Grassland species root response to drought: consequences for soil carbon and nitrogen availability

Plant Soil (2016) 409:297–312 DOI 10.1007/s11104-016-2964-4 REGULAR ARTICLE Grassland species root response to drought: consequences for soil carbon and nitrogen availability Franciska T. de Vries & Caley Brown & Carly J. Stevens Received: 1 April 2016 / Accepted: 14 June 2016 / Published online: 23 June 2016 # The Author(s) 2016. This article is published with open access at Springerlink.com Abstract Background and Aims Root traits are increasingly used to predict how plants modify soil processes. Here, we assessed how drought-induced changes in root systems of four common grassland species affected C and N availability in soil. We hypothesized that drought would promote resource-conservative root traits such as high root tissue density (RTD) and low specific root length (SRL), and that these changes would result in higher soil N availability through decreased root N uptake, but lower C availability through reduced root exudation. Methods We subjected individual plants to drought under controlled conditions, and compared the response of their root biomass, root traits, and soil C and N availability, to control individuals. Results Drought affected most root traits through reducing root biomass. Only SRL and RTD displayed plasticity; drought reduced SRL, and increased RTD in small plants but decreased RTD in larger plants. Responsible Editor: Elizabeth M Baggs. Electronic supplementary material The online version of this article (doi:10.1007/s11104-016-2964-4) contains supplementary material, which is available to authorized users. F. T. de Vries (*) Faculty of Life Sciences, The University of Manchester, Oxford Road, Manchester M13 9PT, UK e-mail: C. Brown : C. J. Stevens Lancaster Environment Centre, Lancaster University, Lancaster LA1 4YQ, UK Reduced root biomass and a shift towards more resource-conservative root traits increased soil inorganic N availability but did not directly affect soil C availability. Conclusions These findings identify mechanisms through which drought-induced changes in root systems affect soil C and N availability, and contribute to our understanding of how root traits modify soil processes in a changing world. Keywords Aboveground-belowground linkages . Plant functional traits . Plasticity . Soil microbial properties . Soil processes . Climate change Introduction Ecologists are increasingly using plant traits for explaining and predicting ecosystem functioning. These approaches generally use the leaf economics spectrum (Wright et al. 2004), where exploitative leaf traits that maximise photosynthesis, such as high specific leaf area and leaf nitrogen content, maximize plant growth and nutrient uptake, and accelerate rates of soil nutrient and carbon cycling (e.g. Fortunel et al. 2009; Garnier et al. 2004; Grassein et al. 2015; Laughlin 2011; Orwin et al. 2010). Recently, ecologists have shifted their focus from aboveground plant functional traits to belowground traits for explaining soil and ecosystem processes (Bardgett et al. 2014). In contrast to leaves, roots are in contact with the soil and modify the soil environment directly by penetrating the soil, taking up water and 298 nutrients, releasing root exudates, and through the process of root turnover (Bardgett et al. 2014). Therefore, root functional traits might be better predictors of soil and ecosystem processes than leaf traits. Indeed, in recent work, root traits have been shown to explain a range of ecosystem properties and processes better than leaf traits. For example, root traits have been found to explain soil microbial community composition better than leaf traits in field and pot experiments (Legay et al. 2014; Orwin et al. 2010), as well as the availability of inorganic N and rates of denitrification and nitrification (Cantarel et al. 2015; Moreau et al. 2015; Orwin et al. 2010), and plant performance at a population level (Schroeder-Georgi et al. 2016). As a consequence of this growing body of evidence that links root traits to measures of ecosystem functioning, it has been proposed that root traits are central to ecosystem response to climate change (Bardgett et al. 2014). Root system properties have been shown to respond to climate change (Beidler et al. 2015; Nie et al. 2013), and these changes in root traits might have cascading effects on soil properties and ecosystem functioning. Particularly drought, which is expected to increase in some regions with global climate change, can have strong impacts on soil functioning by killing soil microbes and animals and causing a flush in C and N mineralization upon rewetting (as reviewed by Borken and Matzner 2009). Drought also strongly impacts on plant communities and can cause changes in aboveground and belowground species abundances through impacting on individual plant growth. Moreover, drought can alter root system architecture, and induce phenotypic plasticity in root traits. Thus, because drought simultaneously affects root systems and soil nutrient availability, there is the potential of these plant and soil responses to interact: roots can directly affect soil properties via uptake of water and nutrients, but roots can also indirectly affect soil nutrient and C availability via root exudation and turnover. In addition, root traits can display plasticity to changes in soil nutrient concentrations (e.g. Hodge 2004; Lambers et al. 2003). Plants can cope with drought through drought avoidance and drought tolerance strategies, which both depend on a combination of different functional traits. Drought avoidance strategies include high water use efficiency and low stomatal conductance through dense leaves, and investing in high root to shoot ratio; drought tolerance involves increased osmoprotectants and accumulation of carbohydrates in plant tissues (Brunner et al. 2015; Plant Soil (2016) 409:297–312 Kooyers 2015). These strategies are likely related to plant functional traits associated with the trade-off between fast growth or acquisitive-resource-use strategies and slow growth or conservative-resource-use strategies: slow growth confers stress resistance by reducing C demand for growth, thereby allowing for greater investment in defence traits (Chapin et al. 1993). In support of this hypothesis, drought tolerance through foliage senescence has been linked to resource-conservative growth strategies (Perez-Ramos et al. 2013), and traits like high root tissue density (RTD) and root dry matter content (RDMC) have been linked to drought resistance (Fort et al. 2013; Ryser 1996; Tjoelker et al. 2005; Wahl and Ryser 2000). However, in contrast with this hypothesis, thinner roots and the ability to elongate roots into deeper soil layers—both root traits linked to resource-acquisitive strategies—have been linked to drought avoidance and maintained growth under drought conditions (Comas et al. 2013; Padilla et al. 2013; Perez-Ramos et al. 2013; Zwicke et al. 2015). In addition to overall growth responses of plants to (...truncated)