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WITHIN-STAND NUTRIENT CYCLING IN ARCTIC AND BOREAL WETLANDS.

INTRODUCTION

Geogenous ("mineral-fed"), often-acidic fens and ombrogenous ("rain-fed") bogs (terminology follows Bridgham et al. 1996) are dominant wetland types in the boreal, subarctic and low-arctic zones, while acidic, wet sedge-moss tundra or circum-neutral tundra meadows become increasingly dominant from the low Arctic towards middle Arctic (Frenzel 1983, Bliss and Matveyeva 1992). These northern wetlands are dominated by a restricted number of plant functional types (see Shaver 1995) or growth forms, within which the species are assumed to react similarly to environmental influences and, conversely, also may influence the environment in a similar way (Chapin et al. 1996). Deciduous shrubs or dwarf shrubs and grasses are most common in moderately acidic, eutrophic fens and geogenous tundra wetlands, while evergreen shrubs or dwarf shrubs, sedges, and mosses are the most common plant functional types in acidic wetlands (Malmer et al. 1992, Bridgham et al. 1996).

Among the functional types, Sphagnum mosses are mostly restricted in their occurrence to low-pH bogs and fens where they usually are dominant (Verhoeven et al. 1990). As pH and alkalinity increase, they are replaced by so called "brown" mosses (Amblystegiaceae) (Malmer et al. 1992, Bridgham et al. 1996). A succession of sedge species, e.g., of the genuses Eriophorum, Carex, and Scirpus, generally dominates different sections of the broad interval of pH and soil moisture from bogs to eutrophic fens, and sedges together with grasses are common in tundra wetlands (Bliss and Matveyeva 1992). Evergreen, ericaceous sclerophyllous shrubs and dwarf shrubs occur mostly in low-pH wetlands, and several species, such as Vaccinium vitis-idaea and Empetrum nigrum also have a distribution along broad soil-moisture gradients from bogs and mesic tundra, to dry forests and arctic heaths (Larsen 1982, Moore 1981).

Plant productivity is generally higher in fens than in bogs (Bradbury and Grace 1983) coincident with a general increase of electrolytes and pH from acidic ombrogenous bogs, through low-pH fens to alkaline, high-pH fens (Sjors 1950). In tundra, plant productivity decreases with increasing latitude (Moore 1989, Shaver et al. 1997) and as in fens and bogs (Malmer 1988, Aerts et al. 1992), plant growth usually increases with addition of phosphorus (P) or nitrogen (N) (Shaver and Chapin 1995), suggesting main growth limitation by low availability of these elements.

In the following, we first summarize some common and differentiating traits in soil nutrient conditions and nutrient transformations in northern wetlands, with focus on N and P. We then discuss the nutritional characteristics of the common plant functional groups, and end with a synthesis of controls of within-stand and ecosystem nutrient cycling.

NUTRIENT INPUT AND TRANSFORMATION IN NORTHERN WETLANDS

Input and retention of nutrients from external sources

Both external and internal sources contribute to the supply of plant nutrients in northern wetlands. Geogenous wetlands and wet tundra receive external nutrients from the surrounding watersheds, from groundwater, or by atmospheric deposition of particles or solutes in the precipitation, and from atmospheric [N.sub.2] fixation. In contrast, the ombrogenous, precipitation-dominated wetlands receive external nutrients mainly from atmospheric sources. The nutrient input from the atmosphere generally is lower in the arctic and boreal regions than in the temperate region because the air is relatively unpolluted and precipitation is low (Van Cleve and Alexander 1981, Chapin 1983). However, some elements can be deposited in large amounts regionally. For instance, sodium (Na) and magnesium (Mg), of oceanic origin, show steep gradients, with high deposition near the coast and low deposition in the continental inlands (Malmer 1988, Malmer et al. 1992).

Nitrogen and P in precipitation are efficiently trapped by the mosses, particularly by Sphagnum species [ILLUSTRATION FOR FIGURE 1 OMITTED], while other elements are less tightly retained (Malmer 1992, Lee and Woodin 1988). Atmospheric deposition of N and P, together with [N.sub.2] fixation, are considered to be the main sources of these elements for mosses in ombrogenous bogs and acidic fens (Malmer 1992). For N in the Arctic, both deposition and microbial N2 fixation generally ranges between 30 and 250 mg[multiplied by][m.sup.-2][multiplied by][yr.sup.-1] (Van Cleve and Alexander 1981, Chapin and Bledsoe 1992). These amounts are an order of magnitude lower than in temperate ecosystems (Chapin 1983). Maimer and Nihlgard (1980) estimated the annual input of dry- and wet-deposited N to a subarctic mire to be [greater than]100 mg[multiplied by][m.sup.-2][multiplied by][yr.sup.-1], with [N.sub.2] fixation contributing another 180 mg N/[m.sup.2] annually (Granhall and Selander 1973). Together, this corresponded to [approximately]25% of the annual incorporation of N into the plant biomass. Loss of N in outflowing water was insignificant, indicating that the mire trapped and immobilized N efficiently in plant biomass, deposited it in litter, and eventually incorporated it into the biologically inert peat in the anaerobic deep peat (catotelm) horizon.

Once incorporated in the Sphagnum mosses, the immobilization capacity for ions depends on the growth demand of the mosses for the element (Lee and Woodin 1988). This was illustrated by Aerts et al. (1992), who examined the response in Sphagnum growth and N and P retention after addition of N and P to Sphagnum carpets in a north and a south Swedish mire with low and high N deposition, respectively. They found a strong growth response to N addition and high N recovery after the end of the growing season in sphagna of the northern mire with a tissue N-to-P ratio [less than] 10. In contrast, the sphagna in the southern mire, having a tissue N-to-P ratio [greater than]14, responded with increased growth to P but not to N addition, and the proportional recovery of the added P was much greater than of the added N. The differences in responses were related to site-specific differences in the deposition load of N. The high absorption and retention capacity of N in the northern mire was, presumably, because of N-limited moss production in this region where atmospheric N deposition is low. In contrast, the higher N deposition in the southern region had caused a relative shortage of P, reflected in the high tissue N-to-P ratio, which limited Sphagnum growth and led to more tight retention of P than N.

Leaching, litter decomposition, and mineralization

It is generally assumed that the leaching losses from dominant living wetland plants are low. This has been inferred from the sclerophyllous leaves and the well-developed, waxy cuticula on the leaves of many plant species in these communities, which protects the leaves from leaching (Chapin 1980). It is also supported by nonsignificant differences between the nutrient content in rain-protected and unprotected leaves - both living and senescing - of the bog plant Eriophorum vaginatum (Jonasson and Chapin 1985).

After litterfall, mass losses and [CO.sub.2] evolution are normally rapid during a first phase of physical leaching and microbial degradation of labile compounds. This phase is followed by slower mass loss during the decomposition of more recalcitrant tissues (Updegraff et al. 1995). Mass loss after one year of decomposition of litter varied between zero and 11% for moss litter, 6-15% for stem, shoot, and leaf litter of ericoids and 6-33% for less sclerophyllous leaf litter across various mires and wet sedge tundras in arctic and subarctic North America and Europe (Heal and French 1974). Similar tissue- and life-form-related mass loss has been observed also in other arctic (e.g., Giblin et al. 1991, Hobbie 1996) and boreal (e.g., Bartsch and Moore 1985, Ohlson 1987, Rochefort et al. 1990, Johnson and Damman 1991) wetlands. In general, these studies have shown that the decomposition rate is more closely associated with the composition of the carbon (C) compounds than with the nutrient content of the substrate, with the slowest loss from litter with high-lignin, low-cellulose content (Brinson et al. 1981). Decomposition is particularly slow in wetlands with high abundance of Sphagnum mosses (Verhoeven et al. 1990, Hobbie 1996). Some studies also have shown large differences in decay rates among different Sphagnum species. For instance, Johnson and Damman (1991) observed a much slower decay rate of litter from Sphagnum fuscum, a common hummock species, than from congeners growing in wet hollows. The lower decomposition rate persisted after reciprocal transplantation of the species, suggesting that it was related to tissue quality and not to differences in microhabitats.

Although decomposition is associated with release of nutrients, [CO.sub.2] evolution or rates of mass loss cannot necessarily be used as indices for the release rates of nutrients. This is because different nutrients are released at different rates, and there is sometimes even an inverse relation between the rates of decomposition and net nutrient mineralization. For instance, Verhoeven et al. (1990), Updegraff et al. (1995) and Bridgham et al. (1996) found that net N and P mineralization rates were higher in bog peat with low rates of decomposition than in more rapidly decomposing fen peat. Similarly, in soil incubated at 3 [degrees], 9 [degrees], and 15 [degrees] C, Nadelhoffer et al. (1991) found a steep increase in [CO.sub.2] evolution and net N mineralization with increasing temperature, while phosphorus mineralization decreased. This resulted in ratios of respired C to mineralized P ranging from 8600 at 3 [degrees] C to 143900 at 15 [degrees] C. These differences between respired C and mineralization of N, on one hand, and P mineralization on the other, can be due to inequalities in microbial immobilization of the elements or to chemical adsorption to soil particles of nutrients released from the gross mineralization of the organic matter (Damman 1988, Verhoeven et al. 1990, Nadelhoffer et al. 1991, Walbridge 1991).

Microbial nutrient mobilization and immobilization

Annual rates of net N mineralization decrease sharply from south to north (Nadelhoffer et al. 1992). Mineralization studies of soils incubated in situ, using the buried-bag technique (Eno 1960), i.e., which prevented plant nutrient uptake, have often shown that growing-season net N and/or P mineralization is negative in subarctic (Rosswall and Granhall 1980) and arctic (Chapin et al. 1988, Giblin et al. 1991) wetlands. This indicates that the direction of the net flux of the elements is from the soil solution and degraded soil organic matter (SOM) into the soil microorganisms. In contrast to negative summer mineralization, Giblin et al. (1991) found that net mineralization in a wet sedge tundra was positive during the autumn, winter, and early spring, when the elements presumably were released from declining microbial populations. A similar pattern of a pronounced loss of N in winter followed by a summer increase of N was found in leaf litter incubated in moss mats and E. vaginatum tussocks (Hobbie and Chapin 1996). This suggests high summer immobilization of nutrients in soil microbes and a net release of the nutrients in winter when the microbial populations presumably decline. The supply of nutrients to the vegetation may therefore depend on how efficiently the plants compete with soil microbes for nutrients during the growing season (Harte and Kinzig 1993), or on the ability of the vegetation to absorb nutrients during periods when the nutrients are released from soil microbes (Jonasson et al. 1999).

This strong seasonal variation in net mineralization, probably due to fluctuations in microbial biomass and activity, is not surprising when one considers the nutrient content of soil microorganisms. High values of microbial C, N, and P content have been reported from subarctic and arctic ecosystems. Jonasson et al. (1996) found that the microbial biomass, including both bacteria and fungi, contained 2.8-3.6% of the total soil C, 6.1-7.3% of the soil N, and [greater than]30% of the soil P in dwarf shrub-dominated subarctic montane heaths, which resemble subarctic bogs in the composition of plant functional groups. These amounts increased strongly after addition of inorganic N and P fertilizer, i.e., the microbial uptake of inorganic N and P increased with increasing availability of these elements in the soil solution. Similarly, Clarholm and Rosswall (1980) estimated that the bacterial populations of a subarctic mire contained 1-3% of the total soil C and Giblin et al. (1991) reported that the extractable inorganic P fraction increased almost 20-fold after killing of the microbial biomass by fumigation of soils from an Alaskan wet sedge tundra.

The reported proportions of microbial nutrients from northern wetlands and heaths are within the ranges of microbial C, N, and P that normally are found in organic soils (Smith and Paul 1990, Wardle 1992), although sparse data indicate that the proportions of N and P in microbial biomass may be higher in the Arctic than in more southern ecosystems (Wardle 1992). However, values between 45% and 56% of the total soil P were found in the microbial biomass of warm, temperate pocosin (evergreen shrub bog) soils (Walbridge 1991), showing that high microbial P immobilization may not be a function of differences in climatic conditions latitudinally.

The high proportions of soil nutrients fixed in soil microorganisms suggest that the microbial mobilization-immobilization cycle is extremely important for seasonal ecosystem nutrient dynamics in northern wetlands. Also, the high microbial P immobilization indicates that the dynamics of the P cycle in organic soils is regulated by changes in microbial populations and activity (Chapin et al. 1978), with high microbial sink strength during periods of rapid expansion of the populations and high P release during periods of population decline. This also implies that periodic competition for P and N between expanding plant and soil microbial populations may be intense (Shaver and Chapin 1995, Jonasson et al. 1996). Plant uptake of these productivity-limiting nutrients may therefore occur during pulses of low microbial activity that follow episodes of soil drying or freeze-thaw cycles (Malmer 1962, Jonasson and Chapin 1991, Jonasson et al. 1996).

NUTRITIONAL CHARACTERISTICS OF NORTHERN WETLAND PLANTS

Nutrient resorption and storage

Plants growing under nutrient-limited conditions have often been shown to resorb nutrients efficiently. High resorption, particularly of P, has been reported from evergreen peatland plants at both northern (Small 1972) and temperate latitudes (e.g., Walbridge 1991, DeLucia and Schlesinger 1995). Many dominant sedges and grasses, growing in nutrient-deficient wetlands, show the same characteristics. For instance, Eriophorum vaginatum has among the most efficient nutrient resorption measured in vascular plants. Its resorption efficiency results from a combination of its leaf growth pattern and nutrient translocation within leaves (Jonasson and Chapin 1985). In an Alaskan muskeg, E. vaginatum formed two to three leaves sequentially at about 1.5-mo intervals during the growing season. A new leaf appeared when the previous leaf had grown to near maximum length. As the new leaf appeared, the previously formed one started to export nutrients that, consequently, became available to the new leaf (Jonasson and Chapin 1985). Before senescence, the plant typically had resorbed more than 90% of the leaf P and 80% the leaf N content [ILLUSTRATION FOR FIGURE 2 OMITTED] so that the annual uptake requirement to replenish the canopy nutrients lost to litter was reduced to [approximately]10% of the peak season's leaf P pool and 20% of the N pool (Jonasson and Chapin 1991). Hence, in comparison with other species with a less distinct sequential pattern of leaf development (Jonasson and Widerberg 1988, Shaver and Laundre 1997), E. vaginatum could reuse nutrients at a near-constant rate during the entire period of growth simply by transporting nutrients from old leaves to new ones.

Similar conservative use of nutrients is known from other northern species. Chapin et al. (1980) found that growth of Dupontia fisheri, a dominant grass in Alaskan wet sedge tundras, was almost entirely dependent on stored N reserves, retrieved from last year's growth for use by the current year's growth. Leaf growth was supported by early-season translocation of N from belowground plant parts. Uptake started much later in the season and continued until the end of September after senescence of the aboveground tillers was completed and the soil started to freeze. About 40% of the annual uptake took place after late July. As with E. vaginatum (Jonasson and Chapin 1985, Shaver et al. 1986), the peak season's nutrient pool in the canopy of D. fisheri was reached in mid-July, 1-2 wk before the shoot biomass peaked. After reaching the nutrient peak, the stock of nutrients in the aboveground shoots declined in spite of the ongoing accumulation of leaf mass and late-season nutrient uptake, as the leaf nutrients were translocated to and stored in roots and rhizomes.

The timing of growth, nutrient uptake, and allocation is a consequence of the asynchrony between the conditions above- and belowground in northern boreal and arctic ecosystems. When the snow has melted, the progression of soil thaw is slow (Kummerow et al. 1983) and the thawed soil is often strongly waterlogged. Hence, except in shallow-rooted species, nutrient uptake is prevented or strongly impeded, while the conditions for photosynthesis are favorable. Furthermore, in the Arctic where snowmelt generally coincides with the summer solstice, after which daily irradiance declines, a delay in the onset of growth until the conditions for soil nutrient uptake improve a week or two later could decrease the potential C assimilation by nearly 40% (Tieszen 1978). Hence, to optimize C acquisition, photosynthesis and growth must start when soil nutrients are bound in the frozen soil or when the low soil temperature impedes nutrient uptake, which necessitates dependence on stored reserves. On the other hand, nutrient replenishment and storage for the coming growing season can continue after the dieback of aboveground shoots in late summer when irradiance is much reduced and the air temperature has dropped, because of the still-favorable thermal conditions of the soil until late in the autumn (Chapin et al. 1980).

Interpretations of tissue longevity

The high N and P resorption suggests that plants in nutrient-deficient environments have been selected so as to minimize nutrient losses rather than selected for adaptations to promote nutrient uptake (Berendse and Jonasson 1992). Plant growth models suggest that equilibrium biomass in these environments can be kept at a higher level by adapting a low loss rate of nutrients rather than by increasing the capacity for nutrient uptake (Aerts and van der Peijl 1993, Aerts 1995). High potential rates of nutrient uptake may be superfluous in any event if the plants are already taking up nutrients at the rate of supply from the soil (Nadelhoffer et al. 1997). In addition, the long leaf longevity that is characteristic of mosses and evergreen plants leads to high nutrient conservation (Chapin et al. 1995).

In nutrient-poor northern wetlands where the constraints on nutrient uptake are particularly strong due to the short growing season and the wet and cold soil conditions, traits that promote high internal nutrient circulation within plants and those that increase nutrient retention time within the plants should have high adaptive significance. Increased longevity of the leaves may be particularly important in conserving nutrients in relation to high resorption (Aerts 1995). However, as leaf longevity declines, resorption should theoretically gain importance (Jonasson 1989, Aerts 1995).

Several studies have attempted to demonstrate that plants in nutrient-deficient environments exhibit these traits. For instance, Small (1972) found that nutrient resorption and nutrient-use efficiency, defined as the amount of C assimilated per unit nutrient, was higher in evergreens than in deciduous plants, and in bog plants compared with non-bog plants. The increased nutrient-use efficiency was a combination of both longer leaf longevity and higher nutrient resorption in evergreens and bog plants than in deciduous and non-bog plants. Because evergreenness is a common leaf trait in nutrient-poor bogs, Small (1972) suggested that the occurrence of evergreens in bogs was in part explained by their adaptations to cope with low nutrient levels through their high resorption efficiency. However, other studies have questioned Small's calculations of both leaf longevity and nutrient resorption because they probably overemphasized traits leading to long nutrient retention time in evergreens (Jonasson 1989). Several studies have failed to demonstrate any difference in resorption efficiency between plants growing in nutrient-poor and nutrient-rich conditions (Aerts 1995) or between evergreen and deciduous plants. For instance, Jonasson (1989) showed that neither the retention times of nutrients in the leaves nor resorption in evergreens were likely to be higher in evergreen leaves of moderately long leaf longevity than in deciduous leaves across a range of wetland and non-wetland species with different geographical distribution. Ledum palustre, a common evergreen shrub in boreal mires, retained its leaves for [approximately]1.5 yr, and its resorption of N and P was 65% and 70%, respectively. This is of about the same order as reported previously from other evergreen and deciduous plants (Chapin and Kedrowski 1983, Chapin and Shaver 1989). Similarly, except for a slightly higher C gain per unit N in an evergreen shrub than in co-occurring deciduous species, Chapin and Shaver (1989) did not detect any differences in resorption between arctic evergreens and deciduous plants, nor was there any significant correlation between resorption efficiency and soil nutrient availability.

Sphagnum mosses that typically occur in ombrogenous bogs and in nutrient-deficient tundras have much longer leaf longevity (8 yr) than other mosses occurring in more geogenous environments (3 yr; Chapin et al. 1995). This may reflect the advantage of increasing leaf longevity in the most nutrient-poor environments discussed above. Interestingly, the decumbent form of L. palustre in the Arctic is evergreen (Shaver 1981) and not wintergreen (i.e., with leaves retained over winter only), which could reflect a nutritional advantage of extended leaf longevity in nutrient-poor tundras.

Although leaf longevity has a clear relationship with nutrient conservation and may be an adaptation to low soil nutrient levels, the relationship between high resorption efficiency and nutrient availability is less clear. A plant with high peak seasonal nutrient content and high resorption efficiency may lose more nutrients to litter than a plant with low peak seasonal nutrient concentration and low resorption efficiency. Thus, in spite of efficient resorption, some plants must absorb large amounts of nutrients to replenish the nutrients lost to the litter. Killingbeck (1996) proposed that the adaptation to low nutrient availability is better described as "nutrient proficiency," i.e., the level to which nutrients are reduced during the senescence proceeding leaf abscission, than as "resorption efficiency." This is because proficiency is an absolute, and not relative, measure of the amounts of lost nutrients. He pointed out that a plant with high resorption proficiency may have low resorption efficiency and vice versa. To our knowledge, there is no compilation of nutrient proficiency for northern wetland plants. However, Aerts (1997) argued that evergreens, even if they have similar resorption efficiency as deciduous plants, generally are more proficient because their peak nutrient concentrations usually are lower. As a consequence, leaf-level nutrient-use efficiency in evergreens, defined as the inverse of litter nutrient concentration (Aerts 1997), also should increase in comparison with deciduous plants, because more leaf biomass is produced per unit lost or "used" nutrient in the evergreen leaves. Indeed, E. vaginatum, discussed in the previous section, compensates relatively short leaf longevity with high nutrient proficiency and leaf-level nutrient-use efficiency as leaf litter N and P concentrations are reduced to about 0.4% and 0.03%, respectively [ILLUSTRATION FOR FIGURE 2 OMITTED].

Carbon-nutrient interaction and leaf longevity

Instead of, or in addition to, conserving nutrients through increased leaf longevity, a long retention time of nutrients may be an indirect effect of the energy constraints operating on photosynthesis and growth. For a plant's C economy, leaf longevity would depend on the benefit to the plant of keeping its leaves vs. the cost in terms of C investment of shedding its leaves and forming a new canopy, with higher photosynthetic capacity. When conditions for C assimilation are unfavorable, e.g., when the growing season is short or where nutrient availability is low, a plant may get a higher C return by keeping its leaves for an extended period of time rather than replacing them at shorter intervals of time (Mooney and Gulmon 1982, Kikuzawa 1991). During the short northern growing season, evergreenness and wintergreenness allow plants to maintain photosynthesis during an extended period of time in autumn and resume photosynthesis earlier in spring than deciduous plants with a programmed phenology of leaf formation and loss the same year. Hence, an extended period of C acquisition could be at least as important for these plants as an increased retention time of nutrients within the plant, and the residence time of nutrients within a plant could be an indirect consequence of the conditions for carbon acquisition rather than a direct expression of a nutrient-saving strategy.

There are, in fact, some experimental data that give support for this view. Because evergreen plants usually form new leaves at the same time as old leaf cohorts senesce, it has been considered that the old leaves supply nutrients to the new leaves through translocation (Shaver 1981, 1983). This would minimize the requirement of nutrients in the same way as if the nutrients were stored in other perennial tissues overwinter. Removal of the oldest leaves before the translocation starts would, consequently, deplete the amount of stored nutrients and reduce growth of the new leaves.

Jonasson (1989) removed the old leaves of several evergreen species, including L. palustre and Rhododendron lapponicum, growing in sites ranging from arctic/alpine wetlands to moist and dry heaths, before the new leaf growth and senescence of old leaves started in spring. The proportion of the whole plant nutrient content lost with the leaves was between 20 and 25% of the total N and P pools in the plants and [greater than]30% of the K pool. The expected response, if the growth was nutrient limited by recycling of nutrients from old to new leaves, would have been a sharp decline in the growth of new leaves and a low rate of nutrient incorporation into them. However, defoliated plants did not incorporate lower absolute amounts of nutrients in the new leaves than non-defoliated plants, even though the biomass accumulation into the new leaves was delayed during the first weeks of spring growth. In a later study, it was shown that this mobilization of nutrients to new growth was not due to extra allocations of nutrients from stems and roots (Jonasson 1995a). Hence, although this observation does not preclude that nutrients normally are translocated from old to new leaves, it appears that losses of nutrients from the old leaves before senescence can be fully compensated for by increased nutrient uptake within a relatively short period of time.

However, leaf growth was hampered if the old leaves were removed a few weeks before budbreak of the current year's vegetative bud, suggesting that the reduced C assimilation rather than nutrient deficiency caused the response (Jonasson 1995a, b). Furthermore, conservation of nutrients cannot explain leaf longevity in the boreal L. palustre, which is wintergreen (Jonasson 1989), in contrast to the evergreen L. palustre ssp. decumbens (Shaver 1981), since the boreal, wintergreen plants, in fact, must form a full canopy each year in the same way as deciduous species. The most obvious advantage is that they can extend the period of photosynthesis. A nutritional advantage can be achieved first for plants with leaf longevity exceeding 2 yr (Jonasson 1989, Aerts 1995). This interpretation also agrees with observed relatively short leaf longevity of less than two growing seasons in several bog ericoids, e.g., Ledum groenlandicum, L. palustre, Rhododendron lapponicum, Chamaedaphne calyculata, and others (Jonasson 1989, Larsen 1982), which also casts doubt over the strict nutritional interpretation of the extended leaf longevity of many bog plants.

There is also a possibility that evergreenness provides for increased nutrient uptake. Kummerow et al. (1983) found that evergreen dwarf shrubs in an Alaskan muskeg started the development of the new fine-root system in the shallow, thawed soil above the slowly retreating ground ice in early May, soon after snowmelt and a few days before the canopy regreened. The early root development was supported by stored carbohydrates in the stems, which were replenished rapidly when the leaves regreened. In contrast, the development of new roots in the more deeply rooted deciduous shrubs started [approximately]3 wk later and coincided with the development of the new canopy. Presumably, development of new leaves in the deciduous shrubs was delayed until the temperature conditions stabilized to reduce the risk of frost damage. The simultaneous development of roots and leaves resulted in strongly reduced content of non-structural carbohydrates in the stems. From the study of Kummerow et al. (1983), it thus appears that evergreen shrubs not only prolong the period of photosynthesis in the early and late season but that they also develop a root system earlier than the deciduous plants. Hence, evergreenness provided for increased nutrient absorption, implying that the evergreen habit can play a role in both C and nutrient economy.

Organic nutrient sources and mycorrhiza

Although it has been commonly held that plant availability of N and P in northern wetlands is low and declines as the supply rate of nutrients declines from fens to bogs, this might not be correct in all cases. For instance, several studies have shown that both N and P mineralization rates and the inorganic pools of these elements increase from fens to bogs, which speaks against the notion of decreased plant nutrient availability from geogenous to ombrogenous wetlands (Verhoeven et al. 1990, Updegraff et al. 1995, Bridgham et al. 1996). Furthermore, recent research has shown that the common wetland species E. vaginatum and Carex aquatilis can compensate for the low availability of inorganic N by uptake of organic N as low-molecular-mass amino acids (Chapin et al. 1993, Kielland 1994, Schimel and Chapin 1996). Because the concentration of amino acids in the soil of the plant communities dominated by these species is high, often exceeding the concentration of inorganic N by several fold (Kielland 1994), amino acids may be an important additional source for plant N. However, the amino-acid uptake across taxa is still poorly investigated, so that broader generalizations are not possible.

Similarly, ericaceous dwarf shrubs are known from laboratory experiments to utilize N from organic sources through their fungal symbionts (Read et al. 1989, Read 1993). Across a broad range of arctic and subarctic ecosystem types, these plants with their mycorrhiza differ strongly from arbuscular mycorrhizal and non-mycorrhizal plants in their leaf [[Delta].sup.15]N (Michelsen et al. 1996, 1998). It is likely that the ericoids utilize an N source with different [[Delta].sup.15]N than the other plant groups, although it has not been possible to confirm this with direct measurements of the isotopic signature of the soil N pools. However, high uptake of organic N is also supported by an observation that addition of inorganic fertilizer with a different [[Delta].sup.15]N signature than that of the plant leaves to a mixed ericoid and non-ericoid vegetation did not change the [[Delta].sup.15]N in the ericoids within the first 5 yr after the addition. In contrast the [[Delta].sup.15]N of the non-ericoid plants changed towards that of the fertilizer (A. Michelsen, personal communication). The different response among the plant groups indicates that the non-ericoid plants took up N from the fertilizer, while the ericoids maintained their uptake from their normal N source.

These observations are important because they suggest that bog plants of several functional types have access to a broader spectrum of N sources than recognized earlier, and that they thereby may decrease competition for N from other plant groups lacking these adaptations.

WITHIN-STAND AND ECOSYSTEM NUTRIENT CYCLING

Implications of leaf and plant longevity for within-stand nutrient cycling

Based on the information we have presented, there are arguments both for and against the notion that increased leaf nutrient resorption and longevity are advantageous as nutrient availability declines. Hence, it is not possible to relate high internal circulation and retention of nutrients within plants to the availability of nutrients in the environment except in species with leaf longevity of several years and possibly in highly proficient plants. However, extended longevity of leaves, stems, and individuals, together with high nutrient proficiency, does play a role in nutrient economy at the ecosystem level because both result in an entirely different nutrient demand compared to systems with a high turnover of individuals and high recruitment from seeds (Jonasson 1997). In the latter systems, new resources must be absorbed by seedlings and juvenile stages to replace the nutrients lost annually in the biomass of whole individuals. In contrast, to achieve a steady-state community nutrient content, ecosystems with a large dominance of perennial plants only need to replace nutrients lost from the dying plant parts after resorption. Hence, with a larger fraction of perennials, a smaller proportion of the annual supply of nutrients to biomass production needs to be circulated within the plant-soil system.

Herbivory and nutrient turnover

The rates of nutrient cycling and the tight nutrient cycles within plants, between plants and mycorrhizal fungi, and within stands are likely to be modified by herbivory. However, except for certain wetlands such as coastal marshes and wet sedge tundras, herbivory usually removes only a small percentage of the available plant biomass (Jefferies et al. 1994) and is unlikely to play any important role for nutrient turnover in general. In contrast to the generally low grazing effects, Jefferies (1988) showed that heavy grazing from lesser snow geese in coastal marshes accelerated the turnover of essential plant nutrients. Similarly, rodents in wet sedge tundras at Barrow, Alaska, can remove up to 90% of the aboveground vegetation (Thompson 1955). Pitelka (1964) and Schultz (1964, 1969) proposed that this consumption may create a nutrient-driven negative feedback on the rodent populations. The heavy grazing leads to immobilization of a large proportion of available plant nutrients, particularly P, in the rodent bodies, carcasses, and feces. The year following peak rodent abundance, plant tissue quality declines because of this immobilization together with changes in plant nutrient uptake caused by alterations in rooting depth of the graminoids as a consequence of changed depth of the active layer when a large part of the plant biomass has been removed. Due to the reduced forage quality, the rodent population densities drop and do not recover again before the immobilized nutrients are mineralized. This nutrient-driven feedback between plant nutrient content, mineralization, and rodent population density was suggested to explain the commonly observed strong cyclicity of northern populations of lemmings and voles.

However, later studies demonstrated that certain aspects of the nutrient-recovery hypothesis had to be modified (Batzli et al. 1980). Studies of rodent cycles in other arctic community types elsewhere, e.g., shrub tundras, also showed that the consumed proportion of the plant biomass was small compared to the plant-tissue types that were not consumed. These observations cast doubt on the so-called "nutrient recovery hypothesis" as an explanation for the lemming and vole cycles on a circumpolar scale (Andersson and Jonasson 1986). Nevertheless, it seems likely that rodent herbivory, when heavy, may influence the nutrient dynamics of some wetlands and may also have a significant impact on species composition of the vegetation, even when only a small portion of the total biomass or production is eaten (Jefferies et al. 1994).

Biomass and nutrient turnover

The northern wetland types occur across wide, multiple environmental gradients, e.g., in hydrology, pH, and biogeochemistry, which is reflected in different plant assemblages (Bridgham et al. 1996). For instance, wet and moist nutrient-rich sites such as riparian areas are generally dominated by deciduous Salix shrubs, geogenous fens by sedges, and ombrogenous bogs by evergreen shrubs, rushes, and Sphagnum mosses (Chapin et al. 1995). This sequence of functional plant groups also coincides with declining relative growth rates, reduced demand for soil nutrient uptake, and increased turnover time of the leaf tissue (Shaver and Chapin 1991). It can be expected, therefore, that nutrient turnover should also decline. However, recent observations, e.g., those of higher N and P mineralization rates in bogs than in fens, cited previously (see Nutrient input and transformation . . .: Leaching, litter decomposition, and mineralization, above), and studies of nutrient and biomass turnover in tundra (Shaver and Chapin 1991, Shaver et al. 1996) have shown that it is not necessarily the case. Indeed, the turnover time of both plant biomass and nutrients along gradients of soil fertility in the Arctic is surprisingly similar when calculated as the ratio of mass (biomass and/or mass of nutrients) to annual production. This is because plants with easily decomposable tissues also had a large proportion of decomposition-resistant tissues of woody stems and coarse roots or rhizomes that, for instance, made up [approximately]80% of the total biomass in sedges of wet sedge tundras. This integration across different functional plant and tissue types tends to narrow the turnover time of whole vegetation despite order-of-magnitude differences in biomass and productivity among the ecosystem types.
TABLE 1. Biomass, net primary production (NPP), and soil organic
matter (SOM) data from three low-arctic wetlands in Alaska. (Data
are from Shaver et al. [1997]).

                            Tussock      Wet sedge      Riverside
Measure                      tundra        tundra         willow

Biomass (g/[m.sup.2])(a)      462           161           833
NPP (g/[m.sup.2])(a)          118            82           175
SOM (g/[m.sup.2])           102 000        49 000        7000
Biomass/NPP                   3.9           2.0           4.8
SOM/NPP                       864           598            40

a Aboveground and belowground biomass excluding roots.


At the same time as the environment influences vegetation, the vegetation also feeds back on environmental conditions. This is perhaps most clearly demonstrated by the peat accumulation by Sphagnum that, under certain hydrological and topographical conditions, may turn mineral-influenced fens into ombrogenous bogs (Sjors 1948, Damman 1986). When this transition is completed, the mosses that lack vascular tissues are strongly dependent on supply of growth-controlling nutrients from the atmosphere (Malmer and Nihlgard 1980) and possibly on some contribution by uptake of mineralized nutrients absorbed by their stems in the surface peat (Rydin and Clymo 1989). By contrast, the vascular plants are able to absorb nutrients by their roots from the aerated surface peat (acrotelm) and are probably more dependent on the cycling of nutrients through the soil-decomposer system. Hence, different functional plant groups making up the plant community may be differently dependent on nutrients transported to and nutrients cycled within the ecosystem (Bridgham et al. 1996).

The accumulation of peat in ombrogenous bogs (Clymo 1984) and of organic matter in geogenous wetlands (Shaver et al. 1997) is determined mainly by the decay rate and less by the productivity. Data from a range of arctic wetlands (Table 1) show that the proportion of the ecosystem soil organic matter (SOM) compared to plant biomass and annual biomass production increases steeply when the soil is periodically waterlogged. In the most extreme cases (a moist tussock tundra with similar species composition as bogs, and a wet sedge meadow) the plant biomass and plant nutrient mass made up [less than] 1% of the soil-plus-vegetation pool (Shaver et al. 1997), which is similar to figures of the ratios in the upper 30 cm of the acrotelm of a subarctic mire (Jonasson and Michelsen 1996). By contrast, a willow scrub, although with high soil water content, but well drained, had [greater than] 10% of the organic matter in the phytomass. In the wet sedge tundra with a 40-cm-deep organic horizon, the turnover time of the organic matter was [approximately]600 yr when calculated roughly as the ratio of plant-plus-soil-mass matter to annual primary production (Table 1), i.e., neglecting that the organic horizon probably contained pools of differently decomposable organic matter. The organic matter in the moist tussock tundra with a 30-cm-deep organic horizon had a turnover time of 860 yr, contrasting with a turnover time of [less than]50 yr in the riparian riverside Salix-dominated system with a few centimeters of organic matter. Hence, variation in turnover times of biomass and nutrients in the vegetation is uncorrelated with variation in turnover times of SOM and there is no correlation between vegetation productivity and the amount of SOM.

CONCLUSIONS

In general, it appears that organic-matter accumulation in northern wetlands is regulated by hydrological conditions and soil temperature. Hence, different characteristics at the stand or vegetation levels are relatively unimportant for the accumulation and turnover of soil organic matter. Instead it seems that characteristics of the plants (nutrient resorption, tissue type and longevity) mirror the functioning of the system rather than play a major role in regulating overall element cycling. However, this compilation of research in northern wetlands has revealed several uncertainties in the detailed function of the ecosystems of which we highlight the following.

1) The generally held notion that both decomposition and nutrient (P and N) mineralization rates decline from fens to bogs, coincident with a decline of tissue nutrient concentrations, is not agreed upon as a general pattern. At least in some cases it appears to be an inverse relationship of decreasing decomposition rates but increasing net mineralization rates, which is poorly understood.

2) The role of microbial P and N mobilization and immobilization is poorly explored, particularly in the presumably most nutrient-deficient ecosystem types. There is a divergence between measurements that have shown extremely high microbial immobilization and hypotheses of low potential for microbial nutrient immobilization due to, e.g., shortage of a labile C source for the microbes. Furthermore, there are uncertainties about the ability of wetland plants to compete with soil microbes for inorganic nutrients.

3) The recent observations that many wetland plants, or entire functional plant groups, can utilize organic N sources by direct uptake or indirectly through mycorrhiza are still poorly explored. Indeed, high capacity for organic N uptake may change the picture of plant N availability and may also explain plant distribution patterns.

4) The divergent evidence presented for and against the notion that nutrient resorption in many wetland plants, or in plant functional groups, is an adaptation to low nutrient availability is still unresolved. This question may be resolved by re-examination of data using nutrient proficiency rather than nutrient-resorption efficiency as a basis for inference about possible adaptations. Indeed, the low turnover rate of individuals in many wetlands with low nutrient levels due to high abundance of clonal, adult plants suggests that nutrient losses at the stand level are lower than in systems with higher turnover rates of individuals and with larger proportions of nutrient-accumulating juveniles.

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