Coupling of nutrient cycling and carbon dynamics in the Arctic, integration of soil microbial and plant processes

Applied Soil Ecology 11 (1999) 135±146

Coupling of nutrient cycling and carbon dynamics in the Arctic, integration of soil microbial and plant processes Sven Jonasson*, Anders Michelsen, Inger K. Schmidt Department of Plant Ecology, Botanical Institute, Copenhagen University, é. Farimagsgade 2D, DK 1353 Copenhagen K, Denmark Received 20 May 1997; received in revised form 14 December 1997; accepted 21 May 1998

Abstract Most studies of nutrient cycling in arctic ecosystems have either addressed questions of plant nutrient acquisition or of decomposition and mineralization processes, while few studies have integrated processes in both the soil and plant compartments. Here, we synthesize information on nutrient cycling within, and between, the soil/microbial and the plant compartments of the ecosystems and integrate the cycling of nutrients with the turnover of organic matter and the carbon balance in tundra ecosystems. Based on this compilation and integration, we discuss implications for ecosystem function in response to predicted climatic changes. Many arctic ecosystems have high amounts of nutrients in the microbial biomass compared to the pools in the plant biomass both due to large nutrient-containing organic deposits in the soil and low plant biomass. The microbial pools of N and P, which are the most commonly limiting nutrients for plant production, may approach (N) or even exceed (P) the plant pools. Net nutrient mineralization is low, the residence time of nutrients in the soil is long and the nutrients are strongly immobilized in the soil microorganisms. This contributes to pronounced nutrient limitation for plant productivity, implies that the microbial sink strength for nutrients is strong and that the microbes may compete with plants for nutrients, but also that they are a potential source of plant nutrients during periods of declining microbial populations. The extent of this competition is poorly explored and it is uncertain whether plants mainly take up nutrients continuously during the summer when the microbial activity and, presumably, also the microbial sink strength is high, or whether the main nutrient uptake occurs during pulses of nutrient release when the microbial sink strength declines. Improved knowledge of mechanisms for plant-microbial interactions in these nutrient-limited systems is important, because it will form a basis also for our understanding of the C exchange between the ecosystems and the atmosphere under the predicted, future climatic change. High microbial nutrient immobilization, i.e. low release of plant-available nutrients, paired with high microbial decomposition of soil organic matter will lead to a loss of C from the soil to the atmosphere, which may not be compensated fully by increased plant C ®xation. Hence, the system will be a net source of atmospheric C. Conversely, if plants are able to sequester extra nutrients ef®ciently, their productivity will increase and the systems may accumulate more C and turn into a C sink, particularly if nutrients are allocated to woody tissues of low nutrient concentrations. # 1999 Elsevier Science B.V. Keywords: Arctic; Carbon balance; Microbial nutrient immobilization; Nutrient cycling; Nutrient mineralization; Plant-microbial interactions

*Corresponding author. Tel.: +45-353-22268; fax: +45-353-22321; e-mail [email protected] 0929-1393/99/$ ± see front matter # 1999 Elsevier Science B.V. All rights reserved. PII: S0929-1393(98)00145-0

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1. Introduction In the arctic and subarctic ecosystems, most organically bound nutrients are ®xed in the soil and litter and a low proportion is in the plant biomass. For instance, across various ecosystem types with relatively low accumulation of soil organic matter (SOM), such as dry heaths and fell®elds in the Swedish Subarctic, the vegetation contained <35% of the ecosystem N pool, while the remaining 65% was ®xed in the recalcitrant soil organic matter and in the litter. Furthermore, most plant nitrogen (N) was tied into perennial, woody stems or coarse roots and contributed little to the annual cycling of nutrients between plants and soil. In fact, none of these ecosystems contained more than 14% of the nutrient pool in leaves and ®ne roots with rapid turnover (Jonasson and Michelsen, 1996). In ecosystem types with higher accumulation of soil organic matter, as in mesic dwarf shrub tundra and in Betula and Salix dominated shrub tundra, the percentage N in the soil plus litter increased to between 90 and 95% and, hence, only 5±10% of the ecosystem pool was incorporated in the plant biomass (Jonasson, 1982; Jonasson, 1983; Jonasson and Michelsen, 1996). Consequently, although these ecosystems often contain large pools of nutrients (Jonasson, 1983; Shaver et al., 1996), these are tied into recalcitrant soil organic matter or, when absorbed by plants, a high proportion is locked into tissue with a slow turnover. It is not surprising, therefore, that ecosystem productivity generally is nutrient limited (Haag, 1974; Ulrich and Gersper, 1978; Chapin, 1987) and that the dominant plants are mostly species or functional groups of low nutrient requirement (Chapin et al., 1995a), or species with a conservative use of nutrients (Jonasson and Chapin, 1985; Berendse and Jonasson, 1992; Chapin et al., 1995a). The adaptations of the dominant plants to low nutrient availability make the systems vulnerable to changes. Across the Arctic, numerous studies of plant community responses to experimental addition of nutrients, or changes in nutrient availability associated with human activity, have shown that both community productivity and plant species composition are sensitive to changes in the soil pools of plant available nutrients, mostly N and phosphorus (P). For instance, the productivity of vascular plants, particularly gra-

minoids, generally increases strongly after addition of N and P even in relatively small amounts (e.g. Shaver and Chapin, 1980; Shaver and Chapin, 1986; Jonasson, 1992; Parsons et al., 1994) and also after human disturbance of tundras (Forbes, 1995). This suggests that any changes in the input or cycling of these nutrients, for instance from air-borne pollutants or increased rate of nutrient mineralization (Rastetter et al., 1997) caused by a predicted future warming of the Arctic (Cattle and Crossley, 1995), will change the species composition and, most likely, increase plant productivity. Most studies of nutrient cycling in arctic ecosystems have either addressed questions of plant nutrient acquisition or of decomposition and mineralization processes while few studies have attempted to integrate processes in both the soil and plant compartments (but see Rastetter et al., 1997). The aim of this paper is to synthesize information on nutrient cycling within, and between, the soil/microbial and the plant compartments of the ecosystems and integrate the cycling of nutrients with the turnover of organic matter and the carbon balance of selected tundra ecosystems. We use data mostly from North Scandinavian, subarctic montane ecosystems. Based on this compilation and integration, we discuss possible scenarios for biological responses to predicted, future changes in the tundra environment (Cattle and Crossley, 1995; Callaghan et al., 1997). 2. Sources of nutrients to plants Inferred from several studies across the Arctic, slow net mineralization rate is a main reason for the limitation of community nutrient uptake. For instance, Rosswall and Granhall (1980); Chapin et al. (1988); Giblin et al. (1991); Nadelhoffer et al. (1991); Jonasson et al. (1993) and Schmidt et al. (1998) have shown very low rates of net nutrient mineralization of various tundra soils and in some cases even lack of, or negative, net mineralization during entire growing seasons. However, low net mineralization during the summer, apparently, is compensated for by higher net mineralization during the non-growing season. Giblin et al. (1991) reported negative net summer mineralization of SOM across ®ve of six examined Alaskan

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tundra types. In all cases, however, the annual net mineralization reached values far above zero as the mineralization during late autumn, winter and spring was high and the annual N mineralization reached between 0.1 and 0.5 gmÿ2. Similar ¯uctuation between negative net summer mineralization and positive annual mineralization has also been shown recently for litter in Alaskan tundra (Hobbie and Chapin, 1996). Presumably, this occurs because nutrients, including part of the early season's inorganic nutrient pool, are being locked into the microbial biomass during summer, followed by a release of nutrients from dying microorganisms during the non-growing season. However, in a North Scandinavian, subarctic heath both the summer and winter net N and P mineralizations were low and the annual mineralization did not even reach 0.1 g mÿ2 for any of the elements (Schmidt et al., 1998). The mineralization studies referred to above have been performed with the buried-bag technique (Eno, 1960) by which net nutrient mineralization is measured as the difference in inorganic nutrient content of the soil before, and after, incubation of soil in polyethylene bags with no plant roots included. Hence, these experiments show the capacity of soil microorganisms to re-assimilate nutrients released from decomposed organic matter. However, low net mineralization does not necessarily indicate that plants could not have absorbed part of the nutrient if they had been given that possibility. The plant nutrient uptake rate depends on how ef®cient the plants are in sequestering the nutrients in the presence of soil microorganisms (Harte and Kinzig, 1993). In addition to nutrients released to the inorganic, plant-available form through mineralization of organic matter, there are also other sources of nutrients for the plants. For instance, bryophyte- and lichen-rich communities probably receive a substantial part of their nutrients from atmospheric deposition. Rosswall and Granhall (1980) estimated that 40% of the annual amount of N incorporated in the biomass of a subarctic mire came from absorption of nutrients deposited on the leaves of bryophytes. Also, mosses in drier ecosystems take up considerable amounts of nutrients. In a North Scandinavian Cassiope heath, mosses took up 20±25% of the total N and P incorporated annually into the vegetation (Jonasson et al., in press). Presumably, a large part of these nutrients came from

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atmospheric deposition and from leachates from the vascular plant canopy. In addition to taking up inorganic nutrients, ericaceous dwarf shrubs with their particular type of mycorrhiza and ectomycorrhizal species (e.g. Betula, Salix and Dryas spp.) may utilize soil organic N directly through their mycorrhizas without previous mineralization of the organic compounds to inorganic N (Michelsen et al., 1996a), and some plant species even take up organic N without the aid of mycorrhizas (Chapin et al., 1993; Kielland, 1994). At present, there are no estimates of the annual amounts of organic N that are absorbed, but indirect evidences indicate that a major part of the N absorption by dominant ericaceous plants in subarctic heaths may be from organic sources though their mycorrhizas (Michelsen et al. unpublished data). Once the nutrients are incorporated in the plant biomass, they can generally be used repeatedly because a large fraction of at least the leaf, and presumably also the ®ne-root nutrients are translocated to stores in perennial organs in stems and coarse roots before the short-lived tissues are shed. This translocation often withdraws 50% or more of most nutrients (Berendse and Jonasson, 1992), which reduces the need for uptake to support next year's plant tissue production. 3. The microbial nutrient mobilization± immobilization cycle Most conclusions on the effects of nutrients in tundra systems are based on the reactions by plants after addition of inorganic fertilizers. Such experiments, although they give realistic answers to questions of physiological reactions in plants, cannot be uncritically used to predict the changes in other components of the ecosystem. For instance, nutrients added in the inorganic form, contrary to nutrients added with litter, give an instantaneous increase in the plant-available nutrient pool and circumvent microbial mineralization as they need not be mineralized in the microbial food web. Hence, responses to addition of inorganic nutrients give limited information on the processes of, e.g. mobilization and immobilization, which take place naturally at the interface between soil, microbes and plants.

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In fact, microbial nutrient immobilization can be very high in these soils. This has been demonstrated indirectly by fertilizer additions which have given appreciable increase in plant productivity only after addition of inorganic N and P in amounts which are far above the annual plant nutrient uptake (Shaver and Chapin, 1980; Marion et al., 1982). Presumably, the soil microorganisms absorb the nutrients ef®ciently and need to be `nutrient saturated' before any substantial amount is left to the plants (Marion et al., 1982; Chapin et al., 1986; Harte and Kinzig, 1993). Similarly, the lack of summer net nutrient mineralization of litter and soil organic matter, referred to above, is evidence for strong seasonal immobilization and indicates that microbes and plants compete for nutrients (Harte and Kinzig, 1993; Shaver and Chapin, 1995; Kaye and Hart, 1997). These examples show the importance of integrated studies across several ecosystem compartments of reactions to natural ¯uctuations or man-made changes in the environment. 4. Nutrient partitioning between plants, microorganisms and soil organic matter A critical question for evaluation of the possible competitive interaction between microbes and plants is whether the soil microorganisms really have the capacity to absorb enough nutrients to be serious competitors to the plants. Data from the North Scandinavian heath on C, N and P pools in soil, plants and microbes (measured after fumigation and extraction) and the exchange of nutrients between these compartments indeed suggest that this is highly probable. The C, N and P pools in a ca. 15 cm deep organic layer were 3000, 115 and 7 g mÿ2, respectively, while the inorganic N and P pools were about 0.1 (N) and 0.02 (P) g mÿ2 (Fig. 1) (Jonasson et al., in press). Of the total ecosystem C pool, 19% and 2.5% was found in plant and microbial biomass, respectively, and the remaining 78.5% was found in the dead soil organic matter. For nitrogen, the proportion in plants was ca. 10%, largely because of low N content in woody tissues, while the proportion in microbes was 6.5%, leaving 83.5% to SOM. For P, the corresponding proportions were 11%, 30% and 59%, respectively. Hence, the plant C and N pools were about 8 and 1.5 times the pools in soil microorgan-

Fig. 1. Content of C, N and P (g mÿ2) in soil organic matter, soil microorganisms and in plant biomass, and the pools of inorganic N and P in a subarctic heath, North Scandinavia.

isms, respectively, while the proportion in the plant P pool was much smaller and only reached slightly more than one-third of the size of the microbial pool (Fig. 1). This re¯ects the difference in C, N and P incorporation in plants and microbes and suggests that small changes in the soil microbial populations can lead to an increase in plant-available nutrients when

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the microbial populations decline and release at least part of their nutrient content in plant available form. Conversely, it also shows a potential for decline of the plant-available nutrient pools in periods of rapid increases in the microbe populations. 5. Microbial biomass C, N and P in relation to plant nutrient uptake The annual net above- and belowground plant production of the heath was estimated at ca. 250 g mÿ2, corresponding to C ®xation of 125 g C mÿ2, assuming 50% C in the tissue, and the incorporation of N and P in the annual production was ca. 2.5 and 0.17 g mÿ2, respectively. Of these nutrients, mosses incorporated ca. 0.6 (N) and 0.06 (P) g mÿ2 and the remaining 1.9 and 0.11 g mÿ2 in the annual production of vascular plant tissue probably were equally divided between nutrients translocated from perennial stores within the plants and nutrient uptake (Jonasson and Michelsen, 1996). Hence, ca. 1.0 g N and 0.06 g P were absorbed by the vascular plants from the soil nutrient pools (Fig. 2), which are similar to estimates from Alaskan tundra ecosystems (Shaver and Chapin, 1991). The amount of N taken up is low, but still appreciably above an estimated annual net mineralization of 0.05±0.1 g mÿ2 (Schmidt et al., 1998), while the uptake of P is closer to an estimated net P mineralization of at most 0.05 g mÿ2, as measured by the buriedbag technique in the absence of plant roots. The difference re¯ects the amount of nutrients sequestered by the plants in competition with the soil microbes or, for N, an additional uptake from organic sources through mycorrhizal fungi in symbiosis with shrubs and dwarf shrubs. These growth forms constituted ca. 95% of the aboveground vascular plant biomass or, including mosses, 50% of the total biomass aboveground. However, the vascular plant uptake of 1.0 g N mÿ2 and, particularly, of the 0.06 g P mÿ2 was only a fraction of the pools present in the microbial biomass (Fig. 2). The turnover time for the elements in vascular plants, estimated roughly by dividing the element pools by the ¯uxes through them, was about 5 years for C, whereas it increased to between 11 and 13 years for plant N and P. The more than double turnover time

Fig. 2. Pools (bold face figures, g mÿ2) of C, N and P in plants, microbes (Mic) and dead soil organic matter (Soil) and annual fluxes (g mÿ2) between the ecosystem compartments of a North Scandinavian Cassiope heath. Steady state is assumed for fluxes of C between plants, soil and atmosphere and for the fluxes of N and P between plants and soil. MIN is net mineralization measured by the buried-bag technique. For each element, the boxes for microbial and plant pools are proportional to the pools in soil organic matter plus microbes.

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for N and P in comparison to C re¯ects the community resorption of the nutrients in plants during senescence, and is realistic considering that 50±70% of N and P is resorbed from leaves of vascular plants (Berendse and Jonasson, 1992). Calculated in the same way, the turnover time of microbial C was 0.65 years while it increased to 7.5 and 36 years for N and P, respectively, as a consequence of low annual plant nutrient uptake and high pools in the microbes. The long turnover time of N and P in comparison to C re¯ects that these nutrients were ef®ciently reassimilated by the microbes after they had decomposed the organic matter and respired its C content. Hence, the nutrients were recycled over and over again within the decomposer food web without being taken up by the plants. Surprisingly, the nutrients were locked into the soil microbial biomass for a longer period than in the vegetation and the calculation reinforces the foregoing statement that small changes in the microbial populations will have large consequences for the availability of plant nutrients. 6. Interactions between microbial nutrient immobilization and plant growth To our knowledge, there are no ®eld data from arctic ecosystems which demonstrate the effect of ¯uctuating microbial populations on plant growth and nutrition. However, such data are available from a greenhouse experiment (Schmidt et al., 1997a, b).

Festuca vivipara, an arctic grass, was planted in soil from the North Scandinavian Cassiope heath and low and high levels of N and P were added in a factorial manner. Half of the potted plants were grown in soil which had been autoclaved and the other half were grown in non-autoclaved soils. At the end of the experiment, three months after planting, plants grown in non-autoclaved soils with addition of high levels of N and P had accumulated about four times as much biomass as those planted in soils with low levels of N and P or with a high level of either N or P (Fig. 3). This indicates that plant production was limited by a combination of N and P de®ciency. Furthermore, plants grown in autoclaved soils accumulated much more biomass than those in non-autoclaved soils. In comparison to the plant growth in nonautoclaved soils, the biomass at harvest was about 50% higher in the combined high N and P autoclaved treatments; it was three-to-four times higher in the low N and P treatment and in the combination of low N and high P addition, whereas in the high N and low P treatment, the biomass increased about six times. The difference between the responses was most likely due to the release of nutrients from killed microorganisms in autoclaved soil. The concentration of inorganic N after autoclavation increased from 2.6 to 32.5 mg gÿ1 dw of ash-free SOM and the P concentration increased from 0.4 to 13.2 mg gÿ1. Hence, there was a proportionally higher increase in the P than the N concentration, which was expected due to a low N/P ratio in soil microbes (Williams and Sparling,

Fig. 3. Responses in plant production of potted Festuca vivipara (means with SE) to additions of low (0), medium (580 ppm) and high (1130 ppm) levels of glucose to plants grown in non-sterilized and sterilized soils with low (ÿ) and high (‡) levels of added N and P. After Schmidt et al. (1997a).

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1984; Smith and Paul, 1990), in this case 4.8 in the non-autoclaved control soil. That is, the high release of P from the microbial biomass was enough to reach non-limiting or close to non-limiting levels for plant growth, and the response to further addition of P was small as N alone controlled the growth. The partitioning of nutrients between plants and soil microbes followed essentially the same pattern. In cases when plant growth increased, the nutrients were redistributed from the microbial to the plant biomass and vice versa (Schmidt et al., 1997b). If glucose was added to the pots, plant growth and the plant N and P pools continuously declined with the level of addition, at the same time as the microbial N and P content increased (Fig. 4; Schmidt et al., 1997a, b). Hence, since microbial growth is stimulated by addition of labile C in these soils (Jonasson et al., 1996), the microbial biomass absorbed increasing amounts of inorganic nutrients as the size of the C source increased, and left less nutrients to the plants, causing a reduction in plant growth. It can be concluded from this experiment that changes in the partitioning of nutrients between microbes and plants indeed can have a strong effect on plant nutrition and growth if plants are limited by nutrient de®ciency. It can also be concluded that the ef®ciency of nutrient uptake by plants is considerably reduced when there is a microbial population of high sink strength for nutrients present. Even if this experiment was done under greenhouse conditions, it is likely that similar conditions of high sink strength for nutrients are present during the growing season under natural conditions when the soil warms up and the activity of the microbial population increases. 7. Microbial responses to fertilizer addition and temperature enhancement Responses in plant and microbial growth and nutrient uptake to fertilizer addition and temperature enhancement have been measured in a series of experiment at the Scandinavian heaths (Jonasson et al., 1993; Jonasson et al., 1996; Michelsen et al., 1996b; Graglia et al., 1997; Schmidt et al., 1998). Jonasson et al. (1996) showed that the microbial N content almost doubled (Fig. 5) and the P content more than doubled after addition of NPK fertilizer

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Fig. 4. Responses in plant (Festuca vivipara) and microbial N and P after additions of low (0), medium (580 ppm) and high (1130 ppm) levels of glucose to plants grown in soils from a North Scandinavian Cassiope heath.

to a fell®eld soil while the microbial C content did not undergo any changes. Hence, the microbes absorbed nutrients without changing the population sizes. The inorganic soil N and P pools increased strongly after fertilizer addition except when it was combined with sugar (sucrose) amendment (Fig. 5) showing that the soil microbes could absorb extra nutrients only when they were supplied with additional labile C. Similar responses, although slightly weaker, were observed at a Cassiope heath (Jonasson et al., in press). These responses were almost identical to those observed by Schmidt et al. (1997b) in the greenhouse experiment. At the Cassiope heath, the extra P remained in the microbial biomass throughout the winter and summer, following 4 years of NPK application, while there was no remaining effect on microbial N in spring the year after the last addition (Fig. 6). This experiment demonstrates that the soil microorganisms can absorb inorganic N and P during pulses of high nutrient availability, and that at least the absorbed extra P will remain in the microbes for a year or more after uptake. This observation gives strong support to the suggestion that microbial immobilization of nutrients, when these are added to the soil in relatively small amounts,

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Fig. 5. Microbial N and soil inorganic N (mg gÿ1 dw of ash-free SOM, means with SE) in controls (0), sugar amended (C), NPK fertilized (F) and carbohydrate amended‡fertilized plots (CF) of a subarctic montane fellfield, measured about 1 month after the additions. Data are from Jonasson et al. (1996).

prevents any appreciable plant uptake and response in growth in spite of the strong plant-nutrient limitation (Shaver and Chapin, 1980; Marion et al., 1982). In contrast, increase in the air temperature by 2.5 and 4.58C, corresponding to a soil temperature increase of 1±28C had no effect on microbial nutrient uptake (Fig. 6). This agrees with the low effects on C evolution and N mineralization after an increase in the temperature of an Alaskan soil from 58 to 108C in the laboratory (Nadelhoffer et al., 1991) and after increases of 1±28C in situ in northern Sweden (Jonasson et al., 1993) and indicates that the response to temperature increases within an interval of a few degrees centigrade above the present soil temperature may not be so strong as has been thought previously.

8. The carbon balance in a changing Arctic environment The carbon balance of the Arctic depends on the equilibrium between the incorporation of atmospheric CO2 in the primary producers, and the subsequent input of plant organic matter into the litter and soil on one hand, and the release of CO2 through microbial activity, on the other. This balance may change in the future if the temperature increases as a consequence of increased emission of trace gases or if the soil-moisture conditions change (Flanagan and Veum, 1974; Heal and French, 1974; Billings et al., 1982; Billings et al., 1983). The Arctic has a low biomass at present compared with most other biomes and vast areas are poorly

Fig. 6. Effects of 4 years of NPK addition on microbial N and P pools (mg gÿ1 dw of ash-free SOM, means with SE) in control (Con) plots and in plots subjected to two levels of air temperature enhancement (T1: ‡2.58C; T2: ‡4.58C). Measurements in spring, midsummer and late summer the year after the last addition of fertilizer. Data are from Jonasson et al., (in press).

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vegetated or even lack vegetation. Consequently, even if the C loss from the soil may increase, the Arctic has the potential to act as a large sink for CO2 if the rate of C accumulation through enhanced plant productivity overrides the loss of C from the soil. However, since arctic soils contain ca. 14% of the world's stores of soil C (Post et al., 1982), the Arctic can also act as a large source of atmospheric CO2 if the rate of C loss from the soil overrides the C ®xation in the primary producers. Presumably, the changes in C balance are likely to be different both at regional and local scales (Callaghan and Jonasson, 1995a, b). For instance, the middle and high arctic regions are likely to be sinks for atmospheric C because of expansion of vegetation into the presently large unvegetated areas (Alexandrova, 1980). This assumption is reinforced by observed strong responses to increased temperature in plant biomass formation (HavstroÈm et al., 1993; Parsons et al., 1994; Michelsen et al., 1996b; Graglia et al., 1997) and increased viability of seeds (Wookey et al., 1993) in the coldest regions. Also, because the soil C content is low in such areas, these plant processes are likely to have greater importance for the C balance than any changes in the rate of CO2 release from the soil. The low Arctic and Subarctic, on the contrary, with much higher proportions of soil C, are more likely to act as sources for CO2 if changes in the environment lead to increased rate of decomposition, e.g. by warming of the soil or changed soil moisture conditions. However, the predictions are complicated by numerous possible interactions and feedbacks, for instance those between the microbial and plant components. As an example, increased rates of decomposition and mineralization in the southern Arctic will probably lead to increased CO2 output to the atmosphere, but also to increased ®xation of atmospheric CO2, because plant growth generally is stimulated by increases in soil inorganic nutrient pools. Hence, carbon will be redistributed from the soil to the plant biomass. Because the C-to-nutrient ratio generally is higher in the plants than in the soil, such redistribution would increase the ecosystem sink strength for carbon as the nutrients, particularly N, when moved from the soil to the vegetation will increase the ecosystem C ®xation (Rastetter et al., 1997). Note that this will occur with the existing amount of N.

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The increase in C sink strength will be particularly high if the increased mineralization leads to enhancement of growth of woody plants, rather than of forbs or graminoids, because woody tissue has a higher C-tonutrient ratio than non-woody tissue and a much higher ratio than the soil organic matter. Such a change in the relative abundance of life forms has, indeed, been observed on graminoid-dominated tussock tundra in Alaska. After less than a decade of fertilizer application, the graminoids declined and shrubs increased dramatically (Chapin et al., 1995b), while changes in dominance were weaker in dwarf shrub heaths in North Scandinavia (Jonasson et al., in press). Any increased sink strength for atmospheric C may, however, be counteracted by a number of buffering systems. For instance, in nutrient-limited ecosystems any loss of nutrients, say by increased leaching in a wetter climate or by increased denitri®cation, will lead to reduced plant growth and loss of sink strength. Similarly, increased sequestration of nutrients by microbes like that shown after fertilizer addition (Figs. 5 and 6) or strong ®xation of released inorganic nutrients, most likely P (Black, 1968; Jonasson and Chapin, 1991), will lead to a similar growth reduction. 9. Summary and conclusions Compared with most other ecosystems, arctic ecosystems have a high proportion of microbially ®xed nutrients in relation to the amounts ®xed in the vegetation. This is basically because most arctic ecosystems have large deposits of nutrient-containing soil organic matter and low plant biomass. The release of nutrients from the soil organic matter is slow because of environmental constraints to decomposition, paired with high nutrient immobilization by the soil microorganisms. Mineralization experiments, performed without possibility for plant nutrient uptake have shown very low, or even lack of, net mineralization of N and P, i.e. the elements which most commonly limit plant productivity, during the entire growing season. This is probably because the microbes absorb all nutrients that are released during decomposition, which implies that the microbes constitute a strong potential sink for nutrients. It is yet uncertain to what extent plants can sequester mineralized nutrients in competition with the microbes. It is possible that plant

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nutrient uptake occurs mainly during periods of declining microbial populations, when nutrients are leached out from the microbial biomass. Improved knowledge of the mechanisms behind the plant±microbial interactions in these nutrient-limited systems is important, because it will form a basis for our understanding of the C exchange between the ecosystems and the atmosphere under the predicted, future climatic changes. For instance, high microbial nutrient immobilization, i.e. low release of plantavailable nutrients, paired with high microbial decomposition of soil organic matter in warmer soils, will lead to a loss of C from the soil to the atmosphere, which will not be compensated fully by increased plant C ®xation. Hence, the system will become a net source of atmospheric C. Conversely, if plants are able to sequester extra nutrients ef®ciently, their productivity will increase and the systems may accumulate more C and turn into a sink for C. This sink will be particularly strong if growth of shrubs and dwarf shrubs is promoted, because woody plants can increase their biomass and, hence, their C content strongly with investment of small amounts of nutrients compared with non-woody plants. Acknowledgements Most research on which this article is based has been ®nancially supported by the Danish Natural Science Research Council, grant Nos. 11-0421-1, 11-0611-1 and 9501046 and by the Swedish Environmental Protection Board, Grant No. 127402. References Alexandrova, V.D., 1980. The Arctic and Antarctic: Their Division into Geobotanical Areas. Cambridge University Press, Cambridge. Berendse, F., Jonasson, S., 1992. Nutrient use and nutrient cycling in northern ecosystems. In: Chapin, F.S., III, Jefferies, R.L., Reynolds, J.F., Shaver, G.R., Svoboda, J. (Eds.), Arctic Ecosystems in a Changing Climate. An Ecophysiological Perspective. Academic press, San Diego. pp. 337±356. Billings, W.D., Luken, J.O., Mortensen, D.A., Peterson, K.M., 1982. Arctic tundra: a source or sink for atmospheric carbon dioxide in a changing environment? Oecologia (Berl.) 53, 7±11. Billings, W.D., Luken, J.O., Mortensen, D.A., Peterson, K.M., 1983. Increasing atmospheric carbon dioxide: possible effects on arctic tundra. Oecologia (Berl.) 58, 286±289.

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