One of the most likely impacts of global change on ecosystems is a change in plant species distributions, and therefore in the structure of the plant community (Bardgett, Freeman & Ostle 2008; Cornwell et al. 2008; Wookey et al. 2009). Such changes in plant community structure have an impact on the soil microbial community and the processes they mediate, and this in turn is likely to feedback to global climate change by altering the storage and loss of soil carbon (C) and primary production (Wardle 2002; Bardgett, Freeman & Ostle 2008; De Deyn, Cornelissen & Bardgett 2008; Bardgett, De Deyn & Ostle 2009). Understanding the mechanisms behind these effects and being able to predict how ecosystems may respond to global change are therefore of importance. One emerging approach aimed at gaining a more mechanistic understanding of how plant species affect ecosystem functioning is to study relationships of plant traits to ecosystem properties (Grime 2001; Lavorel & Garnier 2002; Chapin 2003; Diaz et al. 2007; De Deyn, Cornelissen & Bardgett 2008). Indeed, links of plant traits to litter decomposition and net nitrogen (N) mineralization have already been demonstrated (Tilman & Wedin 1991; Cornelissen et al. 1999; van der Krift & Berendse 2001; Garnier et al. 2004; Kazakou et al. 2006; Cornwell et al. 2008; Fortunel et al. 2009). Given the strong inter-dependence of the above-ground and below-ground subsystems, it is likely that plant traits could also be useful for predicting how, and understanding the mechanisms by which, plants influence C and phosphorus (P) cycling (Wardle et al. 2004; Eviner, Chapin & Vaughn 2006; De Deyn, Cornelissen & Bardgett 2008; van der Heijden, Bardgett & van Straalen 2008). However, very few studies have comprehensively examined whether plant traits can be related to a broad range of key soil properties.
Plant species influence the below-ground subsystem primarily by determining the quantity and quality of leaf litter and root inputs that enter the soil (Gill & Jackson 2000; Norby & Jackson 2000; Wardle 2002; De Deyn, Cornelissen & Bardgett 2008). Theory and recent global-scale studies show that the quality of leaf litter inputs to soil is strongly related to evolutionary trade-offs in plant growth strategies to maximize resource gain or to conserve nutrients (Reich et al. 1998; Grime 2001; Wright et al. 2004). Species that maximize resource gain are more typical of fertile soils, tend to have a fast growth rate and produce high-quality, short-lived, N-rich leaves and subsequently high-quality litter. These plant traits are thought to promote bacterial-based food webs with a corresponding fast and ‘open’ nutrient cycle, which results in a positive feedback to plant growth and the quality of litter inputs by maintaining high nutrient availability, but reduces soil C storage because of fast decomposition rates. Species that conserve nutrients show the opposite trends: they are more typical of infertile soils, tend to have slower growth rates and produce long-lived, low-N leaves. These plant traits are thought to promote a fungal-based food web with slow and conservative rates of nutrient cycling, which maintains low soil fertility levels, slow plant growth rates and low-quality litter inputs, but leads to high C storage because of low decomposition rates (Reich et al. 1998; Grime 2001; Wardle et al. 2004; Wright et al. 2004). Although these theories emphasize the fertility of the soil as a key determinant of plant growth strategies, it is also clear that species with very different strategies can co-exist on soils of the same initial fertility (Bowman et al. 2004; Personeni & Loiseau 2004; Ward et al. 2009).
The degree to which root traits show the same evolutionary trade-offs as above-ground traits is uncertain: some studies demonstrate that root traits may fall along a similar growth rate continuum (Grime et al. 1997; Wahl & Ryser 2000; Craine et al. 2002; Tjoelker et al. 2005; Roumet, Urcelay & Diaz 2006), but others show that relationships of leaf traits to root traits are weak (Craine et al. 2005) and that the same plant can have above-ground traits associated with the opposite growth strategy to that of its roots (Personeni & Loiseau 2004). Roots may also influence nutrient and C cycling through their exudates. The quantity of these is thought to be higher for faster-growing species (van der Krift et al. 2001; De Deyn, Cornelissen & Bardgett 2008), which may contribute to the proposed faster C and N cycling under these species through priming effects (van der Krift et al. 2001; Kuzyakov 2006). However, higher levels of root exudation may also result in reduced N cycling rates due to higher net N immobilization (Kuzyakov 2006). These results suggest that where root traits align with leaf traits, they could strengthen feedbacks between above-ground traits and soil properties, but that they also have the potential to weaken these feedbacks where they show different trends to above-ground traits, or where they have opposite effects on soil functioning. Although links of plant traits to N cycling in particular have been shown (Wedin & Tilman 1990; Scott & Binkley 1997; Eviner, Chapin & Vaughn 2006), to date no study has tested the proposed links with the soil microbial community, or comprehensively examined a wide range of leaf, litter and root traits and soil properties within a single study.
The overall goal of our study was to test whether differences in the traits of co-existing grassland species with different growth strategies are sufficient to cause divergence in soil properties when species are grown on the same initial soil, and whether this divergence is associated with leaf, litter and root traits in a predictable, consistent way. We aimed to cover an extensive range of soil properties relevant to below-ground ecosystem functioning, including soil microbial community structure, soil microclimate and C, N and P cycling. Specifically, we tested the hypotheses that: (i) plant traits associated with fast-growing species (e.g. high-quality leaves and litter) are associated with bacterial-dominated soil microbial communities and fast rates of soil C, N and P cycling, which in turn results in high nutrient availability and low C sequestration; and (ii) root traits show the same evolutionary trade-offs as leaf traits, and will therefore show similar relationships to soil properties as those of above-ground traits. These hypotheses were tested by sampling a unique, long-term field experiment at Sourhope, Scotland, UK (established in 1999/2000), which involves monoculture plots of common herbaceous species of semi-natural upland grassland that vary significantly in their nutrient requirements and growth strategies.