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A Soil respiration • Ecosystem respiration □ Leaf organic matter

Figure 8,2 Relationship between carbon isotope signatures of leaf organic matter, and ecosystem and soil respiration. (^Buchmann et al., 1997; ^Fessenden and Ehleringer, 2002; sBuchmann et al., 1998; 4Mortavazi and Chanton, 2002; 5Flanagan et al., 1996). It should be noted that although the isotopic composition of leaf organic matter is sometimes a poor indicator of the isotopic composition of recent photosynthates (Pate and Arthur, 1998) and leaf respiration (Duranceau et al., 1999; Ghashghaie et al., 2001 ), the data indicate the potential for differences between nighttime soil, ecosystem and aboveground plant respiration.

recent photosynthates (e.g., Pate and Arthur, 1998) or plant respiration (Duranceau et al, 1999; Ghashghaie et al, 2001), the data depicted in Fig. 8.2 indicate the potential for differences between aboveground and belowground respiration.

Recent studies indicate a general pattern of 13C enrichment in microbial (largely fungal) biomass relative to plant organic matter (Fig. 8.3). Although early studies suggested there is significant fractionation during microbial respiration (Blair et al., 1985; Mary et al., 1992) recent studies indicate small (Santruckova et al., 2000; Hogberg et al, this volume) or negligible fractionation (Henn and Chapela, 2000; Ekblad et al, 2001). Nevertheless, the isotopic differences in microbial biomass indicated in Fig. 8.3 are clearly suggestive of the potential for isotopic differences in respired CO2, both between microbial functional groups (particularly saprotrophic vs mycorrhizal fungi) and between plants and microbes (autotrophic vs heterotrophic).

Figure 8.3 Relationship between carbon isotope signatures of leaf and mycorrhizal and saprotrophic fungal biomass across biome types. Error bars represent the standard error.

Kozhu et al., 1999; 2Hobbie el al, 1999; 3Hogberg et al., 1999; 4Henn and Chapela, 2001; 5Hobbie etal., 2001.)

a Saprotrophic fungi ■ Mycorrhizal fungi □ Leaves

Tropical Temperate Mixed Temperate Subalpine Boreal rainforest1 deciduous temperate coniferous coniferous forest3 forest1 forest2,3 forest4,5 forest1

Causes of Variation in Respiration Signatures

Differences in respiration signatures among ecosystem components (Figs 8.2 and 8.3) can result from (1) temporal lags in the movement of carbon sisotope signals through various ecosystem pools, (2) metabolic fractionation, (3) anaplerotic CO2 fixation, (4) compound-specific effects, and (5) kinetic fractionation. Each of these factors is discussed below.

Temporal Lags Variation in photosynthetic discrimination combined with temporal lags in the movement of photosynthates through plant and soil pools caused by different turnover rates of each pool can result in disequilibrium among substrates and the resulting respiration. For example, soil respiration signatures can lag behind that of the dominant vegetation in temperate grasslands with seasonal transitions from C3 to C4 plants (Still et al., 2003). Similar lags can occur as a result of environmental rather than plant-related effects. For example, the decrease in the carbon isotope ratio of atmospheric CO2 of ~1.4%o over the last 250 years, the so-called Suess effect (Ehleringer et al., 2000), could cause an equivalent change in photosynthates over this same time period. The temporal lag of this carbon moving through the soil is believed to contribute to the 13C enrichment commonly observed with depth (Ehleringer et al., 2000). Additionally, a change in humidity can cause a change in stomatal conductance and photosynthetic discrimination which, in turn, can cause a change in the carbon isotope ratio of photosynthates and plant respiration before the photosynthates reach the soil microbial community and appear in heterotrophic respiration (Ekblad and Hogberg, 2001). Lags on the scale of decades or even centuries might also be observed under special circumstances such as when organic matter, like peat, thaws after years of being frozen in permafrost. The CO2 released from such a C source may in turn have a unique S13C.

Metabolic Fractionation Kinetic isotope effects (see Kinetic Fractionation below) as well as isotope effects associated with C moving preferentially in particular directions at metabolic branching points during synthesis (Gleixner et al, 1993; Schmidt and Gleixner, 1998) can cause variation in the carbon isotope signature of CO2 released during the biosynthesis of secondary compounds (e.g., lipids, lignin, cellulose). For example, lignin and lipids can be depleted in 13C by as much as 3-6%o relative to bulk organic matter whereas carbohydrates such as glucose and sucrose and related polymers such as starch and cellulose can be enriched by l-3%o (Fig. 8.4; O'Leary, 1981; Schmidt and Gleixner, 1998). By mass balance, any depletion (or enrichment) of 13C in a synthesized compound, must necessarily complement an enrichment (or depletion) of 13C in some other compound. This may be a solid or gas such as respired C02

Organic acids

Carbohydrates

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Figure 8.4 Variation in carbon isotope ratios of various leaf compounds. From Ghashghaie et al. (2001). Points with an asterix (*) are from Nadelhoffer and Fry (1988) and were adjusted so that their organic matter value equaled that of Ghashghaie et al. (2001).

(Park and Epstein, 1961; DeNiro and Epstein, 1977; Rossmann etal, 1991). Accordingly, Park and Epstein (1961) suggest that CO2 evolved during lipid synthesis can be enriched by as much as 8%o relative to sugars. Those sorts of effects have been largely ignored in studies conducted at the ecosystem scale.

Anaplerotic CO% Fixation Heterotrophic co2 fixation (Wood et al., 1941) can occur when CO2 is fixed by PEP carboxylase in roots and microbes to replace the carbon that was removed from the tricarboxylic acid cycle (TCA) during the biosynthesis of secondary compounds such as amino acids (Wingler et al, 1996, Dunn, 1998). As soil C02 has an isotopic signature between that of the atmosphere (e.g., — 8%o) and soil respiration (e.g., —27%o), fixation of soil CO2 will result in the 13C enrichment of microbial biomass relative to plants (e.g., —27%o). Fixation contributing to only a small fraction of the microbial biomass (e.g., 5%), may cause a significant shift (1-1.5%o) in microbial carbon isotope composition (Ehleringer et al., 2000). Subsequent decomposition of the enriched microbial biomass will then lead to enriched 13CC>2 released during respiration.

Compound-Specific Effects Selective use of specific compounds as substrates for respiration that differ in their isotope composition as a result of fractionation during their formation (see Metabolic Fractionation above) can lead to isotopic differences in respired CO2. That is, although it may be true that microbes 'are what they eat,' not all microbes eat the same things. For example, isotopic differences among microbial functional groups (Fig. 8.5) are consistent with the isotopic variation among their respective substrates; wood decay fungi are more enriched than litter decay fungi, which are more enriched than mycorrhizal fungi (Kohzu et al., 1999; Hobbie et al, 2001). Cellulose appears to be the preferred substrate for saprotrophic fungi, regardless of whether or not they are capable of decomposing lignin (Gleixner etal, 1993; Hobbie etal, 2001). In fact, 14C tracer studies indicate lignin-derived C is not assimilated into microbial biomass (Hoffrichter et al, 1999) but is mostly solubilized and, to a lesser extent, mineralized to CO2 (Hackett et al, 1977). Thus, the typical 13C-enrichment of wood cellulose relative to leaf cellulose of 3%o (Leavitt and Long, 1982) can explain the observed differences between wood decay and litter decay fungi (Hobbie et al, 2001). Mycorrhizal fungi feed on soluble root sugars (Finlay and Soderstrom, 1992) and, correspondingly, their isotope signature is closer to that of intact leaves and roots than either litter or wood decay fungi. The mechanisms underlying the offsets between plants and mycorrhizae (Fig. 8.3) are not known but may stem from the fact that most ecto-mycorrhizal fungi engage in saprotrophic activity to some extent (Gadgil and Gadgil, 1987) and thereby incorporate 13C-enriched cellulose signatures,

Figure 8.5 Site-specific differences among the carbon isotope ratios of wood decay, litter decay, and mycorrhizal fungi. Error bars represent the standard error.

in addition to potential fractionation during the transfer of carbon from the root to the fungi (Hogberg et al., 1999; Henn and Chapela, 2000).

Kinetic Fractionation Kinetic fractionation refers to mass-dependent isotope effects and principally involves fractionation during respiration or fractionation during the incorporation of sugars by microbes. Lin and Ehleringer (1997) found minimal fractionation during autotrophic respiration in isolated plant protoplasts. As discussed above (see Metabolic Fractionation), further research is needed to determine if fractionation during auto- or heterotrophic respiration occurs and to what extent it may occur under different substrate and environmental conditions. Fractionation can occur during sugar uptake by fungi because hydrolysis of sucrose can yield 13C-enriched glucose and 13C-depleted fructose fractions if hydrolysis is not allowed to reach completion (Gonzalez et al., 1999) (see also Henn and Chapela, 2000). Fungi do not appear to take up sucrose directly (Chen and Hampp, 1993; Buscot et al., 2000) and they have a higher affinity for glucose than fructose (Chen and Hampp, 1993) such that incomplete hydrolysis and fractionation may occur during uptake. This may explain some of the isotopic shift between roots and mycorrhizae (Fig. 8.3). Bacteria on the other hand, do not appear to rely on glucose as the primary carbon source (Abraham et al., 1998). They exhibit no clear trend in the isotopic difference between substrate and biomass, as fractionation effects are highly substrate-specific (Abraham etal., 1998). Sugar amendments to intact

• Wood decay fungi A Litter decay fungi ■ Mycorrhizal fungi

Japan and Malaysia Kohzu etal. (1999)

Oregon, USA Hobbie etal. (2001)

soil organic horizons, where bacterial activity generally predominates, indicate no significant microbial fractionation during respiration (Ekblad and Hogberg, 2000; Ekblad et al, 2002).

Implications of Variation in Respiration Signatures on Soil C-Dynamics

It should be noted that 13C enrichment of microbial respiration relative to plant substrates (Figs 8.3 and 8.5) that in turn leads to 13C enrichment of soil respiration (root and microbial) relative to plant substrates (Figs 8.2 and 8.4), implies the selective loss of enriched carbon that should eventually cause 13C depletion of soil organic carbon (SOC). This contrasts with the typical pattern of 13C enrichment by l-3%o observed with depth in soil profiles (Nadelhoffer and Fry, 1988; Ehleringer et al, 2000). However, as noted by Ehleringer et al (2000), 13C enrichment with depth may be explained by a combination of (1) the historical trend of 13C depletion in atmospheric CO2 and incorporation of this signal in photosynthates and plant litter inputs over time (Suess effect) and (2) incorporation of 13C enriched carbons through anaplerotic CO2 fixation (see above) during microbial biosynthesis (Ehleringer et al, 2000) with selective preservation of microbial products as a progressively more significant component of soil organic matter (SOM) over time. The latter will cause a progressive enrichment of resynthesized microbial C, and is thus consistent with an enrichment of both soil microbial biomass (Fig. 8.3) and soil respiration (Fig. 8.2) relative to plant organic matter. The extent of microbial recycling and overall influence of microbial products on SOC with depth is evidenced by the overall decrease in C content (Nadelhoffer and Fry, 1988; Bird and Pousai, 1997), decrease in C/N ratio (Nadelhoffer and Fry, 1988) towards that of microbes themselves (fungi 5-15:1, bacteria 3-6), decrease in particle size (Bird and Pousai, 1997), and compound-specific shifts in SOC reflecting products of microbial origin (Huang et al, 1996; Marseille et al, 1999; Kracht and Gleixner, 2000).

Enrichment of 13C with depth in the soil profile also indicates that preferential preservation of 13C-depleted lignin does not occur during decomposition (Nadelhoffer and Fry, 1988). Although enrichment with depth is unlikely to result from preferential preservation of 13C-enriched compounds such as sugars, amino acids, and cellulose, for example via Maillard reactions (Maillard, 1917) or abiotic recondensation (see discussion by Burdon, 2001), the 13C-enriched signatures of these relatively labile compounds can be transferred to humus through consumption by microorganisms and subsequent biosynthesis of resistant secondary compounds such as aliphatic biopolymers (Lichtfouse et al, 1995, 1998) and proteinaceous materials (Gliexner et al., 1999) including derivatives of malanins and other polyketides (Burdon, 2001). Since the greater part of plant litter is composed of either polysaccharides (e.g., cellulose and hemicellulose) or lignin (Aber and Melillo, 1991), the balance between lignin-derived and polysaccharide-derived products retained in soils may ultimately determine its carbon isotope ratio. The extent of isotopic enrichment or depletion may therefore depend on the initial isotopic difference between cellulose and lignin, and on the factors that influence their rates of decomposition including temperature, pH, moisture, oxygen tension, soil texture, microbial community composition, nutrient availability, and litter quality (e.g., ratio of lignin to cellulose). For example, anaerobic conditions (e.g., peat soils) that limit lignin degradation can lead to 13C depletion whereas aerobic conditions conducive to lignin degradation can lead to 13C enrichment. In theory, isotope effects caused by discrimination against 13C during respiration (Blair et al., 1985; Mary et al, 1992; Santruckova et al., 2000) can lead to depleted respiration and enriched microbial biomass and SOC, as shown by Agren et al. (1996). However, it is possible that other processes including compound-specific discrimination (e.g., preferential use of cellulose over lignin), anaplerotic CO2 fixation and the Suess effect can lead to enriched microbial biomass and SOC without fractionation during respiration.

Figure 8.6 depicts the results of a model we have developed for describing the variation that can result in the <513C of decomposing litter solely from compound-specific effects alone. The model follows the fate of key C-pools through the microbial metabolic processes and into SOC while maintaining S13C mass balance and tracking the subsequent fate of the dissolved organic carbon (DOC) flux. The aforementioned discussion and the figure caption provide the details underlying time-dependent C-transformations and their specific isotope effects. The results of the model reveal that such effects can be quite large and therefore must be accounted for if robust partitioning is to be accomplished.

Mass balance dictates that enrichment with depth can only occur if the 12C losses exceed those of 13C (or conversely, if 13C gains exceed those of 12C, for example as a result of anaplerotic CO2 fixation). For this reason, observations of soils enriched in 13C often lead to the expectation that microbial respiration is depleted in 13C (Nadelhoffer and Fry, 1988; Agren et al, 1996). The latter is consistent with the notion that 'light' 12C is preferentially metabolized whereas 'heavy' 13C is polymerized (Schmidt and Gleixner, 1998; Santruckova et al, 2000). Further, laboratory 14C tracer studies suggest lignin mineralization efficiencies can reach 75% (Hoffrichter et al, 1999; Tuomela et al, 2000). However, rates in natural soils are generally low except at high temperatures conducive to thermophilic microbes (>35°C; Hackett et al, 1977) such that 13C-depleted lignin losses via respiration co

Years

Litter extractives

Litter acid solubles

Litter Litter protected acid acid solubles insolubles

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