SCOPE 21 - The Major Biogeochemical Cycles and Their Interactions, Chapter06, Interactions of Biogeochemical Cycles in Forest Ecosystems

This paper presents four topics in the study of interactions among carbon, nitrogen, phosphorus, and sulphur in forest ecosystems. In section 6.2, we consider element ratios in foliage and litter, and discuss what these ratios imply about the availability of nutrients to higher plants and the efficiency of nutrient-use by plants. The carbon to nitrogen ratio in litter varies inversely with the mass of nitrogen in the litter across a broad range of forest types. A qualitatively similar pattern is described for phosphorus. From extant data we conclude that a high carbon to nutrient ratio in litter is characteristic of an efficient use of the nutrient under consideration, with translocation of nutrients out of senescing tissue contributing to this efficiency. We also conclude that the efficiency of nutrient use is inversely related to the availability or rate of circulation of that nutrient.

In Section 6.3, we review the ways in which plant nutrient status can influence the amount of carbon flowing through an ecosystem, the pathways of flow, and the proximate fate of the carbon. We develop the argument that net carbon storage in forest ecosystems is determined by the balance among three distinct processes: (1) the net amount of carbon fixed by the vegetation (i.e. carbon fixed in excess of plant respiratory demand); (2) the relative amounts of this fixed carbon allocated to vegetation growth increment versus plant litter; and (3) the decomposition dynamics of carbon compounds entering the soil system. This argument has several implications for the study of the global carbon budget. First, to determine whether or not elevated atmospheric levels of CO₂ will enhance carbon storage rate in terrestrial ecosystems, it is insufficient to consider only the relationship between CO₂ concentration and photosynthetic rate. The subsequent fate of the fixed carbon must be considered. Second, the chronic low level additions of fertilizer to forests, such as is occuring through air pollution and subsequent rain-out may be: (1) enhancing overall carbon storage in ecosystems; and (2) shifting a larger fraction of the annual carbon storage to the vegetation component of the system.

We explore how man's impact on the global cycles of nitrogen, phosphorus, and sulphur may influence the ability of forest ecosystems to store carbon in Section 6.4. Man may be inadervertently fertilizing the world's forests with 6 Tg N through the burning of fossil fuels. We estimate that the maximum amount of additional carbon storage that could be promoted by a nitrogen fertilization of this magnitude is 300 Tg C/yr.

In section 6.5, we evaluate the possibility that the terrestrial biosphere is on a carbon accumulation trend that is dependent on the dynamics of phosphorus availability during soil development and that is independent of the activities of man. We estimate that on an annual basis only a small amount of carbon, in the range of 79 Tg C, could be stored by this mechanism.

6.1 INTRODUCTION

The forests and woodlands of the world occupy between 50 x 10¹² and 60 x 10¹² m² or slightly more than one-third of the earth's land area (Whittaker and Likens, 1973), and they contain major fractions of the terrestrial stocks of C, N, S, and P. During the past two decades, studies of the fluxes of elements among the structural components of forests have intensified. Today, carbon and nitrogen budgets are available for a variety of forest ecosystems, although most are incomplete; sulphur and phosphorus budgets are much less common and they are fragmentary. However, as the work proceeds, we are beginning to recognize that an understanding of the mechanisms that control cycling rates of an element requires consideration of element interactions.

Element interactions fall into two general categories; carbon-nutrient interactions, and nutrient-nutrient interactions. An example of a carbon-nutrient interaction is the stimulation of net primary productivity in a forest by added nitrogen (Miller and Miller, 1976). An example of a nutrient-nutrient interaction is the stimulation of nitrogen fixation by the addition of phosphorus (Griffith, 1978). Carbon-nutrient interactions are the central concern of this paper.

This paper presents four topics in the study of interactions among carbon, nitrogen, phosphorus, and sulphur in forest ecosystems. First, we consider element ratios in foliage and litter, and discuss what these ratios imply about the availability of nutrients to higher plants and the efficiency of nutrient use by the plants. Second, we review the ways in which plant nutrient status can influence the amount of carbon flowing through an ecosystem, the pathways of flow, and the proximate fate of the carbon. Third, we explore how man's impact on the global cycles of nitrogen, phosphorus, and sulphur may influence the ability of forest ecosystems to store carbon. And fourth, we evaluate the possibility that the terrestrial biosphere is on a carbon accumulation trend that is dependent on the dynamics of phosphorus availability during soil development and that is independent of the activities of man. J. R. Gosz is the principle author of section 6.2, and J. M. Melillo is the principle author of sections 6.3

6.5.

6.2 ELEMENT RATIOS IN FOLIAGE AND LITTER

Uptake of a nutrient is reflected in the amounts accumulated in plant tissues, and so nutrient concentrations and ratios in plant tissues have long been of interest to scientists concerned with mineral nutrition of higher plants. Nutrient concentrations in the green foliage of a tree species can vary from site to site because of different supplies of individual nutrients at the sites, and these variations are usually reflected in nutrient concentrations in leaf litter. In this section of the paper we consider some of the recent analyses relating variations in element concentrations and ratios in green foliage and leaf litter to nutrient availabilities in forests. This information relates to the uptake and return portions of the biogeochemical cycles.

The demand for nitrogen is closely related to tree growth, and nitrogen deficiency is, after water stress, the most frequently reported limitation to growth (Kozlowski, 1971; Kramer and Kozlowski, 1979). Phosphorus, like nitrogen, is in short supply in forest ecosystems in many parts of the world and the roles of phosphorus and nitrogen in plant metabolism are clearly interrelated in a number of ways (Loveless, 1962). Sulphur is primarily a constituent of amino acids and proteins. The stoichiometry between nitrogen and sulphur is fairly constant, indicating that on the average there are 36 atoms of nitrogen for each atom of sulphur in proteins. The ratio of total nitrogen to total sulphur in plants is close to this value under conditions where there is no luxury consumption of either element (Epstein, 1972).

Although the requirement for these elements in various organic compounds would suggest rather constant element ratios in green tissues, the ratios may vary considerably because of different supplies of individual nutrients. Each of the above nutrients has been shown to be taken up in excess (i.e. luxury consumption) and stored. Slowly growing species that absorb nutrients in excess of immediate growth requirements during times of high nutrient availability may use these reserves to support growth after soil reserves are exhausted (Chapin, 1980). The nutrients available for plant uptake may be present in ratios much different from those needed by plants. As many studies have shown, nitrogen can be taken up in excess and stored as amino acids, for example, arginine (Barnes and Bengtson, 1968; Kramer and Kozlowski, 1979). The absorption of sulphate from excess supply may be faster than its reduction and assimilation of the sulphur atoms into organic compounds. Thus, an appreciable fraction of total sulphur in plants may be in the form of sulphate (Epstein, 1972; Turner et al., 1980). Although phosphorus is absorbed as a complex anion like its nitrogen and sulphur counterparts (i.e. nitrate, sulphate), the phosphorus atom of phosphate is not reduced in the cell to a lower oxidation state (Epstein, 1972). In mature plants, phosphorus is temporarily stored as phosphate while seasonal storage may occur as phospholipids, nucleic acids, and other complex organic compounds. Luxury consumption and maintenance of inorganic phosphorus reserves by slowly growing species from infertile habitats are responsible for the high proportion of inorganic phosphorus and low proportion of structurally bound phosphorus characteristic of these species (Chapin, 1980).

Although concentration in foliage is commonly used to identify nutrient deficiencies and imbalances, variations in nutrient ratios have also been found useful. For example, conifers have total foliar nitrogen very nearly equal to organic foliar nitrogen. However, any sulphur in excess of that required to balance the nitrogen in protein formation is accumulated as sulphate-sulphur. Foliar sulphate-sulphur is low when sulphur is deficient and nitrogen is adequate, and sulphate-sulphur is high when sulphur is abundant and nitrogen is deficient. Turner et al. (1980) demonstrated that on nitrogen-deficient sites, additions of nitrogen resulted in the incorporation of sulphate-sulphur into organic forms. Thus, while the cycles of organic nitrogen and organic sulphur are closely coupled, excess sulphur can cycle as sulphate and operate somewhat independently of the nitrogen or carbon cycles (Turner et al., 1980). Some plants accumulate inorganic nitrogen (e.g., nitrate) and phosphate during conditions of excess supply (Dijkshoorn and Van Wijk, 1967), and therefore, these elements also can be expected to cycle independently. Relatively large differences in total nitrogen to total phosphorus ratios in tissue occur for various ecosystems, suggesting different cycling rates. Cole and Rapp (1980) report nitrogen to phosphorus ratios in uptake ranging from about 4:1 to 17:1 and 11:1 to 22:1 for 13 temperate conifer and 14 temperate deciduous forests, respectively. The nitrogen: phosphorus ratios for the requirements of these forests ranged from 5:1 to 16:1 and 8:1 to 19:1, respectively. The range of phosphorus uptake values was larger than the range of nitrogen uptake values, indicating that phosphorus availability may have caused most of the variation in the ratios.

Very low uptake rates of an element in relation to demand by current growth results in efficient conservation and re-use of that element within the tree. Translocation of nutrients within the individual is an important mechanism for this efficiency. In much the same way that translocation of carbohydrates and their partitioning are controlled by the size of the food supply and relative sizes of various sinks, we suggest the translocation of nutrient elements is controlled by strength of the sink (i.e. demand) and magnitude of the source (i.e. supply). During the height of the growing season the relative strengths of the various sinks are: fruits and seeds > young leaves and stem tips > mature leaves > cambia > roots > storage (Kramer and Kozlowski, 1979). Relative distance from source to sink is also important, because sinks are supplied from the nearest source. Due to the asynchrony of growth of different plant parts, the same nutrient capital can serve several functions during the growing season. Tissues with an imbalance of nutrients such as an excess of sulphur and deficiency of nitrogen will have proportionately more of the nitrogen translocated (Turner et al., 1980). Nutrients in excess can be transported to storage areas. For example, leaves with high concentrations of nitrogen and phosphorus have a larger percentage of soluble and inorganic forms and may actually retranslocate a larger total quantity of nitrogen and phosphorus from leaves than would occur in leaves with nutrient deficiencies (Chapin, 1980). The most deficient element may possibly be transported to stronger sinks while storage, being a weaker sink, may draw a larger proportion of elements in excess. The true measure of the efficiency of this internal cycle may not be the total quantity translocated, but the ability to withdraw nutrients, leaving very low levels in senescing tissues. Thus, the percentage translocation may not be as important as the level to which the nutrient concentration can be decreased. A better measure of efficiency may be the quantity translocated divided by the amount remaining.

If there are ample soil supplies of a nutrient element, then less demand is put on the internal cycle and greater quantities may remain to accumulate in tissues as they age; an accumulation that is eventually reflected in higher nutrient concentrations in litterfall. This has been demonstrated in a number of fertilization studies (Barnes and Bengston, 1968; Miller et al., 1979; Turner et al., 1980). Similarly, studies that have decreased availability, and hence uptake, by practices such as sugar

sawdust application, caused increased translocation efficiency in senescing tissues and decreased nutrient levels in leaching and litterfall (Turner, 1977; Turner et al., 1980). This also has been demonstrated across gradients of nutrient availability within natural stands. Sites with low nutrient availability have individuals and species that translocate proportionately more out of leaves before leaf fall than do the species on sites with abundant nutrients (Lamb, 1975; Stachurski and Zimka, 1975; Zimka and Stachurski, 1976). The relatively high concentrations of nutrients left in senescing leaves on nutrient-rich sites speed the decomposition and mineralization processes that enhance the high availability (Gosz, 1981). Figure 6.1 presents data for six communities showing a very good relationship between k values for nitrogen in leaf litter, a measure of the decomposition and release of this element, and percentage retranslocation out of leaves during senescence (Zimka and Stachurski, 1976).

Figure 6.1 The relationship between percent leaf nitrogen translocated prior to leaf abcission and the decay rate (k) for nitrogen in the litter for six forest ecosystems along a nutrient availability gradient in Poland (constructed from data of Zimka and Stachurski, 1976, and Stachurski and Zimka, 1975)

While many studies have demonstrated a reduction in nutrient concentrations between green and senescent tissues, Chapin (1980) reports that the limited evidence available does not confirm that species adapted to infertile soils are particularly effective in retranslocating nutrients prior to leaf abscission. Much more work is necessary in this important area.

In an attempt to determine whether nutrient cycling and nutrient use efficiency vary with forest type, we analysed 102 data sets taken from boreal to tropical sites in the northern and southern hemispheres for nutrients in litterfall. The quantity of a nutrient in litterfall is a measure of nutrient circulation (Gosz, 1981; Vitousek et al., 1982), particularly for nutrients such as nitrogen and phosphorus that are lost from the plant primarily through litterfall (Cole and Rapp, 1980). Vitousek (1982) suggested two extreme hypotheses to aid the interpretation of patterns of nutrient use efficiency in litterfall. One is that the efficiency of nutrient use, as measured by the amount of organic matter discarded in litter per unit of N, is constant for any level of nutrient supply and circulation; the concentration of a nutrient in litterfall would then be constant. The variable nutrient concentrations in litter prove this hypothesis false. Alternatively, it could be hypothesized that nutrient circulation is unrelated to litterfall mass. Litterfall mass would vary independently or randomly from nutrient circulation. If this were true then a plot of the carbon:nutrient ratio of litterfall versus the nutrient content of litterfall would result in a random scatter of points with an upper limit of the form Y = 1/X (Figure 6.2). The upper limit is a result of autocorrelation; the X-axis values are used in the calculation of Y-axis values (Vitousek, 1982).

Figure 6.2 The relationship between the amount of nitrogen in litterfall and the carbon:nitrogen ratio of that litterfall. Data from 102 forest sites world-wide (T-tropical, D-deciduous, C-conifer, E-Eucalyptus). The dashed line is the upper limit for the relationship for randomly generated data. See text for explanation

In Figure 6.2 we have plotted carbon:nitrogen ratio versus nitrogen content of litterfall for tropical hardwood, temperate conifer, temperate deciduous, Eucalyptus (Australia), and Nothofagus (New Zealand) forests. The overall plot reveals a strong inverse relationship between carbon:nitrogen ratio and the mass of nitrogen in litterfall. This inverse relationship differs from one generated with random data by being more confined (less variation) and having a steeper logarithmic function.

An analysis by vegetation types shows that the relationship between carbon:nitrogen ratio and nitrogen in litterfall varies markedly. Regression coefficients for these communities were significantly different (P < 0.05) from coefficients of randomly generated data. Tropical vegetation has a very high litter nitrogen content and, although the slope of the regression lines is significantly different from 0 (P < 0.05), it is the closest to a horizontal line (i.e. the hypothesis stating that the efficiency of nitrogen use is unchanged at different rates of nitrogen circulation). The higher nitrogen levels in litter suggest nitrogen circulation is always high, however. One interpretation is that nitrogen is in excess in these forests with respect to other elements and may be cycling somewhat independently.

The regression for temperate deciduous forests has a slope somewhat greater than that for the tropics and differs primarily in the lower nitrogen content of the litter. These two vegetation types seem to comprise a continuum across a large portion of the range of nitrogen contents of litterfall.

Conifer forests show a marked increase in slope, and have some of the lowest litter nitrogen contents. The evergreen Nothofagus forests of New Zealand show similar plots. The conifer vegetation type shows a curvilinear relationship (Figure 6.2) and may be divided into two parts; more than or less than 3 g m^-2yr^-1 nitrogen in litterfall. Forests with nitrogen masses of less than 3 g m^-2yr^-1 in litter have an almost vertical slope for their plots. For forests with nitrogen values greater than 3 g m^-2yr^-1, the plots are similar to deciduous forest plots. Interestingly, these sites are 20

33 year-old plantations of various conifer species on former hardwood sites (Gloaguen and Touffet, 1976). Vitousek (1982) also reports a high nitrogen content in the litter of a balsam fir forest in New Hampshire. However, this native conifer forest is nitrogen-rich perhaps because of high nitrogen inputs in acid precipitation. The Eucalyptus forests of Australia also plot along a steep slope (P < 0.05, Figure 6.2) showing a strong relationship between nitrogen circulation and litterfall carbon to nitrogen ratio.

The data of Figure 6.2 are based on annual litterfall measurements. A comparison of tropical forests with temperate forests on an annual basis may not be appropriate because decomposition rates are so rapid in the tropics. With litter decomposing in a matter of months, a pool of high available ntirogen may be circulated several times in the course of a year. Assuming that the nitrogen pool was used three times per year (i.e. nitrogen content of litter/3) would increase the carbon:nitrogen ratio of annual litterfall by a factor of three. A plot of such data would result in a steep slope more similar to those of conifer and Eucalyptus communities. These data suggest a much more efficient use of nitrogen at the ecosystem level in the tropics than annual litterfall nitrogen values indicate. The resolution of this difference is an important research objective.

Figure 6.3 The relationship between the amount of phosphorus in litterfall and the carbon: phosphorus ratio of that litterfall. Data from 102 forest sites world-wide (T-tropical, D-deciduous, C-conifer, E-Eucalyptus)

Although the data of Figure 6.2 indicate that tropical forests have high nitrogen levels in litterfall, this is not the case for all tropical forests. Many areas in the tropics (e.g., certain parts of Venezuela and Brazil) are nutrient-poor and have lower nitrogen levels in litterfall (R. Herrera, personal communication). These sites plot with the conifer forests in Figure 6.2. Similarly, conifer and deciduous forests can have high nitrogen levels in litterfall and plot more like tropical sites.

The results for phosphorus (Figure 6.3) differ somewhat from those for nitrogen in that there are steeper slopes for tropical and Eucalyptus forests, while slopes for conifer and deciduous forests are similar. Also, the range of phosphorus in tropical litterfall is very large. The data for Eucalyptus forests give a plot that is nearly a vertical line; a situation where phosphorus circulation is low and almost constant. This is of interest because of the marked phosphorus deficiency cited for most of Australia (Loveless, 1962). The results for conifer, Nothofagus, and deciduous forests are less obvious and although they have similar and significant regression lines (P < 0.05), the scatter of points is appreciable.

Figure 6.4 The relationship between the amount of phosphorus in litterfall and the nitrogen: phosphorus ratio of that litterfall. Data from 102 forest sites world-wide

The relationship between nitrogen and phosphorus in litterfall appears different for different forests. In Figure 6.4 we have plotted nitrogen:phosphorus ratios versus the phosphorus content of litterfall. A highly significant relationship exists for the tropical forests (P < 0.001). The tropical forests are normally described as nitrogen-rich forests, as can be seen from Figure 6.2. The major factor in the relationship seems to be the quantity of phosphorus in litter, with the range of phosphorus values almost four times the range of nitrogen values (Figure 6.5). High phosphorus in litter reduces the nitrogen to phosphorus ratio in litter and low phosphorus increases the ratio. This suggests that nitrogen acts like an element in excess (i.e. the efficiency of nutrient use is unchanged at various levels of nutrient circulation) while phosphorus use efficiency is more strongly related to phosphorus circulation. The relationship for conifers also is statistically significant (P < 0.05), although the scatter of points is appreciable. The other vegetation types did not have significant relationships.

Figure 6.5 The relationship between the phosphorus and nitrogen concentrations in litterfall. Data from 102 forest sites world-wide

The relatively strong relationships between carbon and nutrients (Figures 6.2, 6.3) and the lack of a relationship between nutrients (Figures 6.4, 6.5) for most forests again indicate the nutrient use efficiency of one nutrient is somewhat independent of that for another nutrient. Unfortunately, little data are available for sulphur, preventing us from testing this result with other nutrient combinations.

If correct, these data support our previous discussions that the efficiency of nutrient use is inversely related to the availability or rate of circulation of that nutrient. At high levels of availability, the mass of litterfall (a measure of productivity) is not related to levels of the nutrient in litterfall. At lower nutrient levels, the carbon to nutrient ratio in litterfall is markedly influenced and the efficiency of use of the nutrient increases. This also agrees with previous discussions that the requirement for this nutrient causes strong sinks and translocation out of senescent tissues, resulting in high carbon to nutrient ratios in litterfall. At very low nutrient levels (nutrient deficiency) litterfall mass again appears unrelated to the nutrient content of litterfall. It is as if there is a minimum level to which the nutrient content of litterfall can be reduced despite a strong sink effect and effective translocation.

Figure 6.6 The relationship between phosphorus content of litterfall and the fibre:protein ratio of that litterfall (data of Loveless, 1962)

A high carbon to nutrient ratio or high litterfall mass with low nutrient content can be described as an efficient use of the nutrient (i.e. high litter production per unit of nutrient (Vitousek, 1982)). Translocation of nutrients out of senescing tissue would contribute to this efficiency, although the extremely high carbon to nutrient ratios in litter of some conifer and Eucalyptus forests suggest other physiological processes are involved. Loveless (1962) proposed that sclerophylly was related to nutrient availability. Sclerophyllous leaves have a high fibre:protein ratio caused by reductions in protein content and concomitant increases in fibre (cellulose, lignin). A plot of fibre to protein versus phosphorus concentration is suggestive of a limiting factor curve (Loveless, 1962); that is, the fibre:protein ratio decreases with increased phosphorus content up to a certain level (i.e. 0.3%) above which increased phosphorus content does not result in a further proportional decrease in the fibre to protein ratio (Figure 6.6). The roles of phosphorus and nitrogen in plant metabolism are interrelated in many ways and both are essential for protein synthesis. Thus, lowered protein levels could be a result of either low nitrogen or low phosphorus content. Furthermore, it is reasonable to expect that the intermediate products of metabolism that otherwise might have formed protein should, in the absence of either adequate phosphorus or nitrogen, be diverted along alternative metabolic pathways to form other end-products, including fibre (Loveless, 1962; Neish, 1964; Gosz, 1981).

Gnanam et al. (1980) proposed a mechanism of action for ammonium in regulating the photosynthetic carbon flow. In this scheme ammonium ions seem to regulate the photosynthetic carbon flow by abolishing the light activation of the enzymes that would normally favour the flow of carbon toward sugar biosynthesis, thereby facilitating the increased synthesis of amino acids.

These results suggest that in addition to translocation of scarce nutrients from senescing tissues to other sinks within the plant, tissue chemistry in nutrient deficient sites also is different. For nutrient deficient sites, the diversion of proportionately more carbon into fibrous material along with a more complete removal of nutrients by translocation may account for the very high carbon to nutrient ratios in litterfall.

Several conclusions can be drawn from an analysis of element ratios in foliage and litter:

6.3 CARBON

NUTRIENT INTERACTIONS AT THE ECOSYSTEM LEVEL

Net carbon storage in forest ecosystems is determined by the balance among three distinct processes: (1) the net amount of carbon fixed by the vegetation (i.e. carbon fixed in excess of plant respiratory demand); (2) the relative amounts of this fixed carbon allocated to vegetation growth increment versus plant litter; and (3) the decomposition of carbon compounds entering the soil system. All three of these processes are regulated by temperature, moisture and the availability of key nutrients such as nitrogen, phosphorus, and sulphur. Light and carbon dioxide concentration of the atmosphere serve as additional regulating factors on the process of carbon fixation by vegetation.

The primary objective of this section is to examine how the cycles of nutrients are linked to both the paths of carbon transfer and the amounts of carbon storage in forest ecosystems. We present a simple model (summarized in Figure 6.7) that we use to identify the linkages between carbon and nutrient dynamics in forests. Our analysis suggests that the nutrient dynamics of a system can control the amount of carbon that moves through a system, the pathways of its movement, the amount of carbon accumulated in the system, and the distribution of the accumulated carbon in the system. We envision a series of switches in the carbon flow pathway, which are in part under the control of the nutrient status of the plants in a system.

Photosynthesis and net primary production (net dry matter production by green plants) are distinct components of the carbon budget of a forest ecosystem. Carbon flux through a forest begins with photosynthesis, or the conversion of CO₂ to organic carbon compounds. Some fraction of the total photosynthate is consumed in plant respiration, with the carbon returned to the atmosphere as C0₂. The remainder of the photosynthate is used to build plant tissues (e.g. leaves, stems, roots) and soluble organic compounds (e.g. root exudates). The tissues and soluble compounds produced during the course of a year comprise the system's annual net primary production.

Plant nutrient status along with light, temperature, and water availability are important controlling parameters for photosynthetic rate. Several comprehensive reviews document the relationship between leaf nutrient status and photosynthetic rate (e.g. Keller, 1967; Natr 1972, 1975). According to these reviews, nitrogen occupies a special place among nutrients involved in photosynthesis. One generalization that emerges is that a quantitative relationship exists between rate of photosynthesis and nitrogen content of leaves. Photosynthetic capacity often increases linearly with increases in leaf nitrogen concentration if light, water and other nutrients are not limiting. This relationship is well documented for crop plants and non-woody wild plants (Natr, 1975), and for both deciduous (Keller, 1960) and coniferous (Keller, 1971) tree species.

The nutrient status of plant parts other than leaves also influences photosynthetic rate through complex source-sink control mechanisms (Wareing and Patrick, 1975). Under conditions where the potential rate of carbon fixation in the leaves exceeds the rate of carbon consumption throughout the rest of the plant, there is a feedback mechanism whereby the rate of assimilation is regulated to meet demand. The demand for carbon by various plant parts is, in turn, related to their nutrient status. For example, nitrogen deficiency limits the formation of new tissue and thus the demand for photosynthate (Kramer, 1981).

By influencing a plant's demand for photosynthate, plant nutrient status exerts an influence on the ability of a plant to respond to elevated levels of CO₂. Working with tobacco plants, Raper and Peedin (1978) reported a close relationship between nitrogen supply and the ability of the plants to respond to enhanced CO₂ levels. During a 35 day study, tobacco plants growing at `low' levels of nitrogen supply in CO₂ concentrations of both 400 ppm and 1000 ppm had per plant photosynthetic rates that were only 60 percent of the photosynthetic rates exhibited by tobacco plants growing at `high' levels of nitrogen supply in the same two CO₂ concentrations. Other nutrients besides nitrogen can also influence photosynthetic rates. Sulphur deficiency prevented photosynthesis of sugar beet from responding to an increase in CO₂ concentration (Thomas and Hill, 1949). Unfortunately, no studies have been conducted to examine the relationship between the nutrient status of forest trees and their ability to respond to elevated levels of CO₂. Such studies are important for our understanding of the carbon flux through forest ecosystems and the role of forest vegetation in the global carbon budget.

B. Partitioning of Total Photosynthate between Respiration and Net Primary Production

All biomass production ultimately depends on photosynthesis. This fact does not imply that the rate or extent of net primary production bears a close relationship to the photosynthetic rate, or is determined by it. The processes that follow photosynthesis, such as respiration, can be major determinants of productivity. The loss of photosynthate by dark respiration can be substantial, particularly in communities having a large biomass, and growing under high temperatures. In the massive forests of southern Thailand, for example, Kira (1975) estimates that about three-quarters of the carbon assimilated in photosynthesis is lost by dark respiration.

The partitioning of the total photosynthate between respiration and net primary productivity is controlled by a variety of factors. In non-woody plants there is some evidence that plant nutrient status is in part responsible for determining the fate of photosynthate. Based on work with the grassland species Plantago lanceolate, Lambers et al. (1981) have suggested the existence of an overflow metabolism or SHAM (salicylhydroxamic acid) pathway in roots of plants growing in environments with fluctuating nutrient availabilities. In such environments, plants may maintain sink strength in leaves that allows high rates of photosynthesis. To maintain photosynthate demand in leaves, which have limited carbon storage capacity, the fixed carbon is transported to other plant parts such as the roots. At times of high nutrient availability, and thus high nutrient status throughout the plant, there will be high demand for the photosynthate and it will be incorporated into plant tissues and become part of the net primary production of the system. At times of low nutrient availability and thus low nutrient status throughout the plant, there will be low demand for the photosynthate and it will be respired via the SHAM pathway.

The importance of the SHAM pathway and other biochemical pathways for wasteful oxidation (Solomos, 1977) has not been established for forest tree species. Both woody and non-woody plants certainly have other strategies for photosynthate management in environments of fluctuating nutrient availability. As mentioned in the previous section, the capacity of a plant to engage in luxury consumption of nutrients may be an important mechanism for dealing with the asynchronies that often exist between nutrient availability and carbon fixation.

The relative distribution of plant carbon between above-ground parts (shoots) and below-ground parts (roots) is closely related to plant nutrient status, which in turn reflects soil nutrient availability (cf. Figure 6.7). Shoot:root ratios of both deciduous and coniferous tree species tend to be lower in infertile habitats than in fertile habitats (Yen et al., 1978; Grier et al., 1980; Keyes and Grier, 1981).

The initial response of forest trees to improved soil nutrient availability, and thus plant nutrient status, seems to be an increase in the relative amount of annual net primary production allocated to roots (Safford, 1974; Miller and Miller, 1976; Brix and Mitchell, 1980). The enhanced root growth presumably increases uptake of both water and nutrients and permits increased above-ground growth.

Above-ground growth response to fertilization appears to be closely related to increases in leaf area. Brix and Ebell (1969) reported that the only above-ground plant factor associated with increased diameter growth of a 20-year-old Douglas fir stand fertilized with nitrogen was increased leaf area. In a subsequent experiment on Douglas fir, Brix (1971) found that, although rates of photosynthesis and dark respiration increased after nitrogen fertilization, most of the increase in diameter growth was caused by the increase in leaf area. Fertilization was most effective in open stands where the leaf area was below the optimum and water supply was not limiting. Tamm (1979) also reported that the close correlation between leaf area and stem growth observed in young conifer stands decreased as the stands closed and shading effects increased in importance.

Figure 6.7 Model describing the interaction between the nutrient and carbon budgets of forest ecosystems. Ä Symbols indicate switches in the carbon budget that can be influenced by the nutrient status of the plants or nutrient availability in the system

In closed canopy stands, fertilization may affect stand composition more than it affects overall stand growth. The larger trees in the stand will often accumulate nutrients more rapidly than smaller trees, with the result being more rapid growth of the larger trees. This causes the loss of lower crown classes from the stand, but the rapid growth of the dominant trees maintains the stand's leaf area and sapwood cross-sectional area (Jarvis, 1975). However, increases in sapwood cross-sectional area are not always related in a simple way to biomass increment. For example, Brix and Ebell (1969) reported that the effect of nitrogen fertilization on dry matter production in Douglas fir is lower than it is on volume increment, since the specific gravity of treated trees consistently decreased after fertilization and was 12 percent lower than that of the controls.

The carbon component of net primary production in forest ecosystems can have three fates: (1) it can be allocated to perennial parts and become incorporated into the vegetation's growth increment (the vegetation increment of net ecosystem production); (2) it can be transferred from the vegetation to the soil in plant parts as litter; and (3) it can be transferred from the vegetation to the soil as soluble organic compounds that are leached from above-ground plant parts or exuded from roots.

The evidence to date suggests that soluble carbon transfer to the soil in leachates and exudates is a small part of the carbon component of net ecosystem production in forests (e.g. Gosz et al., 1976). And at this time it is not clear how plant nutrient status affects the relative magnitude of this transfer.

As an aside, it is interesting to note that in plants with very limited storage capacity, the management of photosynthate during periods of low nutrient availability involves the exudation of photosynthate. This is evident, for example, in some communities of algae growing in oligotrophic waters (Fogg, 1975). For many of these algae, growth is limited to such an extent by nutrient supply that they cannot use most of their photosynthate and may excrete up to 90% of it. At first glance, this means of managing excess photosynthate would seem to further lower nutrient availability by promoting blooms of micro-organisms that have nutrient demands. If nitrogen is the limiting nutrient, as it may be in some river waters, the excretion of simple carbon compounds by algae may promote nitrogen fixation by micro-organisms, thus aleviating some of the nutrient stress. An analogue of this scenario may be occurring in forest ecosystems. Trees growing in nitrogen-poor soils may promote nitrogen fixation by micro-organisms in the root zone by allocating a larger percentage of their photosynthate to root exudation than trees growing on nitrogen-rich soils. There is some evidence that this may be occurring in dwarf willows in Alaska, with mycorrhiza acting as intermediates in the process (Linkins, personal communication). Mycorrhizal fungi associated with the dwarf willows can convert the sucrose they receive from the willows to mannitol, some fraction of which is then exuded from the mycorrhizae into the soil. Since mannitol is a preferred carbon form for free living nitrogen-fixers, the allocation of photosynthate to the root-mycorrhizal complex of plants growing in nitrogen-poor sites can promote fixation.

Turning now to a consideration of the major fates of the carbon component of net primary production, we ask the following question: Does the nutrient status of the trees in a forest influence the relative distribution of net primary production between litter and the vegetation growth increment? Studies relevant to this question are few. One of the most useful is the work of Turner (1977) on the effects of nitrogen availability on nitrogen cycling in a Douglas fir stand. Turner created a gradient of nitrogen availabilities in a 50-year old Douglas fir stand in Washington State, U.S.A. The annual net primary production was highest in fertilized sites and lowest in the site where nitrogen availability was lowered relative to the control by the additions of carbohydrate to the soil, which promoted microbial immobilization of nitrogen. In the first year of the study, trees growing in high nitrogen availability sites allocated a smaller percentage of their net primary production to litter than to growth increment compared to trees growing in the control and nutrient stressed sites (Table 6.1). Part of this response is associated with the fact that fertilization increases leaf longevity of conifers in the first year of application (Miller et al. 1976, Chapin 1980). The relative distribution of the net primary production among stem increment, branch increment, and new foliage production was similar in the control and fertilized trees. In the stressed trees, the relative distribution of the net primary production was similar to that of the others for branch increment and new foliage production, but substantially less than the others for stem increment (Table 6.1). These data suggest that the relative amount of net primary production allocated to stem growth is variable under nutrient stress conditions in the Douglas fir.

From a study of the effect of nitrogen supply on net primary production in Corsican pine, Miller and Miller (1976) reported that repeated fertilization over a 3-year period: (1) increased the amount of net primary production substantially; and (2) reduced the relative amount of net primary production allocated to litter (Table 6.2). In fertilized trees the relative allocation of net primary production to new foliage production, stem increment, and root growth generally increased compared to non-fertilized trees.

In section 6.2, we suggested that litter quality is related to the nutrient status of the plant. We argued that nutrient stressed plants retranslocate large amounts of nutrients into woody parts before leaf fall, thus lowering the nutrient content of the litter. Also, plants growing on nutrient-poor sites contain a larger proportion of complex carbon compounds (e.g., lignin and polyphenols) in their litter than plants growing on nutrient-rich sites (Loveless, 1962; Davies et al., 1964 a, b; Lamb, 1976; Gosz, 1981). We will now present evidence that litter quality can affect both the decomposition rate of fresh litter and the relative amount of that litter that is ultimately transformed to meta-stable `humus'.

Table 6.1 Net primary production rates and allocation of net primary production in treated and control Douglas-fir forests (calculated from Turner, 1977)

Table 6.2 Net primary production rates and allocation of net primary production rates in fertilized and control Corsican pine forests (Miller and Miller, 1976)

Treatment

8.4

16.8

33.6

50.4

(g N m^-2yr^-1

Net Primary Production*

560

845

930

935

950

(g C m^-2yr^-1)

Allocation of NPP

(percentage)

Foliage

Live Branches and twigs

Dead Branches

Stem Wood

Stem Bark

Root System

Litterfall

*Carbon calculated as 50% of dry matter.

Little quality, as defined by chemical composition of the material, has long been considered a critical factor in determining rate of decay (Waksman and Tenney, 1927). Chemical indices of litter quality include element concentrations and concentrations of various classes of organic compounds.

Cromack (1973), Cromack and Monk (1975), and Fogel and Cromack (1977) have reported that the initial lignin concentration in the litter is an excellent index to the rate of weight loss of litter samples. Initial lignin concentration also gave a high correlation with decomposition rate when the data of Lockett (1937) were re-analysed by Cromack (1973).

A high correlation between initial nitrogen concentration and decomposition rate has been demonstrated by a number of researchers, including Bal (1922), Hill (1926), Waksman and Tenny (1928), Waksman and Gerretsen (1931), Monnier and Jeanson (1964), Cowling and Merrill (1966), Satchell and Lowe (1966), Witkamp (1966), and Zimka and Stachurski (1976). But the high correlation between initial nitrogen concentration and decomposition is not universal. Melin (1930), and Daubenmire and Prusso (1963) have found poor correlation between decomposition rates and the initial nitrogen percentage in litter.

Figure 6.8 The relationship between the percent biomass remaining in decomposing leaf litter at the end of 12 months of decomposition in the field and the initial lignin:nitrogen ratio of the various litter materials. At the New Hampshire site the leaf litters are as follows: Be, American beech; SM, sugar maple; PB, paper birch; RM, red maple; PC, pin cherry; and A, ash. At the North Carolina site the leaf litters are as follows: WP, white pine; CO, chestnut oak; WO, white oak; RM red maple; and FD, flowering dogwood. From Melillo et al. (1982)

Melillo et al. (1982) have found that the ratio of initial lignin concentration to initial nitrogen concentration is a better predictor of decomposition rate than is either initial lignin concentration or initial nitrogen concentration (Figure 6.8). Since lignin is among the most difficult organic compounds to decompose, and since nitrogen is, for many ecosystem processes, the most limiting nutrient, it is reasonable that the lignin: nitrogen ratio of litter would be a good predictor of decomposition rate.

Slow rates of litter decomposition can result in the accumulation of large unavailable nutrient stocks in a forest soil's surface horizons, and nutrient limitations for primary producers (Siren, 1955; Weetman, 1962; Heilman and Gessel, 1963; Florence, 1965; Watt and Heinselman, 1965; Heilman, 1966; Miller, 1969; Adams et al., 1970; Lamb, 1971). It is not difficult to envision a positive feedback loop that would result in the perpetuation of an unproductive forest stand: plant nutrient stress promotes the production of low-quality litter that decomposes slowly, releasing nutrients slowly, and thereby perpetuating plant nutrient stress.

Formation of humus, the meta-stable organic fraction of soils, is still a poorly understood process. Evidence suggests that lignin and polyphenols contribute to humus formation (Allison, 1973). DeHaan (1977) found a high correlation between humus formation and the amount of lignin introduced into soils over a 10 year period. Given that lignin concentrations are generally higher in litter of nutrient-poor sites, it may be that in relative terms, more of the litter entering the soil in a nutrient-poor site would be transformed to humus than would be the case in a nutrient-rich site. If this speculation is true, then the nutrient status of plants would affect carbon flow in soils. In absolute terms, the higher litter inputs associated with nutrient-rich sites may ultimately lead to more humus formation per unit time, despite the fact that a smaller percentage of the litter will be transformed into humus. This may be a critical component of calculations on the effects of forest fertilization on carbon storage.

To this point, we have only considered above-ground litter input. Root litter input to soils, especially fine root litter input, can be very large. For example, Edwards and Harris (1977) estimate a fine root litter input of 900 g C m^-2 yr^-1 in a temperate zone hardwood forest.

The fraction of root litter input transformed to refractory humus in forests is not known. Relatively labile carbon compounds can also have a prolonged residence time in soils if they are physically protected from decomposition. Allison (1973) suggested that this process may be very important in determining the fate of root litter input. He notes that roots have some advantages over top residues as carbon sources to soils. Roots are intimately mixed with the soil at all times and, as they decompose, produce a gum-like material, that is well distributed. These polysaccharide `gums' are in a position to act as cements between soil particles as they are being formed into aggregates by various forces. When fixed in aggregates there is much evidence that the polysaccharide `gums' are protected for a time against oxidation by micro-organisms.

Table 6.3 Total net primary production in g m^-2yr^-1 for two 40-year-old Douglas fir stands (Keyes and Grier, 1981)

Component

Poor site

% of total

Good site

% of total

Stem wood

420

820

Stem bark

170

Living branch

Foliage

200

320

Large root (> 5 mm)

110

160

Small root (2

5 mm)

140

110

Fine root (< 2 mm)

560

140

Total

1540

100

1780

100

Polysaccharides are also produced during decomposition of surface litter, but the polysaccharides are usually not in intimate contact with the soil. Furthermore, the polysaccharides produced in the surface litter are decomposed so rapidly that there is only limited movement from the immediate areas where they are formed.

As mentioned earlier, both relative and absolute amounts of net primary production allocated to roots may be larger in nutrient-stressed stands than in nutrient-rich stands. This is clearly seen in the data of Keyes and Grier (1981; Table 6.3). On the nutrient-rich site the net primary production allocated to fine roots in a 40-year old Douglas fir stand was 140 g C m^-2yr^-1, which amounted to 7.9 percent of the net primary production. In the nutrient-poor site, the primary production allocated to fine roots in a 40-year old Douglas fir stand was 560 g C m^-2yr^-1, which amounted to 36.4 percent of the net primary production. It is currently hypothesized that the annual fine root production dies off and becomes root litter. Combining the concept of physical protection from decomposition of relatively labile compounds with the fact that both the relative and absolute amounts of carbon entering the soil in root litter can be larger in nutrient-poor sites than in nutrient-rich sites, it is logical to suspect that plant nutrient status acting on the shoot

root ratio switch may affect the respiration

net soil increment switch in the soils (cf Figure 6.7). By increasing the amount of carbon input in litter from above-ground entry to below-ground entry, the rate of carbon storage at depth in soils may increase.

In this section we have discussed the ways in which plant nutrient status can influence the amounts of carbon flowing through an ecosystem, the pathways of flow, and the proximate fate of the carbon. We envision nutrients acting on a series of switches in the carbon flow pathway. It is not surprising that our arguments suggest that the net primary production per unit area in forests growing on nutrient-rich sites is greater than that on nutrient-poor sites. More interestingly, on nutrient-rich sites as compared with nutrient-poor sites, a greater percentage of the net primary production is allocated to plant growth increment. Carbon accumulations in soils of nutrient-poor sites may be larger per unit of carbon in net primary production because of the increased fraction of net primary production that is allocated to fine roots and eventually fine root litter.

These considerations raise a series of interesting questions at the global scale. Will chronic low level additions of fertilizer to forests, such as may be occurring through air pollution and subsequent rain-out, shift the pathways of carbon flux in these ecosystems? Is the fertilization causing not only an increase in net primary production, but an increase in the amount of net primary production that is stored in the vegetation? If we define the efficiency of carbon storage in vegetation as the annual plant growth increment divided by annual net primary production, the fertilizer studies just reviewed would suggest that an improvement in plant nutrient status results in increased carbon storage efficiency. This result is consistent with the source

sink concept of photosynthate use discussed earlier.

6.4 ELEMENT INTERACTIONS AND THE GLOBAL CARBON CYCLE

The global carbon cycle is linked to other element cycles in many complex ways. For example, the burning of fossil fuels not only releases large amounts of carbon to the atmosphere, but it also increases the input of nitrogen, phosphorus, and sulphur to the atmosphere. Some of this nitrogen, phosphorus, and sulphur may enter terrestrial ecosystems in bulk precipitation, resulting in an increase in nutrient availability in these systems. This rise in available nutrients may in turn stimulate both carbon fixation and storage in terrestrial ecosystems, as has been suggested by Deevey (1970) and Simpson et al. (1977), thereby altering the dynamics of the global carbon cycle. In this section of the paper we consider how man's alteration of the global cycles of nitrogen, sulphur, and phosphorus could potentially increase the carbon storage capacity of the world's forests and thereby alter the global carbon balance.

The carbon dioxide concentration of the atmosphere has risen at least 40 ppm since the beginning of the industrial revolution. The present annual rate of increase is between 1.0 and 1.5 ppm, translating to an increase in the atmospheric carbon load of about 2700 Tg of carbon per year.

The annual carbon budget for the atmosphere can be formally stated as a mass balance equation (Equation 1) with two source terms and two sink terms. The two source terms are: (1) the release of carbon dioxide to the atmosphere from the combustion of fossil fuels (FFR in Equation 1); and (2) the net release of carbon dioxide to the atmosphere resulting from land use changes (e.g., forest to cultivated field, pasture to forest) and the oxidation of harvested renewable resources (TR in Equation 1). The two sink terms are: (1) the net uptake of carbon from the atmosphere by a variety of processes in the world's oceans (OU in Equation 1); and (2) the net uptake of carbon from the atmosphere by terrestrial ecosystems due to `fertilization' of these systems with carbon dioxide or nutrients, or both (TU in Equation 1). In the mass balance equation, AI is the annual increase in the carbon stock of the atmosphere.

Table 6.4 contains the current best estimates of the variables in Equation 1. The magnitude of the release of carbon dioxide to the atmosphere from the combustion of fossil fuels is well known; This process is now estimated to release about 5200 Tg of carbon annually (Rotty, 1981). Estimates have ranged over an order of magnitude for the net release of carbon dioxide to the atmosphere from terrestrial vegetation and soils as a consequence of land use changes and the oxidation of harvested renewable resources (Table 6.5). To date, the most systematic analysis of the terrestrial source term has been conducted by Houghton et al (1983). According to their `population' based estimate, the magnitude of this source term is currently 2600 Tg of carbon annually. The net annual uptake of carbon dioxide from the atmosphere by the world's oceans is now estimated to be 2100 Tg of carbon (40% of the amount of carbon released from the combustion of fossil fuel).

With four of the five terms in the mass balance equation defined, we can calculate TU, the net annual storage of carbon by terrestrial ecosystems due to `fertilization' of these systems with carbon dioxide or nutrients, or both. By difference, the `fertilization' factor required to balance the global carbon budget is 3000 Tg of carbon.

A central question in the global carbon cycle is: Will carbon storage on land increase in response to man's acceleration of the global cycles of N, S, and P? We will assume that N, S, and P added to forests in bulk precipitation act as fertilizer. In this section of the paper we attempt to evaluate the consequences of such a fertilization.

We will use a simple element-matching approach to evaluate the expected increase in carbon storage in a terrestrial ecosystem following the addition of a given amount of a plant nutrient. Two assumptions are made in an element-matching analysis: (1) carbon will be stored in some constant proportion to nitrogen, sulphur, and phosphorus; and (2) the concept of a single limiting nutrient for plant growth and organic matter decomposition is valid.

	Abstract
	6.1 Introduction
	6.2 Element Ratios in Foliage and Litter
		6.2.1 Element Ratios in Foliage
		6.2.2 Nutrient Translocation within Trees and Nutrient Use Efficiency
		6.2.3 Summary
	6.3 Carbon Nutrient Interactions at the Ecosystem Level
		6.3.1 Photosynthesis and Net Primary Production
		6.3.2 Shoot:Root Ratio and the Response of Shoots and Roots to Fertilization
		6.3.3 Carbon Allocation to Perennial Versus Deciduous Plant Parts
		6.3.4 Litter Decomposition
		6.3.5 Summary
	6.4 Element Interactions and the Global Carbon Cycle
		6.4.1 The Global Carbon Cycle: An Overview
		6.4.2 Element Composition of Forest Ecosystems
		6.4.3 Fossil Fuel Combustion and the Acceleration of the N, P, and S Cycles
		6.4.4 CarbonNitrogen Interactions
		6.4.5 Phosphorus and Sulphur Inputs and Carbon Storage
		6.4.6 Summary
	6.5 Phosphorus 'The Master Element'
		6.5.1 Phosphorus Availability and Carbon, Nitrogen and Sulphur Accumulation in Soils
		6.5.2 Pedogenesis and The Global Carbon Cycle
		6.5.3 Concluding Statement
	References