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- Materials and Methods
A substantial fraction of the flux of CO2 from the soil is from roots (Rouhier et al., 1996; Thierron & Laudelout, 1996), with the rest coming from soil organisms. Published values for the proportion of total soil CO2 efflux originating from roots vary from < 10% to > 90% (Hanson et al., 2000), thus, the loss of carbon through root respiration can be an important component of forest carbon budgets. More than 50% of total net primary productivity (NPP) in forest ecosystems may be allocated below-ground (Vogt et al., 1982; Fahey & Hughes, 1994), and the extent to which NPP becomes long-term carbon storage greatly affects the capacity of forests to store atmospheric CO2. The increase in atmospheric CO2 may alter the partitioning of respiration among functional processes, as well as its absolute magnitude, thereby affecting the carbon cycling of ecosystems.
Fine root respiration supports three important functions: maintenance, growth and nutrient uptake (Johnson, 1983; Lambers et al., 1983). Maintenance respiration provides the energy to turnover proteins and to maintain ion gradients, growth respiration provides energy for construction of new cells and nutrient uptake respiration provides the energy required by epidermal root cells to actively transport ions against a concentration gradient. The partitioning of energy among these major functions will influence water and nutrient uptake by fine roots, which will affect tree growth, yet relatively few studies have quantified the proportional investment in these processes (Veen, 1980, 1981; de Visser & Lambers, 1983; Johnson, 1983; Van der Werf et al., 1988; Poorter et al., 1991; Bouma et al., 1996; Mata et al., 1996).
Nutrient uptake respiration is as high as 60% of total root respiration for maize (Veen, 1980, 1981). By contrast, Quercus suber used the majority of respiration for maintenance and used only 19–31% of its total respiration for nutrient uptake (Mata et al., 1996), reflecting the lower nutrient demand and greater nutrient use efficiency of this species. Nutrient uptake respiration has not been determined in an intact forest ecosystem, where the percentage of total fine root respiration used for nutrient uptake could be high, particularly for trees growing in nutrient-poor soils.
Growth in elevated atmospheric CO2 may alter the absolute rate, as well as the partitioning of fine root respiration. Several studies have documented a decrease in the specific rate of fine root respiration for trees grown in elevated atmospheric CO2 (Callaway et al., 1994; BassiriRad et al., 1997; Crookshanks et al., 1998). Growth under elevated CO2 causes a decrease in the nitrogen concentration of roots (Cotrufo et al., 1998) suggesting a reduction in protein concentration. Thus, the energy required for protein turnover may decline in elevated CO2 causing a reduction in maintenance respiration. If maintenance respiration of fine roots grown in elevated atmospheric CO2 is reduced, then more energy could potentially be available to support growth and nutrient uptake. By contrast to maintenance respiration, elevated atmospheric CO2 stimulates fine root production (Norby et al., 1986; Pregitzer et al., 1995; Crookshanks et al., 1998; Janssens et al., 1998; DeLucia et al., 1999). The decrease in maintenance respiration with elevated CO2 may contribute to increases in growth respiration.
The objective of this study was to estimate total fine root respiration and the proportions used for maintenance, growth and nitrogen uptake in loblolly pine and sweetgum forests growing under ambient and elevated atmospheric CO2. In addition, a survey of the literature was conducted for values of fine root respiration to provide comparisons for the rates reported in this study. Few studies report nitrogen uptake respiration, and none, to our knowledge, have attempted to estimate this process for an intact forest ecosystem. Nitrogen was investigated in this study as it was assumed that it represents the greatest expenditure of energy for nutrient uptake (Veen, 1980, 1981). We hypothesized that a reduction in nitrogen concentration of fine root tissue grown in elevated CO2 would reduce maintenance respiration, and that more energy would be used for fine root growth and nitrogen uptake. Fine root maintenance respiration was measured from gas-exchange of nongrowing roots in the absence of nutrients, and growth respiration was quantified from construction costs and production rate of fine roots. Nitrogen uptake respiration was estimated from the annual nitrogen uptake of trees at each site and from a literature value representing the respiration rate associated with nitrogen uptake.
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Instantaneous RM on a mass basis was significantly reduced by the elevated CO2 treatment for loblolly pine but not for sweetgum. It has been suggested that a reduction in tissue nitrogen concentration, possibly caused by an increase in carbon content (Cotrufo et al., 1998), reduced respiration rates of tree roots grown under elevated CO2 (Callaway et al., 1994; BassiriRad et al., 1996; Crookshanks et al., 1998). We were unable to detect an effect of elevated CO2 on the nitrogen concentration of fine roots for either species. Instantaneous RM on a mass basis was higher for sweetgum than loblolly pine and this difference was eliminated when expressed per unit N (Table 1), suggesting that the rate of CO2 flux may have been related to nitrogen concentration. However, no relationship was apparent between individual root respiration measurements and corresponding nitrogen concentrations (n = 53 for loblolly pine and n= 33 for sweetgum; data not shown). It appears that while expressing instantaneous RM on a nitrogen basis reduces some of the variation in respiration rates, the observed differences in fine root respiration are not explained completely by nitrogen concentration.
There was a trend of greater construction respiration (RC) under elevated atmospheric CO2 for loblolly pine fine roots but not for sweetgum. The increase in the ash-free heat of combustion of loblolly pine fine roots in elevated CO2 resulted in a small increase in construction costs and RC. The increase in construction costs from elevated CO2 may be related to increases in the lignin concentration of fine roots (Eissenstat, 1992). In terms of glucose equivalents, lignin is one of the most expensive compounds to produce (Penning de Vries et al., 1974) and elevated CO2 has been found to increase the lignin concentration of roots (Booker et al., 2000). Elevated CO2 also affects RC of other plant tissues. Construction costs and RC were reduced in leaves with increasing atmospheric CO2 (Wullschleger & Norby, 1992; Wullschleger et al., 1992; Griffin et al., 1993; Ziska & Bunce, 1994), which was primarily associated with changes in nonstructural carbohydrates and to a lesser extent by lignin (Griffin et al., 1996). Elevated CO2 may result in the construction of more expensive structural compounds in fine roots.
The stimulation of annual RG for loblolly pine under elevated CO2 was caused primarily by the increase in fine root production (Table 2). Both increased RC and fine root production, when extrapolated to the entire forest, contributed to an increase in RG under elevated CO2. But, the stimulation of fine root production by elevated CO2 (87%) was considerably greater than the stimulation of RC (37%). There was no detectable effect of elevated CO2 on RC in sweetgum and only increased root production contributed to the trend of greater RG under elevated CO2 for this species (Table 2). For these two forests it appears that an increase in fine root production is the primary factor contributing to the increase in annual RG under elevated CO2. Loblolly pine had lower fine root production than sweetgum and consequently also had lower annual RG. Trees commonly exhibit an increase in fine root growth under elevated CO2 (Norby et al., 1986; Pregitzer et al., 1995; Crookshanks et al., 1998; Janssens et al., 1998) and in these cases we would also predict an increase in annual RG.
Our estimates of annual RT for loblolly pine were similar to those for another young loblolly pine stand in the Piedmont of North Carolina (663–1062 g C m−2 y−1; Maier & Kress, 2000), but considerably higher than those reported by Matamala & Schlesinger (2000; 349.4 and 401.0 g C m−2 year−1 in ambient and elevated CO2, respectively) at the same site. Differences in methodology may have contributed to this disparity, though this remains uncertain. Unlike this study, Matamala & Schlesinger (2000) measured fine root respiration on severed roots using an oxygen electrode. Over two thirds of the studies in the survey used severed roots and the average respiration was higher for attached than for detached roots. However, the distribution of rates reported in the literature was highly skewed towards lower values, and the greater average for attached roots was caused by a few studies reporting very high rates (> 40 nmol CO2 g−1 s−1; Fig. 2).
Annual soil CO2 efflux from ambient and elevated plots in the pine forest were 928 g C m−2 and 1176 g C m−2, respectively (Andrews & Schlesinger, 2001; Hamilton et al., 2002), and the values for ambient and elevated plots in the sweetgum forest were 960 g C m−2 and 1271 g C m−2, respectively (Norby et al., 2002). The values of total soil CO2 efflux in these forests are close to the average annual value of 1050 g C m−2 for 34 different forest types and similar to other temperate forests (Davidson et al., 2002). In the pine forest, RT estimated from this study contributed 69% and 45% of the total CO2 efflux from ambient and elevated plots, respectively. Using the unusual C isotopic composition of newly fixed C in the elevated plots, Andrews et al. (1999) estimated that 45% of total soil CO2 efflux originated from roots. The proportion of soil CO2 from fine roots was somewhat lower in the sweetgum forest than in the pine forest (ambient, 25%; elevated, 36%).
To calculate the proportion of respiration to support RN annually, we multiplied estimates of total nitrogen uptake in both forests by a literature value for the specific respiration associated with nitrogen uptake. The rate of respiration per unit nitrogen uptake by the trees was taken from a study of Quercus suber. This slow growing evergreen tree species, from xeric, nitrogen-poor soils (Mata et al., 1996), was the best match to loblolly pine and sweetgum in our study (Table 3). Mata et al. (1996) also found similar rates to ours for tissue specific root maintenance (7.13 nmol CO2 g−1 s−1 at 25°C) and growth respiration (51.8 g C kg−1 compare to RCTable 2). The value of RN was 1.8 g CO2 g−1 N for Quercus suber, which was similar to studies of herbaceous plants (Table 3). For example, five studies of herbaceous plants found a narrow range of RN 1.0–3.2 g CO2 g−1 N (Table 3; Veen, 1980, 1981; Johnson, 1983; Van der Werf et al., 1988; Poorter et al., 1991; Bouma et al., 1996). Because RN and the absolute rates of nitrogen uptake are relatively small, the choice of the instantaneous value of RN is not likely to have a large effect on our annual estimate.
Table 3. Published estimates of nitrogen uptake respiration (RN) and corresponding values of instantaneous maintenance respiration (RM) at 25°C and construction respiration (RC) for various species. The value of RN from Poorter et al. (1991) was based on total anion uptake and is a median of 24 herbaceous species. The values of RN from the other studies were based on the uptake of nitrate.
|Species||RM (nmol CO2 g−1 s−1)||RC (g C kg−1)||RN (g CO2 g−1 N)||References|
|Zea mays|| 3.7||104.6||3.2||Veen (1980, 1981)|
|Helianthus annuus||–||–||2.0||Johnson (1983)|
|Carex species|| 4.9|| 60.5||1.8||Van der Werf et al. (1988)|
|24 Herbaceous species||–|| 64.8||1.7||Poorter et al. (1991)|
|Solanum tuberosum||13.3|| 47.0||1.0||Bouma et al. (1996)|
|Quercus suber|| 7.1|| 51.8||1.8||Mata et al. (1996)|
In our study annual RN was much greater in sweetgum than loblolly pine. This was because the uptake of nitrogen on a ground area basis in the sweetgum stand was nearly double the uptake of nitrogen in the loblolly pine stand. Annual RN required a small expenditure of energy in relation to annual RT, but this proportion was greater for the sweetgum stand (4.1%) compared to the loblolly pine stand (1.1%). The higher nitrogen availability in the sweetgum stand resulted in lower fine root standing mass and RT and greater RN per unit fine root mass compared to the loblolly stand.
In summary, the majority of fine root respiration was used for maintenance and was not reduced by changes in the nitrogen content of the fine roots grown in elevated atmospheric CO2, as initially hypothesized. The future investment of carbon in RM will depend upon the balance between the C : N ratio of tissues and the size of fine root standing biomass. In the loblolly pine forest annual RT was 26% and 19% of gross primary productivity (GPP) in ambient and elevated atmospheric CO2, respectively (Hamilton et al., 2002). Because of its large contribution to RT and total soil CO2 efflux, changes in RM caused by warming or other factors have the potential to greatly alter carbon losses from forests to the atmosphere.