Short-term effects of defoliation on the soil microbial community associated with two contrasting Lolium perenne cultivars

Abstract

Intra-species variation in response to defoliation and soil amendment has been largely neglected in terms of the soil microbial community (SMC). The influence of defoliation and soil fertiliser amendment on the structure of the SMC was assessed with two Lolium perenne cultivars contrasting in ability to accumulate storage reserves. Plant response to defoliation was cultivar specific and depended on the nutrient amendment of the soil. Results suggested a greater ability to alter plant biomass allocation in the low carbohydrate accumulating cultivar (S23) compared to the high carbohydrate cultivar (AberDove) when grown in improved (IMP), but not in unimproved (UNI), soil. Although differences in plant growth parameters were evident, no treatment effects were detected in the size of the active microbial biomass (total phospholipid fatty acid (PLFA) 313.8 nmol g⁻¹ soil±33.9) or proportions of PLFA signature groups. A lower average well colour development (AWCD) of Biolog sole carbon source utilisation profiles (SCSUPs) in defoliated (D) compared to non-defoliated (ND) treatments may be indicative of lower root exudation 1 week following defoliation, as a consequence of lower root non-structural carbohydrate (NSC) concentrations. Within the bacterial community the lower cyclopropyl-to-precursor ratio of PLFAs, and the trans/cis ratio of 16:1w7, in UNI relative to IMP soil treatments indicates lower physiological stress in UNI soils regardless of L. perenne cultivar. Discrimination of broad scale SMC structure, measured by PLFA analysis, revealed that soil treatment interacted strongly with cultivar and defoliation. In IMP soils the SMCs discriminated between cultivars while defoliation had little effect. Conversely, in UNI soils defoliation caused a common shift in the SMC associated with both cultivars, causing convergence of overall community structure. Separation of SMC structure along the primary canonical axis correlated most strongly (P<0.001) with root:shoot ratio (47.6%), confirming that differences in cultivar C-partitioning between treatments were influential in defining the rhizosphere microbial community.

Introduction

The physiological adaptations of grasses to tolerate periodic defoliation by grazing animals have been studied previously (Ferraro and Oesterheld, 2002). However, much less is known about how plant physiological responses to constraints on growth affect feedbacks between the soil microbiota and plant productivity. In systems receiving little or no fertiliser input, the availability of nutrients for plant growth is heavily dependent on cycling through the microbial biomass. The quantity and quality of plant inputs to soil (litter, root turnover, and root exudation) are key drivers of microbial activity and community structure (Campbell et al., 1997, Grayston et al., 1998). Plant productivity is therefore coupled to the functioning of the soil microbial community (SMC) through mineralisation and immobilisation processes that are driven by root derived C (rhizodeposition). Determining the factors which illicit change in the SMC is of fundamental importance to understanding these interactions.

Plant growth in grassland ecosystems, where fertiliser inputs are uncommon, is often limited by available nutrients (Tisdale and Nelson, 1975). There is evidence that root exudation accounts for a greater proportion of assimilated C under N limited conditions compared with N sufficient conditions (Paterson and Sim, 1999, Paterson and Sim, 2000), possibly contributing to a larger, more active SMC in unfertilised grassland soils (Yeates et al., 1997). Through stimulating the SMC, increased exudation may increase nutrient turnover. Bardgett et al., 1996, Bardgett et al., 1997 have demonstrated a positive relationship between grazing intensity, the size and activity of the SMC and dominance by bacteria. Quantitative and qualitative changes in detrital inputs to the soil are likely determinants of herbivore-induced changes in the SMC (Bardgett et al., 1997). However, the control of plant physiological responses affecting these inputs on microbial activity and community structure are less well understood. Defoliation is a strong perturbation to plant C flow, dramatically reducing photosynthetic capacity, and resulting in preferential carbon allocation above-ground at the expense of below-ground allocation (Morvan-Bertrand et al., 1999). Re-growth potential has been correlated to the concentration of stored carbohydrates in the basal stubble region of forage species (Donaghy and Fulkerson, 1998). Water-soluble carbon (WSC) and amino components, collectively termed non-structural carbon (NSC) (Davis et al., 1995), are rapidly re-mobilised following defoliation to ensure continued assimilate supply to the growing meristems (Morvan-Bertrand et al., 1999). As a result of differential effects on C partitioning and ability to re-grow, the extent to which defoliation alters the quality and quantity of carbon flow from roots is likely to differ between species and cultivars. The SMC often responds to defoliation independently of changes in the root biomass, suggesting that they result from changes in root exudation (Guitian and Bardgett, 2000). While species comparisons are common, the effects of cultivar-specific responses to defoliation have been largely neglected in terms of the SMC, despite significant cultivar-specific responses being reported in terms of altered C partitioning and root functioning (Fulkerson et al., 1994). New forage varieties are often developed for high productivity and nutritional value, without particular attention being paid to the effects on below ground carbon and nutrient cycling. Understanding the driving forces on the SMC is particularly important in developing sustainable management practices.

This study aimed to determine the influence of defoliation and soil fertiliser amendment on the structure of the rhizosphere SMC associated with two Lolium perenne cultivars with contrasting carbon storage characteristics. The L. perenne cultivars selected were AberDove and S23, previously reported as high and low WSC accumulating cultivars, respectively (Humphreys, 1989a, Humphreys, 1989b, Smith et al., 2001). It was hypothesised that: (i) due to differences in below-ground C allocation, the SMC associated with the two L. perenne cultivars would differ in size and structure; (ii) following defoliation the SMC is likely to respond to altered resource availability resulting from changes to C assimilation, C allocation, and nutrient uptake. The perturbation is likely to be more evident in L. perenne S23 due to lower C reserves available to buffer the defoliation effect. In AberDove, greater C reserves are likely to be used for rapid re-growth and a faster return to undisturbed C assimilation, C allocation and nutrient acquisition; (iii) soil fertility will affect the SMC directly through influencing microbial available N, and indirectly as a consequence of increased primary production, and through cultivar specific effects on C partitioning, root production, and rhizodeposition.