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There are two ways by which herbivores can influence the quantity of resources entering the soil. In the short-term, the quantity of resources supplied to soil can be altered through effects of herbivory on plant C allo- cation and root exudation patterns, whereas in the long-term, the amount of organic matter returned to soil is affected by herbivore-induced shifts in net primary productivity (NPP). Both these mechanisms are intimately linked and collectively influence plant productivity and composition.

Plant allocation and exudation

Plants allocate large proportions of their assimilated C to root exudation (Bokhari 1977), which may stimulate the growth and activity of hetero- trophic microbes in the rhizosphere (Whipps and Lynch 1986). Both foliar (Holland et al. 1996; Paterson and Sim 1999; Murray et al. 2004) and root (Yeates et al. 1998; Denton et al. 1999; Grayston et al. 2001b) herbivory have been shown to lead to short-term increases in root exudation, which stimu- lates microbial biomass and C use efficiency by microbes in the rhizosphere (Mawdsley and Bardgett 1997; Denton et al. 1999; Guitian and Bardgett 2000; Hamilton and Frank 2001). In turn, this has been shown to increase the abundance of microbial-feeding fauna (Mikola et al. 2001; Hokka et al. 2004), but reduce AM infection (Gehring and Whitham 1994). Evidence is accumulating to show that these positive effects of herbivory on free-living rhizosphere microbes and higher level consumers in the soil food web can feedback positively to the plant through enhanced soil N availability. Hamilton and Frank (2001), for example, showed that simulated defoliation

of the grazing tolerant grass Poa pratensis led to increased leaf photosynthesis and root exudation of recently assimilated 13_{C, which in turn stimulated}

microbial biomass in the root zone. This in turn increased soil N availability and plant N acquisition, which ultimately benefited plant growth. It was proposed that such mechanisms could explain, in part, the compensatory response of grasses to grazing in high fertility grasslands (Hamilton and Frank 2001) (Fig. 5.1). Similarly, simulated herbivory of tree seedlings has been shown to lead to enhanced N mineralization and inorganic N avail- ability in rhizosphere soil, presumably owing to a stimulation of biological activity resulting from increased rhizodeposition (Ayres et al. 2004). While there is much interspecies variability in the response of plants to defolia- tion (Guitian and Bardgett 2000; Hokka et al. 2004)—and responses are likely to vary with growth stage of the plant—these findings collectively suggest that physiological responses of plants to herbivory have the potential to stimulate rhizosphere processes that ultimately feedback positively on plant nutrition and plant productivity (Bardgett and Wardle 2003).

Changes in plant productivity

In the long-run, herbivory is often observed to significantly alter NPP, both above- and below-ground. Optimization of above-ground NPP by grazing mammals is well known to occur in grassland ecosystems at intermediate levels of herbivory (McNaughton 1985), and there is theoretical support for promotion of NPP by foliar herbivores occurring at the level of the whole plant community especially in areas of high soil fertility, such as pro- ductive grassland ecosystems (De Mazancourt et al. 1999). Similarly, there is evidence that moderate densities of invertebrate herbivory, for example,

Fig. 5.1 Positive effects of defoliation of the grass Poa pratensis on the transfer of recently photosynthesized 13_{C to rhizosphere microbes, leading to stimulation of microbial}

biomass, net N mineralization, and plant N acquisition. Data are expressed as % increase relative to undefoliated control. These data indicate that grazed plants stimulate soil microbes and their own N supply. (Data from Hamilton and Frank 2001.)

Soluble C Microbial biomass Microbial13_C N mineralization Shoot N Defoliation response (%) 80 100 120 140 160 180 200 220

by grasshoppers, can promote NPP through enhancing soil N cycling (Belovsky and Slade 2000).

There is mixed evidence about how herbivory affects root productivity. Pot experiments consistently show that repeated defoliation reduces root biomass (e.g. Guitian and Bardgett 2000; Mikola et al.2001), and field stud- ies have shown that moose and hare browsing reduces fine root productivity in Alaskan Taiga forest (Ruess et al. 1998). However, fenced exclusion studies on Serengeti grasslands show that mammalian grazers do not necessarily inhibit root biomass and productivity (McNaughton et al. 1998), and in a global literature synthesis Milchunas and Lauenroth (1993) reported both enhancements and reductions in root biomass as a result of herbivore exclu- sion. There are numerous reports of root herbivores negatively affecting NPP in a range of ecosystems (e.g. Brown and Gange 1990; Ingham and Detling 1990), and also incidences where infestation of roots by insects has led to proliferation in the growth of lateral roots (Brown and Gange 1990). Herbivore-induced changes in NPP have important knock-on effects to the soil food web and nutrient cycling, but these tend to be quite variable. For example, increasing NPP has been shown to have both positive and negative effects on both microbial biomass and higher trophic levels of the soil food web (Bardgett and Wardle 2003). There are two reasons for such idiosyncratic responses of decomposers to NPP. First, the relative import- ance of top–down and bottom–up forces in regulating soil food-web components may be context dependent. Second, plants not only provide C resources for microbes but also compete with them for nutrients (Kaye and Hart 1997). Therefore, the direction of effects of herbivore-induced changes in NPP on decomposer organisms and nutrient cycling may be governed by which of the two opposing effects (stimulation of microbes by C addition, inhibition of microbes by resource depletion) dominates. However, despite this uncertainty, it is most likely that positive effects of herbivory on soil biota and nutrient mineralization dominate in sites of high soil fertility, especially in grasslands where C addition to soil from plants typically stimulates soil biological activity since it alleviates C limitation of microbes.