• carbon balance;
  • carbon dioxide (CO2);
  • climate change;
  • fertilization;
  • global warming


  1. Top of page
  2. I.Introduction
  3. II. Net ecosystem exchange and changes in carbon stocks
  4. III. Elevated [CO2]
  5. IV. Temperature
  6. V.Fertilization and nitrogen deposition
  7. VI. Disturbances and forest management
  8. VII. Feedbacks and interactions
  9. VIII. Will we have forest carbon sinks in the future?
  10. Acknowledgements
  11. References


II.Net ecosystem exchange and changes in carbon stocks466
III.Elevated [CO2]468
V.Fertilization and nitrogen deposition471
VI.Disturbances and forest management472
VII.Feedbacks and interactions474
VIII.Will we have forest carbon sinks in the future?475


  1. Top of page
  2. I.Introduction
  3. II. Net ecosystem exchange and changes in carbon stocks
  4. III. Elevated [CO2]
  5. IV. Temperature
  6. V.Fertilization and nitrogen deposition
  7. VI. Disturbances and forest management
  8. VII. Feedbacks and interactions
  9. VIII. Will we have forest carbon sinks in the future?
  10. Acknowledgements
  11. References

Forest ecosystems contain a large part of the carbon stored on land, in the form of both biomass and soil organic matter (SOM). The long-term fate of C in forest ecosystems depends on whether it is stored in living biomass or soils. Forest trees also control the major terrestrial bidirectional transfer of C between the atmosphere and the soil: forests take up large amounts of CO2 from the atmosphere through photosynthesis, and return large amounts through respiration by vegetation and decomposers in the soil. Carbon stocks in soil exceed those in vegetation by c. 2 : 1 in northern temperate forests to over 5 : 1 in boreal forests (Dixon et al., 1994; Schlesinger, 1997). Thus changes in soil C stocks can be more important than changes in vegetation C stocks for forest C budgets (Medlyn et al., 2005). Increasing atmospheric carbon dioxide concentration [CO2] with subsequent changing climate, increased nitrogen deposition, and changing land use have changed (and will change) the forest C stocks.

Over the past 200 yr, approx. 405 ± 30 Pg C has been emitted into the atmosphere as CO2 as a result of fossil fuel burning and cement production (75%), and of land use and land-use change (25%), predominantly deforestation (IPCC, 2001). As a result, the global average atmospheric [CO2] has risen by approx. 35%, from 280 ± 5 to 377 ppmv, in 2004 (WMO, 2006). This increase in [CO2] accounts for approx. 40% of these anthropogenic emissions, the remainder having been absorbed by the oceans and terrestrial ecosystems. On average during the 1990s, annual global emissions of greenhouse gases amounted to 6.4 ± 0.3 Pg C from fossil fuels, plus 1.7 ± 0.8 Pg C from land use and land-use change, mainly deforestation in the tropics. There are four main global sinks for these emissions: the atmosphere (3.2 ± 0.1 Pg C); the oceans (1.7 ± 0.5 Pg C); tropical vegetation (1.9 ± 1.3 Pg C); and temperate and boreal vegetation, mainly forests (1.3 ± 0.9 Pg C) (Read et al., 2001). In particular, plant photosynthesis is responding to this increase in [CO2].

Deposition of N – wet and dry, oxidized and reduced – to forests is between 1 and 100 kg ha−1 yr−1. The smaller amounts occur in the more remote forests, particularly in rural areas at high latitudes; the large amounts in industrialized central Europe (Jarvis & Fowler, 2001). Part of the N delivered to forests in this way is absorbed directly by the leaves and needles of trees without reaching the ground, and fine roots, mycorrhizae and decomposer organisms quickly scavenge the N that does reach the ground. A key uncertainty is to what extent, and for how long, high annual rates of N deposition will be able to stimulate the production of mature forests, and whether detrimental effects such as N saturation will eventually appear (Aber et al., 1989, 1998; Binkley & Högberg, 1997).

The average global temperature increased during the 20th century by 0.6°C, and projections are for an additional increase of 1.4–5.8°C during the 21st century (IPCC, 2001). The likely effects of temperature extend from straightforward, direct effects on biochemical reactions to indirect effects through lengthening growing seasons (Myneni et al., 1997), with potential risks of passing temperature thresholds to particular responses.

Forests in the northern hemisphere are in a transient state of development when considered on both long and short time scales. At mid-to-high latitudes, the forests present today have been migrating, evolving and developing since the ice retreated after the last glaciation. Large amounts of C have accumulated in these forests over the past 10 000 yr, and are continuing to accumulate in many forests. In central Europe there has been a long history of forest exploitation and management, so that many of today's forests were relatively recently established in the 18th century. In North America, particularly in the north-east, land was cleared for agriculture in the 17th and 18th centuries, but was abandoned to forest regrowth (so-called ‘old field succession’) in the 19th century as farmers moved westwards. Elsewhere, areas of forest are recovering from naturally occurring fires caused by lightning strikes and windthrow resulting from severe storms.

The global increase in [CO2], temperature and N that has occurred so far has also probably contributed to the current C sinks in forests of the north temperate and boreal regions. In particular, N has been identified as a driving factor in European forests (Binkley & Högberg, 1997; Karjalainen et al., in press). A stand of trees is a C sink if the uptake of CO2 in gross photosynthesis (gross photosynthetic production, GPP) exceeds the losses of CO2 in total ecosystem respiration (RE = RA + RH) and volatile organic compounds (Fig. 1). In general, a stand has the potential to be a C sink in daytime, a C source at night, a C sink in summer, and a C source in winter. Stands will also be sinks or sources of varying strength, depending on their stage in the life cycle of trees and the management cycle of forest stands.


Figure 1. Gross primary production (GPP) is the uptake of carbon in photosynthesis by foliage of trees in the forest from the atmosphere. Carbon losses as a result of autotrophic respiration (RA) and loss of volatile organic C (VOC) from the foliage reduce this uptake to net primary production (NPP). At the scale of the stand, further C losses occur because of heterotrophic respiration (RH) associated with decomposition of dead organic matter, resulting in the net ecosystem exchange (NEE). Additional losses of dissolved inorganic C (DIC) and dissolved organic C (DOC) in drainage through the soil profile into rivers and into the atmosphere reduce this amount to the net ecosystem production (NEP). Finally, at the scale of the forest and landscape, losses caused by disturbances (D), such as fire, herbivory and management activities, further reduce the amount of C stored in the forest. The resulting net imbalance of the forest ecosystem can be interpreted as the net biome productivity (NBP). The nitrogen cycle parallels the C cycle, but has an additional flux through uptake of N from the soil. Note: Chapin et al. (2006) recently suggested the use of somewhat different, and more consistent, terms related to carbon cycling. A change to their terminology would, however, not alter the conclusions in the present paper.

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Mature and over-mature forests are of particular concern with respect to the long-term permanence of forest C sinks. On the basis of the ‘climax concept’ (Clements, 1916), it has long been believed that largely undisturbed, old-growth forests are in a state of equilibrium, such that over a period of years they are C-neutral, with neither net gain nor loss of C. This view has been challenged in recent years with increasing evidence from long-term measurements of tree growth on sample plots and measurements of CO2 fluxes in old-growth stands that indicate widespread increases in growth and net primary production (NPP) of stands across Europe (Spiecker et al., 1996) and in the neotropics (Malhi et al., 2004). There are several possible explanations as to why natural and seminatural mature stands and old-growth forests are C sinks today, a likely driving force being the human-induced changes in the atmosphere that have occurred over the past one and a half centuries.

In this review we address C storage in northern forests as affected by (1) accumulation of C in managed forests between major disturbances; (2) recovery and management of C stocks; (3) permanence of C stocks – the climax concept vs increase in growth of old-growth stands; and (4) impacts on C stocks of [CO2], N and temperature. This review updates earlier reviews (Ceulemans & Mousseau, 1994; Saxe et al., 1998, 2001; Poorter & Navas, 2003; Nowak et al., 2004; Ainsworth & Long, 2005), takes an ecosystem perspective, and emphasizes interactions between individual factors and management options.

II. Net ecosystem exchange and changes in carbon stocks

  1. Top of page
  2. I.Introduction
  3. II. Net ecosystem exchange and changes in carbon stocks
  4. III. Elevated [CO2]
  5. IV. Temperature
  6. V.Fertilization and nitrogen deposition
  7. VI. Disturbances and forest management
  8. VII. Feedbacks and interactions
  9. VIII. Will we have forest carbon sinks in the future?
  10. Acknowledgements
  11. References

Changes in the total C stocks in forest stands (net ecosystem exchange, NEE) can be assessed by summing the changes in both vegetation and soil (Fig. 1). Changes in tree C stocks over a 5-yr period (the length of the Kyoto commitment period) can be assessed with reasonable precision by standard inventory methods, such as those used in national forest inventories (Gower et al., 2001). Changes in soil C stocks can also be determined by standard sampling techniques, but very many samples are required to achieve adequate precision over a period as short as 5 yr (Conen et al., 2003, 2005; Smith, 2004). Another way to estimate annual C balances is to measure biomass accumulation, net photosynthesis, and the autotrophic and heterotrophic respiration fluxes. This usually involves integrating and scaling up point measurements in space and time, with a relatively large uncertainty in the final, annual storage term because of the many assumptions involved (Malhi et al., 1999).

Alternatively, the net turbulent flux of CO2 over a canopy can be determined by eddy-covariance measurements, and may be extrapolated to the overall net CO2 exchange, over periods of hours to years (Aubinet et al., 2000). According to definitions illustrated in Fig. 1, eddy-covariance measurements of CO2 net flux, Fc, may not be interpreted strictly as NEE, but correspond to the difference between GPP and ecosystem respiration (RE). This may be important as C is also exchanged in the gas phase by forest ecosystems as nonCO2 organic forms such as isoprene and methane (Harley et al., 1997). The accuracy of eddy-covariance measurements used under ideal site conditions is believed to be ±50 g C m−2 yr−1 (Baldocchi, 2003). Spatial variation originating from underlying variability in ecosystem attributes (e.g. leaf-area index, LAI) may, however, result in coefficients of variation (SD relative to the mean) of 10%, even over very uniform forests (Oren et al., 2006). Recent measurements made on >100 young and mature forest stands worldwide, with a range of species and management histories, have yielded annual values of CO2 exchange from approx. −100 to 250 g C m−2 yr−1 for boreal forests; from 250 to 700 g C m−2 yr−1 for temperate forests; and from 100 to 600 g C m−2 yr−1 for humid tropical forests (Malhi et al., 1999). (We are using the sign convention that NEE is positive when the forest is taking up CO2.)

Net ecosystem exchange from eddy-covariance measurements shows a decreasing trend with latitude (Fig. 2a). The forest stands in the temperate region tend to be stronger C sinks than the boreal forest stands, although the boreal evergreen conifer stand in an oceanic climate is a sink comparable with the best of the temperate forest stands. Growing-season length, temperature and humidity index appear to be the important variables determining the potential size of the C sink (Fig. 2b,c). Measurements of NEE made over several years on boreal forest stands have shown major variations in the annual amount of C sequestered, depending largely on when the thaw occurred. A thaw occurring 2 wk earlier than usual may lead to an additional annual sequestration of 100 g C m−2 (Black et al., 2005). Under the same temperature regime, evergreen stands tend to be stronger sinks than stands of deciduous trees.


Figure 2. Net ecosystem exchange (NEE) as a function of (a) latitude, (b) growing-season temperature and (c) humidity index (evapotranspiration minus precipitation) (from Black et al., 2005). The same site may be represented by data from more than 1 yr.

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Eddy-covariance measurements show, in general, that young forest stands (<25 yr old) are stronger C sinks than old stands (Fig. 3c). Data collected over chronosequences in managed European forests demonstrate that NEE peaks at an age varying from 10 to 60 yr and generally declines thereafter. This pattern is consistent with the results obtained in a fire chronosequence in a temperate dry forest in North America (Law et al., 2003). Although NEE clearly can be maintained without significant decline beyond 60 yr (Lloyd et al., 2002), NEE has been found to reach neutral status in some old-growth boreal forests (Law et al., 2003; Carrara et al., 2004; Kolari et al., 2004). Some of the stands in Fig. 3c, particularly the older ones, are close to C-neutral or are C sources, and there are other observations of old-growth stands close to a neutral C balance (Goulden et al., 1998; Lindroth et al., 1998; Valentini et al., 2000; Janssens et al., 2001; Carrara et al., 2004; Pregitzer & Euskirchen, 2004), although 100-yr-old oak–hickory forest can be as strong a sink as a fast-growing young Pinus taeda plantation (Stoy et al., 2006), and Siberian Pinus sylvestris forests continued to be C sinks even at an age of 200 yr (Schulze et al., 1999). The age-related trend in NEE still appears to be poorly documented for the postmature stage, and firm conclusions cannot be drawn so far from the present data.


Figure 3. Net ecosystem exchange (NEE) as a function of (a) nitrogen deposition, (b) leaf-area index (LAI) and (c) stand age (from Black et al., 2005). The same site may be represented by data from more than 1 yr.

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If we take a relatively short-term snapshot, it is reasonable to assume that undisturbed forests would, over decades, have C balances that are close to equilibrium (NEE ≈ 0). Disturbance will remove a forest from equilibrium; the major questions are how rapidly, and by which routes, a disturbed forest will adjust to a new equilibrium. In the short term, the key question is how net canopy photosynthesis (P) and decomposition are influenced by temperature (T), [CO2] and N, because biomass production and C sequestration are closely connected, and the latter depends on the balance between C uptake through P and release through decomposition. P is a function of T, [CO2] (Ca), availability of water (W), availability of N (Na), absorbed solar radiation (Q), and foliage leaf-area index (L):

  • P = f(T, Ca, W) × f(Na) × f(Q, L)

In a three-pool model, P responds rapidly to Ca and Na. Litter production responds somewhat more slowly, and heterotrophic respiration yet more slowly because the latter can only increase after the build-up of a larger SOM pool. The effect of T is mainly through an initial increase in the specific rate of heterotrophic respiration (shorter residence time of soil C), which eventually declines towards the previous rate when the labile soil C pool has declined. Other single-factor effects on C fluxes will also follow the same qualitative patterns. For example, P will respond to T and heterotrophic respiration to Na (Fig. 4). Conceptually, the effects of increased T, elevated [CO2] and increased N deposition in unmanaged and managed forests can be analysed one at a time with changes in pool size determined by turnover rates of those pools (Fig. 4; Goudriaan, 1990). The following sections expand the single factor responses in more detail and develop chains of responses, with a summary in Table 1.


Figure 4. Qualitative responses of net primary production (NPP), litterfall, heterotrophic respiration (RH), and plant and soil carbon pools to step changes in [CO2], nitrogen and temperature (T).

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Table 1.   Important cause–effect chains for carbon cycling
No.Rate*PerturbationCause–effect chainStrengthKnowledge
  • *

    Rate at which cause–effect chains respond: fast, within-year; intermediate, a few years; slow, decades; very slow, centuries.

  • Strength of the effects.

  • Knowledge of the links in the chain.

  • NPP, net primary production; SOM, soil organic matter.

5Fast[CO2][UPWARDS ARROW]Allocation to roots and mycorrhiza [UPWARDS ARROW][RIGHTWARDS DOUBLE ARROW] Soil respiration [UPWARDS ARROW]MediumHigh
10IntermediateN[UPWARDS ARROW]Litter N concentration [UPWARDS ARROW][RIGHTWARDS DOUBLE ARROW] Litter decomposition rate [UPWARDS ARROW]? [RIGHTWARDS DOUBLE ARROW] Soil C store [DOWNWARDS ARROW]WeakUnclear
11Intermediate[CO2][UPWARDS ARROW]Litter N concentration [DOWNWARDS ARROW][RIGHTWARDS DOUBLE ARROW] Litter decomposition rate [DOWNWARDS ARROW]?[RIGHTWARDS DOUBLE ARROW] Soil C store [UPWARDS ARROW]WeakUnclear

III. Elevated [CO2]

  1. Top of page
  2. I.Introduction
  3. II. Net ecosystem exchange and changes in carbon stocks
  4. III. Elevated [CO2]
  5. IV. Temperature
  6. V.Fertilization and nitrogen deposition
  7. VI. Disturbances and forest management
  8. VII. Feedbacks and interactions
  9. VIII. Will we have forest carbon sinks in the future?
  10. Acknowledgements
  11. References

1. Plant carbon

Hundreds of experiments have shown that increasing [CO2] stimulates tree growth, and the results from short-term studies with seedlings, field studies with saplings, and longer-term, whole-stand manipulations have been reviewed previously (Ceulemans & Mousseau, 1994; Curtis & Wang, 1998; Norby et al., 1999; Gielen & Ceulemans, 2001; Medlyn et al., 2001; Norby et al., 2005). The growth enhancement from CO2 enrichment generally occurs through increases in the rates of net photosynthesis in the order of 40–80% (Saxe et al., 1998; Medlyn et al., 1999), compounded by an increase in leaf area. Observed long-term increases in net photosynthesis are typically somewhat lower than the short-term response. The downward acclimation with time of photosynthesis appears to be related primarily to dilution of the leaf N concentration (Ellsworth et al., 2004). The growth response to elevated [CO2] of young trees with expanding canopies is often further enhanced by increased leaf production, leading to larger LAI (Ainsworth & Long, 2005). Similarly, the leaf area of individual trees growing in a sparse stand with low LAI increased by nearly 22% with increasing [CO2] alone (Kellomäki & Wang, 1997). Increasing [CO2] and temperature resulted in only about half as much increase in LAI, with temperature alone having no effect.

Large, mature forest trees respond physiologically to elevated [CO2] in a manner similar to the younger trees used in most studies (Körner et al., 2005). In closed-canopy stands, the increase in NPP can, however, result from both increase in leaf area and light absorption at low LAI, and increased light-use efficiency at high LAI (Norby et al., 2005). For instance, LAI was not found to increase with elevated [CO2] in dense temperate forest plantations (Sigurdsson et al., 2001; Norby et al., 2003), whereas in young, aggrading forests, leaf area has been found to increase quite rapidly. However, recent analyses of free-air CO2 enrichment (FACE) data show that with increasing soil nutrient supply, stands under elevated [CO2] diverge in LAI from stands under ambient [CO2], even in dense stands, with the aboveground NPP increasing with LAI, without additional effects of elevated [CO2] (McCarthy et al., 2006; Palmroth et al., 2006).

Questions remain as to whether the stimulation by elevated [CO2] will persist over many decades, particularly if sink activity is limited by nutrient availability (Sigurdsson et al., 2001; Körner, 2003, 2006; van Groenigen et al., 2006), or if N is progressively sequestered in SOM and is no longer available (Luo et al., 2004). So far, however, increasing [CO2] has not been found either to stimulate N mineralization (Finzi et al., 2002) or to slow down N availability (Zak et al., 2003).

Respiration is also affected by [CO2]. In a FACE study of a Liquidambar styraciflua stand at Oak Ridge, TN, USA, upper canopy leaves in elevated [CO2] had significantly larger numbers of mitochondria, leaf mass per unit area and leaf starch than did lower canopy leaves, resulting in higher night-time respiration rates (Tissue et al., 2002). Stem respiration was increased by 33% in elevated [CO2]; the increase was driven by increased substrate supply from the leaves (Edwards et al., 2002). Similar results have been reported from experiments with Populus spp., in which effects of elevated [CO2] were modified by crown architecture or by leaf or growth phenology (Sigurdsson, 2001; Gielen et al., 2002). From a FACE experiment with P. taeda, Hamilton et al. (2001) concluded that elevated [CO2] had little direct effect on leaf tissue respiration, and that the influence of elevated [CO2] on respiration was primarily through increased biomass.

The allocation of C to stem biomass or to fast-turnover pools has important implications for the capacity of the forest to retain the assimilated C. Carbon that is allocated to woody biomass will persist in the ecosystem for many years, whereas C allocated to fine roots, which turn over rapidly, may not. Nutrient-limited trees growing in elevated [CO2] have been shown to increase allocation towards belowground sinks for assimilate (Linder & Murray, 1998; Oren et al., 2001; Butnor et al., 2003; Palmroth et al., 2006), and may senesce or drop their leaves earlier (Sigurdsson, 2001). King et al. (2001) observed a 96% increase in fine-root biomass in a mixed stand of trembling aspen and paper birch, and higher proportions of C can be found to be allocated below ground (Janssens et al., 2005), although this does not appear to be the case universally (Tingey et al., 2000). The increased production does not always result in larger standing root biomass, as root turnover can also increase (Phillips et al., 2006). A strong interaction between [CO2] and N is observed in many experiments such that root-growth responses are obtained only at high N levels (Prior et al., 1997; Kasurinen et al., 1999; Pregitzer et al., 2000; Zak et al., 2000). However, fine-root production more than doubled under elevated [CO2] in an N-limited L. styraciflua forest (Norby et al., 2004). Although annual fine-root mortality matched production, standing crop was significantly greater in elevated [CO2] in midsummer, and the increased presence of fine roots was related to increased N uptake (Norby et al., 2004).

It is possible that [CO2] effects are mediated mostly through LAI. The fraction of aboveground NPP allocated to wood, a relatively slow turnover pool, increased with LAI in broadleaf FACE experiments (approx. 50% at low LAI, reaching a maximum of 70% at moderate LAI), with the effect of elevated [CO2] on allocation accounted for entirely by changes in LAI. In pines, allocation to wood decreased with increasing LAI (from approx. 65 to 55%), but is higher (approx. 68–58%) under elevated [CO2] at any LAI level (McCarthy et al., 2006). Total belowground C allocation, most of which returns to the atmosphere as CO2 efflux from the soil, decreased with increasing LAI, reflecting increasing strength of the aboveground sink for C, but the enhancement under elevated [CO2] was constant (approx. 22%) over the entire range of LAI; the response was consistent regardless of the cause of the change in LAI, including increases in LAI with N addition and decreases with droughts (Oren et al., 2001; Palmroth et al., 2006).

The above discussion does not take into account the site-specific balance between water availability and demand, dependent on both soil hydrology and atmospheric conditions. Allocation of the additional carbohydrates generated in elevated [CO2] must reflect this balance in such a way that the root surface area for water uptake is matched with the transpiring leaf surface area, with hydraulic design adjusted accordingly (Hacke et al., 2001). At sites with limited water availability, more carbohydrates allowing the production of a larger leaf biomass and surface area may necessitate increased allocation of biomass to roots below ground, so as to maintain a correspondingly larger standing fine-root biomass (Ewers et al., 2000, 2001).

2. Soil carbon

To date, most studies on the effects of elevated [CO2] have focused on litter properties, and few studies have been made on soil organic C (SOC) stocks in forest ecosystems. Further, the results refer to periods shorter than a decade, often not long enough to fully appreciate SOC changes. Elevated [CO2] is expected to produce energy-rich but nutrient-poor litter, for example, higher C : N ratios (van de Geijn & van Veen, 1993). In a meta-analysis of data from senescent leaves, Norby et al. (2001) found an average N reduction of 7.1% and an increase in lignin of 6.5% in leaves of plants grown in elevated [CO2] compared with those grown in ambient [CO2]. Additionally, plant tissues grown in elevated [CO2] have decreased N concentrations (Cotrufo et al., 1998a; Norby et al., 1999); changes in the composition and concentration of tannins and phenolics (Kainulainen et al., 1998); and modification of physical structure with thicker leaves (Radoglou & Jarvis, 1990a, 1990b; Taylor et al., 2004). On the basis of such observations, the hypothesis arose that plant tissues grown in elevated [CO2] would decompose more slowly than leaves grown in ambient [CO2], with negative feedbacks on N cycling and, in turn, on plant growth enhancement by elevated [CO2] (Strain & Bazzaz, 1983). A comprehensive review showed that leaves grown in elevated [CO2] did not reduce litter decomposition rates significantly (Norby et al., 2001). Growth in elevated [CO2] may, however, affect decomposition by changing the amount and dynamics of litter fall (Schlesinger & Lichter, 2001); by modifying litter quality through changes in plant community composition; and by altering the soil environment and its biological activity (by increase of soil water, C input to soil, rhizosphere activity, etc.). These indirect effects can be tested only by long-term studies on litter decomposition in forests exposed to elevated [CO2], but the current literature comprises results only from short-term incubations (Finzi & Schlesinger, 2002; Cotrufo et al., 2005). Decomposition of root litter has received much less attention, but given the aforementioned increase in fine-root production that often occurs in response to elevated [CO2], the fate of dead roots may be especially important for soil C dynamics. In some cases, elevated [CO2] has promoted root production deeper in the soil profile (Norby et al., 2004; Johnson et al., 2006), where decomposition may be slower.

Hoosbeek et al. (2004) reported a decreased C stock in soils exposed to elevated [CO2] at the end of a 3-yr rotation of a poplar plantation. This change occurred despite larger litter inputs, and was attributed to priming of decomposition of the native SOC. When the study was continued for an additional 2 yr there was, however, a faster increase of SOC in the mineral soil under elevated [CO2] (Hoosbeek et al., 2006). Similarly, the SOC content had increased significantly in a sweetgum (L. styraciflua) plantation after 5 yr of FACE (Jastrow et al., 2005). In the loblolly pine (P. taeda) forest at the Duke University FACE experiment, a build-up of litter on the forest floor occurred in the FACE rings (Schlesinger & Lichter, 2001); this was, however, interpreted as a transient response that would not ultimately lead to significant, long-term C accumulation. In a review of 56 observations of C in mineral soils, mostly from elevated CO2 crop experiments, van Groenigen et al. (2006) noted that unless more than 30 kg N ha−1 yr−1 was added as fertilizer, SOC did not change. Jastrow et al. (2005), however, concluded that although most experiments have been unable individually to document a response of soil C to elevated CO2, meta-analysis indicated that collectively, in outdoor experimental studies lasting at least 2 yr (including forests, grasslands and chaparral), soil C increased by 5.6%, corresponding to an accrual rate of 19 g C m−2 yr−1. This conclusion is consistent with the premise that parts of the additional litter produced under elevated CO2 will eventually enter the SOM in the form of coarse particulate organic matter, where it will initiate aggregate formation and promote C sequestration (Six et al., 1998). This process may contribute to an increase of soil C stocks in the long term.

IV. Temperature

  1. Top of page
  2. I.Introduction
  3. II. Net ecosystem exchange and changes in carbon stocks
  4. III. Elevated [CO2]
  5. IV. Temperature
  6. V.Fertilization and nitrogen deposition
  7. VI. Disturbances and forest management
  8. VII. Feedbacks and interactions
  9. VIII. Will we have forest carbon sinks in the future?
  10. Acknowledgements
  11. References

1. Plant carbon

Air-warming experiments have shown a positive single-factor effect of temperature on photosynthetic rate (Kellomäki & Wang, 1996), but temperature and [CO2] frequently interact. Photosynthetic rate increases substantially with [CO2] and the effect is more pronounced at temperatures around 20°C than at 10°C (Sigurdsson et al., 2002). Taken together, the expected atmospheric changes are likely to stimulate the photosynthetic rate at the leaf scale; but at the stand scale, increasing leaf area may diminish these gains as a result of increased respiratory costs associated with partial shading of more leaf area (Oren et al., 1986). Acclimation of the photosynthetic and respiratory processes may also be important (Atkin & Tjoelker, 2003). Whether or not an increase in canopy leaf area increases C gain depends on the pre-existing canopy leaf area and the canopy structure. Canopies with second- and third-order grouping of the foliage can obtain photosynthetic benefit from an increase in leaf area when this would not eventuate with a random leaf area distribution (Wang & Jarvis, 1991).

Results from a Swedish soil-warming study (Bergh & Linder, 1999) led Majdi & Öhrvik (2004) to suggest that fine-root production was a function of the length of the growing season, and that root mortality increased as soil temperature rose, resulting in a higher C-turnover rate. Future increases in temperature may also increase root mortality more in N-rich soils in temperate forests than in N-poor soils in boreal forests. On suitable sites (e.g. sites with deep, underexploited soils), some of the additional carbohydrates may be allocated to the production of fine roots (Norby et al., 2004) and to mycorrhizal biomass, and the rest may cycle rapidly back to the atmosphere (Schäfer et al., 2003). This rapid cycling may reflect increased rhizodeposition of excess carbohydrates (Schäfer et al., 2003), or fast turnover of fine root (Norby et al., 2004) and mycorrhizal biomass.

2. Soil carbon

In a review, Aerts (1997) showed that, on a global scale, climate (expressed as annual actual evapotranspiration) is the factor that best predicts first-year leaf litter-decay rates. A stimulation of leaf litter decomposition can therefore be anticipated as the result of increasing temperature. Based on a study in four Canadian forests, litter decomposition was predicted to increase by 4–7% relative to the present rate, following an increase in temperature and precipitation estimated from a double [CO2] scenario (Moore et al., 1999). The temperature response of litter at later stages of decomposition and of SOM is debatable, with some studies suggesting increasing sensitivity with decreasing quality (Ågren & Bosatta, 2002; Fierer et al., 2005; Knorr et al., 2005a) and others suggesting no effect (Giardina & Ryan, 2000; Fang et al., 2005); see Davidson & Janssens (2006) for a recent review. Soil-warming experiments indicate that soil respiration, after an initial increase when the heating is first switched on, becomes comparable on unheated and heated plots (Luo et al., 2001; Strömgren, 2001; Melillo et al., 2002). It is possible that such transient initial increases in soil respiration occur, at least partly (Lin et al., 2001), because of increased oxidation of the most labile soil C compounds in the heated plots, leading to the conclusion that, after some time, the decrease in litter quality in the heated plots compensates for the effect of the higher temperature (Kirschbaum, 2004; Eliasson et al., 2005). It remains to be tested if acclimation of autotrophic (Atkin & Tjoelker, 2003) and microbial (Davidson & Janssens, 2006) respiration are also important factors.

V.Fertilization and nitrogen deposition

  1. Top of page
  2. I.Introduction
  3. II. Net ecosystem exchange and changes in carbon stocks
  4. III. Elevated [CO2]
  5. IV. Temperature
  6. V.Fertilization and nitrogen deposition
  7. VI. Disturbances and forest management
  8. VII. Feedbacks and interactions
  9. VIII. Will we have forest carbon sinks in the future?
  10. Acknowledgements
  11. References

1. Plant carbon

If trees respond to N deposition as in fertilization experiments, the leaf area of trees and stands is expected to increase with N deposition in N-limited forests (Linder & Murray, 1998; Ewers et al., 2001; Sigurdsson et al., 2002). In forest ecosystems with severe N limitation, N deposition is likely to increase foliar N concentration with a positive effect on photosynthetic rates and C sequestration, which is observed for oceanic spruce stands (Fig. 3a). Considering that production in most northern temperate and boreal forests is chronically restricted by lack of N (Tamm, 1991; Vitousek & Howarth, 1991), a clear relationship between N deposition and annual NEE (≈CO2 net flux, Fc) could be expected (Fig. 3a). The lack of such a relationship shows that to account for effects of N deposition, all stand factors need to be included.

In ambient [CO2], increased allocation to both leaves and woody tissues was found in an N-fertilization study where the deposition rate was quadrupled in an area already thought to be N-saturated because of a heavy N-deposition load (Nilsson & Wiklund, 1995). From this and other fertilization studies in both ambient and elevated [CO2], it can be inferred that the likely response to increasing N deposition is increased production of leaves and wood, including coarse roots (Oren et al., 2001; Iivonen et al., 2006). In ecosystems approaching N saturation, the effect of N deposition may be less pronounced or even reversed. Fifteen years of high N additions (15 g m−2 yr−1) added to the forest floor in the Harvard Forest Long-Term Research led to N saturation, evidenced by high N-leaching rates and considerably increased tree mortality, although with species differences (Magill et al., 2004).

Increasing leaf area in fertilization experiments can also result in changes in canopy characteristics: for example, a more pronounced gradient in foliar characteristics down the canopy (Palmroth et al., 2002), probably accompanied by reduced photosynthetic rates in the lower canopy, has been observed (Oren et al., 1986). However, forest canopies have considerable acclimation capability. A consequence of this is that the distribution of N adjusts in relation to the distribution of absorbed photosynthetic photon flux density, so as to make effective use of both light and N in photosynthesis (Kull, 2002) leading to transient increase in needle-litter production.

All N deposition does not reach the soil surface, but part of the wet and dry deposition and gaseous forms of N may be directly absorbed in the canopy. The fraction of N entering the ecosystem through canopy uptake is difficult to quantify, and estimates range from a few per cent to 24% (Harrison et al., 2000). It is possible that canopy uptake of N upsets the nutrient balance of trees, with detrimental effects on growth (Schulze, 1989), although this process has not been studied extensively in recent years.

2. Soil carbon

Studies of N effects on decomposition are, in most cases, based on experiments in which large amounts of N have been added once or just a few times. In most cases, the decomposition of leaf and needle litter has also been followed over short periods, with a maximum of 5–8 yr. We are aware of very few experiments in which (1) the effects of long-term additions of small amounts of N have been followed; and (2) the decomposition of SOM has been studied (excluding recent leaf litter). Effects of N fertilization on litter decomposition rates are contradictory (Hobbie, 2005), with some studies showing no effects (Prescott, 1995; Hobbie & Vitousek, 2000); other studies showing increased decomposition rates (Hobbie, 2000; Vestgarden, 2001); and still others showing decreased decomposition rates (Prescott, 1995; Magill & Aber, 1998). A recent meta-analysis by Knorr et al. (2005b) indicates, however, that litter decomposition is stimulated at sites with low ambient N deposition (<5 kg ha−1 yr−1) and for high-quality (low-lignin) litters, whereas decomposition rates are reduced at sites with moderate levels of N deposition (5–10 kg ha−1 yr−1) or for low-quality (typically high-lignin) litters.

From a theoretical point of view, Ågren et al. (2001) identified three variables that can decrease rates of mass loss and thus lead to retention of more C in the soil: (1) decreased decomposer growth rate; (2) increased decomposer efficiency (production-to-assimilation ratio); and (3) more rapid formation of recalcitrant compounds. After applying their model to data from a fertilizer experiment on loss of litter mass, changes in C chemistry, and N concentration, they found that increased decomposer efficiency and more rapid formation of recalcitrant compounds were the most important variables explaining the observed decrease in mass-loss rates of litter of various origins.

Results from a study of N and C cycling in a north–south gradient in Europe are in line with observations by Fog (1988) – a positive relationship between C : N ratio and CO2 evolution rate in the litter and humus layers (Fig. 5), but no clear relationship between C : N and CO2 evolution rate in the mineral soil (Persson et al., 2000). However, along the European gradient, many variables other than C : N might affect the mineralization rate. Manipulation of N at the same site can reduce these confounding variables. In two Swedish forest fertilization experiments (Norrliden and Stråsan), N was added annually over 23 and 27 yr, respectively. Laboratory incubations showed a 30% reduction of the mineralization rate in the mor layer of plots that had received N additions of 60 kg ha−1 yr−1 compared with unfertilized plots (Persson et al., 2000). Results from modelling of bomb-14C data from the Norrliden experiment are in line with the results from these laboratory incubations, showing that 100 yr of addition of 30 kg N ha−1 yr−1 could result in a doubling (1.3 kg C m−2) of the amount of C stored in the mor layer (Franklin et al., 2003). About 60% of this increase was estimated to be the result of decreased decomposition rate and the rest a result of increased litter production. The explanation for the decreased decomposition rate was a fertilizer-induced increase in decomposer efficiency (production-to-assimilation ratio), a more rapid rate of decrease in litter quality, and a decrease in decomposer basic growth rate (Franklin et al., 2003). Interestingly, the addition of NPK fertilizer resulted in a 200% increase (2.6 kg C m−2) of C stored in the mor layer (Franklin et al., 2003). Thus from the above studies it appears that N deposition will lead to a decrease of the mineralization rate and an accumulation of C in the mor layer.


Figure 5. Nitrogen mineralization and heterotrophic respiration in the humus layer as functions of soil C : N ratios. Swedish data (•) from Andersson (2002); European data (▵) from Persson et al. (2000).

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VI. Disturbances and forest management

  1. Top of page
  2. I.Introduction
  3. II. Net ecosystem exchange and changes in carbon stocks
  4. III. Elevated [CO2]
  5. IV. Temperature
  6. V.Fertilization and nitrogen deposition
  7. VI. Disturbances and forest management
  8. VII. Feedbacks and interactions
  9. VIII. Will we have forest carbon sinks in the future?
  10. Acknowledgements
  11. References

Disturbances such as fire, insect outbreaks, windthrow and harvesting have a very large effect on the C cycle in the short term (years to decades), through reducing leaf area and by killing or removing trees that, in combination with the increased amount of dead material undergoing decomposition, may turn the disturbed area of forest into a temporary source of CO2 (Kowalski et al., 2003; Law et al., 2003). Over the long term, the C lost in decomposition is replaced as the disturbed forest area regrows, so that net C storage over a disturbance cycle may approximate zero, as long as a forest replaces itself, or is replaced, and the disturbance frequencies do not change. Short-term increase in the frequency of fire may, however, cause progressive C losses. For example, annual C losses from fire in the Canadian boreal forest are estimated to be 10–30% of average NPP (Harden et al., 2000), and current climate models predict a 25–50% increase in the area burned in the USA over the next 100 yr (Neilson & Drapek, 1998; Dale et al., 2001). On the other hand, an increase in the interval between disturbances may allow the progressive accumulation of C to continue.

As the vegetation recovers after a disturbance and the canopy closes, a transition from C source to C sink occurs, the faster the transition, the more productive is the stand. Only 1 yr after coppicing, the GPP of the regrowing shoots of Quercus cerris counterbalances ecosystem respiration, whereas it takes 20 yr or more for a stand of slow-growing Scots pine (P. sylvestris) in a boreal environment to return to a net C sink after clear-cutting (Law et al., 2001; Rannik et al., 2002; Kowalski et al., 2004). Similarly, on nutrient-poor sandy soils in the south-eastern USA, a P. taeda stand re-established LAI slowly and remained a source of C 6 yr after clear-cutting, whereas a fertilized stand returned to being a C sink within that time as LAI rapidly doubled (Lai et al., 2002). Decomposition of organic matter resulting from harvest residues can dominate NEE during the recovery stage. Immediately after clear-cutting, when the new trees are small, RE is dominated by decomposition of the harvest residues, whereas heterotrophic respiration becomes more closely related to current production of trees as the stand ages (Janssens et al., 2001; Falge et al., 2002a, 2002b; Whitehead et al., 2004).

Management controls stand productivity by changing the competition and LAI of the canopy and thus modifying NEE. In general, stands with large LAI have higher NEE than stands with low LAI (Fig. 3b). Intensively managed forests behave as strong C sources following clear-cutting and site-preparation operations. They reach their maximal C-sink strength earlier than lightly managed or unmanaged forests. By comparison, the NEE–age curve is flattened and lengthened for lightly managed and unmanaged forests, both of which show a large scatter in annual NEE (Fig. 6). Apart from the Fyederovskoye spruce stand, situated at the northern tree line in the Russian taiga, which is a strong C source (Milyukova et al., 2002), unmanaged stands are either close to neutral or weak C sinks in the postmaturation phase. In the long term, thinning has only very small effects on sequestration of C in commercial forests, as long as the thinning operations are not severe (Freeman et al., 2005). The differences in C sequestration between managed and unmanaged forests will be most evident during the self-thinning phase in unmanaged forests. The recent history of the vegetation stand and soil appears to be of primary importance. For instance, the Swedish Norunda forest and the Belgium Brasschaat forest are thought to lose C from the soil stock and vegetation residues because of historical drainage and thinning, respectively (Lindroth et al., 1998; Carrara et al., 2003). There seems to be no consistent effect of management on mineral soil C stocks: both increases and decreases are observed, but N fertilization generally has a positive effect on soil C accumulation (Johnson & Curtis, 2001).


Figure 6. Annual net ecosystem exchange (NEE) according to the age of dominant trees for temperate and boreal forests as classified by management intensity. ▾, plantations and coppiced stands; ◊, lightly managed forest stands thinned or harvested by selection felling or clear-felling; •, unmanaged forests. Values joined by a vertical line belong to a common site; horizontal dashed line, interannual mean value of the site (data in this figure are recalculated from the tables in Black et al., 2005).

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Any measures increasing the productivity of the forest ecosystem may increase C sequestration in the forest (Johnson et al., 2002; Paul et al., 2003). Therefore higher stocking throughout the rotation is preferable if management aims at a high C-sequestration capacity in the forest ecosystem. The productivity of forest ecosystems may be increased through fertilization which, in the form of N combined with other nutrient elements, may drastically increase forest growth in the boreal and temperate regions (Tamm, 1991; Linder, 1995; Bergh et al., 1999; Jarvis & Linder, 2000). At the same time, N fertilization may also decrease the decomposition of SOM in the long run, leading to an increasing stock of C in the soil profile (Johnson, 1992; de Wit & Kvindesland 1999; Johnson & Curtis, 2001; Nohrstedt, 2001; Freeman et al., 2005).

The choice of tree species that are planted and the resulting stand composition may have a major impact on the C-sequestration capacity of the forest ecosystem. For example, mixing birch or other deciduous species with spruce and pine may enhance C sequestration ( de Wit & Kvindesland 1999). On the other hand, forest ecosystems dominated by conifers may, in many cases, sequester C even more effectively and store C longer than ecosystems dominated by deciduous trees (Table 2). This is because the growth rate of many coniferous species is higher over longer periods than that of many deciduous species (cf. Cannell, 1989). Furthermore, the decomposition rate of coniferous litter is generally lower than that of deciduous litter.

Table 2.  Qualitative effects on average carbon stocks of management operation in managed forests over a rotation period compared with the rotation period prior to management (modified from Freeman et al., 2005)
Management measureSoil C stockBiomass C stockEcosystem C stock
  • *

    Biomass and ecosystem C stocks depend on regeneration success and nutrient loss.

  • Ecosystem C stock depends on loss from soil and gain in biomass.

  • Ecosystem C stock after intensive preparation depends on loss from soil and gain in biomass.

  • §

    Soil C depends on the decomposition rate which is generally lower for conifer litter than for broadleaf litter. Biomass and ecosystem C depend on the growth rate which is higher over longer periods for many conifer species than for broadleaf species.

  • Removal of thinning residues can give large transient reductions in soil C.

  • **

    Higher production increases all C stocks. N fertilization increases litter production and may reduce decomposition in soil in the long term.

  • ††

    ††All C stocks depend on developmental stage of the forest when the rotation period is prolonged and on the thinning method.

  • ‡‡

    Soil C depends on the removal of residues. Biomass and ecosystem C for the following rotation period depend on how regeneration and growth conditions are affected by the harvesting operation.

Stand initiation phase
Prescribed burning*DecreasingDecreasing, neutral or increasingDecreasing, neutral or increasing
Drainage of peatlandsDecreasingIncreasingDecreasing, neutral or increasing
Site preparation method
 IntensiveDecreasingIncreasingDecreasing, neutral or increasing
Tree species change§
 To conifers from broadleavesIncreasingIncreasingIncreasing
 To broadleaves from conifersDecreasingDecreasingDecreasing
 To mixed conifers and broadleavesNeutral or decreasingNeutral or decreasingNeutral or decreasing
 from mono-specific coniferous
Stem exclusion phase
Thinning methodNeutral or decreasingDecreasingDecreasing
Increased rotation length††Decreasing, neutral or increasingIncreasingIncreasing
Harvesting method‡‡Decreasing, neutral or increasingDecreasing, neutral or increasingDecreasing, neutral or increasing

In certain regions, forest management induces the conversion of complex forests to more simple stands, often dominated by one or a few species with similar characteristics. For example, the warm temperate forests of the south-eastern USA, the region of highest forest production activity in the USA, are undergoing a rapid conversion to evergreen pine plantations, partly from natural pine and partly from oak–pine forest, but also from pure hardwood stands (Birdsey et al., 2006). Palmroth et al. (2005) assessed the effects on seasonal and annual forest floor CO2 efflux and total belowground C allocation, focusing on a mature oak–hickory forest and a maturing loblolly pine plantation closely located on similar soils. The estimates of total belowground C allocation were inferred from the measured CO2 efflux, litter fall, and published estimates of changes in C storage in the litter layer and mineral soil (Giardina & Ryan, 2002; Lichter et al., 2005). Excluding winter months, CO2 efflux was higher in the oak–hickory stand compared with the adjacent loblolly pine plantation. The higher CO2 efflux in oak–hickory resulted primarily from higher soil temperature, augmented by lower sensitivity to soil moisture. On an annual basis, the combined effect was a similar annual CO2 efflux at the two sites during a wet year, but higher annual CO2 efflux in the oak–hickory than in the loblolly pine stand during a severe drought year. In the wetter year, total belowground C allocation indicated that C in the litter–soil system was at steady state in the oak–hickory stand, and was accruing in the loblolly pine plantation. The oak–hickory stand was, however, probably losing C from the mineral soil during the severe drought year of 2002, while the loblolly pine was accumulating C at a lower rate, as a result of loss of C from the litter layer. Nevertheless, the results indicate that C accumulation in litter and soil of pine plantations in this region is likely to be higher than in mature hardwood forests. It is essential, however, to consider the fate of the soil C already stored in mature forests when these undergo large-scale conversion to managed plantations.

In a broader sense, when considering the effects of forest management one should also consider the life cycle of the forest products removed (Harmon et al., 1990; Ericsson et al., in press). If all the wood harvested is used for products with a long lifespan (for example, constructional timber in buildings instead of concrete), much more C will be gained. Also, when the forest products are used for short-lifespan products, such as biofuel, instead of using fossil fuels, there will be an important net gain of C (Ericsson et al., in press), although C storage in soil, biomass and forest products is lower.

VII. Feedbacks and interactions

  1. Top of page
  2. I.Introduction
  3. II. Net ecosystem exchange and changes in carbon stocks
  4. III. Elevated [CO2]
  5. IV. Temperature
  6. V.Fertilization and nitrogen deposition
  7. VI. Disturbances and forest management
  8. VII. Feedbacks and interactions
  9. VIII. Will we have forest carbon sinks in the future?
  10. Acknowledgements
  11. References

The simple responses depicted above are complicated by factors that affect several fluxes at the same time, and by changes in one part of the system that feed back to other parts of the system. For example, the direct response of photosynthesis, P, to an increase in [CO2] will eventually require additional N, and the NPP response will therefore decline as N limitation sets in (Rastetter et al., 1997). The most severe feedback effects are likely to appear at the ecosystem scale, but there are also feedback effects at the plant and soil scales. At the plant scale, the reason for the conservative NPP : GPP ratio of approx. 0.5 (Waring et al., 1998) may be a carbohydrate-availability feedback acting on respiration (Dewar et al., 1999). At the soil scale, an increase in decomposition rate is likely to increase the amount of available inorganic N, but there have been observations that an increased amount of inorganic N can slow down decomposition (Fog, 1988; Ågren et al., 2001).

The extra C acquired by northern forests as a result of the increasing length of the growing season (the main temperature response), higher LAI (the main N-deposition response), and higher photosynthetic rate (the main [CO2] response) is partitioned to respiration and production of different plant parts. This partitioning is likely to be affected by the amount of additional carbohydrates available relative to other resources. Increasing production requires the use of additional C in growth respiration, and a larger standing biomass may utilize additional C as well (but c.f. Ryan & Waring, 1992; Ryan et al., 1994).

Elevated [CO2] may result in the production of biomass with lower N concentration (Cotrufo et al., 1998b), and this may offset the increase in respiration resulting from the larger standing biomass; respiration being proportional to the amount of N (Ryan, 1991). Where nutrients limit growth, production of leaf and woody biomass may not increase in elevated [CO2] (Oren et al., 2001; Sigurdsson et al., 2001; Körner et al., 2005). Most fertilization studies on N-limited sites show that increasing nutrient availability does not increase fine-root biomass, and may decrease the number of mycorrhizal root tips (Meyer et al., 1988; Fransson et al., 2000; Parrent et al., 2006) as well as the production of mycorrhizal mycelium in the soil (Nilsson & Wallander, 2003). An N-deposition study suggested that fine-root biomass can decrease as a result of enhanced deposition, but that root turnover and thus production may increase (Gundersen et al., 1998; Nadelhoffer, 2000).

Increasing air temperatures with climate change are expected to result in higher soil temperature. A soil-warming experiment in a boreal Norway spruce forest resulted in increased N availability, leading to substantial increases in tree growth (Strömgren & Linder, 2002), and to likely increases in ecosystem C storage because the C : N of vegetation is much larger than the C : N of the SOM that has been decomposed to release N. It is not known, however, how sustainable such increases are. With an increase in N availability, an increase in leaf area, and a consequent increase in tree growth, one might justifiably expect a positive feedback resulting from enhanced future litter deposition, on a time scale of several years in the case of evergreens.

We also emphasize that all FACE studies induce a step change in atmospheric [CO2]. Step changes may induce a sudden, significant increase of labile C in the soil, stimulating rhizosphere activity with consequent priming of the decomposition of old stable organic matter (Hoosbeek et al., 2004). It is likely that, with a gradual annual increment of atmospheric [CO2], the pre-existing forest soil C will not experience a sudden increase of C input, and thus priming of old SOM may be less important than the factors promoting a progressive increase in SOC stock.

Links between litter quality and soil C decomposition under changes in soil temperature are not always straightforward. Plant metabolism (Högberg et al., 2001; Olsson et al., 2005) and the decomposition of recently produced organic material (Trumbore, 2000; Giardina & Ryan, 2002; Giardina et al., 2004) generate most of the ‘soil’ respiration, which strongly reflects plant metabolism (Ekblad & Högberg, 2001; Bowling et al., 2002; Ekblad et al., 2005; Högberg & Read, 2006), thus it is not always easy to determine if increased soil respiration originates from autotrophic or heterotrophic activity. The SOC content had increased significantly in a sweetgum (L. styraciflua) plantation after 5 yr of FACE under nonlimiting N conditions (Jastrow et al., 2005). On the other hand, Hoosbeek et al. (2004) reported a decreased C stock in soils exposed to elevated [CO2] at the end of a 3-yr rotation of a poplar plantation. This change occurred despite larger litter inputs, and was attributed to priming of decomposition of native SOC. Also, soils receiving lower-quality litter may in fact have higher specific decomposition rates (Giardina et al., 2001).

In a transient system, single-factor responses from short-term experiments can be misleading for long-term predictions, because slowly evolving feedback as well as acclimation processes do not have time to exert their full impacts (Hanson et al., 2005). This is particularly relevant when results from experimental studies, which are usually short term, are compared with results from observational studies, in which feedback processes at all temporal scales operate. Moreover, the long-term responses tend to be dominated by feedback loops. The recalcitrant soil C, the largest terrestrial C pool, contributes only a minor portion to soil CO2 efflux at any moment in time (Trumbore, 2000; Giardina et al., 2004). Thus soil respiration is a good indicator of metabolism, but a poor indicator of changes in long-term soil C storage.

VIII. Will we have forest carbon sinks in the future?

  1. Top of page
  2. I.Introduction
  3. II. Net ecosystem exchange and changes in carbon stocks
  4. III. Elevated [CO2]
  5. IV. Temperature
  6. V.Fertilization and nitrogen deposition
  7. VI. Disturbances and forest management
  8. VII. Feedbacks and interactions
  9. VIII. Will we have forest carbon sinks in the future?
  10. Acknowledgements
  11. References

It is not in doubt that newly established young forests will continue to be C sinks for the foreseeable future. The key question is whether the mature forests that are C sinks today will continue to be sinks as the climate changes. The C balance is particularly vulnerable because the balance is the small difference between a large input and a large output of C. If the input diminishes, or the output increases, as a result of global climate change, a C sink may diminish to zero and the forest may become a C source. Forest ecosystem models (e.g. Churkina et al., 2003) indicate that the additional terrestrial sink arising from global climate change is likely to be maintained in the short term (over several decades), but may gradually diminish in the medium term. One reason for this is that the capacity of some forests to sequester C may be approached; another is that photosynthesis will increase less as the [CO2] concentration continues to rise, whereas respiration is expected to continue to increase with the rise in temperature. The balance between forest photosynthesis and respiration is crucially dependent on the nutrient dynamics of the forest ecosystem, as well as on other environmental variables. Simplistic models forecasting that stand photosynthesis will be overtaken by stand respiration, purely on the basis of short-term responses of photosynthesis to [CO2] and respiration to temperature, should be treated with great caution. Because of current limitations on our understanding with respect to acclimation of the physiological processes, the climatic constraints, and feedbacks among these processes – particularly those acting at the biome scale – projections of C-sink strengths beyond a few decades are highly uncertain.


  1. Top of page
  2. I.Introduction
  3. II. Net ecosystem exchange and changes in carbon stocks
  4. III. Elevated [CO2]
  5. IV. Temperature
  6. V.Fertilization and nitrogen deposition
  7. VI. Disturbances and forest management
  8. VII. Feedbacks and interactions
  9. VIII. Will we have forest carbon sinks in the future?
  10. Acknowledgements
  11. References
  • Aber JD, Nadelhoffer KJ, Steudler P, Melillo JM. 1989. Nitrogen saturation in northern forest ecosystems – hypothesis revisited. Bioscience 39: 378386.
  • Aber J, McDowell W, Nadelhoffer K, Magill A, Berntson G, Kamakea M, McNulty S, Currie W, Rustad L, Fernandez I. 1998. Nitrogen saturation in temperate forest ecosystems. Bioscience 48: 921934.
  • Aerts R. 1997. Climate, leaf litter chemistry and leaf litter decomposition in terrestrial ecosystems: a triangular relationship. Oikos 79: 439449.
  • Ågren GI, Bosatta E. 2002. Reconciling differences in predictions of temperature response of soil organic matter. Soil Biology and Biochemistry 34: 129132.
  • Ågren GI, Bosatta E, Magill AH. 2001. Combining theory and experiment to understand effects of inorganic nitrogen on litter decomposition. Oecologia 128: 9498.
  • Ainsworth EA, Long SP. 2005. What have we learned from 15 years of free-air CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy properties and plant production to rising CO2. New Phytologist 165: 351372.
  • Andersson P. 2002. Nitrogen turnover in Swedish spruce forest ecosystems. PhD thesis. Acta Universitatis Agriculturae Sueciae, Agraria 342.
  • Atkin OK, Tjoelker MG. 2003. Thermal acclimation and the dynamic response of plant respiration to temperature. Trends in Plant Science 8: 343351.
  • Aubinet M, Grelle A, Ibrom A, Rannik Ü, Moncrieff J, Foken T, Kowalski AS, Martin PH, Berbigier P, Bernhofer C, Clement R, Elbers J, Granier A, Grünwald T, Morgenstern K, Pilegaard K, Rebmann C, Snijders W, Valentini R, Vesala T. 2000. Estimates of the annual net carbon and water exchange of forests: the EUROFLUX methodology. Advances in Ecological Research 30: 113175.
  • Baldocchi DD. 2003. Assessing the eddy covariance technique for evaluating carbon dioxide exchange rates of ecosystems: past, present and future. Global Change Biology 9: 479492.
  • Bergh J, Linder S. 1999. Effects of soil warming during spring on photosynthetic recovery in boreal Norway spruce stands. Global Change Biology 5: 245253.
  • Bergh J, Linder S, Lundmark T, Elving B. 1999. The effect of water and nutrient availability on the productivity of Norway spruce in northern and southern Sweden. Forest Ecology and Management 119: 5162.
  • Binkley D, Högberg P. 1997. Does atmospheric deposition of nitrogen threaten Swedish forests? Forest Ecology and Management 92: 119152.
  • Birdsey R, Pregitzer K, Lucier A. 2006. Forest carbon management in the United States: 1600–2100. Journal of Environmental Quality 35: 14611469.
  • Black AT, Gaumont-Guay D, Jassal RS, Amiro BD, Jarvis. G, Gower. T, Kelliher FM, Dunn A, Wofsy SC. 2005. Measurement of CO2 exchange between boreal forest and the atmosphere. In: Griffiths H, Jarvis PG, eds. The carbon balance of forest biomes, pp. 151185. Oxford, UK: Taylor & Francis.
  • Bowling DR, McDowell NG, Bond BJ, Law BE, Ehlinger JR. 2002. C-13 content of ecosystem respiration is linked to precipitation and vapor pressure deficit. Oecologia 131: 113124.
  • Butnor J, Lohnsen K, Oren R, Katul G. 2003. Reduction of forest floor respiration on both carbon dioxide-enriched and reference 17-year-old loblolly pine stands. Global Change Biology 9: 849861.
  • Cannell MGR. 1989. Physiological basis of wood production: a review. Scandinavian Journal of Forest Research 4: 459490.
  • Carrara A, Kowalski AS, Neirynck J, Janssens IA, Curiel Yuste J, Ceulemans R. 2003. Net ecosystem CO2 exchange of mixed forest in Belgium over 5 years. Agricultural and Forest Meteorology 119: 209227.
  • Carrara A, Janssens IA, Yuste JC, Ceulemans R. 2004. Seasonal changes in photosynthesis, respiration and NEE of a mixed temperate forest. Agricultural and Forest Meteorology 126: 1531.
  • Ceulemans R, Mousseau M. 1994. Effects of elevated atmospheric CO2 on woody plants. New Phytologist 127: 425446.
  • Chapin III FSG, Woodwell M, Randerson JT, Rastetter EB, Lovett GM, Baldocchi DD, Clark DA, Harmon ME, Schimel DS, Valentini R, Wirth C, Aber JD, Cole JJ, Goulden ML, Harden JW, Heimann M, Howarth RW, Matson PA, McGuire AD, Melillo JM et al. 2006. Reconciling carbon-cycle concepts, terminology, and methods. Ecosystems 9: 10411050.
  • Churkina G, Tenhunen J, Thornton P, Falge EM, Elbers JA, Erhard M, Grünwald T, Kowalski AS, Rannik Ü, Sprinz D. 2003. Analyzing the ecosystem carbon dynamics of four European coniferous forests using a biogeochemistry model. Ecosystems 6: 1681184.
  • Clements FE. 1916. Plant succession. an analysis of the development of vegetation. Carnegie Institute of Washington Publication 242: 1512.
  • Conen F, Yakutin MV, Sambuu AD. 2003. Potential for detecting changes in soil organic carbon concentrations resulting from climate change. Global Change Biology 9: 15151520.
  • Conen F, Zerva A, Arrouays D, Jolivet C, Jarvis PG, Grace J, Mencuccini M. 2005. The carbon balance of forest soils: detectability of changes in soil carbon stocks in temperate and Boreal forests. In: Griffiths H, Jarvis PG, eds. The carbon balance of forest biomes, pp. 235249. Oxford, UK: Taylor & Francis.
  • Cotrufo MF, Briones MJI, Ineson P. 1998a. Elevated CO2 affects field decomposition rate and palatability of tree leaf litter: importance of changes in substrate quality. Soil Biology and Biochemistry 30: 15651571.
  • Cotrufo MF, Ineson P, Scott A. 1998b. Elevated CO2 reduces the nitrogen concentration of plant tissues. Global Change Biology 4: 4354.
  • Cotrufo MF, Drake B, Ehlinger JR. 2005. Palatability trials on hardwood leaf litter grown under elevated CO2: a stable carbon isotope study. Soil Biology and Biochemistry 37: 11051112.
  • Curtis PS, Wang X. 1998. A meta-analysis of elevated CO2 effects on woody plant mass, form, and physiology. Oecologia 113: 299313.
  • Dale VH, Joyce LA, McNulty S, Neilson RP, Ayres MP, Flannigan MD, Hanson PJ, Irland LC, Lugo AE, Peterson CJ, Simberloff D, Swanson FJ, Stocks BJ, Wotton BM. 2001. Climate change and forest disturbances. Bioscience 51: 723734.
  • Davidson EA, Janssens IA. 2006. Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 440: 165173.
  • Dewar RC, Medlyn BE, McMurtrie RE. 1999. Acclimation of the respiration photosynthesis ratio to temperature: insights from a model. Global Change Biology 5: 615622.
  • Dixon RK, Brown S, Houghton RA, Solomon AM, Trexler MC, Wisniewski J. 1994. Carbon pools and flux of global forest ecosystems. Science 263: 185190.
  • Edwards NT, Tschaplinski TJ, Norby RJ. 2002. Stem respiration increases in CO2-enriched sweetgum trees. New Phytologist 155: 239248.
  • Ekblad A, Högberg P. 2001. Natural abundance of 13C in CO2 respired from forest soils reveals speed of link between tree photosynthesis and root respiration. Oecologia 127: 305308.
  • Ekblad A, Boström B, Holm A, Comstedt D. 2005. Forest soil respiration rate and δ13C is regulated by recent above ground weather conditions. Oecologia 143: 136142.
  • Eliasson PE, McMurtrie RE, Pepper DA, Strömgren M, Linder S, Ågren GI. 2005. The response of heterotrophic CO2 flux to soil warming. Global Change Biology 11: 167181.
  • Ellsworth DS, Reich PB, Naumburg ES, Koch GW, Kubiske ME, Smith SD. 2004. Photosynthesis, carboxylation and leaf nitrogen responses of 16 species to elevated pCO2 across four free-air CO2 enrichment experiments in forest, grassland and desert Global Change Biology 10: 21212138.
  • Ericsson E, Gillespie AR, Gustavsson L, Langvall O, Olsson M, Sathre R, Stendahl J. in press. Integrated carbon analysis of forest management practices and wood substitution. Canadian Journal of Forest Research.
  • Ewers BE, Oren R, Sperry JS. 2000. Root hydraulic conductance: a reflection of water balance and a constraint on canopy stomatal conductance. Plant, Cell & Environment 23: 10551066.
  • Ewers BE, Oren R, Phillips N, Strömgren M, Linder S. 2001. Mean canopy stomatal conductance responses to water and nutrient availabilities in Picea abies and Pinus taeda. Tree Physiology 21: 841850.
  • Falge E, Baldocchi D, Tenhunen J et al. 2002a. Seasonality of ecosystem respiration and gross primary production as derived from FLUXNET measurements. Agricultural and Forest Meteorology 113: 5374.
  • Falge E, Tenhunen J, Baldocchi D et al. 2002b. Phase and amplitude of ecosystem carbon release and uptake potentials as derived from FLUXNET measurements. Agricultural and Forest Meteorology 113: 7595.
  • Fang C, Smith P, Moncrieff JB, Smith JU. 2005. Similar response of labile and resistant organic matter pools to changes in temperature. Nature 433: 5759.
  • Fierer N, Craine JM, McLauchlan K, Schimel JP. 2005. Litter quality and the temperature sensitivity of decomposition. Ecology 86: 320326.
  • Finzi AC, Schlesinger AH. 2002. Species control variation in litter decomposition in a pine forest exposed to elevated CO2. Global Change Biology 8: 12171229.
  • Finzi AC, DeLucia EH, Hamilton JG, Richter DD, Schlesinger WH. 2002. The nitrogen budget of a pine forest under free air CO2 enrichment. Oecologia 132: 567578.
  • Fog K. 1988. The effect of added nitrogen on the rate of decomposition of organic matter. Biology Review 63: 433462.
  • Franklin O, Högberg P, Ekblad A, Ågren GI. 2003. Pine forest floor carbon accumulation in response to N and PK additions – bomb 14C modelling and respiration studies. Ecosystems 6: 644658.
  • Fransson PMA, Taylor AFS, Finlay RD. 2000. Effects of continuous optimal fertilisation upon belowground ectomycorrhizal community structure in a Norway spruce forest. Tree Physiology 20: 599606.
  • Freeman M, Morén AS, Strömgren M, Linder S. 2005. Climate change impacts on forests in Europe: biological impact mechanisms. In: Kellomäki S, Leinonen S, eds. Management of European forests under changing climatic conditions. Research Notes 163. Joensuu, Finland: Forest Faculty, University of Joensuu, 46115.
  • van de Geijn SC, van Veen JA. 1993. Implications of increased carbon dioxide levels for carbon input and turnover in soils. Vegetatio 104–105: 283292.
  • Giardina CP, Binkley D, Ryan MG, Fownes JH, Senock RS. 2004. Belowground carbon cycling in a humid tropical forest decreases with fertilisation. Oecologia 139: 545550.
  • Giardina CP, Ryan MG. 2000. Evidence that decomposition rates of organic carbon in mineral soil do not vary with temperature. Nature 404: 858861.
  • Giardina CP, Ryan MG. 2002. Total belowground carbon allocation in a fast-growing Eucalyptus plantation estimated using a carbon balance approach. Ecosystems 5: 487499.
  • Giardina CP, Ryan MG, Hubbard RM, Binkley D. 2001. Tree species and soil textural controls on carbon and nitrogen mineralization rates. Soil Science Society of America Journal 65: 12721279.
  • Gielen B, Ceulemans R. 2001. The likely impact of rising atmospheric CO2 on natural and managed Populus: a literature review. Environmental Pollution 115: 335358.
  • Gielen B, Calfapietra C, Claus A, Sabatti M, Ceulemans R. 2002. Crown architecture of Populus spp. is differentially modified by free-air CO2 enrichment (POPFACE). New Phytologist 153: 9199.
  • Goudriaan J. 1990. Atmospheric CO2, global carbon fluxes and the biosphere. In: Rabbinge R, Goudriaan J, van Keulen H, Penning de Vries FWT, van Laar HH, eds. Theoretical production ecology: reflections and prospects. Wageningen, the Netherlands: Pudoc, 1740.
  • Goulden ML, Wofsy SC, Harden JW, Trumbore SE, Crill PM, Gower ST, Fries T, Daube BC, Fan SM, Sutton DJ, Bazzaz A, Munger JW. 1998. Sensitivity of boreal forest carbon balance to soil thaw. Science 279: 214217.
  • Gower ST, Krankina O, Olson RJ, Apps M, Linder S, Wang C. 2001. Net primary production and carbon allocation patterns of boreal forest ecosystems. Ecological Applications 11: 13951411.
  • van Groenigen KJ, Six J, Hungate BA, de Graaff MA, van Breemen N, van Kessel C. 2006. Element interactions limit soil carbon storage. Proceedings of the National Academy of Sciences, USA 103: 65716574.
  • Gundersen P, Emmett BA, Kjønaas OJ, Koopmans CJ, Tietema A. 1998. Impact of nitrogen deposition on nitrogen cycling in forests: a synthesis of NITREX data. Forest Ecology and Management 101: 3755.
  • Hacke UG, Sperry JS, Pockman WT, Davis SD, McCulloh KA. 2001. Trends in wood density and structure are linked to prevention of xylem implosion by negative pressure. Oecologia 126: 457461.
  • Hamilton JG, Thomas RB, Delucia EH. 2001. Direct and indirect effects of elevated CO2 on leaf respiration in a forest ecosystem. Plant, Cell & Environment 24: 975982.
  • Hanson PJ, Wullschleger SD, Norby RJ, Tschaplinski TJ, Gunderson CA. 2005. Importance of changing CO2, temperature, precipitation, and ozone on carbon and water cycles of an upland-oak forest: incorporating experimental results into model simulations. Global Change Biology 11: 14021423.
  • Harden JW, Trumbore SE, Stocks BJ, Hirsch A, Gower ST, O’Neill KP, Kasischke ES. 2000. The role of fire in the boreal carbon budget. Global Change Biology 6: 174184.
  • Harley P, Guenther A, Zimmerman P. 1997. Environmental controls over isoprene emission in deciduous oak canopies. Tree Physiology 17: 705714.
  • Harmon ME, Ferrell WK, Franklin JF. 1990. Effects on carbon storage of conversion of old-growth forests to young forests. Science 247: 699702.
  • Harrison AF, Schulze E-D, Gebauer G, Bruckner G. 2000. Canopy uptake and utilization of atmospheric pollutant nitrogen. In: Schulze E-D, ed. Carbon and nitrogen cycling in European forest ecosystems. Ecological Studies 142. Berlin: Springer-Verlag, 171188.
  • Hobbie SE. 2000. Interactions between litter lignin and soil nitrogen availability during leaf litter decomposition in a Hawaiian montane forest. Ecosystems 3: 484494.
  • Hobbie SE. 2005. Contrasting effects of substrate and fertilizer nitrogen on the early stages of litter decomposition. Ecosystems 8: 644656.
  • Hobbie SE, Vitousek PM. 2000. Nutrient limitation of decomposition in Hawaiian forests. Ecology 81: 18671877.
  • Högberg P, Read DJ. 2006. Towardws a more plant physiological perspective on soil ecology. Trends in Ecology and Evolution 21: 549554.
  • Högberg P, Nordgren A, Buchmann N, Taylor AFS, Ekblad A, Högberg MN, Nyberg G, Ottosson-Löfvenius M, Read DJ. 2001. Large-scale forest girdling shows that current photosynthesis drives soil respiration. Nature 411: 789792.
  • Hoosbeek MR, Lukac M, van Dam D, Godbold DL, Velthorst EJ, Biondi FA, Peressotti A, Cotrufo MF, de Angelis P, Scarascia-Mugnozza G. 2004. More new carbon in the mineral soil of a poplar plantation under free air carbon enrichment (POPFACE): cause of increased priming effect? Global Biogeochemical Cycles 18. doi: 10.1029/2003GB002127
  • Hoosbeek MR, Li Y, Scarascia-Mugnozza GE. 2006. Free atmospheric CO2 enrichment (FACE) increased labile and total carbon in the mineral soil of a short rotation poplar plantation. Plant and Soil 281: 247254.
  • Iivonen S, Kaakinen S, Jolkkonen A, Vapaavuori E, Linder S. 2006. Influence of long-term nutrient optimisation on biomass, carbon and nitrogen acquisition and allocation in Norway spruce. Canadian Journal of Forest Research 36: 15631571.
  • IPCC. 2001. Climate Change 2001. The Scientific Basis. Cambridge, UK: Cambridge University Press.
  • Janssens IA, Lankreijer H, Matteucci G et al. 2001. Productivity overshadows temperature in determining soil and ecosystem respiration across European forests. Global Change Biology 7: 269278.
  • Janssens IA, Medlyn B, Gielen B, Laureysens I, Jach ME, Van Hove D, Ceulemans R. 2005. Carbon budget of Pinus sylvestris saplings after four years of exposure to elevated atmospheric carbon dioxide concentration. Tree Physiology 25: 325337.
  • Jarvis PG, Fowler DG. 2001. Forests and the atmosphere. In: Evans J, ed. The forests handbook, Vol. 1. Oxford, UK: Blackwell Science, 229281.
  • Jarvis PG, Linder S. 2000. Constraints to growth of boreal forests. Nature 405: 904905.
  • Jastrow JD, Miller RM, Matamala R, Norby RJ, Boutton TW, Rice CW, Owensby CE. 2005. Elevated atmospheric carbon dioxide increases soil carbon. Global Change Biology 11: 20572064.
  • Johnson DW. 1992. Nitrogen-retention in forest soils. Journal of Environmental Quality 21: 112.
  • Johnson DW, Curtis PS. 2001. Effects of forest management on soil C and N storage: meta analysis. Forest Ecology and Management 140: 227238.
  • Johnson DW, Knoepp JD, Swank WT, Shan J, Morris LA, Van Lear DH, Kapeluck PR. 2002. Effects of forest management on soil carbon: results of some long-term resampling studies. Environmental Pollution S1: 201208.
  • Johnson MG, Rygiewicz PT, Tingey DT, Phillips DL.. 2006. Elevated CO2 and elevated temperature have no effect on Douglas-fir fine-root dynamics in nitrogen-poor soil. New Phytologist 170: 345356.
  • Kainulainen P, Holopainen JK, Holopainen T. 1998. The influence of elevated CO2 and O3 concentrations on Scots pine needles: changes in starch and secondary metabolites over three exposure years. Oecologia 114: 455460.
  • Karjalainen T, Schuck A, Prietzel J, Mellert K-H, Kahle H-P, Spiecker H, Ågren GI, van Oijen M, Kellomäki S, eds. in press. Causes and consequences of forest growth trends in Europe – results of the RECOGNITION project.
  • Kasurinen A, Helmisaari HS, Holopainen T. 1999. The influence of elevated CO2 and O3 on fine roots and mycorrhizas of naturally growing young Scots pine trees during three exposure years. Global Change Biology 5: 771780.
  • Kellomäki S, Wang KY. 1996. Photosynthetic responses to needle water potentials in Scots pine after a four-year exposure to elevated CO2 and temperature. Tree Physiology 16: 765772.
  • Kellomäki S, Wang KY. 1997. Effects of long-term CO2 and temperature elevation on crown nitrogen distribution and daily photosynthetic performance of Scots pine. Forest Ecology and Management 99: 309326.
  • King JS, Pregitzer KS, Zak DR, Sober J, Isebrands JG, Dickson RE, Hendrey GR, Karnosky DF. 2001. Fine-root biomass and fluxes of soil carbon in young stands of paper birch and trembling aspen as affected by elevated atmospheric CO2 and tropospheric O3. Oecologia 128: 237250.
  • Kirschbaum MUF. 2004. Soil respiration under prolonged soil warming: are rate reductions caused by acclimation or substrate loss? Global Change Biology 10: 18701877.
  • Knorr M, Frey SD, Curtis PS. 2005b. Nitrogen additions and litter decomposition: a meta-analysis. Ecology 86: 32523257.
  • Knorr W, Prentice IC, House JI, Holland EA. 2005a. Long-term sensitivity of soil carbon turnover to warming. Nature 433: 298301.
  • Kolari P, Pumpanen J, Rannik Ü, Ilvesniemi H, Hari P, Berninger F. 2004. Carbon balance of different aged Scots pine forests in Southern Finland. Global Change Biology 10: 11061119.
  • Körner C. 2003. Carbon limitation in trees. Journal of Ecology 91: 417.
  • Körner C. 2006. Plant CO2 responses: an issue of definition, time and resource supply. New Phytologist 172: 393411.
  • Körner C, Asshoff R, Bignucolo O, Hättenschwiler S, Keel SG, Peláez-Riedl S, Pepin S, Siegwolf RTW, Zotz G. 2005. Exposing a mature Swiss forest to elevated atmospheric CO2 increased the flux of carbon through the trees and soils but did not increase net forest growth or carbon storage. Science 309: 13601362.
  • Kowalski S, Sartore M, Burlett R, Berbigier P, Loustau D. 2003. The annual carbon budget of a French pine forest (Pinus pinaster) following harvest. Global Change Biology 9: 10511065.
  • Kowalski AS, Loustau D, Berbigier P, Manca G, Tedeschi V, Borghetti M, Valentini R, Kolari P, Berninger F, Rannik Ü, Hari P, Rayment M, Mencuccini M, Moncrieff J, Grace J. 2004. Paired comparisons of carbon exchange between undisturbed and regenerating stands in four managed forests in Europe. Global Change Biology 10: 17071723.
  • Kull O. 2002. Acclimation of photosynthesis in canopies: models and limitations. Oecologia 133: 267279.
  • Lai C-T, Katul GG, Butnor J, Siqueira M, Ellsworth D, Maier C, Johnsen K, McKeand S, Oren R. 2002. Modeling the limits on the response of net carbon exchange to fertilization in a southeastern pine forest. Plant, Cell & Environment 25: 10951119.
  • Law BE, Thornton PE, Irvine J, Anthoni PM, Van Tuyl S. 2001. Carbon storage and fluxes in ponderosa pine forests at different developmental stages. Global Change Biology 7: 755777.
  • Law BE, Sun OJ, Cambell J, Van Tuyl S, Thorton PE. 2003. Changes in carbon storage and fluxes in a chronosequence of ponderosa pine. Global Change Biology 9: 510524.
  • Lichter J, Barron SH, Bevacqua CE, Finzi AC, Irving KF, Stemmler EA, Schlesinger WH. 2005. Soil carbon sequestration and turnover in a pine forest after six years of atmospheric CO2 enrichment. Ecology 86: 18351847.
  • Lin GH, Rygiewicz PT, Ehleringer JR, Johnson MG, Tingey DT. 2001. Time-dependent responses of soil CO2 efflux components to elevated atmospheric [CO2] and temperature in experimental forest mesocosms. Plant and Soil 229: 259270.
  • Linder S. 1995. Foliar analysis for detecting and correcting nutrient imbalances in Norway spruce. Ecological Bulletins (Copenhagen) 44: 178190.
  • Linder S, Murray M. 1998. Do elevated CO2 concentrations and nutrients interact? In: Jarvis PG, ed. European forests and global change. Cambridge, UK: Cambridge University Press, 215235.
  • Lindroth A, Grelle A, Morén AS. 1998. Long-term measurements of boreal forest carbon balance reveal large temperature sensitivity. Global Change Biology 4: 443450.
  • Lloyd J, Shibistova O, Zolotoukhine D, Kolle O, Arneth A, Wirth C, Styles JM, Tchebakova NM, Schulze ED. 2002. Seasonal and annual variations in the photosynthetic productivity and carbon balance of a central Siberian pine forest. Tellus Series B – Chemical and Physical Meteorology 54: 590610.
  • Luo Y, Wan S, Hui D, Wallace LL. 2001. Acclimatization of soil respiration to warming in a tall grass prairie. Nature 413: 622625.
  • Luo Y, Su B, Currie WS, Dukes JS, Finzi A, Hartwig A, Hungate B, McMurtrie RE, Oren R, Parton WJ, Pataki DE, Shaw MR, Zak DR, Field CB. 2004. Progressive nitrogen limitation of ecosystem responses to rising atmospheric carbon dioxide. Bioscience 54: 731739.
  • Magill AH, Aber JD. 1998. Long-term effects of experimental nitrogen additions on foliar litter decay and humus formation in forest ecosystems. Plant and Soil 203: 301311.
  • Magill AH, Aber JD, Currie WS, Nadelhoffer KJ, Martin ME, McDowell WH, Melillo JM, Steudler P. 2004. Ecosystem response to 15 years of chronic nitrogen additions at the Harvard Forest LTER, Massachusetts, USA. Forest Ecology and Management 196: 728.
  • Majdi H, Öhrvik J. 2004. Interactive effects of soil warming and fertilization on root production, mortality, and longevity in a Norway spruce stand in Northern Sweden. Global Change Biology 10: 182188.
  • Malhi Y, Baldocchi D, Jarvis PG. 1999. The carbon balance of tropical, temperate and boreal forests. Plant, Cell & Environment 22: 715740.
  • Malhi Y, Baker TR, Phillips OL et al. 2004. The above-ground coarse wood productivity of 104 Neotropical forest plots. Global Change Biology 10: 563591.
  • McCarthy HR, Oren R, Finzi AC, Johnsen KH. 2006. Canopy leaf area constrains [CO2]-induced enhancement of productivity partitioning among aboveground carbon pools. Proceedings of the National Academy of Sciences, USA 103: 1935619361.
  • Medlyn BE, Badeck FW, de Pury DGG et al. 1999. Effects of elevated [CO2] on photosynthesis in European forest species: a meta-analysis of model parameters. Plant, Cell & Environment 22: 1999.
  • Medlyn BE, Barton CVM, Broadmeadow MSJ, Ceulemans R, de Angelis P, Forstreuter M, Freeman M, Jackson SB, Kellomäki S, Laitat E, Rey A, Roberntz P, Sigurdsson BD, Strassemeyer J, Wang K, Curtis PS, Jarvis PG. 2001. Stomatal conductance of European forest species after long-term exposure to elevated [CO2]: a synthesis of experimental data. New Phytologist 149: 247264.
  • Medlyn BE, Berbigier P, Clement R, Grelle A, Loustau D, Linder S, Wingate L, Jarvis PG, Sigurdsson BD, McMurtrie RE. 2005. The carbon balance of coniferous forests growing in contrasting climatic conditions: a model-based analysis. Agricultural and Forest Meteorology 131: 97124.
  • Melillo JM, Steudler PA, Aber JD, Newkirk K, Lux H, Bowles FP, Catricala C, Magill A, Ahrens T, Morisseau S. 2002. Soil warming and carbon-cycle feedbacks to the climate system. Science 298: 21732176.
  • Meyer J, Schneider BU, Werk K, Oren R, Schulze ED. 1988. Performance of two Picea-abies (L) Karst stands at different stages of decline. 5. Root-tip and ectomycorrhiza development and their relations to above ground and soil nutrients. Oecologia 77: 713.
  • Milyukova IM, Kolle O, Varlagin AV, Vygodskaya NN, Schulze ED, Lloyd J. 2002. Carbon balance of a southern taiga spruce stand in European Russia. Tellus Series B – Chemical and Physical Meteorology 54: 429442.
  • Moore TR, Trofymov JA, Taylor B, Prescott C, Camire C, Duschene L, Fyles J, Kozak L, Kranabetter M, Morrison I, Siltanen M, Smith S, Titus B, Visser S, Wein R, Zoltai S. 1999. Litter decomposition rates in Canadian forests. Global Change Biology 5: 7582.
  • Myneni RB, Keeling CD, Tucker CJ, Asrar G, Nemani RR. 1997. Increased plant growth in the northern high latitudes from 1981 to 1991. Nature 386: 698702.
  • Nadelhoffer KJ. 2000. The potential effects of nitrogen deposition on fine-root production in forest ecosystems. New Phytologist 147: 131139.
  • Neilson RP, Drapek RJ. 1998. Potentially complex biosphere responses to transient global warming. Global Change Biology 4: 505521.
  • Nilsson LO, Wallander H. 2003. Production of external mycelium by ectomycorrhizal fungi in a Norway spruce forest was reduced in response to nitrogen fertilization. New Phytologist 158: 409416.
  • Nilsson LO, Wiklund K. 1995. Indirect effects of N and S deposition on a Norway spruce ecosystem. An update of findings within the Skogaby project. Water, Air, & Soil Pollution 85: 16131622.
  • Nohrstedt H-Ö. 2001. Response of coniferous forest ecosystems on mineral soils to nutrient additions: a review of Swedish experiences. Scandinavian Journal of Forest Research 16: 555573.
  • Norby RJ, Wullschleger SD, Gunderson CA, Johnson DW, Ceulemans R. 1999. Tree responses to rising CO2: implications for the future forest. Plant, Cell & Environment 22: 683714.
  • Norby RJ, Cotrufo MF, Ineson P, O’Neill EG, Canadell JG. 2001. Elevated CO2, litter chemistry, and decomposition: a synthesis. Oecologia 127: 153165.
  • Norby RJ, Sholtis JD, Gunderson CA, Jawdy SS. 2003. Leaf dynamics of a deciduous forest canopy: no response to elevated CO2. Oecologia 136: 574584.
  • Norby RJ, Ledford J, Reilly CD, Miller NE, O’Neill EG. 2004. Fine-root production dominates response of a deciduous forest to atmospheric CO2 enrichment. Proceedings of the National Academy of Sciences, USA 101: 96899693.
  • Norby RJ, DeLucia EH, Gielen B, Calfapietra C, Giardina CP, King JS, Ledford J, McCarthy HR, Moore DJP, Ceulemans R, De Angelis P, Finzi AC, Karnosky DF, Kubiske ME, Lukac M, Pregitzer KS, Scarascia-Mugnozza GE, Schlesinger WH, Oren R. 2005. Forest response to elevated CO2 is conserved across a broad range of productivity. Proceedings of the National Academy of Sciences, USA 102: 1805218056.
  • Nowak RS, Ellsworth DS, Smith SD. 2004. Functional responses of plants to elevated atmospheric CO2– do photosynthetic and productivity data from FACE experiments support early predictions? New Phytologist 162: 253280.
  • Olsson P, Linder S, Giesler R, Högberg P. 2005. Fertilization of boreal forest reduces both autotrophic and heterotrophic soil respiration. Global Change Biology 11: 17451753.
  • Oren R, Schulze ED, Matyssek R, Zimmermann R. 1986. Estimating photosynthetic rate and annual carbon gain in conifers from specific leaf weight and leaf biomass. Oecologia 70: 187193.
  • Oren R, Ellsworth DS, Johnsen KH, Phillips N, Ewers BE, Maier C, Schäfer KVR, McCarthy H, Hendrey G, McNulty SG, Katul GG. 2001. Soil fertility limits carbon sequestration by forest ecosystems in a CO2-enriched atmosphere. Nature 411: 469472.
  • Oren R, Hsieh C-I, Stoy P, Albertson J, McCarthy HR, Harrell P, Katul GG. 2006. Estimating the uncertainty in annual net ecosystem carbon exchange: spatial variation in turbulent fluxes and sampling errors in eddy-covariance measurements. Global Change Biology 12: 883896.
  • Palmroth S, Stenberg P, Smolander S, Voipio P, Smolander H. 2002. Fertilization has little effect on light-interception efficiency of Picea abies shoots. Tree Physiology 22: 11851192.
  • Palmroth S, Maier CA, McCarthy HR, Oishi AC, Kim H-S, Johnsen K, Katul GG, Oren R. 2005. Contrasting responses to drought of forest floor CO2 efflux in a loblolly pine plantation and a nearby oak–hickory forest. Global Change Biology 11: 114.
  • Palmroth S, Oren R, McCarthy HR, Johnsen KH, Finzi AC, Butnor JR, Ryan MG, Schlesinger WH. 2006. Aboveground sink strength in forests controls the allocation of carbon belowground and its CO2-induced enhancement. Proceedings of the National Academy of Sciences, USA 103: 1936219367.
  • Parrent JL, Morris WF, Vilgalys R. 2006. CO2-enrichment and nutrient availability alter ectomycorrhizal fungal communities. Ecology 87: 22782287.
  • Paul EA, Morris SJ, Six J, Paustian K, Gregorich EG. 2003. Interpretation of soil carbon and nitrogen dynamics in agricultural and afforested soils. Soil Science Society of America Journal 67: 16201628.
  • Persson T, Karlsson PS, Seyferth U, Sjöberg RM, Rudebeck A. 2000. Carbon mineralisation in European forest soils. In: Schulze ED, ed. Carbon and nitrogen cycling in European forest ecosystems. Ecological Studies 142. Berlin: Springer-Verlag, 257275.
  • Phillips DL, Johnson MG, Tingey DT, Storm MJ, Ball JT, Johnson DW. 2006. CO2 and N-fertilization effects on fine-root length, production, and mortality: a 4-year ponderosa pine study. Oecologia 148: 6475.
  • Poorter H, Navas ML. 2003. Plant growth and competition at elevated CO2: on winners, losers and functional groups. New Phytologist 157: 175198.
  • Pregitzer KS, Euskirchen ES. 2004. Carbon cycling and storage in world forests: biome patterns related to forest age. Global Change Biology 10: 20522077.
  • Pregitzer KS, Zak DZ, Maziasz J, DeForest J, Curtis PS, Lussenhop J. 2000. Interactive effects of atmospheric CO2 and soil-N availability on fine roots of Populus tremuloides. Ecological Applications 10: 1833.
  • Prescott CE. 1995. Does nitrogen availability control rates of litter decomposition in forests? Plant and Soil 168–169: 8388.
  • Prior SA, Runion GB, Mitchell RJ, Rogers HH, Amthor JS. 1997. Effects of atmospheric CO2 on longleaf pine: productivity and allocation as influenced by nitrogen and water. Tree Physiology 17: 397405.
  • Radoglou KM, Jarvis PG. 1990a. Effects of CO2 enrichment on four poplar clones. 1. Growth and leaf anatomy. Annals of Botany 65: 617626.
  • Radoglou KM, Jarvis PG. 1990b. Effects of CO2 enrichment on four poplar clones. 2. Leaf surface-properties. Annals of Botany 65: 627632.
  • Rannik Ü, Altimir N, Raittila J, Suni T, Gaman A, Hussein T, Holtta T, Lassila H, Latokartano M, Lauri A, Natsheh A, Petäjä T, Sorjamaa R, Ylä-Mella H, Keronen P, Berninger F, Vesala T, Hari P, Kulmala M. 2002. Fluxes of carbon dioxide and water vapour over Scots pine forest and clearing. Agricultural and Forest Meteorology 111: 187202.
  • Rastetter EB, Ågren GI, Shaver GR. 1997. Responses of N-limited ecosystems to increased CO2: a balanced-nutrition, coupled- element-cycles model. Ecological Applications 7: 444460.
  • Read D, Beerling D, Cannell M, Cox P, Curran P, Grace J, Ineson P, Jarvis P, Malhi Y, Powlson D, Shepherd D, Woodward I. 2001. Annex 2. Examples of management activities to maximise carbon sequestration. 2.2 ‘Carbon Forestry’– the direct role of forest management. In: The role of land carbon sinks in mitigating global climate change. Policy Document 10/01. London: Royal Society.
  • Ryan MG. 1991. Effects of climate change on plant respiration. Ecological Applications 1: 157167.
  • Ryan MG, Waring RH. 1992. Maintenance respiration and stand development in a subalpine lodgepole pine forest. Ecology 73: 21002108.
  • Ryan MG, Linder S, Vose JM, Hubbard RM. 1994. Dark respiration in pines. Ecological Bulletins (Copenhagen) 43: 5063.
  • Saxe H, Ellsworth DS, Heath J. 1998. Tree and forest functioning in an enriched CO2 atmosphere. New Phytologist 139: 395436.
  • Saxe H, Cannell MGR, Johnsen Ø, Ryan MG, Vourlitis G. 2001. Tree and forest functioning in response to global warming. New Phytologist 149: 369399.
  • Schäfer KVR, Oren R, Ellsworth DS, Lai CT, Herrick JD, Finzi AC, Richter DD, Katul GG. 2003. Exposure to an enriched CO2 atmosphere alters carbon assimilation and allocation in a pine forest ecosystem. Global Change Biology 9: 13781400.
  • Schlesinger WH. 1997. Biogeochemistry, an Analysis of Global Climate Change. San Diego, CA, USA/London, UK: Academic Press.
  • Schlesinger WH, Lichter J. 2001. Limited carbon storage in soil and litter of experimental forest plots under increased atmospheric CO2. Nature 411: 466469.
  • Schulze ED. 1989. Air pollution and forest decline in a spruce (Picea abies) forest. Science 244: 776783.
  • Schulze ED, Lloyd J, Kelliher FM, Wirth C, Rebmann C, Lühker B, Mund M, Knohl A, Milyukova IM, Schulze W, Ziegler W, Varlagin AB, Sogachev AF, Valentini R, Dore S, Grigoriev S, Kolle O, Panfyorov MI, Tchebakova N, Vygodskaya NN. 1999. Productivity of forests in the Eurosiberian boreal region and their potential to act as a carbon sink – a synthesis. Global Change Biology 5: 703722.
  • Sigurdsson BD. 2001. Elevated [CO2] and nutrient status modified leaf phenology and growth rhythm of young Populus trichocarpa trees in a three-year field study. Trees 15: 403413.
  • Sigurdsson BD, Thorgeirsson H, Linder S. 2001. Growth and dry-matter partitioning of young Populus trichocarpa trees during three years of elevated CO2 and fertilisation. Tree Physiology 21: 941950.
  • Sigurdsson BD, Roberntz P, Freeman M, Naess M, Saxe H, Thorgeirsson H, Linder S. 2002. Impact studies on Nordic forests: effects of elevated CO2 and fertilization on gas exchange. Canadian Journal of Forest Research 32: 779788.
  • Six J, Elliott ET, Paustian K, Doran JW. 1998. Aggregation and soil organic matter accumulation in cultivated and native grassland soils. Soil Science Society of America Journal 62: 13671377.
  • Smith P. 2004. How long before a change in soil organic carbon can be detected? Global Change Biology 10: 18781883.
  • Spiecker H, Mielikainen K, Kohl M, Skovsgaard J, eds. 1996. Growth Trends in European Forests. European Forest Institute Report No. 5. Berlin/Heidelberg/New York: Springer-Verlag.
  • Stoy PC, Katul GG, Siqueira MBS, Juang J-Y, Novick KA, Uebelherr JM, Oren R. 2006. An evaluation of models for partitioning eddy covariance-measured net ecosystem exchange into photosynthesis and respiration. Agricultural and Forest Meteorology 141: 218.
  • Strain BR, Bazzaz FA. 1983. CO2 and plants: the response of plants to rising levels of atmospheric carbon dioxide. In: Lemon ER, ed. AAAS Selected Symposium 84 . Boulder, CO, USA: Westview Press, pp. 177282.
  • Strömgren M. 2001. Soil-surface CO2 flux and growth in a boreal Norway spruce stand. Effects of soil warming and nutrition. PhD thesis. Acta Universitatis Agriculturae Sueciae, Silvestria 220.
  • Strömgren M, Linder S. 2002. Effects of nutrition and soil warming on stemwood production in a boreal Norway spruce stand. Global Change Biology 8: 11941204.
  • Tamm CO. 1991. Nitrogen in terrestrial ecosystems, questions of productivity, vegetational changes, and ecosystem stability. Ecological Studies 81. Berlin: Springer-Verlag.
  • Taylor AR, Schröter D, Pflug A, Wolters V. 2004. Response of different decomposer communities to the manipulation of moisture availability: potential effects of changing precipitation patterns. Global Change Biology 10: 13131324.
  • Tingey DT, Phillips DL, Johnson MG. 2000. Elevated CO2 and conifer roots: effects on growth, life span and turnover. New Phytologist 147: 87103.
  • Tissue DT, Lewis JD, Wullschleger SD, Amthor JS, Griffin KL, Anderson R. 2002. Leaf respiration at different canopy positions of sweetgum (Liquidambar styraciflua) grown in ambient and elevated concentrations of carbon dioxide in the field. Tree Physiology 22: 11571166.
  • Trumbore S. 2000. Age of soil organic matter and soil respiration: radiocarbon constraints on belowground C dynamics. Ecological Applications 10: 399411.
  • Valentini R, Matteucci G, Dolman AJ et al. 2000. Respiration as the main determinant of carbon balance in European forests. Nature 404: 861865.
  • Vestgarden LS. 2001. Carbon and nitrogen turnover in the early stage of Scots pine (Pinus sylvestris L.) needle litter decomposition: effects of internal and external nitrogen. Soil Biology and Biochemistry 33: 465474.
  • Vitousek PM, Howarth RW. 1991. Nitrogen limitation on land and in the sea – how can it occur? Biogeochemistry 13: 87115.
  • Wang YP, Jarvis PG. 1991. PAR absorption and its relation to above-ground dry matter production of Sitka spruce. Journal of Applied Ecology 28: 547560.
  • Waring RH, Landsberg JJ, Wiliams M. 1998. Net primary production of forests: a constant fraction of gross primary production? Tree Physiology 18: 129134.
  • Whitehead D, Griffin KL, Turnbull MH, Tissue DT, Engel VC, Brown KJ, Schuster WSF, Walcroft AS. 2004. Response of total night-time respiration to differences in total daily photosynthesis for leaves in a Quercus rubra L. canopy: implications for modelling canopy CO2 exchange. Global Change Biology 10: 925938.
  • de Wit HA, Kvindesland S. 1999. Carbon stocks in Norwegian forest soils and effects of forest management on carbon storage. Rapport Fra Skogforskningen S14: 52.
  • WMO. 2006. WMO Greenhouse Gas Bulletin 1. Geneva: World Meteorological Organization/Global Atmosphere Watch.
  • Zak DR, Pregitzer KS, Curtis PS, Vogel CS, Holmes WE, Lussenhop J. 2000. Atmospheric CO2, soil-N availability, and allocation of biomass and nitrogen by Populus tremuloides. Ecological Applications 10: 3446.
  • Zak DR, Holmes WE, Finzi AC, Norby RJ, Schlesinger WH. 2003. Soil nitrogen cycling under elevated CO2: a synthesis of forest FACE experiments. Ecological Applications 13: 15081514.