Scaling Rhizosphere Respiration and Priming Effect from Single Plants to Field Ecosystems
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1 06-11 Mission Kearney Foundation of Soil Science: Understanding and Managing Soil-Ecosystem Functions Across Spatial and Temporal Scales Final Report: 06013, 1/1/08-12/31/08 Scaling Rhizosphere Respiration and Priming Effect from Single Plants to Field Ecosystems Weixin * 1, Jessica Gutknecht 1, Daniel Keck 1, and Biao Zhu 1 Objectives Plant roots are widely recognized as an important soil-forming agent (Jenny, 1941) and interact with virtually all soil components. Many soil processes are largely controlled or directly influenced by roots. These processes are commonly called rhizosphere processes. Rhizospheredependent soil organic matter (SOM) decomposition and rhizosphere respiration are two key rhizosphere processes. The substrates of rhizosphere respiration primarily come from recently fixed C through photosynthesis, whereas SOM decomposition is primarily a function of soil heterotrophic activities utilizing solely soil carbon. The two processes are often intricately linked through rhizosphere interactions (, 1999; Personeni et al., 05), even though the C substrates for these two processes have different origins, one is from current plant photosynthesis and the other comes from SOM. Because of method limitations, rates of SOM decomposition are commonly assessed by incubating soil samples in the absence of live roots with an implicit assumption that rhizosphere processes have little impact on the results (e. g., Parton et al., 1987; Bolker et al., 1998; Dalias et al., 01). However, our recent studies have overwhelmingly proved that this implicit assumption is often invalid. The rate of SOM decomposition in the presence of live roots can be inhibited by as much as 50% or accelerated by as much as 382% ( and Kuzyakov, 05), depending on the kind of plant-soil couplings and experimental conditions. The rhizosphere effect on SOM decomposition is large in magnitude and significant in mediating plant-soil interactions. As key regulators of energy flows and cycling of water, nutrients, and carbon in most terrestrial ecosystems (Coleman et al., 1992), rhizosphere processes are expected to play a crucial role in modulating ecosystem functions. Several recent reports have indicated that rhizosphere processes significantly affect ecosystem productivity, plant community structure and diversity (Bever, 03; Klironomos et al., 00; Reynolds et al., 03). At the global scale, approximately 70% of the photosynthetically-fixed energy in terrestrial ecosystems is channeled to soil via litter and roots (Schimel, 1995); between one-thirds and two-thirds of this energy is allocated directly to rhizosphere processes (Bowden et al., 1993; Hanson et al., 00). Yet, our understanding about these processes has been limited to model systems under laboratory conditions (e.g., Fu et al., 02; Jones et al., 04; Kuzyakov, 02). It is widely recognized that extrapolating these existing results from laboratory-scale studies to field ecosystems can be highly unrealistic and potentially erroneous. To what degree are results from these laboratory studies relevant to our understanding of rhizosphere processes at the ecosystem level? One approach to address this issue is to search for general patterns across different experimental 1 Environmental Studies, University of California, Santa Cruz, CA *Principal Investigator For more information contact Dr. Weixin (wxcheng@ucsc.edu).
2 scales. The main objective of the project has been to address the key research question: are rhizosphere processes scalable among different plant species, different growth conditions in various soil types, and at different temporal and spatial scales? We have aimed to find the answer to this research question by testing two hypotheses: (1) rhizosphere respiration rate scales isometrically with live root N content, and this scaling relation is independent of plant taxonomic groupings or growth conditions; and (2) there exists an invariant scaling relationship between the rate of rhizosphere-primed soil organic matter decomposition and live root N content, live root biomass, and/or plant productivity when plants are grown in similar soils. Approach and Procedures We carried out a pot experiment in a continuous 13 C-labeling greenhouse and a field experiment using natural 13 C-tracers by growing C 4 -plants in a C 3 -soil. The greenhouse experiment had the following treatments: monocultures of six plant species (3 grassland species: wild oats, tomcat clover and common fiddleneck; and four tree species: ponderosa pine, California blue oak, trembling aspen, and coast redwood) grown in pots of two sizes (15 and 30 cm diameters) filled with coastal grassland soil taken from a field near the UC Santa Cruz Campus. Unplanted controls and a mixture of the three grassland species in bigger pots were also included. The continuous 13 C-depleted labeling method of & Dijkstra (07) was used in this greenhouse experiment. In the greenhouse, continuous 13 C-labeling was maintained by treating the whole greenhouse as a single chamber. The air temperature inside the greenhouse was controlled by two AC units. The humidity inside the greenhouse was controlled by a dehumidifier. Personnel only entered the greenhouse after sunset, or exhale through a hose while inside the greenhouse. The natural 13 C tracer experiment in the field had these treatments: two C 4 plant species (corn and Sudan grass) grown in an organic farm field with C 3 -soils both in field plots and in buried pots near the field plots. Unplanted controls were also included. The method of (1996) and et al. (00) was used in this experiment. This field experiment was carried out on the Agroecology Farm of UCSC in a field that was converted from a coastal annual grassland that lacked any C 4 plants and that had never been used for any C 4 crops (i.e., C 3 -soil) before. The soil was a well-drained sandy loam formed on calcareous bedrock, and has been organically farmed during the last 30 years. SOM decomposition and rhizosphere respiration in the greenhouse experiment were measured using the method of et al. (03). Briefly, each PVC container was sealed at the base of the plants using non-toxic silicone sealant (Kuzyakov and, 01), then CO 2 from the soil column was periodically circulated through the trapping system for 48 hours and trapped in an alkaline trapping solution (0.5 M NaOH). Using this system, CO 2 trapping efficiency was greater than 99% ( & Coleman, 1989), eliminating preferential sorption of 13 CO 2 vs 12 CO 2. Blanks were included to correct for handling errors. An aliquot of the NaOH solution was analyzed for total C using a TOC Analyzer. The remainder of the trapping solution was mixed with excess SrCl 2 and the δ 13 C of the precipitate (SrCO 3 ) was analyzed by mass spectrometry (Harris et al., 1997). The δ 13 C values of the CO 2 in the atmosphere were determined in the same way as the soil CO 2. Analytical and experimental controls were employed. Soil-derived CO 2 and plant-derived CO 2 were separated using the δ 13 C value of plant
3 shoots as one end-member and using the δ 13 C values of CO 2 from the unplanted soil only treatments as the other end-member. Soil-derived CO 2 was a measure of SOM decomposition. Plant-derived belowground CO 2 was a measure of total rhizosphere respiration. In the field experiment, the closed circulation chamber method was used ( et al., 00). A narrow inverted box ( cm long by 5 cm wide by 5 cm deep) with air inlets and outlets attached and covered with aluminum foil was installed into each plot at the beginning of the experiment. During each measurement period, total CO 2 from soil efflux was absorbed in a NaOH trap for 24 hours and its δ 13 C was analyzed and partitioned into plant-derived and soil-derived C as described above. At the end of the experiments, shoots were cut at the base and separated into species. Roots in soil cores (5 cm ID, 60 cm depth) taken from field plots and roots in each container in the greenhouse experiment were hand-picked and washed. Shoots, roots, and soil were dried at 60 C for 48 hours, weighed on an analytical balance, and their δ 13 C values were determined by mass spectrometry. The δ 13 C values of total soil organic C were also determined. Plant-derived soil organic C, or rhizodeposition, was separated from original soil C using the 13 C method. Total N contents of shoots, roots, and soil were measured on a CHN Analyzer. Results Results from the herbaceous species in the greenhouse experiment show consistently negative rhizosphere effects on SOM decomposition, meaning that SOM decomposition was greater in unplanted treatments than in treatments with plants (Figure 1). Analysis of variance (ANOVA) revealed a significant effect of container size (P = 0.001) with priming effects consistently more negative in the large buckets than the small pots, but no effect of species or interaction between species and container size. Priming Effect (%) Buckets Pots -60 Grass Forb Clover Combo Figure 1. Rhizosphere priming effect as a percentage of respiration from unplanted controls for three plant species and a combination of all three in two container sizes. Error bars = 1 SD.
4 In contrast, the tree species in the greenhouse experiment induced consistently positive rhizosphere effects on SOM decomposition (Figure 2). ANOVA revealed a significant effect of container size and species (P = and 0.03, respectively), and a significant interaction between species and container size (P = 0.003) Pots Buckets Priming Effect (%) Oak Pine Redwood Aspen Figure 2. Rhizosphere priming effect as a percentage of respiration from unplanted controls for four tree species in two container sizes. Error bars = 1 SE. Measurements from the field experiment and of the herbaceous species in the greenhouse experiment indicate that rhizosphere respiration scales with total root N with similar exponents and intercepts across species and growth conditions (Table 1 & Figure 3). Field measurements were highly variable and had higher, although not significantly different, scaling exponents and intercepts compared to those obtained from greenhouse measurements (Table 1). These discrepancies may be due to difficulties with determining the appropriate soil volume and root N contained therein for field plots. Lateral diffusion of CO 2 or significant contributions of CO 2 from below our 60 cm sampling depth could cause systematic errors in the calculated ratio of respiration to soil volume and accompanying root N. Most rates of rhizosphere priming were negative, meaning that SOM decomposition was greater in unplanted treatments than in treatments with plants. In both the greenhouse and the field, total root biomass was the best predictor of the magnitude of rhizosphere priming (Figure 4). Once analyses from the final respiration measurements and destructive harvest of the tree species are complete we will be able to include them in these analyses and determine whether they conform to the same scaling relationship and whether root biomass explains their rates of rhizosphere priming or if another variable is a better predictor.
5 Table 1. Scaling of rhizosphere respiration with total root N. Site Plant n Intercept Exponent Lower CI Upper CI R 2 All All Greenhouse All Greenhouse Grass Greenhouse Forb Greenhouse Clover Field All All relations were significant (P < 0.001). There were no significant differences (P < 0.05) in slopes or intercepts among relations. All equations were fit using the log log version of the equation: Y = Y O M b. Reduced major axis intercepts and slopes (exponents) are shown, as well as the lower and upper 95% confidence interval (CI) of the exponent, and R 2. Total rhizosphere respiration (nmol s -1 ) Greenhouse Field Total root nitrogen (g) Figure 3. Root N in relation to rhizosphere respiration. Both are on log (base 10) scales. Primed C (mg day -1 ) y = x P < 0.001, r 2 = Total Root Biomass (g) Figure 4. Root biomass in relation to rhizosphere primed soil C for both field and greenhouse experiments. Primed C = soil -derived CO 2 -C in planted treatment minus unplanted control.
6 There is a gap in our knowledge about how rhizosphere respiration may scale with root biomass or other related quantities. Based on a synthesis of four experiments, Reich et al. (06) have shown that whole-plant respiration rate scales isometrically (i.e., scaling exponent 1) with total plant biomass N content, and that this scaling relation is independent of plant taxonomic groupings or growth conditions (e.g., lighting, nutrients, temperature and atmospheric CO 2 ). Unfortunately, they did not provide the scaling relation between root respiration rate and root nitrogen content. However, based on the information given in the paper, one may deduce that the scaling relation between root respiration rate and root N content should be very similar to the scaling relation for the whole plant because the scaling for the aboveground part is virtually identical to that for the whole plant. One cautionary note is that their root respiration rates were all based on measurements using excised roots, which is highly controversial because the respiration rate of an excised root may not truly represent the respiration rate of an intact root. Furthermore, respiration rates of excised roots are no doubt different from total rhizosphere respiration rates because rhizospheric microbial associations are either absent or highly destructed after root excision. Our results suggest that rhizosphere respiration can indeed be scaled using total root N content and that rhizosphere priming effects on SOM decomposition can potentially be scaled using total plant biomass. This is the first attempt to fill the gap of our knowledge in scaling rhizosphere processes. References Bever, J.D. 03. Soil community feedback and the coexistence of competitors: conceptual frameworks and empirical tests. New Phytologist 157: Bolker BM, Pacala SW, and Parton WJ Linear analysis of soil decomposition: Insights from the CENTURY model. Ecological Applications 8: Bowden, R.D., K.J. Nadelhoffer, R.D. Boone, J.M. Melillo, and J.B. Garris Contributions of aboveground litter, belowground litter, and root respiration to total soil respiration in a temperature mixed hardwood forest. Can. J. For. Res. 23: , W Measurement of rhizosphere respiration and organic matter decomposition using natural 13 C. Plant and Soil 183: , W Rhizosphere feedbacks in elevated CO 2. Tree Physiology 19: , W. and Coleman D.C A simple method for measuring CO 2 in a continuous airflow system: Modifications to the substrate-induced respiration technique. Soil Biol. Biochem. 21: , W. and F.A. Dijkstra. 07. Theoretical proof and empirical validation of a continuous labeling method using naturally 13 C-depleted carbon dioxide. Journal of Integrative Plant Biology 49: W. and Kuzyakov Y. 05. Root effects on soil organic matter decomposition. In: Zobel RW, Wright SF (eds.) Roots and Soil Management: Interactions between Roots and the Soil, Agronomy Monograph no. 48. ASA-SSSA, Madison, Wisconsin., W., D. A. Sims, Y. Q. Luo, D. W. Johnson, J. T. Ball, and J. S. Coleman. 00. Carbon budgeting in plant-soil mesocosms under elevated CO 2 : locally missing carbon? Global Change Biology 6:
7 , W. X., D. W. Johnson, and S. L. Fu. 03. Rhizosphere effects on decomposition: Controls of plant species, phenology, and fertilization. Soil Science Society of America Journal 67: Coleman, D. C., Odum E. P., and Crossley D. A Soil biology, soil ecology, and global change. Biol. Fert. Soils 14, Dalias P., Anderson J.M., Bottner P. et al. 01. Temperature responses of carbon mineralization in conifer forest soils from different regional climates incubated under standard laboratory conditions. Global Change Biology 7: Dijkstra, F.A., and W Interactions between soil and tree roots accelerate long-term soil carbon decomposition. Ecology Letters 10: Fu, S. L., and W Rhizosphere priming effects on the decomposition of soil organic matter in C-4 and C-3 grassland soils. Plant & Soil 238: Fu, S., W., and R. Susfalk. 02. Rhizosphere respiration varies with plant species and phenology: A greenhouse pot experiment. Plant & Soil 239: Hanson, P.J., N.T. Edwards, C.T. Garten, and J.A. Andrews. 00. Separating root and soil microbial contributions to soil respiration: A review of methods and observations. Biogeochemistry 48: Jenny H Factors of Soil Formation: A system of Quantitative Pedology. McGraw-Hill, New York. Jones, D.L., A. Hodge, and Y. Kuzyakov. 04. Plant and mycorrhizal regulation of rhizodeposition. New Phytologist 163: Klironomos, J.N., J. McCune, M. Hart, and J. Neville. 00. The influence of arbuscular mycorrhizae on the relationship between plant diversity and productivity. Ecology Letters 3: Kuzyakov, Y. 02. Separating microbial respiration of exudates from root respiration in nonsterile soils: a comparison of four methods. Soil Biology & Biochemistry 34: Kuzyakov, Y. and W Photosynthesis controls of rhizosphere respiration and organic matter decomposition. Soil Biology & Biochemistry 33: Parton W.J., Schimel D.S., Cole C.V. et al Analysis of factors controlling soil organic matter level in Great Plains grasslands. Soil Science Society of America Journal 51: Personeni E., Lüscher A., and Loiseau P. 05. Rhizosphere activity, grass species and N availability effects on the soil C and N cycles. Soil Biology and Biochemistry 37: Reich, P.B., M. G. Tjoelker, J-L Machado, and J. Oleksyn. 06. Universal scaling of respiratory metabolism, size and nitrogen in plants. Nature 439: Reynolds, H.L., A. Packer, J.D. Bever, and K. Clay. 03. Grassroots ecology: Plant-microbesoil interactions as drivers of plant community structure and dynamics. Ecology 84: Schimel, D.S Terrestrial ecosystems and the carbon-cycle. Global Change Biology 1: This research was funded by the Kearney Foundation of Soil Science: Understanding and Managing Soil-Ecosystem Functions Across Spatial and Temporal Scales, Mission ( The Kearney Foundation is an endowed research program created to encourage and support research in the fields of soil, plant nutrition, and water science within the Division of Agriculture and Natural Resources of the University of California.
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