EFFECTS OF CLIMATE AND ECOSYSTEM DISTURBANCES ONBIOGEOCHEMICAL CYCLING IN A SEMI-NATURAL TERRESTRIAL

ECOSYSTEM

CLAUS BEIER1∗, INGER KAPPEL SCHMIDT2 andHANNE LAKKENBORG KRISTENSEN3

1 RISØ National Laboratory, P.O.B. 49, DK-4000 Roskilde, Denmark; 2 Danish Forest andLandscape Research Institute, Hørshom Kongevej 11, DK-2970 Hørsholm, Denmark; 3 DanishInstitute of Agricultural Sciences, Dept. of Horticulture, P.O.B. 102, DK-5792 Aarslev, Denmark

(∗ author for correspondence, e-mail: claus.beier@risoe.dk; phone: +45 4677 4161;fax: +45 4677 4160)

(Received 8 May 2002; accepted 15 May 2003)

Abstract. The effects of increased temperature and potential ecosystem disturbances on biogeo-chemical cycling were investigated by manipulation of temperature in a mixed Calluna/grass heath-land in Denmark. A reflective curtain covered the vegetation during the night to reduce the heat lossof IR radiation from the ecosystem to the atmosphere. This ‘night time warming’ was done for 3years and warmed the air and soil by 1.1 ◦C. Warming was combined with ecosystem disturbances,including infestation by Calluna heather beetles (Lochmaea suturalis Thompson) causing completedefoliation of Calluna leaves during the summer 2000, and subsequent harvesting of all abovegroundbiomass during the autumn. Small increases in mineralisation rates were induced by warming andresulted in increased leaching of nitrogen from the organic soil layer. The increased nitrogen leachingfrom the organic soil layer was re-immobilised in the mineral soil layer as warming stimulatedplant growth and thereby increased nitrogen immobilisation. Contradictory to the generally moderateeffects of warming, the heather beetle infestation had very strong effects on mineralisation rates andthe plant community. The grasses completely out-competed the Calluna plants which had not re-established two years after the infestation, probably due to combined effects of increased nutrientavailability and the defoliation of Calluna. On the short term, ecosystem disturbances may have verystrong effects on internal ecosystem processes and plant community structure compared to the morelong-term effects of climate change.

Keywords: defoliation, ecosystem disturbance, experimental manipulation, ecosystem response,heathland, nitrogen cycling, temperature increase, warming

1. Introduction

Historical records show an increase in global mean temperatures of 0.6 ◦C overthe last 100 years (Houghton et al., 2001), which has co-occurred with elevatedatmospheric CO2 (Watson et al., 1991; Luxmoore et al., 1998). The increase overland has been due mainly to an increase in the diurnal minimum temperatures(Tmin), which have increased twice as much as maximum temperatures (Tmax),primarily because of increased cloudiness (Watson et al., 1995). Scenarios foranthropogenic emissions of CO2 and other greenhouse gases have been predicted

Water, Air, and Soil Pollution: Focus 4: 191–206, 2004.© 2004 Kluwer Academic Publishers. Printed in the Netherlands.

192 C. BEIER ET AL.

to cause increased global temperatures of 1–3.5 ◦C and changes in precipitationpatterns with more severe droughts and floods (Watson et al., 1995).

Temperature and water are the main drivers for many biological and chemicalprocesses and climatic changes are therefore likely to have a large influence on thefunctioning of natural and semi-natural environments (Watson et al., 1995). Partic-ularly, global warming is expected to stimulate mineralisation processes leadingto increased loss of C and nutrients, but also stimulating plant growth leadingto increased C fixation and nutrient immobilisation (Shaver et al., 2000). In arecent meta-analysis study synthesising results from a large number of warmingexperiments, a general warming-induced increase in soil respiration of 20% andin nitrogen mineralisation of 46% was found, while the effects on biomass accu-mulation were less clear (Rustad et al., 2001). The net result of these processesdetermines the overall feedback between carbon cycle and climate, and thereby theacceleration or deceleration of the global warming (Shaver et al., 2000). Increasedmineralisation may lead to other effects, such as increased nutrient availability. Ifnutrient availability exceeds plant and microbial demand, nutritional constraints onthe ecosystem will be altered and increase the potential, not only for plant growth,but also for changes in species composition (Heil and Bobbink, 1993) and nutrientlosses by leaching to ground or surface waters (Lukewille and Wright, 1997). Inthis sense global warming may have cascading effects on biogeochemical pro-cesses silimar to those that have been described for increased atmospheric nitrogeninput to terrestrial ecosystems (Galloway and Cowling, 2002).

Also, vegetation defoliation can cause disturbance to biogeochemical cyclingin terrestrial ecosystems. In Calluna heathlands, infestation by heather beetles(Lochmaea suturalis Thompson) is a naturally occurring disturbance that can causecomplete defoliation of the Calluna vegetation and have major effects on biogeo-chemical cycling in heathlands (Heil and Bobbink, 1993). Defoliation increases thetransfer of litter and frass to the soil, increases light penetration, and reduces plantnutrient uptake leading to accelerated decomposition of the top organic soil layer,increased N mineralization, and leaching of soluble organic matter and nutrientsto deeper soil layers (Kristensen and McCarty, 1999; Nielsen et al., 2000). Manyof the biogeochemical processes affected by such ecosystem disturbances also areaffected by climatic changes, and ecosystem disturbances therefore are likely to in-teract with climatic changes to amplify or reduce the effects. However, interactionsbetween climate and ecosystem disturbances and the effects on biogeochemicalcycling are little known.

The present paper describes a field scale manipulation experiment in a Danishheathland as part of the EU-projects CLIMOOR (Climate Driven Changes in theFunctioning of Heath and Moorland Ecosystems) and VULCAN (VulnerabilityAssessment of Shrubland Ecosystems in Europe under Climatic Changes). Thetreatments included simulation of global warming. After one year of experimentalmanipulation, the site was severely affected by infestation with heather beetles, fol-lowed by cutting of the vegetation in an attempt to restore the Calluna vegetation.

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The aims of the present paper are to investigate the effects of warming on the mainecosystem processes driving changes in biogeochemical cycling and to contrastthese climate driven changes with the effects caused the heather beetle infestationand cutting of vegetation.

2. Material and Methods

2.1. SITE DESCRIPTION

The study was conducted in a heathland area at Mols Bjerge (56◦23 N; 10◦57W) 5 km from the east coast of Jutland in central Denmark. The site is 57 mabove sea level in a hilly glacial sandy moraine from the late phase of the Würmglaciation. The climate is relatively dry with an average annual precipitation of550 mm (1960–1990). During the three year study reported here, average annualair temperature and precipitation was 8.7 ◦C and 750 mm, respectively. The siteis affected by the nearby sea and the surrounding agriculture with high depositionlevels of sea salts and moderate levels of nitrogen (wet deposition 38.6 kg Cl− ha−1

yr−1 and about 13 kg N ha−1 yr−1, respectively). The soil type is a sandy podzolwith a 1–4 cm organic mor layer on top. The soil contains 11 mg N g−1 and 0.34mg P g−1 in the organic layer and 0.4 mg N g−1 and 0.2 mg P g−1 in the minerallayer.

The site was cultivated until the 1950’s and was grazed by sheep and cattleuntil 1992. Since 1992, the area has been a nature reserve with no managementactions except some selective removal of pine trees and bushes. The vegetation inthe experimental area was generally dominated by the evergreen dwarf shrub Cal-luna vulgaris (L.) Hull until the 1960’s, whereafter an increasing amount of grass,mainly Deschampsia flexuosa (L.) Trin, has been observed. When the warmingexperiment was initiated in 1999, the aboveground biomass was about 1050 g m−2.The vegetation was dominated by a mixture of Calluna (about 45%) and grasses,mainly D. flexuosa (about 46%). A naturally occurring outbreak of heather beetles(Lochmaea suturalis Thompson) started in July/August 1999 and peaked duringthe summer of 2000, defoliating and killing the main part of the Calluna plants(>95%). To help restore the Calluna vegetation after the heather beetle infestationall aboveground vegetation was cut and removed from the experimental plots inSeptember 2000. During the autumn of 2000, and especially the following year of2001, the vegetation re-established with complete dominance of D. flexuosa.

2.2. TREATMENTS

A field warming experiment was conducted as ‘night time warming’ at three studyplots of 5 m H 4 m each. The warming plots were covered by a light scaffoldingof galvanised steel tubes carrying a reflective aluminium curtain (ILS ALU, ABLudvig Svensson, Sweden). The curtains reflected 97% of the direct and 96% of the

194 C. BEIER ET AL.

diffuse radiation and allowed transfer of water vapour. The study plots were openat all sides. The movement of the curtains was automatically controlled accordingto pre-set climatic conditions:

• Light intensity – at sunset, the curtains were drawn over the vegetation to re-duce the IR reflection, thereby conserving energy and leading to an increasedtemperature in the heated plots. At sunrise, the curtains were automaticallyremoved to keep the plots open during the day.

• Rain – during rain events at night the curtains were automatically removed.• Wind – a high wind speeds (>10 m/s) during the night, the curtains were

automatically retracted to avoid damage to the systems.The warming treatment increased the monthly average midnight air temperat-

ures by 0.6–1.9 ◦C (average yearly increase 1.1 ◦C) and midnight soil temperaturesby 0.6–1.6 ◦C (average yearly increase 1.1 ◦C). Parallel to the warming treatment,three untreated control plots were operated for comparison. The control plots werecovered by a similar light scaffolding as for the warming treatment, but without anycurtain. The control and warming plots were placed in three blocks within an areaof 25 m H 40 m in the heathland. Three additional experimental plots dominatedby intact Calluna that had not been infested by heather beetles were included inthe investigation of N mineralisation. These plots were situated within a distanceof less than 50 m from the control and warming plots.

2.3. MEASUREMENTS

2.3.1. Input and Climatic MeasurementsThe input of water and nutrients were measured by two open air rain gaugessampled in monthly intervals and analysed for NH+

4 , NO−3 and DON (Autoanalyzer

3, Bran+Luebbe, Norderstedt, Germany). The functioning of the curtains and theextent of the treatment were recorded and checked by bihourly measurements ofair and soil temperature (110 Termocouple Reference Thermistor types – probe107, Campbell scientific, Logan, Utah, USA), radiation balance (NR-lite, Kipp &Zonen, Delft, the Netherlands), air humidity (VAISALA humitter 50, Helsinki,Finland), wind speed (2 RISØ Cup anemometer P2546A, Roskilde, Denmark), andmonthly measurements of water input to each plot (funnels). For more details onthe experimental setup, see Beier et al. (in press).

2.3.2. Litter DecompositionLitter decomposition was studied by the litterbag technique. Fresh litter was collec-ted in September 1999, air-dried in the lab and put into polyethylene litterbags (10g litter, mesh size 1 mm, three bags per plot and species and sampling time) and in-stalled in the field in May 2000 at the starting date of the drought period. Litter fromCalluna and D. flexuosa was incubated separately and incubations were terminatedafter 1, 6 and 18 months. After collection litterbags were air-dried and cleaned ofsoil and ingrown plants. The remaining litter was weighed for estimation of weight

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loss and analysed for total C, N (EA 1110 elemental analyser, CE instruments,Milan) and lignin, determined by ADF (Acid Detergent Fibre=cellulose+lignin)followed by acid digestion (van Soest, 1963).

2.3.3. Soil MineralisationSoil nitrogen mineralisation and nitrification were measured by the buried bagtechnique. Measurements were conducted seasonally during one year starting inwinter 1999/2000. At each sampling date, two replicate paired intact soil cores, 5cm in diameter were taken from the top soil horizon under Calluna in each studyplot including plots with intact Calluna outside the treatment. One of each pairwas analysed for initial NH+

4 and NO−3 content. The other core was placed in a

polyethylene bag and replaced in the ground. After incubation in the field for 1–2months, cores were removed and analysed similarly. All soil cores were analysedindividually for soil moisture (105 ◦C in 48 hr), organic matter content by combus-tion, and NH+

4 and NO−3 by extraction in 1M KCl (1:10 soil to extract ratio) and

the change in inorganic-N (net mineralisation) and NO−3 -N only (net nitrification)

during the incubation period was calculated as the change in extractable nitrogencontent per gram organic matter (µg N g OM−1).

2.3.4. Soil RespirationSoil respiration was measured biweekly or monthly during 2000 and 2001 at twopermanent chamber-bases (100 mm diameter) installed on bare soil in each plot.Measurements were done by an infrared gas analyser (PP-systems – EGM-2, Hert-fordshire, UK) with a standard chamber, which was fitted onto the permanentchamber bases in the plots during the measurements.

2.3.5. Soil SolutionSoil water was collected monthly at two soil depths. Water percolating throughthe organic layer was collected by a 10 cm H 20 cm PVC tray placed beneath theorganic layer and connected to a sampling bottle placed in a 50 cm soil pit outsidethe plot. Three samples were taken from each plot and pooled before analyses.Seepage water was collected continuously and sampled monthly in each plot bythree PTFE tension soil suction cups (PRENART super quarz, Copenhagen, Den-mark) connected to the same sampling bottle placed in a cold and dark soil pitoutside the plot. Soil water samples were analysed for NO−

3 , NH+4 and TON (as

for precipitation) and TOC (Shimadzu TOC-5000 Analyzer, Duisburg, Germany).TON was only measured campaign-wise.

2.3.6. Element FluxesWater balances in the soil were estimated with the water model EVACROP (Olesenand Heidmann, 1990) using measured numbers of temperature, precipitation andsoil moisture. The element fluxes were calculated by multiplying the average

196 C. BEIER ET AL.

Figure 1. Decomposition of Deschampsia flexuosa and Calluna vulgaris litter in relation to treatmentshown as remaining weight after incubation in litterbags for 30–500 days. Incubation started on 25thMay 2000. Lines are best fitted 2nd order polynomials. Error bars indicate SE.

monthly concentrations in precipitation or soil solution with the average precipi-tation or modelled drainage in the soil.

The relative mobilization or retention in percentage was estimated as the differ-ence between the estimated input and output fluxes (Equation 1).

Retention = (Inputprecipitation – Outputleachate / Inputprecipitation) × 100 (1)

2.4. STATISTICAL METHODS

A mean weight loss of litterbags was calculated for each plot, log transformedand rates of decomposition were analysed by a one-way ANOVA at each samplingperiod to determine the effect of warming. Repeated measures analyses of variance(rmANOVA) with temperature and block as main factors were applied to test theeffects of the main factors on soil respiration and seasonal (e.g., winter, spring,early summer, late summer, autumn) mean concentrations of soil solution chem-istry during the three years of measurement. Net N mineralisation and nitrificationdata were log(x+1) transformed before analysis in order to obtain homogeneousvariances and analysed separately for each season (e.g., winter, spring, summerand autumn) by one-way ANOVA with temperature or vegetation type as mainfactor. All statistical analyses were performed with SAS using the GLM procedureand type II sum of squares. Differences were considered significant at p < 0.05level.

3. Results

The decomposition of plant litter followed a general pattern with a fast initial phasefollowed by a slower phase (Figure 1). 40% of the litter material was decomposed

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Figure 2. Net N-mineralisation and nitrification at Mols during winter 1999 to autumn 2000 (µg Ng−1 OM−1 d−1 (mean + SE)). Control and warming plots were subject to heather beetle infestationthroughout the mineralisation study. ‘Intact’ samples were taken in the same area but from plots notaffected by heather beetles. The last sampling in autumn 2000 weas done before the vegetation wascut. Significance levels of * indicates p < 0.05.

within the 500 days of incubation independent of litter type and treatment. Thedecomposition rates were not significantly different among treatments and showedalmost similar patterns for both treatments and plant species despite large differ-ences in litter quality between D. flexuosa and Calluna, in particular lignin contentbeing 7.8 % and 35.4% respectively (Figure 1).

The N-mineralisation was in the order of 0.5-15 µg N g−1 OM d−1 and was notsignificantly higher in the warming (p < 0.0559) and control (p < 0.3082) plotscompared to the ‘intact’ Calluna plots outside the treatment plots (Figure 2). Min-eralisation rates in the intact cores showed a seasonal pattern with low winter andspring rates and high summer rates. The control plots showed low mineralisationrates in the winter and more or less constant rates for the rest of the year with no dis-tinct seasonal pattern (Figure 2). Warming tended to increase N-mineralisation (p< 0.2342) especially during the winter and autumn in the organic layer (Figure 2).

198 C. BEIER ET AL.

Figure 3. Soil respiration (g CO2 m−2 hr−1) during 2000 and 2001 in the warming and controlplots at Mols. Error bars indicate SE. Arrow indicates time of vegetation removal from the plots.Significance levels of * indicates p < 0.05.

Nitrification rates were 10 times lower than the N-mineralisation rates with aseasonal pattern almost similar to net mineralisation although the control plotsshowed a seasonal pattern with highest rates in the summer (Figure 2). In con-tradiction to mineralization, the ‘intact’ cores and cores from the control plotsgenerally showed similar rates. Nitrification in the warming treatment showed noseasonal trends but generally the rates tended to be higher relative to the control (p< 0.1296), significantly so in the autumn (p < 0.0220).

Soil respiration rates were 0.1-0.8 g CO2 m−2 hr−1 with a clear seasonal patternover the year with significantly higher rates during the summer compared to thewinter (Figure 3). The soil respiration rates were almost identical for the controland warming plots for all sampling dates except from a significant effect of thewarming treatment during the summer 2000 which did not appear again in 2001.

Soil water concentrations of dissolved organic matter in the organic layer were20–30 mg L−1 at the start of the experiment increasing to 40–60 mg L−1 during thesummer 1999 (Figure 4). DOC levels were almost identical and not significantlydifferent in the warming treatment and the control and showed a similar pattern asfor the N-mineralisation with a relatively constant level over year 2000 in the con-trol and a slight increase in the summer 2000 in the warming (Figure 4). Beneaththe root zone (90 cm depth) the DOC concentration was 10 times smaller than inthe top soil, and showed no clear seasonal patterns (data not shown).

Soil water concentrations of nitrogen in both the organic layer and beneath theroot zone were generally low and constant over the year although a slight seasonalpattern with lower N-concentrations in the peak of the growing seasons were seenbelow the root zone (Figure 5). The nitrogen retention in the soil was high (>80%)in the first treatment year and dropped significantly in the control plot to about24% in 2000 when heather beetle infestation progressed (Table I). The increasedN mineralisation caused by the warming resulted in increased leaching losses of

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Figure 4. Soil water concentrations DOC and DON beneath the organic layer in the control (fullline and bullets) and the warming treatment (dashed line and triangles). Times of infestation (dashedarrow) and cutting (solid arrow) are indicated.

NO−3 and NH+

4 beneath the organic layer, while in contrast, the nitrogen concen-trations in the soil solution in the warming treatment decreased under the root zonecompared to the control in the second year of treatment (Figure 5, Table I). Thehigher N retention after defoliation in the warming treatment indicates a muchhigher immobilization of N in soil and plants.

4. Discussion and Conclusion

At the beginning of the experiment in 1999, the heathland ecosystem at Molswas already subject to grass invasion. This is a result of natural heathland suc-cession towards grass dominance on relatively nutrient rich soils (Holmsgaard,1986; Gimingham, 1995). The heathland had received inputs of nitrogen from

200 C. BEIER ET AL.

Figure 5. Soil solution concentrations of NO−3 and NH+

4 beneath the organic layer and in the seepagewater in the control (full line and bullets) and the warming treatment (dashed line and triangles).Overall significant effects of the rmANOVA are given in top left corner. Seasonal effects are givenfor each time. Significance levels of + and * indicates p ≤ 0.1 and p ≤ 0.05, respectively. Times ofinfestation (dashed arrow) and cutting (solid arrow) are indicated.

atmospheric deposition, probably for decades, being close to the critical loads leveldefined for lowland dry heathlands of 15–20 kg N ha−1 yr−1 (EEA, 1999), and itis likely that the grass invasion has been stimulated by increased nitrogen avail-ability. The mineralisation and nitrification rates found in the organic layer underintact Calluna are comparable to rates found in Dutch heathlands, which have beensubjected to very high inputs of atmospheric N deposition (e.g., van Vuuren etal., 1992), which further indicates a relatively high N availability compared to thevery low or negative rates found in other northern Calluna heath (Rangeley andKnowles, 1988; Kristensen and Henriksen, 1998; Kristensen, 2001). On the otherhand, the heathland at Mols is still capable of immobilising the incoming nitrogenby either microbial immobilisation as has been shown in another similar heathland(Kristensen and McCarty, 1999) or by increased plant uptake as the vegetationshifts to grasses that have a much lower C/N ratio.

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TABLE I

Nitrogen fluxes (kg N ha−1 yr−1) at the Danishheatland site at Mols following experimental tem-perature manipulation. In the second treatment year(2000), the Calluna vulgaris was completely de-foliated by heather beetles followed by cutting topromote regrowth of Calluna. Input = wet depos-ition; OM-leaching = leaching from the organichorizon; Output = leaching under the root zone in90 cm depth; Retention = Input-Output; % retention= % of input retained

Treatment Control Warming

NO−3 NH+

4 NO−3 NH+

4

1999

Input 5.8 7.1 5.3 6.5

OM-leaching 2.9 1.8 11 5.3

Output 1.2 0.14 0.47 0.18

Retention 4.6 7.0 4.8 6.3

% Retention 80 98 91 97

2000

Input 5.8 7.1 5.3 6.5

OM-leaching 3.4 2.2 10 9.8

Output 4.4 0.42 1.2 0.10

Retention 1.4 6.6 4.1 6.4

% Retention 24 94 79 99

The effects of the warming treatment on biogeochemical processes were gen-erally moderate, which may be expected with the relatively small temperatureincrease of about 1 ◦C. Even though warming only led to relatively small increasesin mineralisation rates and soil respiration with the largest effects in the summer,warming increased nitrogen leaching from the top soil layer 3–4 fold, mainlyattributed to a strong increase in soil water N concentrations during the winter1999/2000, one year after the start of the experiment (Figure 5). Correspondingly,increased N leaching in response to warming has also been reported in a fores-ted catchment (Lukewille and Wright, 1997) and upland grassland (Ineson et al.,1998). The increased mineralisation and leaching of N from the organic layer wasnot seen beneath the root zone as the mobilization of nitrogen was counteractedby a 30% increased plant production in the warmed plots (Torben Riis Nielsen,unpublished data) illustrating that interactions between the plants and the soil maycomplicate demonstration of climate induced effects on biogeochemistry, at leastin the short term.

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The infestation by the heather beetles in the late summer 1999 and subsequentdefoliation and harvesting of all vegetation in all plots during the summer andautumn 2000 increased the mobilization of DOC and nitrogen from the organicsoil layer but not below the root zone (Figures 4 and 5, Table I (year 2000)). Thiscorresponds to findings in forest ecosystems, where insect infestations, defoliation,and clear-cutting have been shown to increase nitrogen fluxes in the soil water(Swank et al., 1981; Pedersen and Bille-Hansen, 1999) and in particular to findingsfrom another Danish heathland (Nielsen et al., 2000) where leaching of DOC fromthe organic soil layer was doubled due to heather beetle infestation. but all of thereleased DOC was trapped again in the B-horizon. The mobilizing effect of thebeetle infestation and vegetation removal on nitrogen leaching was much smallerin the warmed plots compared to the control, probably as a consequence of fasterand stronger regrowth of the grass Deschampsia flexuosa in the warming treatment,rapidly re-established the plant sink for nitrogen supported by an observed 30 %increase in grass biomass in the summer 2000 in the heated plots (Torben Riis-Nielsen, unpublished data). So, warming seemed to reduce N losses by stimulatingplant growth. However, the increase of about 1 ◦C in the warming treatment is onthe low end of projected temperature rises (Houghton et al., 2001). A larger degreeof warming might be expected to cause larger increases in N-mineralization, atleast transient, and thereby potentially increase the risk of nitrogen leaching belowthe root zone in cases where the plants nitrogen demand is exceeded.

In general, the results indicate alterations in the soil processes, but the responsesoften were not significant. In contrast, plants integrate the small yearly miner-alisation increases over several years. Similar patterns of low response in soilrespiration, net mineralisation but larger increases in plant biomass have beenshown in several warming experiments in the Arctic (Christensen et al., 1997;Jonasson et al., 1999; Schmidt et al., 2002).

The increase in soil solution nitrogen concentrations in the warmed plots dur-ing the first autumn and winter may be due alone to warming induced increasedmineralisation of organic material which to some extent was supported by themineralisation data. However, it may also be due to interaction between the heatherbeetle infestation and the warming. The seasonal measurements of nitrogen min-eralisation and nitrification in the control plots infested by heather beetles indicatean increase in N mineralisation by more than 50% compared to the measurementsfrom the intact areas outside the plots. This agrees well with previous findingsshowing that heather beetle infestations can alter nitrogen cycling in Calluna heath-lands by switching soils from net immobilisation of NH+

4 to net ammonification(Kristensen and McCarty, 1999). The increase of NH+

4 availability caused by beetleinfestation in Mols did, however, stimulate nitrification contrary to results from theprevious study. The observed increase in soil solution N may therefore be due toa combination stimulation of mineralisation by both the heather beetle infestationand the warming treatment.

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Subsequent to the heather beetle infestation and the removal of all vegetation,the study plots relatively quickly developed a thin grass cover over the autumn of2000 and further a dense grass cover during the spring and summer of 2001. TheCalluna plants did not re-establish within the first two growing seasons after theinfestation and cutting. This crucial role of heather beetles in the conversion ofheathlands to grasslands when the heathland is under pressure for grass invasionand increased nutrient availability has been described previously (Brunsting andHeil, 1985; Prins et al., 1991). In the present study, the attempt to restore theCalluna vegetation by cutting and removing all aboveground plant biomass afterthe beetle infestation was not found to enable regrowth of Calluna within the firsttwo years after cutting.

Based on the results of this study five important aspects have to be considered:1) The area of Calluna heathlands in Europe is decreasing due to invasion by

grasses and trees. This development is stimulated by increased nutrient availabi-lity due to increased atmospheric N deposition (Heil and Bobbink, 1993). Theincreased temperature was in the present study found to stimulate mineralisa-tion and N availability in the heath ecosystem. This indicates that global warm-ing may, at least during the time of transition add to the nutritional pressure onheathlands.

2) The occurrence of heather beetle infestation of Calluna is thought to be in-creased by increased N deposition and availability in heathlands (Heil andBobbink, 1993). The problem may also increase the risk of herbivory leadingto increased pressure or increased frequency of insect infestations (Penuelaset al., in press). As seen in this study, the insect infestation in ecosystemsalready under pressure may have detrimental effects and change the ecosystemcharacteristics fundamentally.

3) Ecosystem disturbances will interact with increased temperatures to reduceor amplify the effects on biogeochemical cycling. The direction and extentof the interaction among disturbances and climatic changes depends on therelative extent of the stimulation of plant and soil processes. In this study,with moderate temperature increases the stimulation of the plant growth bywarming caused rapid and efficient re-immobilization of nutrients immobilizedby the ecosystem disturbance. At more extensive temperature increases theinteractions may lead to loss of nutrients from the ecosystem.

4) The change in vegetation from Calluna bushes to grasslands may also affectcarbon and nutrient budgets in the ecosystem. In the present study, a conver-sion from a pure Calluna cover to a pure grass cover reduces the abovegroundcarbon stock by about 40%, while aboveground nitrogen content will almostdouble in the grassland ecosystem as the C/N ratio is only half the Callunaplants. These aboveground effects have to be balanced with the adjacent be-lowground effects, which are uncertain at this level. One might expect theturnover rate of the organic matter in the soil to be faster in the grasslandleading to reduced carbon storage, but the results from the warming study

204 C. BEIER ET AL.

are not conclusive yet. Recent findings on dry grasslands indicate an overallreduction in carbon storage in grasslands compared to shrublands under drierconditions (Jackson et al., 2002).

5) The measurements show that on the short term (year to year) ecosystem dis-turbances can have a much stronger impact on the biogeochemical cyclingcompared to moderate changes in climatic conditions. However, climatic con-ditions act on a much longer time scale, and the effects therefore have to beassessed on a long term. Furthermore, ecosystem disturbances may potentiallyact simultaneously with changes in climatic conditions and the frequency mayeven be increased leading to synergistic effects on ecosystem biogeochemistry.

Acknowledgments

The project was funded by EU under the projects CLIMOOR (Contract ENV4-CT97-0694) and VULCAN (Contract EVK2-CT-2000-00094) and the particip-ating research institutes. We owe a lot of grateful thanks to all other institutesand researchers involved with the Climoor and Vulcan projects for inspirationand enthusiasm and in particular to the technical staff at our institutes for theirskillful field and lab work. Further information about the project can be found onwww.vulcanproject.com.

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