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New Approach for Capturing Soluble Root Exudates in Forest Soils

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New Approach for Capturing Soluble Root Exudates in Forest Soils Functional Ecology 2008, 22, 990–999 doi: 10.1111/j.1365-2435.2008.01495.x BELOWGROUNDBlackwell Publishing Ltd RESPONSES TO CLIMATE CHANGE New approach for capturing soluble root exudates in forest soils Richard P. Phillips*, Yael Erlitz, Raven Bier and Emily S. Bernhardt Department of Biology, Duke University, Durham, NC 27708, USA Summary 1. Soluble root exudates are notoriously difficult to collect in non-hydroponic systems because they are released in a narrow zone around roots and are rapidly assimilated by rhizosphere microbes. This has substantially limited our understanding of their rates of release and chemical composition in situ, and by extension, their ecological significance. 2. Here we describe the advantages and limitations of several commonly employed methods for measuring exudation with respect to their potential adaptability for field use in forest ecosystems. Then, we introduce a novel in situ method for measuring exudation in forest soils, and present preliminary results of the spatial and temporal dynamics of loblolly pine (Pinus taeda L.) exudation at the Duke Forest FACTS-1 site, North Carolina, USA from April 2007 to July 2008. 3. Exudation rates varied by an order of magnitude, with the highest rates occurring in late-June 2007 and mid-July 2008, and the lowest rates occurring during late-August 2007. On an annual basis, we estimate pine roots in the upper 15 cm of soil release c. 9 g C m–2 year–1 via this flux, which represents 1–2% of net primary productivity at the site. 4. The magnitude of exudation rates did not differ across an N availability gradient but did track general patterns of below-ground C allocation at the site. Exudation was well-predicted by root morphological characteristics such as surface area and the number of root and mycorrhizal tips, further supporting a possible link between root C allocation and exudation. 5. Because all methods for estimating exudates introduce experimental artefacts, we suggest that only a limited amount of ecologically relevant information is probably gleaned from a single method. Thus, a complementary suite of experimental approaches will best enable researchers to understand consequences of changing patterns of exudation in the wake of global environmental change. Key-words: below-ground C allocation, fine roots, rhizodeposition, rhizosphere Functional Ecology (2008) xx, 000–000 consist of sugars, amino acids, and organic acids (Neumann Introduction & Romheld 2001), and this flux is believed to represent Because they occur in a narrow zone of soil around roots and between 1% and 10% of net assimilated C (Jones et al. 2004). are rapidly assimilated by soil microbes, root exudates are Despite the relatively small magnitude of this flux, root exudates one of the most poorly quantified components of the below- are believed to play an important role in mediating soil nutri- ground C cycle (Wardle 2002; Paterson 2003). Root exudates ent availability in ecosystems due to their chelating properties are soluble, low molecular weight organic compounds that can and their role in stimulating microbial activity (Lynch 1990; be passively released to soil due to the concentration gradient Marschner 1995). Furthermore, exudates are primarily derived between root cells and soil solution or which are actively from recently-assimilated photosynthate (Neumann & Romheld secreted in response to metal toxicity, nutrient stress and the 2001) and thus, may represent a semi-continuous input of labile presence/absence of plant and microbial taxa (Marschner C to soil in contrast to transient inputs of C resulting from leaf 1995; Jones et al. 2004; Bais et al. 2006). Most exudates litter inputs (Kuzyakov & Cheng 2001). Significant methodological challenges limit our ability to *Correspondence author. Department of Biology, Indiana University, accurately measure exudation or to determine how environ- Bloomington, IN 47405, USA. E-mail: [email protected] mental variables affect exudation composition or rates. In © 2008 The Authors. Journal compilation © 2008 British Ecological Society Root exudation in trees 991 general, all exudation methods attempt to overcome a set of have generally been used because the exudates can be more common challenges: (i) capturing exuded C before microbial readily trapped and separated from the medium (Jones et al. assimilation, (ii) selecting a medium that does not affect root 2004). physiology and exudate recovery, and (iii) distinguishing Two primary types of culture-based systems are static and exuded compounds from other soluble C compounds in the percolating (i.e. non-static) trap solutions. In general, both medium. Such challenges become even more formidable when systems are similar in that root systems are submerged in a adapting a method for field use. In most cases, roots need to medium from which exudates are trapped and collected over be temporarily removed from the soil to be studied, which a set period of time. The primary difference between the two may stress or injure the root and disrupt mycorrhizal networks systems is the replenishment of the trap solution in the (Neumann & Romheld 2001). Moreover, root and rhizosphere percolating system which maintains the diffusion gradient processes are highly variable in space and time (Hinsinger between root cells and trap solution, and minimizes the et al. 2005), which pose challenges to developing experimental re-uptake of exuded sugars and amino acids by roots. Thus, protocols that capture this variability, and to scaling measured an important first step in employing a static trap solution is values to the ecosystem-scale. deciding when to sample the trap solution. The challenge is to Not surprisingly, there have been few measurements of sample the solution after a sufficient amount of C has been exudation from trees in situ (but see Smith 1976). This is parti- exuded (i.e. to reduce signal to noise artefacts), but before cularly true for forest ecosystems where deep roots are difficult exudation rates are affected by C accumulation in the trap to access and whole-system isotopic tracers are difficult to solution and re-uptake of exudates by roots (Jones et al. 2004; employ. Exudation measurements of tree seedlings grown in Personeni et al. 2007). An advantage of percolating solutions controlled experimental systems suggest that differences in is that there is no bias associated with exudate accumulation biotic factors (e.g. plant species, phenology, mycorrhizal status), affecting efflux or influx of compounds, and thus percolating abiotic factors (e.g. soil fertility, moisture, temperature), and systems may better reflect a rhizosphere environment where the experimental system employed may all influence the rates microbes are present. However, percolating solutions have a and composition of exudates (Grayston et al. 1996). This has disadvantage in that they generally require a much greater led many researchers to conclude that exudation in forest eco- volume of solution, and several post-collection steps may be systems should be placed into a ‘black box’ of soil processes necessary to for subsequent chemical analyses. In addition, and estimated through modelling approaches (Luo et al. percolating solutions may not uniformly collect exudates 2001) or as residual terms in mass-balance calculations of released by roots if the solution follows preferential flow- below-ground C flux (Fahey et al. 2005; van Hees et al. 2005). paths in the medium. Because percolating solutions require However, such approaches contribute little to our under- the continuous pumping of solution through the medium, standing of the mechanisms that control this process, and they may also be less amenable for adaptation to field studies. by extension, the potential role of exudates in mediating In both static and percolating systems, the type of growth microbial activity, nutrient transformations, and feedbacks to medium selected is known to have important consequences primary productivity and ecosystem C storage (Cheng 1999; for root growth, architecture and exudation. Pure solution Phillips 2007). cultures (generally a dilute salt or nutrient solution) offer Below-ground processes such as exudation mediate the flux simplicity in maintenance and sample collection. However, of energy and materials in terrestrial ecosystems, but our under- the lack of mechanical impedance for roots in non-solid media standing of how such processes influence feedbacks to eco- may affect root morphology and exudation rates (Neumann system C and N cycling remains limited owing to significant & Romheld 2001). Small glass beads and acid-washed sand methodological obstacles. The goals of this paper are to: (i) have commonly been employed but such media have limitations review existing methods for collection of exudates, (ii) describe as well, as sorption of exuded compounds to these media may a newly-developed method for collecting exudates from tree result in incomplete recovery of exudates or mischaracterization roots in situ, and (iii) present data collected over a 15 month of the exudate composition (Neumann & Romheld 2001). In period from trees at the Duke Forest Free Air CO2 Enrichment our own experiments, we have found that acid-washed sand Experiment. (3 m HCl) can be both a source and sink for C (R.P. Phillips, unpublished data). Thus, careful consideration should be given to selecting an appropriate medium for the trapping solution EXISTING EXUDATION METHODS as small amounts of sorbed C or contamination of C from the Several different approaches have been
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