Large Mammalian Herbivores and the Paradox of Soil Carbon in Grazing Ecosystems: Role of Microbial Decomposers and Their Enzymes

Grazing is the dominant land use across the world, and large mammalian herbivores exert strong influence over biogeochemical cycles. Grazing ecosystems feature C-rich soils, even though herbivores consume a major fraction of plant production to reduce detrital input to soil. Yet, counter-intuitively, moderate grazing can promote net soil-C storage in many ecosystems compared to grazer-exclusion. We address this enigmatic influence of grazers on soil-C and test their indirect effect on proximate drivers of decomposition: microbial extracellular enzyme activity. We used a replicated long-term grazer-exclusion experiment to measure responses in above- and belowground plant biomass, soil-C stock, microbial biomass, labile/recalcitrant C pools and three enzymes relevant to the C-cycle: peroxidase-which initiates decomposition of recalcitrant matter, alongside beta-glucosidase and cellobiohydrolase-which act further downstream on more labile fractions. Consistent with other ecosystems, upto 12 years of herbivore exclusion did not increase soil-C in the fenced plots despite higher plant biomass and higher potential detrital C-inputs. Grazer-exclusion did not alter microbial biomass; peroxidase increased threefold and beta-glucosidase was doubled; cellobiohydrolase was unaffected. Grazer-exclusion also led to twofold increase in recalcitrant-C and in microbial respiration, but it did not influence labile-C. Structural equation models supported the hypothesis that grazing favours soil-C via its indirect effect on peroxidase, but they did not support that the effects can run in the opposite direction where soil-C affects enzymes. Grazer-mediated shifts in how microbes deploy enzymes emerge as a plausible mechanism that affects soil-C. These linkages may be important to maintain soil-C sequestration in drylands which support large mammalian herbivores.