from both climate warming and increased levels ofherbivory. In this study we examined the combined role of herbivores and climate warming asdrivers of CO2 fluxes in two typical high-latitude habitats (mesic heath and wet meadow). Wehypothesized that both herbivory and climate warming would reduce the C sink strength ofArctic tundra through their combined effects on plant biomass and gross ecosystemphotosynthesis and on decomposition rates and the abiotic environment. To test thishypothesis we employed experimental warming (via International Tundra Experiment [ITEX]chambers) and grazing (via captive Barnacle Geese) in a three-year factorial field experiment.Ecosystem CO2 fluxes (net ecosystem exchange of CO2, ecosystem respiration, and grossecosystem photosynthesis) were measured in all treatments at varying intensity over the threegrowing seasons to capture the impact of the treatments on a range of temporal scales(diurnal, seasonal, and interannual). Grazing and warming treatments had markedly differenteffects on CO2 fluxes in the two tundra habitats. Grazing caused a strong reduction in CO2

assimilation in the wet meadow, while warming reduced CO2 efflux from the mesic heath.Treatment effects on net ecosystem exchange largely derived from the modification of grossecosystem photosynthesis rather than ecosystem respiration. In this study we havedemonstrated that on the habitat scale, grazing by geese is a strong driver of net ecosystemexchange of CO2, with the potential to reduce the CO2 sink strength of Arctic ecosystems. Ourresults highlight that the large reduction in plant biomass due to goose grazing in the Arcticnoted in several studies can alter the C balance of wet tundra ecosystems. We conclude thatherbivory will modulate direct climate warming responses of Arctic tundra with implicationsfor the ecosystem C balance; however, the magnitude and direction of the response will behabitat-specific.

Key words: Arctic; Barnacle Goose; Branta leucopsis; carbon fluxes; climate change; herbivory;vegetation.

INTRODUCTION

High-latitude ecosystems have been important sinks

of carbon dioxide (CO2) from the atmosphere and

currently store approximately one-third of the global

soil carbon (C) pool (Gorham 1991, Prentice et al. 2001).

However, current estimations of the source–sink

strength of the Arctic suggest that source areas now

exceed sink areas (ACIA 2005). In order to understand

this change in the C balance of the Arctic it is essential to

quantify the impact of environmental drivers that either

reduce primary production or increase decomposition

and hence contribute to a loss of C sink capacity. This

study examines the influence on tundra C flux of two

environmental drivers: climate change, which operates

at a global scale, and herbivory, which operates at a

local scale. Climate warming has been shown to impact

Arctic ecosystem C fluxes through both vegetation and

decomposition processes; however, results have been

variable both temporally and spatially. For example,

early-season photosynthetic rates increased with exper-

imental warming at a wet sedge tundra site but these

effects diminished later in the growing season (Johnson

et al. 2000). Welker et al. (2004a) found that the effects

of experimental warming varied between two High

Arctic tundra sites, with increased net C uptake in dry

tundra and reduced C uptake in wet tundra. A meta-

analysis of the impact of warming on soil respiration

and plant productivity across a range of Arctic sites

showed generally increased soil respiration and above-

ground plant productivity as a result of experimental

warming (Rustad et al. 2001). Our understanding of the

manner in which herbivory influences ecosystem C

Manuscript received 2 October 2007; revised 19 December2007; accepted 2 January 2008. Corresponding Editor: R. W.Ruess.

5 E-mail: [email protected]

2103

balance is limited, and there are very few investigations

from high-altitude/-latitude environments. Two Arctic

studies suggest that grazing can strongly influence

ecosystem C fluxes in some habitats: grazing enhanced

C losses from an alpine grassland (Welker et al. 2004b),

but reduced soil respiration in Arctic tundra heath

(Stark and Grellmann 2002). Grubbing by geese early in

the growing season has also been found to reduce the C

sink strength of wet tundra in the High Arctic (Van der

Wal et al. 2007). Working in temperate grasslands,

Risch and Frank (2006) found no effect of grazing on

net ecosystem exchange (NEE) of CO2. Our study is, to

our knowledge, the first to address the combined role of

herbivores and climate warming as drivers of NEE and

its components, gross ecosystem photosynthesis (GEP)

and ecosystem respiration (Re), in Arctic ecosystems.

Global warming has been predicted to reduce the

high-latitude C sink strength by increasing decomposi-

tion to a greater extent than net primary production

(Kirschbaum 2000, Davidson and Janssens 2006). In

contrast, recent evidence of increased net primary

production in the Arctic supports global models of

plant productivity and soil decomposition processes that

suggest climate warming will actually enhance the C sink

strength of the Arctic (ACIA 2005). However, these

predictions are constrained by uncertainty associated

with soil, nutrient, and permafrost processes (Lemke

et al. 2007). There is also uncertainty over the magnitude

of these responses (Rustad et al. 2001), and it is likely to

be strongly spatially variable in relation to other factors

such as soil moisture availability (Welker et al. 2004a,

Sjogersten et al. 2006). One of the main controls of

ecosystem response to climate warming is the low

nutrient availability in high-latitude ecosystems (Press

et al. 1998, Arft et al. 1999, Jonasson et al. 1999, Hobbie

et al. 2002). If climate warming accelerates decomposi-

tion rates, then this has the potential to increase nutrient

availability and hence primary production (Hobbie et al.

1998, Rustad et al. 2001, van Wijk et al. 2004). On the

other hand, increased evapotranspiration in response to

higher temperatures and associated surface dryness can

reduce litter decomposition and soil respiration rates

and also reduce productivity of key vegetation compo-

nents, e.g., mosses and lichens, which are strongly linked

to moisture availability (Latter et al. 1998, Sjogersten

and Wookey 2002, Illeris et al. 2004, Rixen and Mulder

2005, Sjogersten et al. 2006). The balance of all such

responses will eventually dictate the change in C sink

strength of tundra ecosystems.

Herbivory is a strong local driver of ecosystem

function in high-latitude environments, controlling

vegetation biomass and composition, as well as physical

properties of the ecosystem (Person et al. 2003, van der

Wal 2006). We hypothesize that herbivores play a

central role in the C cycling and balance in Arctic

ecosystems by: (1) modifying aboveground biomass and

net primary production (Wilson and Jefferies 1996,

Welker et al. 2004b, McIntire and Hik 2005, Derner

et al. 2006), (2) influencing nutrient cycling (Bazely and

Jefferies 1986, Stark and Grellmann 2002, Zacheis et al.

2002, Olofsson et al. 2004, van der Wal et al. 2004), (3)

altering physical properties, such as soil moisture and

soil temperature (Zimov et al. 1995, van der Wal and

Brooker 2004, Gornall et al. 2007), and (5) altering litter

quality through changes in leaf chemistry of existing

species and through herbivore-driven changes in plant

species composition (Bardgett and Wardle 2003, Olofs-

son et al. 2004). Low levels of grazing may increase net

primary production relative to ungrazed swards (Hik

and Jefferies 1990, van der Graaf et al. 2005) that is

sustained by higher nutrient availability resulting from

faster nutrient turnover rates, largely due to the presence

of animal excreta or through incorporation of litter into

soil by trampling (Zacheis et al. 2002, Olofsson et al.

2004, van der Wal et al. 2004). Higher nutrient

availability also has implications for decomposition

rates (Stark et al. 2000, Olofsson et al. 2004), potentially

increasing CO2 efflux from soil and reducing soil C

storage (Mack et al. 2004, Welker et al. 2004b).

However, increased herbivore abundance can, in the

long term, reduce productivity and even cause severe

ecosystem deterioration (Handa et al. 2002, Ngai and

Jefferies 2004, Rietkerk et al. 2004, van de Koppel et al.

2005). For example, in Arctic Canada a dramatic

increase in the Lesser Snow Goose (Anser caerulescens

caerulescens) population has dramatically impacted salt

marsh ecosystems along the coast north of Hudson Bay

and led to complete suppression of plant productivity,

increased nutrient loss, and accelerated erosion of the

soil organic horizon (Srivastava and Jefferies 1996,

Jefferies et al. 2006).

Geese are the most abundant terrestrial vertebrate

herbivore in the Arctic (van der Wal 2005). In northwest

Europe and North America, arctic breeding goose

populations have increased due to land use changes

and reduced hunting pressure in their wintering grounds,

but also in response to increased food availability in

staging areas due to warmer temperatures (Abraham

et al. 2005, Fox et al. 2005, Gauthier et al. 2005, Kery

et al. 2006). There is concern that, as greater numbers of

geese utilize breeding areas throughout the Arctic

(Jensen et al. 2008, Wisz et al. 2008), ecosystem

degradation parallel to that along the Hudson Bay

coast could occur on a much wider pan-arctic scale. We

selected Spitsbergen as a High Arctic model system to

address this concern and explore the mechanisms by

which geese impact Arctic ecosystems. On Spitsbergen,

populations of both the Pink-footed Goose (Anser

brachyrhynchus) and the Barnacle Goose (Branta

leucopsis) have increased dramatically over the past 50

years. The current population on Spitsbergen is esti-

mated to be 40 000–50 000 Pink-footed Geese and

;24 000 Barnacle Geese (Fox et al. 2005, Wetlands

International 2006). This is of particular concern as the

Spitsbergen habitats are regarded as fragile; low

temperature and poor drainage in the region result in

SOFIE SJOGERSTEN ET AL.2104 Ecology, Vol. 89, No. 8

low plant cover and productivity, low nutrient avail-

ability, and vulnerability to erosion (Robinson et al.

1995, Gordon et al. 2001, van der Wal et al. 2007).

The overall objective of this study was to quantify the

impact of herbivory and climate warming on the C sink

strength of Arctic tundra and determine the mechanisms

by which goose grazing and warming influence growing

season NEE. A factorial combination of experimental

warming and grazing treatments was used in a three-

year field experiment in two habitats (mesic heath and

wet meadow) to test the following specific hypotheses:

(1) Goose grazing at both low and high intensity reduces

the C sink strength of mesic and wet tundra habitats,

and warming will exacerbate this response. (2) The

relative importance of grazing pressure will be greater

than that of warming as a driver of tundra C sink

strength.

MATERIALS AND METHODS

Site description

The study was conducted at two tundra sites (mesic

heath and wet meadow) in Adventdalen, a valley in

southcentral Spitsbergen, Norway (788100 N, 168060 E).

The mean annual temperature in the region is �6.78C,

the January mean temperature is �15.38C, and the July

mean temperature is 5.88C (1961–2000 average), reflect-

ing the oceanic climate in the area. The mean annual

precipitation is 190 mm (1988–2000 average). During the

short growing season, which extends from the end of

June to early August, air temperature is generally above

08C (Table 1; data available online).6 Landscapes are

underlain by permafrost, and surface soils begin to thaw

when air temperature rises in spring (June), the

maximum depth of thaw (in August) reaching 50–70

cm at the mesic site and 50 cm at the wet site. During

summer there is 24-h daylight; the range in photosyn-

thetically active radiation (PAR) was 1450–200

lmol�m�2�s�1 during the middle of the day and 250–50

lmol�m�2�s�1 at midnight. Until recently the study area

was not heavily used by geese; however, since 2002

increasing numbers of Pink-footed Geese and Barnacle

Geese have used the area as pre-breeding foraging

grounds (Fox and Bergersen 2005).

Two habitats representative of those used by geese

during their pre-breeding and breeding season were

selected for experimental work. The two habitats have

contrasting hydrology, one being a wet meadow along a

meandering meltwater stream and the other being a

more exposed and well-drained mesic heath located on

the outermost part of an alluvial fan. These habitats are

hereafter referred to as wet and mesic sites, respectively.

Vegetation at the mesic site is dwarf shrub/grass heath in

which dominant vascular plant species include Salix

polaris and Alopecurus borealis, with some Luzula

confusa and Bistorta vivipara and a 3–6 cm deep moss

mat largely composed of Tomenthypnum nitens, Hylo-

comnium splendens, and Sanionia uncinata providing

continuous ground cover. At the wet site there is also

continuous moss cover, the dominant moss being

Calliergon richardsonii forming mats of 1.5–13 cm deep.

The most abundant vascular plants are the grasses

Dupontia spp. and Calamagrostis stricta, contributing

;7% ground cover. Other species include Equisetum

arvense and some forbs, e.g., Cardamine nymanii.

Differences in hydrology, timing of snowmelt, and

exposure between the wet and mesic sites strongly

influence temperature in the rooting zone, with deeper

snow accumulation on the wet site preventing the

occurrence of very low soil temperatures characteristic

for the mesic site and the high water table in summer

buffering large temperature fluctuations. The daily mean

maximum and minimum soil temperatures (based on

hourly means measured at the moss/soil interface during

2004) were 9.48C and �7.58C at the wet site and 9.08C

and �19.18C at the mesic site. At the wet site there is a

relatively long period in autumn, of approximately three

months, compared to only one month at the mesic site,

during which the soil temperature fluctuates between

08C and �58C after the first excursion below 08C in

September. Whereas soil moisture content in the mesic

site gradually decreases over the growing season

(Gornall et al. 2007), at the wet site the soil is water

saturated throughout the growing season and is anoxic

below ;10–20 cm. Also the organic horizon differs

between the sites: at the wet site the organic horizon has

a variable depth with a large proportion of poorly

decomposed moss and tends to be mixed with silt, while

the organic horizon at the mesic site is shallower and

more decomposed (Table 2). Further site characteristics

are provided in Table 2. The mesic site is currently

TABLE 1. Mean air temperature and total precipitation atLongyearbyen airport, Spitsbergen (;10 km from the fieldsite), Norway, during the growing season (June–August) of2003, 2004, 2005, and the long-term average.

Year Air temperature (8C) Precipitation (mm)

2003 5.4 2.62004 5.1 24.42005 6.1 12.71961–1990 4.2 11.3

TABLE 2. Soil description of the two experimental sites (mean6 SE; n ¼ 5).

Characteristic Wet site Mesic site

Depth of live moss (mm) 10.0 6 0.9 3.1 6 0.3Total moss layer depth (mm) 43.5 6 4.7 15.0 6 1.4Organic horizon (mm) 63.0 6 4.7 39.7 6 3.1C:N ratio in the organic

horizon (top 2 cm)34.9 6 2.1 20.2 6 0.5

pH in the organic horizon 6.0 6 0.04 5.6 6 0.076 hwww.met.noi

August 2008 2105HERBIVORY, CO2 FLUXES IN A WARMER ARCTIC

lightly used as foraging ground by Pink-footed Geese

during a brief period in spring and is grazed by Svalbard

reindeer throughout the year (Rangifer tarandus platy-

rhynchus). Neither geese nor reindeer currently use the

wet site (in the case of geese due to a lack of safe

breeding ground while reindeer avoid the site probably

due to the deep boggy conditions), but the vegetation is

representative of other areas on Spitsbergen that are

intensely used by Barnacle Geese during the breeding

season.

Experimental design

To investigate the effects of grazing and climate

warming on CO2 flux at sites with contrasting hydrol-

ogy, we used a fully factorial randomized block design (n

¼5) with no, low, and high levels of grazing and ambient

and elevated temperature, i.e., six treatments in each

block. The blocks were located over a 1003 200 m area,

with a minimum distance between blocks of ;10 m.

Each block was fenced, and the plots were accessed via

boardwalks to eliminate trampling and damage around

the plots.

The grazing treatments were carried out during the

growing seasons of 2003, 2004, and 2005 using pairs of

adult wild captured Barnacle Geese. The Barnacle

Goose was selected since it is common and currently

expanding across Spitsbergen and has been successfully

used in field experiments (van der Wal et al. 1998). One

pair of geese was allowed to graze a 232 m plot for a set

time period of either 1 h or 5 h (low and high treatment,

respectively), to generate either ‘‘natural’’ or ‘‘high’’

grazing pressure. The geese were not allowed to graze

for 1 h prior to being placed on the plots. These grazing

treatments were repeated twice over the growing season,

in early July and in early August, apart from the last

season, when only the early July grazing event was

carried out to allow for a plant biomass harvest later

that month. After three years there was no significant

effect of grazing on soil temperature (P . 0.5) at either

site (Table 3). However, grazing reduced volumetric soil

moisture content from 0.35 6 0.01 to 0.31 6 0.03 m3/m3

at the mesic site (mean 6 SE; F2,38¼ 5.36, P , 0.01) and

increased volumetric moisture content from 0.7 6 0.07

to 1.0 6 0.03 m3/m3 at the wet site (F2,61 ¼ 3.35, P ,

0.05) as here the moss mat was compacted and its depth

reduced following trampling and grazing by geese; after

the high-grazing treatment the moss surface was level

with the water surface in several plots. The grazing

behavior of the geese was monitored during the

experimental grazing periods, and the time spent

foraging as well as the recorded fecal densities at the

end of the grazing periods confirmed that the ‘‘low’’-

grazing treatment corresponded to natural levels of

goose grazing, while ‘‘high’’ levels were up to twice the

grazing pressure recorded around Barnacle Goose

colonies elsewhere in Spitsbergen (Cooper et al. 2004).

The average time spent foraging during the 2003 and

2004 grazing events at the mesic site were 36 and 111

min per plot in the low- and high-grazing treatments,

respectively, and 59 and 254 min per plot at the wet site.

The greater amount of time spent grazing at the wet site

than at the mesic site reflects the natural grazing

preference of geese in these habitats.

Open-top chambers (OTCs) were used to generate

experimental warming of tundra, and were ‘‘ITEX’’ style

(International Tundra Experiment; Marion et al. 1997):

small, robust greenhouses that are suitable for remote

experimental sites. The polycarbonate hexagonal cham-

bers (0.5 m high, 1.5 m ‘‘internal’’ diameter) were

deployed at the onset of the growing season in 2003. The

OTCs were removed from the plots during grazing

treatments and then immediately replaced. At the wet

site the OTCs were left in place throughout the

experiment. At the wind-exposed mesic site the OTCs

were left in place the first winter but, due to concern

about snow accumulation, were removed from the plots

in September 2004 and replaced in spring 2005 as soon

as snow conditions allowed. Sampling from the warmed

plots was only undertaken in the center of each plot ;20

cm away from the inner edges of the OTC. The impact

of the OTCs on surface air temperature was measured

continuously by TinyTag data loggers (Gemini, Chi-

chester, UK) placed on the ground surface in control

and OTC plots at both the wet and the mesic sites.

Continuous logger measurement at the mesic site

demonstrated a warming effect; the OTCs increased

July mean air temperature at ground level by 1.48C on

average. The temperature data from the wet site were

strongly influenced by contact between the temperature

probes and surface water during the growing season and

hence there was no significant warming detected at the

ground surface. However, air temperature measurement

made 10 cm above the ground level within the cuvettes

used for NEE flux measurements showed that the OTCs

raised midday air temperature by ;1.58C at both sites

(based on five sets of measurements made during July

2005; F1, 119¼ 6.80, P , 0.05). The OTCs increased soil

temperature (at 7 cm depth) at the mesic site by ;18C

(F1,51¼ 19.65, P , 0.0001) but not at the wet site (P .

0.8), probably due to the high volumetric water content

of the soil. In summary, during the growing season the

OTCs increased air temperature (;1.58C) at both sites

and at the mesic site increased surface temperature

(;1.48C) and soil temperature (;18C at 7 cm depth).

CO2 flux measurements

Ecosystem CO2 fluxes were measured in all treatments

and replicates, at varying intensity over the three

growing seasons to capture the impact of the treatments

on a range of temporal scales. The main treatment

effects were investigated in the final growing season

through an intensive measurement campaign in July

2005, with five measurement series per plot, all of which

took place between 10:00 and 16:00. To assess interan-

nual variability (i.e., the cumulative treatment effect on

CO2 fluxes during the growing season over the


experimental period) we measured NEE of CO2 and Re

during daytime (10:00–17:00) on one occasion in each

experimental plot (n¼ 60) in July 2003, 2004, and 2005.

One complete set of measurements across all 60

experimental plots took approximately two weeks, so

the measurement point reflects a good cross section of

environmental conditions during peak biomass. To

assess the effects of treatments on diurnal fluctuations

in CO2 fluxes, 24-h measurements were carried out on

three occasions per plot in July 2005. For these

measurements the cuvettes were placed on the plots for

24 h, allowing CO2 fluxes to be measured continuously.

To quantify nighttime fluxes, NEE, Re, and GEP fluxes

were measured at midnight on one occasion in each of

three blocks at each site at peak biomass in late July

2005. A wider seasonal data set was collected in 2004

with measurements taken just after snow melt in June, at

peak biomass in July, and in late August after

senescence had started. Inevitably, the data collected

throughout the study were subject to a wide range of

environmental (light, temperature) and biological (e.g.,

plant phenology) conditions.

Ecosystem CO2 fluxes were measured with custom-

built cuvettes (30 cm diameter, 12-L volume) clamped to

steel rings inserted into the soil. Cuvettes were attached

to an EGM-4 infrared gas analyzer (IRGA; PP Systems,

Hitchin, UK; see Sjogersten et al. [2006] for details)

using an open dynamic system with a through-flow of 11

L/min (to avoid CO2, temperature, and pressure build-

up within the cuvettes), with measurements taken every

2 min. During the midday measurements both NEE and

Re were measured on each plot in the following

sequence: the system was allowed to equilibrate for 5–

10 min, NEE data were collected over the next hour, a

hood was placed over the cuvette to exclude light and

stop photosynthesis, the system was allowed 5–10 min to

equilibrate, and then Re was measured for 45 min. After

the initial period of equilibration, temperature or

humidity did not increase within the cuvette during the

measurement period. From each measurement period

mean values were determined for NEE and Re. To

obtain an estimation of GEP, the mean plot Re fluxes

were subtracted from the mean plot NEE fluxes for each

measurement period. The midday measurements illus-

trate maximum sink strength; negative CO2 flux values

indicate that the process (or system) acts as a sink of

CO2, while positive values represent an efflux of CO2 to

the atmosphere.

Photosynthetically active radiation, air temperature

(;10 cm above the ground surface), and humidity were

recorded simultaneously with the CO2 fluxes within the

cuvettes. Soil temperature was measured at 7 cm depth

with temperature probes (RS Components, Northants,

UK), and soil moisture was measured using a hand-held

Theta probe and meter (Delta-T Devices, Burwell, UK).

Three measurements were taken in each plot to

incorporate some of the spatial variation. On average,

cuvette air temperatures were ;38C higher during NEE

than Re measurements.

Winter CO2 flux measurement with soda lime traps

Soda lime traps were used to estimate overwinter CO2

fluxes (Grogan and Chapin 1999), i.e., from when the

soils froze in autumn until snowmelt in spring. Soda lime

was dried for 48 h prior to the experiment and allowed

to cool in a desiccator. In order to clear the soil pore

space of ‘‘old’’ CO2 and allow only newly respired CO2

to be absorbed by the soda lime left in place over winter,

we used a two-stage approach. First, in each plot a cup

filled with 15 g of soda lime was placed in a 1-dm3

headspace that was carefully inserted into the soil for 48

h. These initial samples were then replaced by fresh

samples of ;40 g of soda lime to which 15 mL of

distilled water had been added to maximize the CO2

absorption capacity at low temperatures (Grogan and

Chapin 1999). The rim of the headspace was inserted ;4

cm into the soil, thereby ensuring that a good seal was

obtained, and left in place over winter. At snowmelt the

headspace was removed and the soda lime was collected

in airtight containers, brought to the laboratory, and

dried for 48 h and weighed. The dry mass increase was

then used to calculate the uptake of CO2 by the soda

lime. To account for uptake of atmospheric CO2 during

handling and processing (e.g., weighing, collection) four

additional samples were placed in closed containers at

each of the two sites. The CO2 absorption in these

‘‘blanks’’ was low (i.e., ,5% of the CO2 absorbed by the

soda lime on the experimental plots was due to uptake of

atmospheric CO2 during handling of the samples) and

was subtracted from the experimental samples prior to

flux calculation. We expected the fluxes calculated from

the soda lime traps to overestimate soil respiration rate

since the traps are likely to (1) create a very sharp

concentration gradient (unlike the IRGA system), (2)

‘‘suck’’ CO2 from a larger soil volume than just under

the headspace, and (3) raise the temperature until the

plots and headspace containers were snow covered.

Since the soda lime traps were placed directly on the

ground rather than on top of the snowpack we do not

expect diffusion through the snowpack to influence our

estimates of overwinter CO2 efflux. The flux rates

calculated from the soda lime traps therefore cannot

be directly compared to the summer fluxes, and in this

paper we use this method only to investigate the relative

effect of the experimental treatments over the winter

period, rather than to attempt annual flux budgeting.

Plant biomass and soil data collection

To determine the relationship between CO2 flux

measurements and the vegetation at each site one 7 3

7 cm turf was removed from at the mesic site, while one

slightly larger turf of 10310 cm was collected from each

plot at the wet site at peak biomass in 2005. These turfs

were collected from the same locations as were the CO2

measurements to enable direct comparison between CO2


fluxes and vegetation. In addition, another three 7 3 7

cm turfs were removed from all plots at the mesic site.

At the wet site two additional turfs of 10 3 10 cm were

collected from each plot at peak biomass. The depths of

the live moss mat, the total moss layer, and the organic

horizon were recorded for each turf. The vegetation was

separated into above- and belowground biomass and

litter. The aboveground vegetation (defined as live

vascular plant material in and above the live moss

layer) was separated into functional groups. The moss

biomass fractions were further separated into photosyn-

thetically active (green) and the brown fractions below

that. The belowground biomass was determined after

root washing. Root material from the wet site was

contaminated with mosses, and a correction factor,

obtained through microscopic inspection (50 subsamples

per sample), was applied to derive a comparable

measure of belowground biomass. The samples collected

for belowground biomass included roots in the organic

and top mineral soil but not deeper mineral soil material

(below 20 cm) that contained some roots at the wet site.

Hence, the root biomass at the wet site might be a slight

underestimation. Samples were dried for 48 h at 708C

prior to weighing. The result from the biomass harvest,

based on all four turfs collected from the mesic site and

the three turfs collected from the wet site, is presented in

the Appendix. The C and N contents of the plant

fractions and soil in the top 2 cm below the moss–soil

interface were analyzed on a Carlo Erba NA1500

elemental analyzer (Carlo Erba, Milan, Italy). Microbial

biomass C and N in soil sampled from each plot at peak

biomass in 2005 was quantified using the fumigation

extraction method (Vance et al. 1987), and the extracts

were analyzed for total organic carbon (TOC) and

nitrogen (TN). Fresh soil samples from the organic

horizon were passed through a 4-mm sieve and 5-g

subsamples were fumigated in a chloroform atmosphere

for 24 h. Control and fumigated samples were extracted

in 25 mL 0.5 mol/L K2SO4 by shaking for 30 min and

then filtered using Whatman 42 filter paper. The extracts

were frozen and analyzed for TOC and TN using a total

organic carbon (TOC)-V1 analyzer with a total nitrogen

(TN) M-1 unit (Shimadzu, Milton Keynes, UK).

Data analysis

Data were analyzed in SAS for Windows version 8.2

(SAS Institute, Cary, North Carolina, USA) primarily

using generalized linear mixed models (GLMM). These

models were fitted for each of the two contrasting sites

separately by the method of residual maximum likeli-

hood (REML) with ‘‘block’’ as a random effect.

Denominator degrees of freedom were estimated using

Satterthwaite’s approximation (Littell et al. 1996), and

the residual variances were modeled as constant to the

mean using PROC MIXED. Autocorrelation between

measurements within plots was modeled as a first-order

autoregressive (AR 1) process (i.e., repeated measures).

At the mesic sites there were some occasions in which

NEE exceeded Re. In the data analysis we included all

NEE data points, but photosynthesis (GEP) data pointsfor which NEE . Re were set to zero as discussed in

Sjogersten et al. (2006).Treatment effects on NEE, Re, and GEP were

analyzed using grazing and warming as fixed effects.Covariates were incorporated thereafter to further

improve model fit and allow better interpretation ofsignificant treatment effects. A wide array of covariateswas tested but only those that contributed significantly

to the models are reported in Results. Interannualvariation in treatment effects was analyzed for by

comparing NEE, Re, and GEP fluxes from July in year1 with those in year 3 to determine whether there was a

build-up of treatment effects over time, i.e., determiningthe significance of the terms year3grazing, year3OTC,

and year 3 grazing 3 OTC. Diel variation in NEE wasassessed on the basis of 24-h measurement runs from

which aggregated hourly means (i.e., only a single valueper plot per hour) were calculated. To highlight

differences in diurnal patterns among treatments,smoothing curves were fitted through the data using

generalized additive model (GAM) procedures. Differ-ences between treatments in this data set were tested for

at midday (10:00–14:00) and midnight (22:00–02:00),allowing only a single mean per period per plot tocontribute to the analysis. Seasonal variation in NEE,

Re, and GEP was examined by establishing whether‘‘season’’ fitted as a fixed factor with three levels (June,

July, August, using data from the second experimentalseason) significantly explained variation in the data.

Subsequently, the effects of grazing at the wet site andwarming at the mesic site were tested for in each of the

three time periods separately. Overwinter CO2 fluxeswere analyzed by first determining differences between

the wet and mesic site in a GLMM, after whichtreatment effects were tested for in site-specific models.

RESULTS

Treatment effects on CO2 fluxes

The grazing and warming treatments had markedly

different effects on the net CO2 fluxes at the two sites(Fig. 1). Grazing caused a strong reduction in CO2

assimilation at the wet site reflecting the higher grazingintensity at this site. This reduction was still detectable

by the end of July (approximately three weeks after thegrazing treatment was applied). At the mesic site

warming reduced CO2 efflux throughout the growingseason. Note that the mesic site generally acted as a

source of CO2 over the measurement period, whichlikely reflects increased soil respiration in response to

higher-than-average summer temperature (Table 1).Treatment effects on NEE largely derived from the

modification of GEP rather than Re.The strong reduction in C sink strength (i.e., less

negative NEE in Fig. 1a) in response to the grazing inthe wet habitat, by 44% and 99% for the low- and high-

grazing treatment, respectively, was driven by a reduced


CO2 assimilation (less negative GEP in Fig. 1c), while Re

was unaffected (Fig. 1b). An even tighter, but qualita-

tively similar, negative effect of grazing on NEE was

established after taking into account variation due to air

and soil temperature (see Table 3). Biomasses of

photosynthetically active moss and aboveground vascu-

lar plants were both strong predictors of NEE at the wet

site, largely accounting for the observed grazing effect

(Table 3). This indicates that the reduction in NEE from

grazing was largely vegetation driven, as illustrated by

the significant relationship of both NEE and GEP with

live plant biomass (Fig. 2). While grazing strongly

influenced NEE at the wet site, the warming treatment

was found to have no effect on NEE and only subtly

increased Re and GEP (Table 3). The fact that the

warming effect on Re and GEP was no longer significant

after accounting for variation in air and soil temperature

(and for GEP also light levels) suggests that temperature

influenced Re and GEP directly and not indirectly

through effects of the OTC treatment on plant biomass.

The effect of warming on CO2 fluxes at the mesic site

was generally greater than the effects of grazing (Fig. 1,

Table 3). The overall effect of the warming treatment on

NEE was a 61% reduction in CO2 efflux (less positive

NEE) compared to controls. The warming treatment

enhanced both Re and GEP (i.e., more positive Re and

more negative GEP in Fig. 1), and the resulting warming

effect on NEE was due to a greater response in GEP

than Re. Both Re and GEP were greatest in plots subject

to low-level grazing and warming, while in plots with

low-level grazing under ambient temperature, Re and

GEP were reduced (i.e., less positive and negative,

TABLE 3. Statistical summary table showing (1) fixed effects (i.e., grazing and warming using open-top chambers [OTC]) on netecosystem exchange (NEE), ecosystem respiration (Re), and gross ecosystem photosynthesis (GEP) at the (a) wet site and (b)mesic site.

Effects, by site

NEE Re GEP

F df P F df P F df P

a) Wet site

Fixed effects

Grazing 6.35 2, 26 ,0.01 11.67 2, 34 ,0.0001OTC 6.00 1, 35 ,0.05 3.65 1, 34 0.06

Abiotic effects

log(PAR) 29.52 1, 126 ,0.0001Tair 150.47 1, 123 ,0.0001 11.13 1, 125 ,0.05Tair

2 24.82 1, 120 ,0.0001 8.21 1, 121 ,0.01 5.39 1, 117 ,0.05Tsoil

2 5.44 1, 119 ,0.05 6.94 1, 120 ,0.01OTC 0.42 1, 25 0.5 1.77 1, 26 .0.15Grazing 9.64 2, 25 ,0.001 11.85 2, 24 ,0.001

Biotic effects

Moss 7.06 1, 26 ,0.05 9.08 1, 25 ,0.01Vascular 10.93 1, 25 ,0.01 16.20 1, 28 ,0.001Grazing 2.58 2, 24 0.1 2.20 2, 24 .0.1

b) Mesic site

Fixed effects

Grazing 8.32 2, 34 ,0.01OTC 3.75 1, 32 0.06 15.99 1, 41 ,0.001 48.68 1, 34 ,0.0001OTC 3 grazing 2.57 2, 41 0.09 8.20 2, 34 ,0.01

Abiotic effects

Tair 9.88 1, 93 ,0.01 86.99 1, 86 ,0.0001 40.60 1, 89 ,0.0001Tsoil 4.60 1, 110 ,0.05 5.07 1, 125 ,0.05OTC 5.59 1, 32 ,0.05 9.18 1, 33 ,0.01 35.71 1, 30 ,0.0001Grazing 7.64 2, 28 ,0.01OTC 3 grazing 3.01 2, 31 0.06 8.72 2, 28 ,0.01

Biotic effects

CN 7.33 1, 25 ,0.05Moss 2.97 1, 30 0.09Vascular 4.01 1, 29 0.05 7.60 1, 35 ,0.01 6.09 1, 27 ,0.05OTC 8.16 1, 31 ,0.01 5.48 1, 30 ,0.05 27.78 1, 29 ,0.0001Grazing 4.69 2, 26 ,0.01OTC 3 grazing 3.90 1, 31 ,0.05 6.60 2, 26 ,0.01

Notes: Significant statistics for the fixed effects are also reported in Fig. 2. Additional statistics show how stepwise fitting ofabiotic and biotic covariates accounts for the variation in the model and the residual variation attributed to the grazing and open-top chamber (OTC) treatments after fitting the covariates. A wide array of covariates (values in italics) was tested for, and onlythose that contributed significantly to the models are reported here, i.e., air temperature (Tair), soil temperature (Tsoil), the C:N ratioin the top 2 cm of soil (C:N), green moss biomass (Moss), photosynthetically active radiation (PAR), and aboveground vascularbiomass (Vascular).


respectively, in Fig. 1). The significant effect of the

warming treatment on Re and GEP was partly

attributable to a direct response to elevated air and soil

temperatures (Table 3). However, vascular plant bio-

mass was a significant covariate and absorbed some of

the variation previously attributed to the warming

treatment, while microbial biomass did not explain any

of the variation in Re. It therefore seems plausible that

the treatment effects on the CO2 fluxes were driven by a

combination of increased plant biomass and enhanced

physiological activity (both plant and microbial) in

response to the elevated temperature rather than

increased biomass per se.

A comparison between the CO2 fluxes (NEE, Re, and

GEP) measured approximately one month after the

experiments were initiated and the final (third) year

showed that there was no change over time in the

treatment effect of either the grazing at the wet site (P .

FIG. 1. Effects of the grazing and warming treatments on CO2 fluxes at the wet and mesic study sites. Values shown are meansand SE based on measurements made at midday throughout July 2005 (five occasions) for (a, d) net ecosystem exchange of CO2, (b,e) ecosystem respiration, and (c, f) gross ecosystem photosynthesis. Negative values indicate CO2 assimilation, and positive valuesindicate CO2 efflux. The statistics shown are significant main effects and their interaction only. The study was conducted at twotundra sites (mesic heath and wet meadow) in Adventdalen, a valley in southcentral Spitsbergen, Norway.


0.5) or the warming at the mesic site (P . 0.6) or for the

interaction between the two treatments. This suggests

that the two habitats responded rapidly to the grazing

and warming treatments, respectively, and that treat-

ment effects on CO2 fluxes at peak biomass were

sustained, but did not increase from the first to the

third experimental year.

Temporal variation in CO2 fluxes in response

to the treatments

Net ecosystem exchange in July showed a clear

diurnal signal despite 24-h light throughout the mea-

surement period. Treatment effects on NEE prevailed

during midday, both the grazing effect at the wet site

(F2,18 ¼ 13.43, P , 0.001; Fig. 3a) and the warming

effect at the mesic site (F1,14¼18.03, P , 0.001; Fig. 3b),

while at night treatments ceased having any effect on

NEE (P . 0.7). The diurnal signal was stronger at the

wet site in response to the greater assimilation of CO2 at

midday; however, this diurnal pattern was flattened

significantly by the application of grazing (Fig. 3a).

Measurements of Re and GEP during the night at peak

biomass confirmed that the daytime grazing effect on the

wet site diminished overnight as suggested by the diurnal

measurements of NEE. At the mesic site, consistently

higher night-time Re and GEP, in parallel with the

daytime fluxes in Fig. 2, were found in warmed plots

(F1,9 ¼ 10.30, P , 0.05 and F1,9 ¼ 42.41, P , 0.0001,

respectively), suggesting that temperature limited both

respiration and photosynthesis at midnight at this High

Arctic site. Additionally, grazing reduced night-time

respiration under ambient conditions, whereas it was

enhanced under warmed conditions (grazing 3 OTC:

F2,9 ¼ 4.09, P ¼ 0.05), similar to the effects of warming

and grazing seen during daytime. The diurnal patterns in

CO2 fluxes further illustrate the contrasting effect the

warming and grazing treatments had on the vegetation

and microbial activity at the two sites.

As expected, the CO2 fluxes showed strong seasonality

both at the wet and the mesic sites, with very low GEP

and Re directly after snowmelt in June, maximum values

in July, and reduced values thereafter in late August. As

a result, NEE was also strongly seasonal at both the wet

site (F2,57¼ 27.03, P , 0.0001) and the mesic site (F2,66¼10.95, P , 0.001). Seasonality was most pronounced at

the wet site, where NEE was generally low in June and

peaked in July, and by onset of autumn, the activity was

clearly reduced again (0.08 6 0.10, �1.16 6 0.20, and

0.30 6 0.19 lmol C�m�2�s�1, respectively). Only in July

did the wet site act as a sink of CO2. The mesic site, on

the other hand, acted as a source of CO2 to the

atmosphere throughout, with maximum efflux in July

(0.68 6 0.18, 1.92 6 0.32, 0.85 6 0.14 lmol C�m�2�s�1,for June, July, and August, respectively).

Overwinter Re was 53% greater in the warming

treatment at the wet site but no significant warming

effect was found at the mesic site (Fig. 4), probably due

to the removal of the OTCs from the mesic site during

winter. The OTCs increased surface temperature during

the freeze-up period (September–October) by ;0.68C at

the wet site and this may have accounted for the higher

Re. The lack of response to the warming treatment over

winter at the mesic site therefore only indicates that

there was no sustained impact of the summer warming

on ecosystem C fluxes during the cold season. The

grazing treatments did not affect overwinter Re, either at

the wet site or the mesic site, suggesting that the negative

effects of the grazing on the ecosystem C sink capacity

FIG. 2. Relationship between total live aboveground plantbiomass at the wet site and (a) net ecosystem exchange of CO2,(b) ecosystem respiration, and (c) gross ecosystem photosyn-thesis. The CO2 fluxes in the regression are mean values basedon measurements made at midday throughout July 2005 (fiveoccasions); negative values indicate CO2 assimilation, andpositive values indicate CO2 efflux.


seen during summer were not compensated for by

reduced CO2 emission in grazed plots during winter at

the wet site. Winter Re (including the prolonged freeze-

up period in September–October and the thaw period in

June) was higher at the mesic site than at the wet site

(F1,8 ¼ 7.81, P , 0.05). Winter flux rates were an order

of magnitude lower than summer fluxes; however, the

different methods used for summer and winter flux

measurements limit the comparison to treatment effects

rather than actual rates. The ‘‘winter’’ measurements do

not allow a separation of autumn and spring from the

coldest winter period. It is, however, likely that a large

part of the respiration occurred during the autumn and

spring periods when soil temperatures were higher.

DISCUSSION

Habitat-specific responses to grazing and warming

In this study we have demonstrated that grazing by

geese can be a strong driver of net ecosystem exchange

of CO2 during the growing season, with the potential to

reduce the CO2 sink strength of Arctic ecosystems. Our

results highlight that the large reductions in plant

biomass associated with goose grazing across the Arctic

(Gauthier et al. 1995, Ngai and Jefferies 2004, van der

Wal et al. 2007) have direct implications for the C

balance of wet tundra ecosystems. In the wet system

warming had little impact on CO2 assimilation during

the growing season and did not compensate for the

reduction in the C sink strength in response to grazing;

in fact, warming increased CO2 efflux during the winter

period. However, in the mesic heath the warming

treatment reduced the CO2 efflux and the combination

of warming and low-level grazing altered the C balanceduring the growing season from a source to a weak net

sink of CO2. Taken together this illustrates that grazing

can result in either increased or decreased C sinkstrength depending upon the habitat and the climatic

conditions, but for the most part grazing reduced the

CO2 sink strength of the wet habitat. The contrasting

FIG. 3. Diurnal variation in net ecosystem exchange (NEE) of CO2 comparing treatment effects of (a) the grazing treatment atthe wet site (solid black, gray, and open symbols are high, low, and no grazing, respectively; circles and diamond symbols areambient and warmed, respectively) and (b) the warming treatment at the mesic study site (open and solid symbols are ambient andwarmed, respectively; diamonds, squares, and circles symbols are high, low, and no grazing, respectively). The splines aregeneralized additive model (GAM) functions that optimally (all P , 0.0001) describe the diurnal variation in NEE in relation to themost influential treatment at each site, i.e., the grazing treatment at the wet site and the warming treatment at the mesic site.

FIG. 4. Winter CO2 fluxes (mean þ SE), i.e., from earlySeptember to early June, in relation to the warming treatmentat the wet and the mesic study sites. The OTCs are open-toppedpolycarbonate warming chambers. Statistics are given only forthe wet site because they are not significant for the mesic site.


impact of grazing seen in the two habitats reflects

natural differential habitat use by geese (in that they

grazed more intensively in the wet habitat) as well as the

wet and loose structure of the moss surface at the wet

site, which makes it sensitive to grazing and trampling.

The different treatment responses also reflect results

reported in the literature from a variety of experimental

manipulations of temperature and nutrient availability

in Arctic ecosystems, in which treatment response is

more strongly dependent upon habitat type than the

level of treatment per se (Robinson et al. 1995, Arft et al.

1999, Rustad et al. 2001, van Wijk et al. 2004, Welker

et al. 2004a). In addition to the different habitat

responses to grazing, herbivory is in itself highly

spatially varied due to forage availability and other

constraints such as availability of safe breeding and

moulting sites in the case of geese (Loonen et al. 1997).

Indeed, the wet habitat type that proved most sensitive

to grazing in our experiment also is the one most utilized

by geese. Thus, in addition to differential habitat

sensitivity to grazing, differential habitat utilization

means that some areas will be strongly influenced by

herbivory, while in other locations the effects of grazing

will be small (van der Wal 2005). Indeed, our study

demonstrates that understanding the mechanisms deter-

mining habitat sensitivity is key to realistic prediction of

ecosystem response to environmental change.

Drivers and processes governing CO2 flux responses

The grazing effects on NEE at the wet site resulted

principally from the reduction of aboveground plant

biomass. By contrast, warming-related differences in

CO2 fluxes at the two sites were largely due to direct

temperature effects leading to enhanced plant and/or

soil physiological activity rather than due to increased

plant or microbial biomass. The significant interaction

between warming and the low-grazing treatment for

both photosynthesis and ecosystem respiration at the

mesic site suggests that plant and microbial activity can

increase in response to the combination of enhanced

temperature and grazing, possibly due to enhanced

nutrient input from the goose droppings having an

impact on the soil environment as well as allowing

compensatory plant biomass production in response to

the grazing (Hik and Jefferies 1990). These findings link

with a study in an alpine area where reduced ecosystem

C storage was found when grazing by livestock was

removed, possibly as a response to nutrient limitation

and lower soil temperature in ungrazed conditions

(Welker et al. 2004b).

In contrast to the mesic site, the lack of a ‘‘nutrient

response’’ of the CO2 fluxes at the wet site suggests that

(1) either the microbial community or the part of the

plant community that contributes most to CO2 assim-

ilation did not access the nutrients derived from goose

feces, (2) the response was insignificant compared to the

reduction in assimilation due to loss of biomass, or (3)

the anaerobic conditions at the wet site controlled

decomposition rates to a large extent, limiting any

potential nutrient response of microbial respiration.

Differences in nutrient responses between the wet and

the mesic sites may be partially explained by two factors.

First, the shallower rooting depth at the mesic site may

have provided vascular plants with greater access to the

nutrients, and second, at the wet site the nutrients may

have been more effectively absorbed by the deeper live

moss mat, and since mosses have lower photosynthesis

rates compared to vascular plants, this would reduce the

GEP response to nutrient addition (Gordon et al. 2001,

Jobbagy and Jackson 2001). Our study shows that Re

and GEP in mesic heath were highly responsive to the

combination of herbivory and warming, while CO2

fluxes in wetland areas appeared more resilient to

increased nutrient input but highly responsive to

herbivore-driven plant biomass removal.

Temporal variability

Both grazing and warming had immediate effects on

the CO2 fluxes at the start of the experiment, but their

effects varied diurnally and seasonally. The stark

reduction in CO2 sink strength in response to the

grazing treatment at the wet site was confined to

daylight hours and the growing season, which coincides

with periods of greatest plant photosynthetic activity.

The warming effect was less sensitive to diurnal

variation and enhanced CO2 effluxes over winter. The

trend for increased C losses associated with winter

warming at the wet site suggests that increased winter

temperature would further enhance the loss of CO2 sink

capacity at this site. Increased CO2 fluxes in response to

warming during autumn have been found elsewhere in

the High Arctic (Mertens et al. 2001), suggesting that

this is a key period determining the impacts of warming

on the annual C budget. Indeed, winter respiration

offsetting summer assimilation in Arctic regions has

recently been reported both from Northern Scandinavia

and the High Arctic (Heikkinen et al. 2004, Welker et al.

2004a, Grogan and Jonasson 2005). The winter fluxes

we detected here are relatively high compared to those

measured with similar methodology by Welker et al.

(2004a) in High Arctic Canada. The high flux rates are

possibly linked to the high organic content in these soils

and a prolonged autumn period of soil temperature just

below zero; microbial activity may continue to as low as

�108C in Arctic soils (Grogan and Chapin 1999, Mikan

et al. 2002, Michaelson and Ping 2003).

Long-term effects of herbivory relative to warming

During this relatively short-term experiment the

immediate vegetation responses, rather than the soil

system, played the key role determining the impact of

external environmental drivers on the ecosystem C

balance. Increased assimilation in response to warming

and in response to combined warming and low-level

grazing at the mesic site might result in higher biomass

in the longer term. A positive feedback of higher


biomass and reduced physiological constraints on

photosynthesis can reduce CO2 effluxes, providing

greater plant growth does not result in stronger nutrient

limitation (Arft et al. 1999, Ngai and Jefferies 2004).

However, the positive interaction between the grazing

and the warming treatment on Re is potentially linked to

enhanced heterotrophic respiration rather than plant

respiration associated with the higher assimilation. In

this study, significant soil warming was only achieved at

the mesic site (being absent at the wet site due to its

riverine nature). However, both climate change and

grazing are predicted to increase both thaw depth and

soil temperature (Prentice et al. 2001, Gornall et al.

2007), and increased soil temperature is likely to increase

ecosystem respiration rates significantly, as illustrated by

the direct effect temperature had on CO2 fluxes in our

study. The high C:N ratios (;35 and 20 at the wet and

mesic sites, respectively) in the organic horizon suggest

that decomposition processes are nutrient limited

(Hobbie et al. 2002), although the recalcitrant nature

of moss litter will also constrain the decomposition

process. We suggest that the long-term effects of climate

warming and herbivory on ecosystem C fluxes will be

modulated by a habitat’s ability to recover from biomass

removal (with access to nutrients from animal excreta

for the plant and microbial community playing a key

role) and the extent to which thicker vegetation will

insulate the soil surface, maintaining low soil tempera-

tures.

In addition to the effects of warming and grazing on

the present vegetation, both long-term warming (Walker

et al. 2006) and grazing (van der Wal 2006) are likely to

restructure plant species composition. In this study, for

example, selective foraging by geese reduced the

graminoid biomass at the wet site, resulting in a more

moss-dominated plant community. Such a shift toward

mosses lowers the photosynthetic capacity of the

vegetation and makes it more sensitive to surface drying

(Uchida et al. 2002, Sjogersten et al. 2006). This shift in

plant species composition will reduce the C input to the

soil and also reduce Re rates in the long term in response

to the recalcitrant litter with low decomposition rates

produced by moss-dominated vegetation (Dorrepaal

et al. 2005).

Conclusion

We conclude that herbivory will modulate climate

warming responses of Arctic tundra, with implications

for the ecosystem C balance; however, the magnitude

and direction of the response will be habitat-specific.

Generally, effects of grazing and warming on ecosystem

C balance were strongly driven by vegetation responses.

The most probable scenario is that increased popula-

tions of Arctic breeding geese will reduce C sink strength

in wetlands that are used most extensively for foraging.

In the extreme case that goose populations increase to

an extent at which all wet areas are used and also mesic

heath areas becoming more widely grazed by geese, CO2

efflux from these areas is likely to be unaffected, or

reduced, under conditions of climate warming due to

enhanced CO2 assimilation by the vegetation. This study

demonstrates clearly that the net effect of increased

herbivory and climate warming on CO2 fluxes across the

Arctic landscape will be strongly linked to the spatial

distribution of plant communities and their herbivoresand the sensitivity of the habitat. Indeed, on the local

scale herbivory can dramatically reduce the CO2 sink

strength of Arctic wetlands.

ACKNOWLEDGMENTS

This work was funded by the European CommissionFramework 5 grant number EVK2-CT-2002-00145 (FRA-GILE). We are grateful to the University Centre on Svalbard(UNIS) for logistical support. We also thank Jani Mannikko,Sam Philips, Anne-Mette Pedersen, and Katrin Sjogersten forfieldwork assistance, the FRAGILE team as a whole for theircontribution to the collection of biomass data, and Ad Huiskesfor chemical analysis of soil C and N.

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APPENDIX

Above- and belowground vascular biomass, live moss tissue, and vascular and moss litter in relation to the treatments at themesic and wet sites and the treatments after three years of experimental manipulation (Ecological Archives E089-121-A1).


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HABITAT TYPE DETERMINES HERBIVORY CONTROLS OVER CO 2 FLUXES IN A WARMER ARCTIC