Genetic‐based plant resistance and susceptibility traits to herbivory influence needle and root litter nutrient dynamics

Abstract

Summary 1.It is generally assumed that the same factors drive the decomposition of both litter and roots and that nutrient release from litter and roots is synchronized. However, few studies have explicitly tested these assumptions, and no studies have examined whether plant genetics (i.e. plant susceptibility to herbivory) could affect these relationships. 2.Here we examine the effects of herbivore susceptibility and resistance on needle and fine root litter decomposition of piñon pine, Pinus edulis . The study population consists of individual trees that are either susceptible or resistant to herbivory by the piñon needle scale, Matsucoccus acalyptus , or the stem-boring moth, Dioryctria albovittella . Genetic analyses and long-term experimental removals and additions of these insects to individual trees have identified trees that are naturally resistant or susceptible to M. acalyptus and D. albovittella . In addition, these herbivores increase litter chemical quality and alter soil microclimate, both of which mediate decomposition in ecosystems. 3. The effects of herbivore susceptibility and resistance on needle litter mass and phosphorus (P) loss, when significant, are largely mediated by herbivore-induced changes to microclimate. But the effects of herbivore susceptibility and resistance on root litter nitrogen (N) and P retention, and needle litter N retention, are largely governed by herbivore-induced changes to litter chemical quality. Whether a particular tree was resistant or susceptible to herbivores exerted a large influence on net nutrient release, but the direction of herbivore influence varied temporally. 4. The controls on decomposition vary between herbivore-susceptible and herbivoreresistant phenotypes. This suggests that understanding decomposition and nutrient retention in some ecosystems may require considering the effects of herbivores on aboveand below-ground processes and how these effects may be governed by plant genetics. 5. Synthesis . Because so few studies have attempted to quantify genetic components of ecosystem processes, the integration of ecosystem ecology with population genetics has the potential to place ecosystem science within a genetic and evolutionary framework. Using field trials of known genetic composition, ecosystem scientists may use quantitative genetics techniques to explore ecosystem traits just as population geneticists have used these techniques to explore traditional traits such as resistance to insects.

Plant genetic effects on soils under climate change

“…In the absence of drought, chronic moth herbivory on susceptible genotypes reduces plant growth (Whitham and Mopper 1985), alters the abundance of ectomycorrhizal fungi (Gehring and Whitham 1991) and alters the abundance and diversity of other soil biota (Classen et al 2006(Classen et al , 2007. Further, litter and root decomposition and nutrient cycling can differ among susceptible and resistant genotypes (Chapman et al 2003;Classen et al 2007).…”

“…Similarly, genetically linked changes in plant C:N ratios, lignin, N, and P concentrations are correlated with both litter decomposition and nutrient availability at the plant-soil interface (e.g., Treseder and Vitousek 2001;Schweitzer et al 2004;Chapman et al 2006a;Fischer et al 2010). Root chemical quality, in particular N concentration, can influence root litter decomposition and nutrient release to soils (e.g., Classen et al 2007). Because roots are embedded in soils and root inputs are known to be especially important in regulating soil C accumulation (Rasse et al 2005), genetically-based differences in root chemical quality and exudates should be an important future focus of research.…”

“…As a result of these changes, susceptible trees release N to the soil while resistant genotypes immobilize soil N, resulting in different soil N fluxes ( Fig. 4; Classen et al 2007). …”

“…Because of their impacts on the tree, susceptibility and resistance to herbivory has cascading impacts on the bulk soil microbial community and their ectomycorrhizal fungal mutualists (Gehring and Whitham 1991;Classen et al 2006;Classen et al 2007). In the absence of drought, chronic moth herbivory on susceptible genotypes reduces plant growth (Whitham and Mopper 1985), alters the abundance of ectomycorrhizal fungi (Gehring and Whitham 1991) and alters the abundance and diversity of other soil biota (Classen et al 2006(Classen et al , 2007. Further, litter and root decomposition and nutrient cycling can differ among susceptible and resistant genotypes (Chapman et al 2003;Classen et al 2007).…”

Long‐term insect herbivory slows soil development in an arid ecosystem

“…Insect herbivores can have variable impacts on nutrient cycling in ecosystems; they can increase (e.g., Chapman et al 2003, Frost and Hunter 2004, Fonte and Schowalter 2005, slow (e.g., Hartley and Jones 2003), have mixed, or no impact on nutrient cycling (e.g., Classen et al 2007a). This variation in response likely reflects the interaction of diverse herbivore traits with the properties of contrasting ecosystems (e.g., outbreak vs. chronic herbivory, mesic vs. arid ecosystems).…”