- Email: [email protected]
Annual CO2 budget of spruce model ecosystems in the third year of exposure to elevated CO2
Acta (Ecologica, 1997, 18 (3), 319-325
Annual CO 2 budget of spruce model ecosystems in the third year of exposure to elevated CO 2 Stephan H~ittenschwiler and Christian KOrner Institute of Botany, University of Basel, Schdnbeinstrasse 6, CH-4056 Basel, Switzerland. Received: 18.t0.96
Accepted: 24.1.97
Abstract Clones of 4-year-old spmce trees (Picea abies) were grown in competition in model ecosystems with nutrient-poor natural forest soil and natural understory vegetation and were exposed to three CO 2 concentrations (280, 420 and 560 pmol mol -~) for three years. Diurnal net ecosystem CO 2 uptake (NECa), nocturnal net ecosystem CO 2 loss (NEC,) and soil CO 2 efflux were measured repeatedly in the third year of CO 2 exposure and were used to estimate an annual ecosystem CO 2 budget. The CO 2induced stimulation of NEC d varied over the year with no measurable stimulation in spring and fall but a high mid-season COz stimulation. Respiratory losses of whole ecosystems and soil CO 2 effiux alone were both progressively increased with increasing CO 2, thus counteracting the CO 2 stimulation of photosynthesis per unit ground area. Consequently, the annual net ecosystem CO 2 uptake was only moderately and non-linearly stimulated by CO 2 (+8% = 84 g C m -2 aq at 420 and +9% = 90 g C m -2 aq at 560 compared to 280 [amol CO 2 mol-l). We conclude that the rising atmospheric CO 2 concentration may Iead to an increase in annual net ecosystem carbon gain of rather nutrient-poor spruce communities. Our results further suggest that CO 2 fertilization effects may be greatest under current CO 2 concentration and that relative increases of net ecosystem CO 2 uptake will become relatively smaller as atmospheric CO 2 will continue to rise.
Keywords: Carbon sequestration, CO 2 budget, dark respiration, ecosy]tem CO 2 exchange, elevated CO2, Picea abies, soil CO 2 efflux.
R~sum~ Des clones d'tpictas (Picea abies) gtg~sde 4 ans ont 6t~ cultiv~s en compttition dans des 6co-syst~mes modeles sur un sol fomstier naturel pauvre en nutriments et avec une vtgttation basse naturelle ; ils ont 6t6 exposts h 3 concentrations en CO 2 (280, 420et 560 lamol mol -~) pendant 3 ans. Le prtl~vement diurne net en CO 2 de l'tcosystbme (NECk), la perte nocturne nette en CO 2 de l'tcosysttme (NECn) et le d~gagement de CO 2 du sol ont 6t6 mesurts ~ plusieurs reprises au cours de la troisi~me annte d'exposition au CO 2 et ont 6t6 utilists pour estimer un budget annuel de l'tcosyst~me en CO 2. La stimulation de NEC d induite par te CO 2 varie au cours de l'ann~e sans stimulation mesu-rable au printemps et ~t l'automne mais avec une forte stimulation du CO 2 en milieu de saison. Seuls les pertes respiratoires de t'tcosystbme entier et le degagement de CO 2 du sol augmentent progressivement avec une ~l~vation du CO2, contrecarrant ainsi la stimulation de la photosynth~se par le CO 2 par unit~ de surface. En consequence, le prtl~vement net annuel de l'~cosyst~me eu CO 2 n'est stimul~ que moder~ment et de fa~on non-lintaire par le CO~, (+8 % = 84 g C m -2 aq h 420 et +9 % = 90 g C m -2 a q ~ 560 h comparer avec 280 pmol CO 2 tool- ). Nous en concluons que l'augmentation de la concentration en CO 2 atmosphtrique peut mener ~ un accroissement de l'accumulation annuelle nette en carbone de 1'6co-
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syst~me de communaut6s d'6pic6as plut6t pauvres en nutriments. Nos r6sultats sugg&ent de plus que les effets de la fertilisation par le CO 2 pourraient ~tre tr~s importants pour des concentrations courantes en CO 2 et que les augmentations relatives du pr61bvement net de l'6cosyst~me en CO 2 deviendront relativement plus faibles ?~mesure que le CO 2 atmosph6rique continuera d'augmenter.
INTRODUCTION The terrestrial biosphere as influenced by a multitude of global change effects is of central importance for the current and the future global carbon cycle (e.g. AMTHOR, 1995; SCHI~L, 1995). While the fluxes among the main four carbon pools (fossil carbon, atmosphere, oceans, terrestrial biosphere) should balance, current estimates of the global C budget led to the so called "missing sink" in the range of 1.1 Gt a -t (D~xoN et al., 1994) to 1.8 Gt a-t (StrNOQUlST, 1993). This is equivalent to 2-3% of the global annual net primary productivity (NPP). Most of this missing carbon is thought to be sequestered in terrestrial ecosystems (ScHIMEL, 1995) as a result of forest regrowth (ca. 0.5 Gt a-l), growth stimulation by atmospheric N deposition (ca. 0.6 Gt a-l), and by CO 2 fertilization (ca. 1.0 Gt a-t). The continued increase of fitmospheric CO 2 concentration up to the predicted doubling of the current concentration within the next century is expected to further increase NPP of terrestrial ecosystems (MzLILLO et al., 1993), which in turn is often assumed to lead to increased terrestrial ecosystem carbon sequestration. However, our knowledge about the effects of elevated CO 2 on the carbon balance of ecosystems is very limited, and most of what we know applies to herbaceous systems (KORr,rER, 1996). The lack of data for forest ecosystems is particularly problematic because they store more than 80% of all above-ground, and 40% of all below-ground-terrestrial carbon (WHia~rar~R & LI~Ns, 1975; OLSONet al., 1983), and represent 40% of the total global NPP (oceans included; WHnwAKZl~& LW,ENS, 1975). The aim of this study was to experimentally quantify the effect of increased atmospheric CO 2 on the CO 2 balance of spruce (Picea abies) model ecosystems and to discuss these data in the context of potential carbon sequestration by forest ecosystems. We provide a data set of ground-area-based diurnal net ecosystem CO 2 uptake (NEC d) and soil CO 2 effiux (SCE) in the third year of continuous exposure to elevated CO 2. We also determined nocturnal net ecosystem CO 2 loss (NECn) for this year and calculated an annual CO 2 budget for the model ecosystems. M A T E R I A L S AND M E T H O D S Six 4-year-old Picea abies Karst. trees (height of 0.7 m), each of a different genotype were planted into each of nine 0.25 m 3 containers (100 • 70 x 36 cm) in early April 1993. Trees were grown in competition with the typical montane spruce forest understory species Oxalis acetosella L., Homogyne alpina L. and Melampyrurn sylvaticum L. (the latter species in the second and third year of the experiment only). The soil (podsol-type, pH ca. 4.5) was collected in a montane old-growth spruce-fir forest of the northern Swiss Alps near Luzern (1140 m, 46~ 8~ and was then re-established by horizons (B-, A-horizon, raw humus, and litter layer) in each of the nine model ecosystems (see H~TI'ENSCHWILER & KOR~R, 1996). Groups of three model ecosystems were exposed to either 280, 420 or 560 lamol mol-l atmospheric CO 2 in three different environmental chambers. We applied different rates of wet N deposition to each model ecosystem within each CO 2 treatment: 0,30 kg ha -I a-1 and 90 kg h a I a-l (as ammonium
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nitrate dissolved in deionized irrigation water) to test for the combined effects of elevated C O 2 and N deposition on tree growth (see H~,TrENSCHWlLER & KOP,NER, 1996). However, the N deposition treatments are not considered here, because our main focus was to look at the effects of rising CO 2 on ecosystem gas exchange (see below). Treatments were started in early April 1993 and continued until late November 1995 when trees were harvested. All environmental chambers were run with the same set of variable weather regimes based on a 3-year (1989-1991) data set from the meteorological station close to the field site where tile soil was collected; i.e. typical lower montane climate in the northern part of the Alps (see HATTENSCnWrLER& KORNER, 1996). Environmental chamber climate and photoperiod was adjusted weekly. Simulated temperatures ranged from -3~ in mid-winter to 24~ in mid-summer, and relative humidity was set to 70% during "clear" days and 85% during "cloudy" days. "Clear days" were characterized by a quantum flux density (QFD) of about 800 lamol m -2 s-1 and "cloudy days" by about 400 lamol m -z s-1 just above the canopy. "Clear days" began and ended with 2 h or 3 h of low QFD ("cloudy day" level), respectively. Precipitation followed the natural seasonal pattern and was applied weekly to the top of the spruce canopy using a rose (a total of 1200 m m per year). Potential chamber and positional effects were minimized by changing model ecosystem position within chambers weekly and between chambers monthly. In the third year of the experiment we measured diurnal net ecosystem CO2 uptake per unit ground area (NECd) in the afternoon of "clear days" (i.e. at 800 lamol m -2 s -l of QFD) eight times throughout the year (fig. IA). During measurements all three model ecosystems in each CO 2 treatment remained in their own environmental chamber which was then used as a closed gas exchange chamber. Chamber CO 2 control during measurements was interrupted. We measured the CO 2 depletion rate within the chamber with an IRGA (type 225-Mk 3, ADC, Hoddesdon, England). The leak rate of each environmental chamber was determined by monitoring the depletion of injected N20 (for an insideoutside CO 2 concentration gradient), and by monitoring the CO z flux into the empty, CO 2 depleted chambers (280 lamol tool -l, for an outside-inside CO 2 concentration gradient). Nocturnal (i.e. predawn) ecosystem CO 2 loss per unit ground area (NECn) was measured in late May and in mid July 1995 in the same way as NEC d. In addition, soil CO 2 effiux (SCE) for each ecosystem was measured separately on three different 0.0314 m 2 areas on bare forest floor in each ecosystem (i.e. 9 patches per CO 2 treatment) using a closed-cup system (SRC-l, EGM-1, PP Systems, Stotfold, Hitchin Herts, UK). These measurements took 1-2 rain each and were made immediately after the NECd measurements. Finally we calculated an annual ecosystem CO 2 budget using the following assumptions and simplifications: (1) The measured NEC a was applied to the hours of high QFD (800 lamol m -2 s-l). For the hours of lower QFD (400 pmol m -2 s-1) at the beginning and end of "clear days" and for "cloudy days" (400 tamol m -z s-J) we reduced NEC a by a factor of 0.8 (estimated from the light response curves of net shoot photosynthesis). (2) Nocturnal soil CO 2 effiux (SCE,) was calculated from daytime rates using a Q10 of 2.2 (estimated from separate measurements at different soil temperatures) to correct for soil temperature differences. (3) Above-ground plant dark respiration (Rn) was expressed as a constant percentage of NEC d determined for each CO 2 treatment separately as R, = NECn - SCE~ at two dates (see below). (4) NEC d, Rn, and SCE. were applied to the entire duration of the specific weather regimes. (5) For periods with a weather regime not covered by measurements, data from the preceding period were used and were adjusted to the actual temperatures using a Ql0 of 2.2 for SCE n and a QJ0 of 2.1 for NEC a (estimated from the measurements made at day 17 and at day 43). Data on NEC a and NEC n could not be tested statistically because all three model ecosystems of each CO 2 treatment were measured together. We measured ecosystems together in one chamber to avoid the profound effects of: disrupting the continuous canopy formed by the three systems leading to large increases in side light, and to ensure the detection of adequate CO z concentration change rates (in particular for the measurements of NECn). SCE was tested for effects of CO 2 or N over time by using Vol. 18, n ~ 3 - 1997
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repeated measures analysis. CO 2 effects on soil CO 2 effiux of single measurement dates were tested by separate one-way ANOVAs.
RESULTS
Differences in diurnal net ecosystem C O 2 uptake (NECd) between C O 2 t r e a t m e n t s were small or absent early and late in the growing season. However, NEC d measured at 420 and 560 ~tmol CO z mo1-1 between day 80 (mid June) and day 168 (early September) was 30% and 42% greater, respectively, than NEC d measured at 280 pmol CO 2 mol "1 (fig. !A). SCE was also significantly greater at the two higher CO 2 concentrations (fig. 1B). Mean SCE for the three model ecosystems per CO 2 level ranged
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Days of growth (Day 0: 1. April) FIG. 1. -- A. Diurnal net ecosystem CO z exchange rate (NECd) at a top-of-canopy QFD of 800 ~mol m 2 s-1 and B" soil CO 2 effiux (measured right after NECd) of spruce model ecosystems over the third year of growth at three different atmospheric CO 2 concentrations ([3: 280, Q: 420, A: 560 }arnol CO 2 mol-l). For each date the average of two successive NEC d measurements (taken in the afternoon between 3 pm and 6 pro, depending on season) per CO 2 level (i.e. 3 model ecosystems, each of a different N deposition rate) are shown. The soil CO 2 effiux was determined as an average of three measurements (taken at three different spots) within each of the nine model ecosystems for each measurement date. Symbols in fig. 1B represent mean values (_+ SE) of 3 model ecosystems per CO 2 level (pooled across N treatments) and stars indicate statistically significant CO2-effects at P < 0.05 (*) or at P < 0.01 (**). Air temperatures (fig. IA) and soil temperatures (fig. tB) are shown for each measurement date.
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from 1.4, 1.5, and 1.3 tamol m -2 s-1 on day 17 to 5.5, 6.6, and 7.4 Nnol m -2 s -1 (in the order of increasing CO 2 concentrations) on day 168 when soil temperatures were highest. Maximum relative CO 2 stimulation o f SCE was +33% at 420 and +57% at 560, when compared to rates measured at 280 ~mol CO 2 mo1-1. Stimulation on an annual basis averaged +11% at 420 and +19% at 560 lamol CO 2 mo1-1. There was a non-significant trend towards increased SCE with increasing N deposition at any o f the CO 2 concentrations (P = 0.50, rep. meas. analysis). The nocturnal net ecosystem CO 2 loss (NECn) was 5.2, 5.2 and 6.5 ~mol m -2 s-l on day 56 and 5.6, 6.8 and 7.9 gmol m -z s -j on day 104 (in the order of increasing CO 2 concentration). Substracting SCE resulted in similar ratios of total above-ground plant dark respiration (R n) to NEC a at both measurement dates (i.e. a mean of 15.2% _+ 1.0 at 280, 15.6% _+ 0.4 at 420, and 19% _ 0.7 at 560 pmol CO 2 mol-1). The net annual ecosystem CO 2 uptake estimated using NEC a, NEC n and SCE was 7.0 tool CO 2 m -2 (= 84 g C) and 7.5 tool CO 2 m -2 (= 90 g C) greater at 420 and at 560, than at 280 pmol CO 2 mol -j (table I). Estimated annual soil CO 2 effiux [Y~SCEn (nocturnal soil CO 2 efflux) + YSCE a (diurnal soil CO2 effiux)] was a major component of the ecosystem CO 2 budget: 73.7, 81.4, and 87.7 mol CO 2 m -2 a -1 (with increasing CO2 concentration). This is equivalent to an annual ecosystem carbon loss of ca. 881,997, and 1052 g C m -2 via root and soil microbial respiration. TABLE][.- - Annual sums of diurnal CO2gain (~ NECa), CO 2 losses through dark respiration of above-ground plant parts (~. R,) and nocturnal soil CO 2 effiux ( Y SCE~), and the annual net CO 2 balance of model spruce ecosystems exposed to three atmospheric CO 2 concentrations (all values in tool CO z per square meter ground area and per year).
CO2 treatment (pmolmol-I) 280 420 560
Y,N E C 142.6 156.2 166.0
d
~. Rn
~ SCE n
24.2 26.5 33.3
33.9 38.2 40.7
Annual net CO2 balance :84.5 91.5 92.0
DISCUSSION
Elevated CO 2 substantially stimulated mid-season ecosystem net CO 2 uptake per unit ground area (NECd) in our spruce model ecosystems, even though we found no stimulation of tree growth (H~TTENSCHWILER& KORNER, 1996; I-I)~TTENSCHWILER& KORNLR, in prep.). We assume that the overall CO2-response likely reflects that of ecosystems receiving medium wet N deposition (ca. 30 kg ha -1 a-l; similar to the maximum currently measured in certain frontal ranges of the northern Alps). The average increase in mid-season NEC a we observed between 280 and 420 pmot C O 2 mo1-1 (30%) and between 280 and 560 pmol CO 2 mol -~ (42%) is similar to that observed between current ambient (350 lamol tool -1) and 600-650 pmol CO 2 mol -l in a number of herbaceous plant communities (DRAKE & LEADLEY, 1991; DIEMER, 1994; STOCKER e t al., 1997). There are no other data on NEC a of tree communities grown under elevated CO 2. In our study, the C O 2 stimulation of NEC d only became apparent around day 80 (mid June), when current-year needles began contributing to the net ecosystem CO 2 uptake. Thus, it appears that the positive response of current-year needle photosynthesis to elevated CO: was responsible for the stimulation of mid-season NEC d at the two higher CO 2 concentrations. Vol. 18, n~ 3 - 1997
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However, down-regulation of current-year needle photosynthesis occurred later in the growing season (unpublished data), similar to what we found in the second year of the experiment (HA~zNSCI-IWILER & KORNER, 1996). From mid September 1995 onwards NEC a was similar at all CO 2 levels, in accordance to what we found for NEC d in the fall of 1994 (HATTENSCHWILER& KORNER, 1996). In addition to physiological down-regulation of photosynthesis at the leaf level, we also found allometric adjustments to elevated CO 2 in the third year at the canopy level, expressed as reductions in LAI (12% lower at 420 and 16% lower at 560 relative to 280 lamol CO 2 mo1-1 = 5.2 m 2 m-2). In relative terms these data are similar to what we measured in the second year (H~,TTENSCHWILER& Ki3RNER, 1996). The increase in the ratio of above-ground plant dark respiration to canopy photosynthesis under elevated CO 2 we found, is in contrast to most, but not all studies reporting respiration/photosynthesis ratios at the whole-plant or the leaf level (review by AMTnOR, 1995). In 1994 (second year of the experiment) we found no differences in current-year branch dark respiration between CO 2 treatments (HATTENSCHWILER& KOP,NER, 1996). We can only speculate about the reasons for the apparent differences in CO 2 effect on current-year branch dark respiration in the second year and on the total above-ground plant dark respiration in the third year. The stimulating CO z effect on SCE measured in 1995 was greater than that measured in 1994 (H,~TTENSCHWILERt~ZKORNER, 1996). Higher SCE at elevated CO 2 may be in part explained by greater root dry mass at the two higher CO 2 concentrations compared to the lowest CO 2 concentration (+15% at harvest, no differences between 420 and 560 pmol CO 2 mol-1; V. WIEMKEN,personal communication). A stimulation of microbial activity linked to increased root exudation and/or fine root turnover (e.g. NORBY et al., 1987; KORNER& ARNONZ, 1992) may also have contributed to the higher SCE at elevated CO 2. The 24% mid-season CO 2 stimulation of SCE reported for artificial yellow poplar communities (NoRBY et al., 1992) is lower than the maximum mid-season stimulation measured here, but somewhat higher than the estimated mean annual CO 2 stimulation. Annual ecosystem carbon loss through SCE in addition to the increased aboveground plant dark respiration with increasing CO 2 largely compensated for the higher mid-season NEC d at elevated CO 2. On an annual basis we estimated a relative increase of net ecosystem CO 2 uptake of about 8.5% at the two higher CO 2 concentrations (only a very small difference was found between 420 and 560 larnol CO 2 mo1-1) compared to 280 lamol CO 2 mo1-1. Despite increased net ecosystem CO 2 uptake under elevated COz, above-ground spruce tree growth and biomass production was not stimulated (H,~TTENSCHWILER& KORNER, 1996; HATTENSCHW1LER& KORNER, in prep.). These findings are similar to those of alpine grassland ecosystems (ScH,~PPI t~ KORNER, 1996). Increased final root biomass would account for ca. 75% of the surplus in carbon fixed at the two higher CO 2 concentrations in year three. We do not know how much of the extra carbon fixed, accumulated as soil organic matter (SOM) via higher fine root turnover, ended up in microbial biomass, or was leached from the soil as dissolved organic carbon (DOC). If our results hold true for natural forests, they indicate that the global increase in atmospheric CO 2 concentration over the past 150 years may have caused an increase in annual forest ecosystem carbon gain. A mean increase in annual net CO a uptake by the world's forests (ca. 45 Mio km2), corresponding to about half (i.e. 45 g C m -2 a-l) of what we found for a change from 280 to 420 lamol CO a mol -', would Acta (Ecologica
CO z budget of spruce model ecosystems
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be sufficient to account for the "missing 2 Gt C" in the current global C budget. Perhaps the most important finding of our study is the non-linear response of the ecosystem CO 2 balance to increasing CO2; the largest change occurring between 280 and 420 lamol CO 2 mo1-1. This suggests (1) a response saturation to increasing CO 2 at rather low CO 2 concentrations, and (2) that natural forests may be responding less to rising CO2 in the future than they have in the past, at least in tree communities comparable to those studied here. ACKNOWLEDGEMENTS The model ecosystems used here were jointly constructed and maintained with the team of Andres WIEMKEN.We thank Jay ARNOr,~ for helpful comments on earlier versions of the manuscript, and Fritz ErmSAM for maintaining the sophisticated environmental chambers. This research was funded as part of the National Program on climate change and natural disasters (NFP 31) through Swiss National Science Foundation grant no. 4031-034220.
REFERENCES AMTHOR J. S., 1995. - Terrestrial higher-plant response to increasing atmospheric [CO2] in relation to the global carbon cycle. Global Change BioL, 1,243-274. DmMER M., 1994. - Mid-season gas exchange of an alpine grassland under elevated CO 2. Oecologia, 98, 429-435. DIXON R. K., BROWN S., HOUGHTONR. A., SOLOMONA. M., TREXLERM. C. & WISNIEWSKIJ., 1994. - Carbon pools and flux of global forest ecosystems. Science, 263, 185-190. DRAKE B. G. ~ LEADLEY P. W., 1 9 9 1 . - C a n o p y photosynthesis of crops and native plant communities exposed to long-term elevated CO 2. Plant, Cell and Envir., 14, 853-860. HATTENSCHWILERS. t~ KORNERCH., 1996. - System-level adjustments to elevated CO 2 in model spruce ecosystems. Global Change Biol., 2, 377-387. KORNER CH., 1996. - T h e response of complex multispecies systems to elevated CO 2. In: WALKERB. H. & STE~EN W. L., Eds., Global Change and Terrestrial Ecosystems. Cambridge University Press, Cambridge, 20-42. KORNERCH. & ARnONE J. A., 1992. - Responses to elevated carbon dioxide in artificial tropical ecosystems. Science, 257, 1672-1675. MELILLO J. M., McGuIRE A. D., K1CKL1GHTERD. W., MOORE III B., VOROSMARTYC. J. & SCHLOSS A. L., 1993. - Global climate change and terrestrial net primary production. Nature, 363, 234-240. NORBY R. J., O'NEILL E. G., GREGORYH. W. & LUXMOORER. J., 1987. - Carbon allocation, root exudation and mycorrhizal colonisation of Pinus echinata seedlings grown under CO 2 enrichment. Tree Physiol., 3, 234-240. NORBY R. J., GUNDERSON C. A., WULLSCHLEGERS. D., O'NEILL E. G. & Mc CRACKEN M. K., 1 9 9 2 . Productivity and compensatory response of yellow-poplar trees in elevated CO 2. Nature, 357, 322-324. OLSON J. S., WATTS J. A. & ALLISON L. J., 1983. - Carbon in live vegetation of major world ecosystems. Report ORNL-5862, Oak Ridge National Laboratory, Oak Ridge, TN. SCH.~PP1 B. & KORNER CH., 1996. - Growth responses of an alpine grassland to elevated CO 2. Oecologia, 105, 43-52. SCHIMELD. S., 1995. - Terrestrial ecosystems and the carbon cycle. Global Change Biol., 1, 77-91. STOCKERR., LEADLEYP. W. & KORNERCH., 1997. - Carbon and water fluxes in a calcareous grassland under elevated CO 2. Funct. Ecol., 11,222-230. SUNDQUISTE. T., 1993. - The global carbon budget. Science, 259, 934-941. WHITTAKERR. H. ~ LIKENS G. E., 1975. - The biosphere and man. In: LIETH H. & WHITTAKERR. H., Eds., Primary productivity of the biosphere (Ecological Studies 14). Springer, Berlin, 305-328.
Vol. 18, n ~ 3 - 1997
Annual CO 2 budget of spruce model ecosystems in the third year of exposure to elevated CO 2 Stephan H~ittenschwiler and Christian KOrner Institute of Botany, University of Basel, Schdnbeinstrasse 6, CH-4056 Basel, Switzerland. Received: 18.t0.96
Accepted: 24.1.97
Abstract Clones of 4-year-old spmce trees (Picea abies) were grown in competition in model ecosystems with nutrient-poor natural forest soil and natural understory vegetation and were exposed to three CO 2 concentrations (280, 420 and 560 pmol mol -~) for three years. Diurnal net ecosystem CO 2 uptake (NECa), nocturnal net ecosystem CO 2 loss (NEC,) and soil CO 2 efflux were measured repeatedly in the third year of CO 2 exposure and were used to estimate an annual ecosystem CO 2 budget. The CO 2induced stimulation of NEC d varied over the year with no measurable stimulation in spring and fall but a high mid-season COz stimulation. Respiratory losses of whole ecosystems and soil CO 2 effiux alone were both progressively increased with increasing CO 2, thus counteracting the CO 2 stimulation of photosynthesis per unit ground area. Consequently, the annual net ecosystem CO 2 uptake was only moderately and non-linearly stimulated by CO 2 (+8% = 84 g C m -2 aq at 420 and +9% = 90 g C m -2 aq at 560 compared to 280 [amol CO 2 mol-l). We conclude that the rising atmospheric CO 2 concentration may Iead to an increase in annual net ecosystem carbon gain of rather nutrient-poor spruce communities. Our results further suggest that CO 2 fertilization effects may be greatest under current CO 2 concentration and that relative increases of net ecosystem CO 2 uptake will become relatively smaller as atmospheric CO 2 will continue to rise.
Keywords: Carbon sequestration, CO 2 budget, dark respiration, ecosy]tem CO 2 exchange, elevated CO2, Picea abies, soil CO 2 efflux.
R~sum~ Des clones d'tpictas (Picea abies) gtg~sde 4 ans ont 6t~ cultiv~s en compttition dans des 6co-syst~mes modeles sur un sol fomstier naturel pauvre en nutriments et avec une vtgttation basse naturelle ; ils ont 6t6 exposts h 3 concentrations en CO 2 (280, 420et 560 lamol mol -~) pendant 3 ans. Le prtl~vement diurne net en CO 2 de l'tcosystbme (NECk), la perte nocturne nette en CO 2 de l'tcosysttme (NECn) et le d~gagement de CO 2 du sol ont 6t6 mesurts ~ plusieurs reprises au cours de la troisi~me annte d'exposition au CO 2 et ont 6t6 utilists pour estimer un budget annuel de l'tcosyst~me en CO 2. La stimulation de NEC d induite par te CO 2 varie au cours de l'ann~e sans stimulation mesu-rable au printemps et ~t l'automne mais avec une forte stimulation du CO 2 en milieu de saison. Seuls les pertes respiratoires de t'tcosystbme entier et le degagement de CO 2 du sol augmentent progressivement avec une ~l~vation du CO2, contrecarrant ainsi la stimulation de la photosynth~se par le CO 2 par unit~ de surface. En consequence, le prtl~vement net annuel de l'~cosyst~me eu CO 2 n'est stimul~ que moder~ment et de fa~on non-lintaire par le CO~, (+8 % = 84 g C m -2 aq h 420 et +9 % = 90 g C m -2 a q ~ 560 h comparer avec 280 pmol CO 2 tool- ). Nous en concluons que l'augmentation de la concentration en CO 2 atmosphtrique peut mener ~ un accroissement de l'accumulation annuelle nette en carbone de 1'6co-
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s. Hiittenschwiler and C. KOrner
syst~me de communaut6s d'6pic6as plut6t pauvres en nutriments. Nos r6sultats sugg&ent de plus que les effets de la fertilisation par le CO 2 pourraient ~tre tr~s importants pour des concentrations courantes en CO 2 et que les augmentations relatives du pr61bvement net de l'6cosyst~me en CO 2 deviendront relativement plus faibles ?~mesure que le CO 2 atmosph6rique continuera d'augmenter.
INTRODUCTION The terrestrial biosphere as influenced by a multitude of global change effects is of central importance for the current and the future global carbon cycle (e.g. AMTHOR, 1995; SCHI~L, 1995). While the fluxes among the main four carbon pools (fossil carbon, atmosphere, oceans, terrestrial biosphere) should balance, current estimates of the global C budget led to the so called "missing sink" in the range of 1.1 Gt a -t (D~xoN et al., 1994) to 1.8 Gt a-t (StrNOQUlST, 1993). This is equivalent to 2-3% of the global annual net primary productivity (NPP). Most of this missing carbon is thought to be sequestered in terrestrial ecosystems (ScHIMEL, 1995) as a result of forest regrowth (ca. 0.5 Gt a-l), growth stimulation by atmospheric N deposition (ca. 0.6 Gt a-l), and by CO 2 fertilization (ca. 1.0 Gt a-t). The continued increase of fitmospheric CO 2 concentration up to the predicted doubling of the current concentration within the next century is expected to further increase NPP of terrestrial ecosystems (MzLILLO et al., 1993), which in turn is often assumed to lead to increased terrestrial ecosystem carbon sequestration. However, our knowledge about the effects of elevated CO 2 on the carbon balance of ecosystems is very limited, and most of what we know applies to herbaceous systems (KORr,rER, 1996). The lack of data for forest ecosystems is particularly problematic because they store more than 80% of all above-ground, and 40% of all below-ground-terrestrial carbon (WHia~rar~R & LI~Ns, 1975; OLSONet al., 1983), and represent 40% of the total global NPP (oceans included; WHnwAKZl~& LW,ENS, 1975). The aim of this study was to experimentally quantify the effect of increased atmospheric CO 2 on the CO 2 balance of spruce (Picea abies) model ecosystems and to discuss these data in the context of potential carbon sequestration by forest ecosystems. We provide a data set of ground-area-based diurnal net ecosystem CO 2 uptake (NEC d) and soil CO 2 effiux (SCE) in the third year of continuous exposure to elevated CO 2. We also determined nocturnal net ecosystem CO 2 loss (NECn) for this year and calculated an annual CO 2 budget for the model ecosystems. M A T E R I A L S AND M E T H O D S Six 4-year-old Picea abies Karst. trees (height of 0.7 m), each of a different genotype were planted into each of nine 0.25 m 3 containers (100 • 70 x 36 cm) in early April 1993. Trees were grown in competition with the typical montane spruce forest understory species Oxalis acetosella L., Homogyne alpina L. and Melampyrurn sylvaticum L. (the latter species in the second and third year of the experiment only). The soil (podsol-type, pH ca. 4.5) was collected in a montane old-growth spruce-fir forest of the northern Swiss Alps near Luzern (1140 m, 46~ 8~ and was then re-established by horizons (B-, A-horizon, raw humus, and litter layer) in each of the nine model ecosystems (see H~TI'ENSCHWILER & KOR~R, 1996). Groups of three model ecosystems were exposed to either 280, 420 or 560 lamol mol-l atmospheric CO 2 in three different environmental chambers. We applied different rates of wet N deposition to each model ecosystem within each CO 2 treatment: 0,30 kg ha -I a-1 and 90 kg h a I a-l (as ammonium
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nitrate dissolved in deionized irrigation water) to test for the combined effects of elevated C O 2 and N deposition on tree growth (see H~,TrENSCHWlLER & KOP,NER, 1996). However, the N deposition treatments are not considered here, because our main focus was to look at the effects of rising CO 2 on ecosystem gas exchange (see below). Treatments were started in early April 1993 and continued until late November 1995 when trees were harvested. All environmental chambers were run with the same set of variable weather regimes based on a 3-year (1989-1991) data set from the meteorological station close to the field site where tile soil was collected; i.e. typical lower montane climate in the northern part of the Alps (see HATTENSCnWrLER& KORNER, 1996). Environmental chamber climate and photoperiod was adjusted weekly. Simulated temperatures ranged from -3~ in mid-winter to 24~ in mid-summer, and relative humidity was set to 70% during "clear" days and 85% during "cloudy" days. "Clear days" were characterized by a quantum flux density (QFD) of about 800 lamol m -2 s-1 and "cloudy days" by about 400 lamol m -z s-1 just above the canopy. "Clear days" began and ended with 2 h or 3 h of low QFD ("cloudy day" level), respectively. Precipitation followed the natural seasonal pattern and was applied weekly to the top of the spruce canopy using a rose (a total of 1200 m m per year). Potential chamber and positional effects were minimized by changing model ecosystem position within chambers weekly and between chambers monthly. In the third year of the experiment we measured diurnal net ecosystem CO2 uptake per unit ground area (NECd) in the afternoon of "clear days" (i.e. at 800 lamol m -2 s -l of QFD) eight times throughout the year (fig. IA). During measurements all three model ecosystems in each CO 2 treatment remained in their own environmental chamber which was then used as a closed gas exchange chamber. Chamber CO 2 control during measurements was interrupted. We measured the CO 2 depletion rate within the chamber with an IRGA (type 225-Mk 3, ADC, Hoddesdon, England). The leak rate of each environmental chamber was determined by monitoring the depletion of injected N20 (for an insideoutside CO 2 concentration gradient), and by monitoring the CO z flux into the empty, CO 2 depleted chambers (280 lamol tool -l, for an outside-inside CO 2 concentration gradient). Nocturnal (i.e. predawn) ecosystem CO 2 loss per unit ground area (NECn) was measured in late May and in mid July 1995 in the same way as NEC d. In addition, soil CO 2 effiux (SCE) for each ecosystem was measured separately on three different 0.0314 m 2 areas on bare forest floor in each ecosystem (i.e. 9 patches per CO 2 treatment) using a closed-cup system (SRC-l, EGM-1, PP Systems, Stotfold, Hitchin Herts, UK). These measurements took 1-2 rain each and were made immediately after the NECd measurements. Finally we calculated an annual ecosystem CO 2 budget using the following assumptions and simplifications: (1) The measured NEC a was applied to the hours of high QFD (800 lamol m -2 s-l). For the hours of lower QFD (400 pmol m -2 s-1) at the beginning and end of "clear days" and for "cloudy days" (400 tamol m -z s-J) we reduced NEC a by a factor of 0.8 (estimated from the light response curves of net shoot photosynthesis). (2) Nocturnal soil CO 2 effiux (SCE,) was calculated from daytime rates using a Q10 of 2.2 (estimated from separate measurements at different soil temperatures) to correct for soil temperature differences. (3) Above-ground plant dark respiration (Rn) was expressed as a constant percentage of NEC d determined for each CO 2 treatment separately as R, = NECn - SCE~ at two dates (see below). (4) NEC d, Rn, and SCE. were applied to the entire duration of the specific weather regimes. (5) For periods with a weather regime not covered by measurements, data from the preceding period were used and were adjusted to the actual temperatures using a Ql0 of 2.2 for SCE n and a QJ0 of 2.1 for NEC a (estimated from the measurements made at day 17 and at day 43). Data on NEC a and NEC n could not be tested statistically because all three model ecosystems of each CO 2 treatment were measured together. We measured ecosystems together in one chamber to avoid the profound effects of: disrupting the continuous canopy formed by the three systems leading to large increases in side light, and to ensure the detection of adequate CO z concentration change rates (in particular for the measurements of NECn). SCE was tested for effects of CO 2 or N over time by using Vol. 18, n ~ 3 - 1997
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s. H/ittenschwiler and C. K6rner
repeated measures analysis. CO 2 effects on soil CO 2 effiux of single measurement dates were tested by separate one-way ANOVAs.
RESULTS
Differences in diurnal net ecosystem C O 2 uptake (NECd) between C O 2 t r e a t m e n t s were small or absent early and late in the growing season. However, NEC d measured at 420 and 560 ~tmol CO z mo1-1 between day 80 (mid June) and day 168 (early September) was 30% and 42% greater, respectively, than NEC d measured at 280 pmol CO 2 mol "1 (fig. !A). SCE was also significantly greater at the two higher CO 2 concentrations (fig. 1B). Mean SCE for the three model ecosystems per CO 2 level ranged
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Days of growth (Day 0: 1. April) FIG. 1. -- A. Diurnal net ecosystem CO z exchange rate (NECd) at a top-of-canopy QFD of 800 ~mol m 2 s-1 and B" soil CO 2 effiux (measured right after NECd) of spruce model ecosystems over the third year of growth at three different atmospheric CO 2 concentrations ([3: 280, Q: 420, A: 560 }arnol CO 2 mol-l). For each date the average of two successive NEC d measurements (taken in the afternoon between 3 pm and 6 pro, depending on season) per CO 2 level (i.e. 3 model ecosystems, each of a different N deposition rate) are shown. The soil CO 2 effiux was determined as an average of three measurements (taken at three different spots) within each of the nine model ecosystems for each measurement date. Symbols in fig. 1B represent mean values (_+ SE) of 3 model ecosystems per CO 2 level (pooled across N treatments) and stars indicate statistically significant CO2-effects at P < 0.05 (*) or at P < 0.01 (**). Air temperatures (fig. IA) and soil temperatures (fig. tB) are shown for each measurement date.
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from 1.4, 1.5, and 1.3 tamol m -2 s-1 on day 17 to 5.5, 6.6, and 7.4 Nnol m -2 s -1 (in the order of increasing CO 2 concentrations) on day 168 when soil temperatures were highest. Maximum relative CO 2 stimulation o f SCE was +33% at 420 and +57% at 560, when compared to rates measured at 280 ~mol CO 2 mo1-1. Stimulation on an annual basis averaged +11% at 420 and +19% at 560 lamol CO 2 mo1-1. There was a non-significant trend towards increased SCE with increasing N deposition at any o f the CO 2 concentrations (P = 0.50, rep. meas. analysis). The nocturnal net ecosystem CO 2 loss (NECn) was 5.2, 5.2 and 6.5 ~mol m -2 s-l on day 56 and 5.6, 6.8 and 7.9 gmol m -z s -j on day 104 (in the order of increasing CO 2 concentration). Substracting SCE resulted in similar ratios of total above-ground plant dark respiration (R n) to NEC a at both measurement dates (i.e. a mean of 15.2% _+ 1.0 at 280, 15.6% _+ 0.4 at 420, and 19% _ 0.7 at 560 pmol CO 2 mol-1). The net annual ecosystem CO 2 uptake estimated using NEC a, NEC n and SCE was 7.0 tool CO 2 m -2 (= 84 g C) and 7.5 tool CO 2 m -2 (= 90 g C) greater at 420 and at 560, than at 280 pmol CO 2 mol -j (table I). Estimated annual soil CO 2 effiux [Y~SCEn (nocturnal soil CO 2 efflux) + YSCE a (diurnal soil CO2 effiux)] was a major component of the ecosystem CO 2 budget: 73.7, 81.4, and 87.7 mol CO 2 m -2 a -1 (with increasing CO2 concentration). This is equivalent to an annual ecosystem carbon loss of ca. 881,997, and 1052 g C m -2 via root and soil microbial respiration. TABLE][.- - Annual sums of diurnal CO2gain (~ NECa), CO 2 losses through dark respiration of above-ground plant parts (~. R,) and nocturnal soil CO 2 effiux ( Y SCE~), and the annual net CO 2 balance of model spruce ecosystems exposed to three atmospheric CO 2 concentrations (all values in tool CO z per square meter ground area and per year).
CO2 treatment (pmolmol-I) 280 420 560
Y,N E C 142.6 156.2 166.0
d
~. Rn
~ SCE n
24.2 26.5 33.3
33.9 38.2 40.7
Annual net CO2 balance :84.5 91.5 92.0
DISCUSSION
Elevated CO 2 substantially stimulated mid-season ecosystem net CO 2 uptake per unit ground area (NECd) in our spruce model ecosystems, even though we found no stimulation of tree growth (H~TTENSCHWILER& KORNER, 1996; I-I)~TTENSCHWILER& KORNLR, in prep.). We assume that the overall CO2-response likely reflects that of ecosystems receiving medium wet N deposition (ca. 30 kg ha -1 a-l; similar to the maximum currently measured in certain frontal ranges of the northern Alps). The average increase in mid-season NEC a we observed between 280 and 420 pmot C O 2 mo1-1 (30%) and between 280 and 560 pmol CO 2 mol -~ (42%) is similar to that observed between current ambient (350 lamol tool -1) and 600-650 pmol CO 2 mol -l in a number of herbaceous plant communities (DRAKE & LEADLEY, 1991; DIEMER, 1994; STOCKER e t al., 1997). There are no other data on NEC a of tree communities grown under elevated CO 2. In our study, the C O 2 stimulation of NEC d only became apparent around day 80 (mid June), when current-year needles began contributing to the net ecosystem CO 2 uptake. Thus, it appears that the positive response of current-year needle photosynthesis to elevated CO: was responsible for the stimulation of mid-season NEC d at the two higher CO 2 concentrations. Vol. 18, n~ 3 - 1997
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However, down-regulation of current-year needle photosynthesis occurred later in the growing season (unpublished data), similar to what we found in the second year of the experiment (HA~zNSCI-IWILER & KORNER, 1996). From mid September 1995 onwards NEC a was similar at all CO 2 levels, in accordance to what we found for NEC d in the fall of 1994 (HATTENSCHWILER& KORNER, 1996). In addition to physiological down-regulation of photosynthesis at the leaf level, we also found allometric adjustments to elevated CO 2 in the third year at the canopy level, expressed as reductions in LAI (12% lower at 420 and 16% lower at 560 relative to 280 lamol CO 2 mo1-1 = 5.2 m 2 m-2). In relative terms these data are similar to what we measured in the second year (H~,TTENSCHWILER& Ki3RNER, 1996). The increase in the ratio of above-ground plant dark respiration to canopy photosynthesis under elevated CO 2 we found, is in contrast to most, but not all studies reporting respiration/photosynthesis ratios at the whole-plant or the leaf level (review by AMTnOR, 1995). In 1994 (second year of the experiment) we found no differences in current-year branch dark respiration between CO 2 treatments (HATTENSCHWILER& KOP,NER, 1996). We can only speculate about the reasons for the apparent differences in CO 2 effect on current-year branch dark respiration in the second year and on the total above-ground plant dark respiration in the third year. The stimulating CO z effect on SCE measured in 1995 was greater than that measured in 1994 (H,~TTENSCHWILERt~ZKORNER, 1996). Higher SCE at elevated CO 2 may be in part explained by greater root dry mass at the two higher CO 2 concentrations compared to the lowest CO 2 concentration (+15% at harvest, no differences between 420 and 560 pmol CO 2 mol-1; V. WIEMKEN,personal communication). A stimulation of microbial activity linked to increased root exudation and/or fine root turnover (e.g. NORBY et al., 1987; KORNER& ARNONZ, 1992) may also have contributed to the higher SCE at elevated CO 2. The 24% mid-season CO 2 stimulation of SCE reported for artificial yellow poplar communities (NoRBY et al., 1992) is lower than the maximum mid-season stimulation measured here, but somewhat higher than the estimated mean annual CO 2 stimulation. Annual ecosystem carbon loss through SCE in addition to the increased aboveground plant dark respiration with increasing CO 2 largely compensated for the higher mid-season NEC d at elevated CO 2. On an annual basis we estimated a relative increase of net ecosystem CO 2 uptake of about 8.5% at the two higher CO 2 concentrations (only a very small difference was found between 420 and 560 larnol CO 2 mo1-1) compared to 280 lamol CO 2 mo1-1. Despite increased net ecosystem CO 2 uptake under elevated COz, above-ground spruce tree growth and biomass production was not stimulated (H,~TTENSCHWILER& KORNER, 1996; HATTENSCHW1LER& KORNER, in prep.). These findings are similar to those of alpine grassland ecosystems (ScH,~PPI t~ KORNER, 1996). Increased final root biomass would account for ca. 75% of the surplus in carbon fixed at the two higher CO 2 concentrations in year three. We do not know how much of the extra carbon fixed, accumulated as soil organic matter (SOM) via higher fine root turnover, ended up in microbial biomass, or was leached from the soil as dissolved organic carbon (DOC). If our results hold true for natural forests, they indicate that the global increase in atmospheric CO 2 concentration over the past 150 years may have caused an increase in annual forest ecosystem carbon gain. A mean increase in annual net CO a uptake by the world's forests (ca. 45 Mio km2), corresponding to about half (i.e. 45 g C m -2 a-l) of what we found for a change from 280 to 420 lamol CO a mol -', would Acta (Ecologica
CO z budget of spruce model ecosystems
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be sufficient to account for the "missing 2 Gt C" in the current global C budget. Perhaps the most important finding of our study is the non-linear response of the ecosystem CO 2 balance to increasing CO2; the largest change occurring between 280 and 420 lamol CO 2 mo1-1. This suggests (1) a response saturation to increasing CO 2 at rather low CO 2 concentrations, and (2) that natural forests may be responding less to rising CO2 in the future than they have in the past, at least in tree communities comparable to those studied here. ACKNOWLEDGEMENTS The model ecosystems used here were jointly constructed and maintained with the team of Andres WIEMKEN.We thank Jay ARNOr,~ for helpful comments on earlier versions of the manuscript, and Fritz ErmSAM for maintaining the sophisticated environmental chambers. This research was funded as part of the National Program on climate change and natural disasters (NFP 31) through Swiss National Science Foundation grant no. 4031-034220.
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