the importance of pulse timing for plant n capture
Although the importance of nutrient pulses for plant nutrient budgets has been extensively demonstrated (Jonasson & Chapin 1991; Fransen et al. 1998; Bowman & Bilbrough 2001), few studies have evaluated how seasonal timing of nutrient pulses impacts plant nutrient capture and growth. In this study, both A. confertifolia and A. parryi captured more N from the mid spring pulse than from the early spring pulse (Fig. 4). Although A. confertifolia captured more N than A. parryi from both pulses, the proportional increase in N capture from the early spring pulse to the mid spring pulse was greater for A. parryi than for A. confertifolia. The importance of pulse timing for plant N capture is consistent with previous observations in cold deserts. In the Great Basin, growth of tussock grasses and annual grasses was greatest when N pulses occurred in early spring, whereas growth of sagebrush was greatest when N pulses occurred in mid spring (Bilbrough & Caldwell 1997). Likewise, on the Colorado Plateau, N capture by the perennial shrubs Coleogyne ramosissima and Ephedra viridis was greatest when pulses occurred early in the growing season, while N capture by the herbaceous perennial Cryptantha flava was greatest when pulses occurred later in the growing season (Gebauer & Ehleringer 2000).
In addition to demonstrating that the magnitude of N capture can depend on pulse timing, our results also show that the rate of pulse exploitation can vary with pulse timing. For example, the proportion of total N captured within 1 day following the early spring pulse was 2% for A. confertifolia and less than 1% for A. parryi. By contrast, the proportion of total N captured within 1 day following the mid spring pulse was over 45% for A. confertifolia and over 40% for A. parryi. Thus, our observations contribute to the emerging view that the seasonal timing of N pulses probably has significant ecological consequences in arid systems; not only does the rate and total amount of N capture depend on the timing of a pulse but it seems that in a number of desert systems, coexisting species may differ in relative abilities to capture N from pulses depending on when the pulse occurs in the season. Path analysis provides insight into interactions among the major mechanisms driving these plant responses.
interacting root and soil processes influence n capture from pulses
RLD and N inflow rate were both strong drivers of short-term and long-term N capture from a pulse (Fig. 8a,b). Because soil volume was constant in our experiment, higher root length RGR increased RLD. This is consistent with the model simulations of Barber (1995), which predicted that both and uptake would increase linearly with root length growth rate and be affected minimally as a result of inter-root competition at high RLD. Sensitivity analysis of this same model also predicted that increased N uptake rates would be most important for capture but less important for because of low soil diffusion rates. This, coupled with the rapid decline in soil in our study (Fig. 7), suggests that the increased plant N capture with higher inflow rates was mainly due to increased inflow rate.
Whereas N inflow rate always had the strongest path to plant N capture, variation in N capture appeared to be influenced more by variation in N flow rates than by variation in RLD over the short term than the long term, partly supporting our initial hypothesis. Similar patterns were observed in simulation models by Jackson & Caldwell (1996) using a modification of the Barber (1995) model so that soil heterogeneity and root plasticity could be assessed. In these simulations, when roots encountered a previously unexplored patch of , elevated root N inflow rates contributed most to N capture within 2 days but proportionately less over 10 days, whereas increased root growth was unimportant for N capture during the first 2 days but more important over 10 days. Our experimental results are consistent with the model results.
Although the total soil inorganic N pool declined by approximately 60% across both pulses (Fig. 7), our path analysis indicated that soil 15N concentration had a limited direct effect on 15N inflow rate (Fig. 8a,b). Thus, our prediction that N inflow rates would decline with soil N through a pulse was not supported. One reason that soil N concentration had a minimal effect on N inflow rate may be because much of the was nitrified through the pulse (West 1991; Schaffer & Evans 2005), resulting in only moderate declines in the soil pool. Nitrate is highly mobile in the soil, and most species have a high affinity (low Km) relative to soil solution (where Km equals the solution concentration equal to half Imax) (Barber 1995). As a result, when dominates the soil inorganic N pool as in our experiment, N inflow rates should remain close to Imax until soil is largely depleted. With the assumption of Michaelis–Menten kinetics and our experimental conditions, factors controlling Imax, and not soil N concentration, should be the major determinant of N inflow rate.
A significant amount of variation in N inflow rate was attributed to variation in root RGR both in the short and long term (Fig. 8a,b). During the mid spring pulse, when root length RGR were highest for both species (Fig. 5), A. confertifolia and A. parryi N inflow rates were 5- and 22-fold greater, respectively, immediately following the mid spring pulse relative to the early spring pulse (Fig. 6c,d). In cropping systems, Imax has been shown to increase substantially as plant growth rate and N demand increase (Siddiqi et al. 1990; Mattson et al. 1991; Steingrobe & Schenk 1994). Although low soil temperatures could also contribute to low N inflow rates in early spring by slowing the rate of biochemical processes, previous work has shown that the degree to which low temperature affects Imax is mainly determined by the degree to which low temperature affects growth rate and plant demand (White et al. 1988; Engels et al. 1992). It appears therefore that low root length RGR and low plant N demand decrease Imax in these Atriplex species and are therefore the major factors limiting N inflow rates in these species in early spring.
Although simulation models and our results suggest an important role for both root growth rate and root N inflow rate for N capture from pulses, not all studies in arid systems have found such a relationship. For example, root growth rate was the major mechanism by which the shrub Larrea tridentata captured N from late-season N pulses, while uptake rates remained unchanged (BassiriRad et al. 1999). By contrast, the major mechanism of N capture by the tussock grass Agropyron desertorum and the shrub Artemisia tridentata following simulated summer rain events was increased N diffusion to the root surface as a result of increased soil moisture; following the pulse, N inflow rates increased minimally and root growth did not increase (Ivans et al. 2003). Our results suggest that the specific timing of the experimental pulse could contribute to differences in responses among these studies. That is, root growth and N uptake rates may not necessarily be expected to increase following late-season N pulses when plant relative growth rates and N demand are low.
Consistent with our prediction, a decline in soil water content following a pulse had a significant indirect effect on plant N capture over the long term (8–28 days) through a direct effect on N inflow rate (Fig. 8b). This could be due to a number of mechanisms. Models of nutrient flow to the root show that declines in soil water content decrease both nutrient mass flow and diffusion (Nye & Tinker 1977). Decreased soil volumetric water content following a pulse would have reduced effective diffusivity and increased the potential for development of depletion zones around roots even though average soil levels were relatively high (Fig. 7). In addition, even moderate water deficits can reduce the Imax of arid land plants (BassiriRad & Caldwell 1992; Matzner & Richards 1996). Thus, the effect of low soil water content on N inflow rate is probably due to a combination of both reduced Imax and reduced soil supply rate.
Although microbial biomass 15N was a significant pool of N following a pulse relative to plant N pools (Table 1), the path coefficient from microbial immobilization to soil N was weak and the indirect path from microbial immobilization to plant N capture was not significant (Fig. 8a,b), contrary to our prediction. It is possible that we underestimated microbial biomass N as microbial biomass is generally concentrated in the upper soil layers but our soil sampling included the entire 0–30-cm layer pooled together. Additionally, because we did not know the efficiency of extracting 15N from microbial biomass in these desert soils, we did not apply a conversion factor (Brookes et al. 1985), as is typically used in forested and agricultural systems to account for 15N not readily extractable by the chloroform fumigation method. These factors combined may have resulted in underestimates of microbial biomass N, and thus contributed to lower total 15N recovery during a pulse (Table 1). Nevertheless, even if the total amount of microbial biomass was underestimated we expected that this underestimate would be similar across species and treatments. Consequently, the interrelationships between microbial biomass N and the other variables in the model would not be expected to change.
The high proportion of unexplained variance (U, Fig. 8a,b) in microbial biomass 15N suggests that we did not include some important factors influencing microbial biomass N in our model. When we constrained our path model to include only root responses the fit of our model improved significantly. This suggests that a better understanding of the factors influencing mineralization and immobilization rates is necessary to predict more accurately plant response to N pulses in these systems. Although we predicted soil water content would influence microbial biomass, this factor explained essentially none of the variance in microbial biomass 15N for the range of water content encountered in this study. Other studies have demonstrated a limited effect of moderate changes in soil water on microbial biomass in arid systems (Mazzarino et al. 1998; Zhang & Zak 1998), and it is possible that microbial biomass N is more related to specific patterns of wet–dry cycles rather than simply to soil water content (Austin et al. 2004). Although we expected that microbes would be N limited and therefore immobilize a large amount of N, poor litter quality in arid systems can result in N or carbon limitations (Aerts & Chapin 2000). It is possible that in our system microbial biomass is more limited by labile carbon substrates than N, as has been demonstrated in a number of other arid systems (Gallardo & Schlesinger 1995; Núñez et al. 2001; Schaffer & Evans 2005).
Taken together, these results demonstrate that interactions among a number of root responses and soil processes influence the amount of N captured during a pulse. When N pulses occur during periods of high relative growth rate, N capture was greater owing to increased RLD and higher N inflow rates related to greater plant N demand. The rapid loss of from the system compared with , potentially due to high nitrification rates, combined with low immobilization rates during the pulses allowed adequate soil supply during a pulse. As a result, soil N supply rates did not initially limit plant N capture from a pulse. Instead, factors reducing Imax, such as low soil water content and low plant N demand, appear to reduce N inflow rate and limit N capture.
Physiological traits allowing rapid capture of a limiting resource or depletion of a limiting resource to low levels are expected to be important determinants of competitive ability (Grime 1977; Tilman 1988). Our results suggest, however, that both the rate at which a species can capture N from a pulse and the extent to which a species can deplete N following a pulse depend strongly on the seasonal timing of a pulse. If such environmental variation impacts on the competitive ability of a species, then competitive hierarchies in any given year could change based on the temporal N dynamics. Thus, by altering competitive advantages over time, seasonal variation in timing of an N pulse may also facilitate species coexistence in these pulse-driven systems (Chesson et al. 2004). Further experiments with plants in competitive environments, however, are needed to assess fully the ecological consequences of this heterogeneity for survival, competitive ability and diversity maintenance.