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Changes in Soil Hyphal Abundance and Viability Can Alter the Patterns of Hydraulic Redistribution by Plant Roots

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Changes in Soil Hyphal Abundance and Viability Can Alter the Patterns of Hydraulic Redistribution by Plant Roots Plant Soil (2012) 355:63–73 DOI 10.1007/s11104-011-1080-8 REGULAR ARTICLE Changes in soil hyphal abundance and viability can alter the patterns of hydraulic redistribution by plant roots José Ignacio Querejeta & Louise M. Egerton-Warburton & Iván Prieto & Rodrigo Vargas & Michael F. Allen Received: 13 June 2011 /Accepted: 22 November 2011 /Published online: 9 December 2011 # Springer Science+Business Media B.V. 2011 Abstract Results Contrary to expectations, both upper soil and Background and aims We conducted a mesocosm receiver seedlings contained significantly greater pro- study to investigate the extent to which the process portions of HLW in mesocosms where the abundance of of hydraulic redistribution of soil water by plant roots mycorrhizal hyphal links between donor and receiver is affected by mycorrhizosphere disturbance. roots had been sharply reduced by fungicide application. Methods We used deuterium-labeled water to track the Reduced soil hyphal density and viability likely ham- transfer of hydraulically lifted water (HLW) from pered soil moisture retention properties in fungicide- well-hydrated donor oaks (Quercus agrifolia Nee.) to treated mesocosms, thus leading to faster soil water drought-stressed receiver seedlings growing together depletion in upper compartments. The resulting steeper in mycorrhizal or fungicide-treated mesocosms. We soil water potential gradient between taproot and upper hypothesized that the transfer of HLW from donor to compartments enhanced hydraulic redistribution in receiver plants would be enhanced in undisturbed fungicide-treated mesocosms. (non-fungicide-treated) mesocosms where an intact Conclusions Belowground disturbances that reduce soil mycorrhizal hyphal network was present. hyphal density and viability in the mycorrhizosphere can Responsible Editor: Angela Hodge. José Ignacio Querejeta, Louise M. Egerton-Warburton and Iván Prieto contributed equally to this work. J. I. Querejeta (*) I. Prieto Departamento de Conservación de Suelos y Aguas, Estación Experimental de Zonas Áridas-Consejo Superior Centro de Edafología y Biología Aplicada del de Investigaciones Científicas (EEZA-CSIC), Segura-Consejo Superior de Investigaciones La Cañada de San Urbano, Científicas (CEBAS-CSIC), Almería, Spain Campus Universitario de Espinardo, 30100 Murcia, Spain R. Vargas e-mail: [email protected] Departamento de Biología de la Conservación, Centro de Investigación Científica y de Educación Superior de Ensenada (CICESE), Ensenada, Mexico L. M. Egerton-Warburton Chicago Botanic Garden, M. F. Allen 1000 Lake Cook Road, Center for Conservation Biology, University of California, Glencoe, IL, USA Riverside, CA, USA 64 Plant Soil (2012) 355:63–73 alter the patterns of hydraulic redistribution by roots HL favors the maintenance of fine root function in dry through effects on soil hydraulic properties. soil (Caldwell et al. 1998;Espeletaetal.2004;Bauerle et al. 2008) and plays a crucial role in the direct transfer Keywords Hydraulic lift . Water redistribution . of water from roots to associated mycorrhizal fungal Mycorrhizal fungi . Quercus agrifolia . Soil water symbionts (Querejeta et al. 2003). This last process retention properties . Mycorrhizosphere disturbance can prolong the lifespan of mycorrhizal fungal hyphae in dry soil (Querejeta et al. 2007a, 2009), which may in Abbreviations turn improve the water and nutrient status of the host HLW Hydraulically lifted water plant (Egerton-Warburton et al. 2008). Furthermore, HL Hydraulic lift shallow-rooted plants growing within the rhizosphere CMN Common mycorrhizal network of a deep rooted plant conducting HL can benefit from δD Deuterium this process, thus leading to water parasitism among EMF Ectomycorrhizal fungi neighboring plants (Caldwell 1990; Ludwig et al. AMF Arbuscular mycorrhizal fungi 2003;Prietoetal.2011). For instance, Dawson (1993) found that shallow rooted plants growing near a large maple tree conducting HL were able to use up to 60% of hydraulically lifted water (HLW), and thereby showed Introduction higher stomatal conductance and photosynthetic rate than those with no access to HLW. Hydraulic redistribution is the passive movement of There are two main pathways by which HLW from water from wet to dry soil layers through plant root deep soil layers can be taken up by shallow-rooted systems (Burgess et al. 1998). Water potential gradients plants: either directly from soil after water efflux from in the soil profile provide the driving force for this the roots of a neighboring deep-rooted plant, or via process, and determine its direction and magnitude common mycorrhizal networks (CMNs) connecting the (Scholz et al. 2008). This phenomenon is termed roots of donor and receiver plants. Egerton-Warburton et “hydraulic lift” (HL) when water moves upward from al. (2007) used deuterium-labeled water and fluorescent deep, wet soil layers to upper, drier layers (Richards and tracers to demonstrate that ectomycorrhizal and arbuscu- Caldwell 1987). Hydraulic redistribution can also occur lar mycorrhizal extraradical hyphae provide a potential in a downward direction, from wet shallow to drier, pathwayforthetransferofHLWbetweenplantssharing deeper soil layers, (e.g., after a rain event; Burgess et common mycorrhizal networks. In their study, the trans- al. 2001; Hultine et al. 2003; Schulze et al. 1998), or fer of water between well-hydrated donor plants and laterally within the plant root system (Smart et al. 2005). drought-stressed receiver plants appeared to be driven Efflux of water from roots to soil usually takes place by source-sink relationships mediated by water potential during the night when plant transpiration is minimal gradients similar to those that drive the process of HL. (Caldwell and Richards 1989; Richards and Caldwell Thus, when the shallow rooted receiver becomes a sink 1987).HLhasbeenreportedinawidearrayofplant during periods when the upper soil is dry, HLW may taxa ranging from small grasses to large trees (Caldwell move from deep, wet soil layers via donor roots and et al. 1998), and in a wide variety of ecosystems, from associated mycorrhizal mycelium into the receiver plant. arid and semi-arid environments (Richards and Caldwell Redistribution of water via CMNs, and/or HLW efflux 1987; Yoder and Nowak 1999; Armas et al. 2010; Prieto from donor roots to soil followed by subsequent uptake et al. 2010) to mesic temperate environments (Emerman by receiver roots, represent two alternative pathways for and Dawson 1996; Kurz-Besson et al. 2006), tropical inter-plant water transfer that are not mutually exclusive forests (Meinzer et al. 2004; Moreira et al. 2003;Scholz (Plamboeck et al. 2007;Warrenetal.2008). However, et al. 2008), and even mangroves (Hao et al. 2009). the relative contributions of these two pathways in the HL exerts multiple beneficial effects on plant water transfer of HLW between neighboring plants has not balance, such as enhancing transpiration during dry been investigated so far. periods and delaying the onset of plant drought In the present study, our primary goal was to assess stress (Caldwell and Richards 1989;Ryeletal. the impact of mycorrhizosphere disturbance (i.e., fungi- 2002;Caldwelletal.1998; Meinzer et al. 2004). cide addition) on hydraulic redistribution of soil water Plant Soil (2012) 355:63–73 65 by plant roots. More specifically, we wanted to Germinated acorns were inoculated by repeated addition determine whether changes in the abundance and of suspensions of spores of the ectomycorrhizal fungi viability of soil hyphae might influence the pat- Pisolithus tinctorius (Pers.) Coker & Couch and Sclero- terns of hydraulic redistribution during moderate derma sp. (Mycorrhizal Applications Inc., Grants Pass, drought. We also investigated the relative contri- Oregon) suspended in deionized water (total 15×108 butions of each pathway (root–soil–root pathway, spores per mesocosm). All mesocosms were irrigated or redistribution through CMNs) to the transfer of to field capacity twice a week for 22 months. The HLW between donor and receiver plants during control plants were watered with a Hoagland nutrient mild drought. We used deuterium-labeled water to solution so that they would achieve a size similar to that track the transfer of HLW from well-hydrated, of the inoculated plants at the end of the experiment. deep-rooted donor oaks to drought-stressed receiver Greenhouse temperatures were maintained at 18–24°C oak seedlings growing together in mycorrhizal or (night/day; October to May), and 22–35°C (June– fungicide-treated mesocosms. We hypothesized that October). The 20 mm air gap between upper and receiver seedlings would contain a greater propor- taproot compartments was initially filled with soil tion of HLW in mesocosms where an intact CMN to allow for root growth and extension into the taproot was present than in mesocosms where mycorrhizal compartment. Seventeen months after mesocosm estab- hyphal links between donor and receiver oaks had lishment, thick woody roots were observed bridging the been severely damaged by fungicide application (i.e., gap between upper and taproot compartments. The soil mycorrhizosphere disturbance). filling the gap was then washed and removed. Eighteen months after mesocosm establishment, coast live oak seedlings (2 cm tall and <10 cm of Materials and methods taproot length) were excavated and transplanted into the upper root compartments of the mesocosms to Mesocosm establishment serve as receiver plants (three receiver seedlings per mesocosm). Receiver
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